Sunteți pe pagina 1din 388






The Fifth Kingdom

Third Edition

......: .... : .... .

'. :'.- . ; .... '. .
'. :." . ' . ' .
. .-.. .
. . .. .".
. .. -.'
- . .

. . . . : ... . :'.:


'." ",







The Fifth Kingdom

Third Edition

Bryce Kendrick



Foclls Publishing
R. Pull ins Company
Newburyport MA 01950


Unlv.r.dod. Federal de Pernamb<Jco

c:.ntro de OMeial Sl;(6gIca IIbIoJeca
1M. "of. MortIeS R6;o, 1235 CIc!Ode LWtntalo
CEP. &1.610-420 Recile PE
FolIe: 1081) 2126.8351 / 2126.1942

Il c,owo - 2(;0 ''H'IJ

(0)(, (,0995:j-CO ~> 1-

IV - E)'"
. ~F_deP""""'bUCO
CEP 50.670-901 Recife pernarnbocO - Brasil
Reg. n- 9957 -2AI1112OO6

I dedicate this book to my wife,


Cover Photo: Lichenized agaric. Omphalina ericelOl1lm. Photo by the author.

Copyri ght C 1992.2000 Mycologue PublicatiollS

ISBN ' 585100226

This book is published by Focus Publishing, R. Pullins Co., PO Box 369, Newburypon MA
01950. All rights are reserved. No pan of this publication, art as wel l as lext, may be
produced, reproduced, ~rfom1ed. stored in a retrieval system. transmitted by any means,
electronic, mechanical. by photocopying record ing, or by any other media or means without
the prior written consent of the publisher.
By arrangement with Mycologue Publications this lext is published and distributed
throughout the United Stales and the world, with the exception of Canada. Canadian sales,
returns. and other inquiries 5hould be di rected to Mycologue Publications. 8727 Lochside
Drive, Sidney. BC, V8L 1M8. CANADA. A CD-ROM that accom panies this ttx t may be
ordered by contacting Myco logue Publications at the above address or through



V03101l 81BQ
800'3 d~n


Table of Contents
Preface ............ ... ..................... ..... _................. _........ ............................... .... ... VII
Acknowkdgments ....................................................................................... viii
Introduction ................................... _............. _................................................. xi







Kingdoms. Classification and Biod i~'ersity .................................................... I

A Mixed Bag: Protozoon 'Pseudofungi' (the so-called "Slime Moulds"Phyla Myxostelida. Dictyostelida. Labyrinthulida,
and Plasmodiophorida). Chromistan Fungi (pbyl a Hypbochytriomycola
and Oomycota) Eumycotan Fungi (Phylum Chyu'idiomycota) .... ................. 9
Eumycoran Fungi - the mainstream - Phyla (2) Zygomycota
and (3) Dikaryomycota ................................................................................. 27
Kingdom Eumycota: Ph ylum 3: Dikaryomycota.
Subphylum I - Ascomycotina ..................... __ ............................................ 38
Kingdom Eumycota: Phylum 3: Dikaryomycota.
Subpfi"ylum 2: Basidiomycotina ................................... _.................... _......... 78
Yeasts: Polyphyletic Fungi ......................................................................... 112
Lichens - Dual (or even triple) Organisms ...................... ........................... 118
Spore Dispersal in Fungi - Airbome Spores andAl1ergies ....................... J 26
Fungal Physiology ...................................................................................... 142
Fungal Genetics - Mendelian and 1I.Ioiecular ............................................ 159
Fungal Ec<llogy .... .... ................................................................................... 184
Fungal Plant Pathology in Agriculture and Forestry ............ ...................... 200
Fungicides ................................ _.......................................................... _...... 216
Fungi as Agen ts of Biological Control ....................................................... 222
Fungi Exploiting Microscopic Animals ..... .................... ...................... ...... 239
Mutalistic Symbioses Between Fungi and Animals ............... ............... _.... 250
Mycorrhizas: MUUlalistic Plant-Fungus Symbioses ................................... 257
Fungi as Food: Mycophagy ........................................................................ 279
Fungi in Food Processing .......... .......... ......... ................. ............... .............. 292
Food Spoilage by Fungi, and Its Prevention ............... ............................... 297
MycolOxins in Food and Feed .................................................................... 303
Poisonous and Hallucinogenic Mushrooms ............................................... 316
Medical Mycology ........................................................ ... .............. ............ 327
Commercial Exploitation of Fungal Metabolites ...................................... 333
Sources of IlluSlrations ................................................................................ 34\
Glossary ........................................................... ,.................................... _...... 343
Index ............................................................................................................ 363


"Fungi probably rival flowering pl:lnts in their species diversity, and outweigh the
animal kingdom. Whilst wield ing great destrocti~'e power as agents of disease and decay,
they drive the global carbon cycle, sustain our forests and grasslands via mycorrhizal
associations. and clothe. as lichens, what wou ld otherwise be bare parts of the plane!.
Their developmentally versatile body forms provide immense scope for industrial exploitation as well as experimentally acce ss ible systems for studying fundamental biological
issue,. Yet most people's appreciation offungi stops at mushrooms. mouldy food and fairy
"Challenged by such ignorance. mycologists need to overcome some deeply rooted
prejudices. On the one hand. the variety. edibility and toxicity of fungal froit bodies has
always been a sOurce of fascination v>'hieh can be relied on to deliver new recroir.s to the
cause of mycology. but if that fascination becomes an obsession. the cause is lost.
hOn the othe r hand, mytologists working on disease tontrol. taxonomy or some
indl.lstria! pllXess often find it difficult to communicate the wider interest of what they are
doing. Because of the vicious cycle of neglect. their task is lUade harder by the need to use
technical' terms: piant scientists tan assl.lme that their audience knows what leaves, roots
and stems are: mycologists always have to explain what hyphae and mycelium are.
50 there are IWO images of the mycologist: one of the eccentric amateur, the other
of the remote profeSSional working on esou::ric problems. Both are damaging."
So writes ProfeSlior Alan Rayncr, one of mycology's mOSt aniculate spoke..~pcrsons,
and it is impQSsiblc to disagree with him. Perhaps this book can do something to produte
a more b~!anced understanding and appreciation of fungi among university students and
intelligent lay persons. Interest is the best st imul3nt to learning, and at least some of the
slOrics in this book will surely tickle even the most jaded p:date. since the fungal lifestyle
is so bi~arre, Ihe faCtS so strange. Science fiction writers. look no funher. Plots lie within .
So far. we ha,c described about 100.000 fungi. yet we estimate these to represe nt
less than onctcnth of the Earth's mycota. Part of this book. then. is a telebTiltion of
biodiversity: jusl think. there arc over len thousand spe-cies of mushrooms alone. Tragically. the world is gf'ddually losing its biological richness. As a resull of human activities.
speties ofliving orgJnisms, fungi among them. are being driven irretrievably imo c~tinc
tion every day. We need you. the readers of this book. to help stop those losses. There rue
many kinds of environmental action: may J urge you to become personally involvcd in
some of them. Our grandchildren wiUlhank us, but only if we succeed.

viii '

The CD-ROM which should be used in parallel with this book con tains many
images of fungi, but Twould like you to look OUt for pictures of fungi that I have found in
my own garden, or on the beach below my house. I have emphasized these to show you
that ifyoti keep your eyes open, you too should be able to find just as many fungi in your
own surroundings.

Mycology has now become so multifaceted, and each of itS many aspectS so spe
daliw:!, that il is increasingly difficult for one person to write a troly comprehensive text.
This book and CD-ROM may well prove that point, though I did nOI prepare them unaided. I am grateful to Joan Bennett (Tulane University), Bernie Glick (University of
Waterloo), and Jim Anderson (University of Toronto), fOf their input to earlier versions of
the genelics chapter, and recently to Brenda Wingfield (University of Pretoria) who made
vital contributions to the molecular aspects of the chapter as it appears in the third edition
and on the CDROM, I thank Shannon Berch of the BC Provincial Forest Service for
giving me access to her fine pbolomicroscOpe, which has provided a number of liIe
photomicrographs to be found on the CDROM.
Donald Barr (Biosystematics Research Institute. Ottawa) made sure the original
chapter on fungi with flagellate cells was up-to date, and supplied several original ill ustrations. George Barron (University of Guelph) supplied interesting new infonnation for
the revision of the chapter on fungi exploiting microscopic animals, and pennission 10
use his excellent photomicrographs. Alan Watson (Macdonald College of McGill Universi ty) sem me new material on biological control of weeds by fungi: John Rippon (Universit)" of Chicago) provided many helpful comments on medical mycology. Dr. Zheng Ru
yong (Academia Sinica, Beijing) gave me invaluable advice about the Erysiphales.l am
grateful to Dr. Henry Descals for a detailed and most helpful critique, which was valuable
in the preparation of the second edition.
I also thank the following professors who used the book in their courses, and provided me wilh useful feedback: Margaret Barr. George Barron. Lynn Margulis. Peler
Neumann, G.B. Ouellette, R.D. Reeleder. John Rippon, Suzanne Schwab, Don Thomas.
Mikoe Tansey reviewed the second edition and many of his suggestions were incorporated
in its second prinling. For the egregious errors and misinterpretations that undoubtedly
remain in thc third edition and the CD-ROM version, I accepl sole responSibility.

I would like to th ank many of my third and fourth-year mycology students. on

campus and clJITcspondence, and particularly my own graduale students, who stroggled
through early versions of scvcral chapters in order to providc me with constructive criti
University life provided me wilil wonderful opportunities for continuing my own
edu,ation, and my students certainly taughl me a lot--perbaps more than I sucreeded in
tea,hing liIem. I hope Th~ Fifth Kingdcm;. as book. web site and CD-ROM, will help to
redress the balance. Early retirement provided me with the time to take advantage of the
new technology which made it simpler to build and produce one's own CDROMs.
Since the fungi ate SO unfamiliar to mOSt students, good illustrations are an essential
pan of any mycology textbook. I was fortunate to have Mary Ann Milne as my artistic
collaboralor for liIe prinled version of liIe book. She drew most of the black-and-white
illustrations with obvious skill. delicacy and taste. Her versatility in producing accurate
line drawings from a variety of sources-vaguely phrased oro.l instructions, indistinct

pencil sketches. line drawings, photographs, colour transparencies. microscope preparations and macroscopic specimens-is dc:c:ply appredated. Some drawi ngs were kindly
provided by Frank DiCosmo, a former graduate student of mine who is now a professor at
the University of Toronto. and Ms. Gracia Murase. my able and versatile technician.
executed a number of drawings and diagrams. She also helped in other ways--compiling
the glossary and the index. making drawings and calligraphing titles. retyping lost files,
doing paste-ups of plates, proofreading and editing. numbering and labelling-and I am
indebted to her for her help, without which the publication of the second edition would
have been much delayed. In 1984-5 I composed the original manuscript on an Apple ll+
Microcom puter, using the Easywriter word processing program (which camouflaged my
almost total lack of typing sltil!). In 1985. the camera-ready copy was produced by a
Muitiwriter IV daisywheel printer using multistrik.c: carbon ribbons. The text for the second edition was prepared in 1991 on a new-generation PC: an MS-DOS clone wi th an
Intel 386 microprocessor runni ng at 25 MHz. using WordPerfect 5.1. The text and the
HTML version of the third edition h(lVe been pm together on 350 MHz and 600 MH z PCs
running WordPerfect 8 and Front Page 98 and 2000. The hundreds of colour illuslr3tions
on the web and CD-ROM versions of the book ha~"e been either scanned by an HP Scanjet
4C flatbed scanner with a transparency adapter. or taken with a Ricoh RDC-S300 2.3
megapixel digital camera. The image files were trdfisfonned and resampled with Web
Graphics Optimizer 4.0. The video sequences on the CD-ROM were imported from my
own Hi8 videotapes by a Matrox Marvel G400-TV video card and Avid Cinema software.
The over 1,100 illustrations have been derived from a variety of sou rces. My own
collection of teaching transparencies and digital images provided the majori ty. but many
othe r mycologists have given me images over the years for teaching purposes. I am
P'!arly indebted to George Barron, my erstwhile colleague at the University of Guelph.
for many fme images (and for almost all of those associated with chapter 15). Credit has
been given in many places. but sometimes I have had an image for so long thaI I have lost
track of its source. I must ask forgiveness of those whose contributions are not acknowledged. and I will be more than happy to add further attribut ions to future versions of the
I retired in 1994 to my dream waterfront home on Vancouver Island. J had no ide a
that 1998, 1999 and 2000 would be filled with the activity of producing web and CDROM editions of my book. and the third edition oflhe printed version. The lure of the new
technologies was too strong. and I succumbed to their possibilities. I hope those who use
the book and CD-ROM in tandem will feel that these efforts have been worthwhile. and
that at least some of those possibilities have been realized.
Bryce Kendrick
British Columbia, Canada, V8 l IM8
September 2000


lmagiflC the picnic of your dreams. You and your loved one float across II flower-filled
meadow, coming to rest under the shade of a giant white pine. There you spread out the
magic ingredients-the champagne(ofwine. or beer, if you prefer), the fresh crusty bread,
the p~te au truffe, the creamy camembert (or brie or roquefort) cheese. You may add other
ingredients -

many spring to mind -

bUI up to Ihis point your tryst is a tri bute to the

beneficenl influence of fungi on our diet and our ~nery.

The grass, the fl owers in the meadow and the pine tr ee have specialized
mltrieot-galhering fungi growing in and around their roots in an obligatel), symbiotic
relationship. Without these fungi" e believe that neither grass nor lree would exis\. Champagne. wine and beer - aU three are direct products of fungal action on specific sub-

str:ues, 3nd thc'i1.lcohol thcy contain is a fungal metabolite highly prized by those who
need an occasional escape from rcality Even those who prefer (0 kecp reality at ann's
length with psilocybin or L.S. D. usually know thaI these psycholropic substances are also
fungal melllbolitcs.
Bread owes its lightness and texture to the ' raising' activities of a fungus. The
mouth-watering fl avour of your pate is enhanced by the presence of pieces of black
trume, a subterranean fungus from Europe. The cheeses are ripened and given their unique
texture and ta51e by specific moulds.
But fungi, like people, ha"e a darker side. On closer inspection, the flowers in the
meadow may be found to be suffering from II host of fUllg~1 diseases - leaf spots, wilts,
mildews, blights lind more -and the pine tree may have problems with root rOl, heart rot,
blister rus.t and needle cast, all caused by fungi. Some oflhe food in your picnic may have
been insidiously infiltrated by fungi. Those ripe. juicy peaches ),ou brought along for
dessert may reveal rapidly spreading brown arcus. You must trust thaI the bread wasn't
made from wheat containing vomilOxin, or if it's rye bread, that no ergot, with its mllll!IUde of alkaloids and hallucinogens, was in the grain. Even your blue cheese and yoor
peanut butler could possibly contain myCOlo;o.:ins,
Homeowners know this other face, too. Has your wooden fence or your deck become rOlten and needed rebuilding? Has yOllr prile elm (fCc died, or your chestnut been
defoliated by leaf blight? Are your roses besmirched by black ~POI. ),our lilacs by powdery mildew, you r hollyhocks by IIlst? Do YOUf tOmatoes suffer from early blight, your
potatoes from late blight, your ~rapes from downy mildew, your strawberries from grey
mould? Are your JX'acbes attacked by leaf curl or soft rot, your apples by scab? Does
damping-off cause your seedlings to keel over? Does food go mouldy, tuming green. pink

XI I h~ ' lKUU Uc...:nUN

or brown, or growing whiskers, even in the refrigerator? And is there aereeping black stain
around the door of that appliance? Have you ever had athlete's fOOl, or jock itch, or
ringwonn of the scalp? All of these, too, are the results of fungal activity.
But there's still another side 10 the fungi. 'The blister rust on your pine tree may itself
be allacked and controlled by anomer fungus, as may the powdery mildew on the grass.
Specialized fungi can control infestations of insects in your garden. A fungal metabolite
is used world-wide to control many bacterial infections (including gonorrhea), while
another can cure some of the fungal diseases that afflict people from time to time. Organ
transplants now have much improved chances of succes.s because of a fungal metabolite
that safely prevents the body from rejecting the new organ, and this same substance seems
to StOp the development of some kinds of diabetes - the nrst actual cure ever discovered
for this disease.
These are a few of the reasons why you should know something about fung i. I hope
that by the end of this book, which I have tried to prepare as a tasry mycological smorgasbord. you will be able to add other reasons of your own.

Kingdoms, Classification
and Biodiversity
Kingdoms -

Now There are Seven!

As you read the text that follows, you rnay come across words that are new 10 you.
Mos t of them will be in the glossary. If even the definitions given there leave you scratching your head, r suggest you find and rcad a first year University Biology tc)(thook before
going much further.

You may not know it, but you are about to become a member of an elitc: group.
Although many people are aware that there are millions of different kinds (s pecies) of
living organisms on'Earth today (although OI.IT own species is doing its beSllOdrivc: many
of them into e;~tinction). surprisingly few people are aware thaI these organisms are now
di vided up among no fewer than se\"en Kingdoms. Before I can effectively develop the
theme of this book [must explain these major panel'Tl5. and those of some of the almost
one hundred distinctive evolutionary pathways known as Phyla (botanists sometimes
call them Di,isions) which make up those Kingdoms.

The really basic division among life fonns is between the simpler Prokar yotes and
the more complex Euka ryo t e.~. Look at the diagram below (after Patterson & Sogin
1992): it shows {he way in whicll we thin k the Kingdoms evolved. It is based on molecular
evidence: base sequences from ribosomal RL'fA.
The earliest foons of life, which appeared about 3,500 million years ago. were
prokaryotC5. We tend to define them by their relative morphological simplicity. and by
the absence of many features found in more modem cells. Although thei r modem descendants have a single ch romosome. this is no! found inside a nu cleus. and thei r cytoplasm
contains no mi IOcho nd r i3 or plastids (cytoplasmic orga nelles). These organisms make
up the baseline Kingdoms Arch:leb:lcteria and Eubactcria.
The prokaryotes had the world to themselves for 1.500 million years (the y did.
however, invent photosYflt hesis during that time). Not until about 2 billion years ago did
life take the next giant step. the evolution of the eukaryotic cell. Many biologists now
believe that th is arose as a result of the mutually beneficial symbiotic uni on of several
different kinds of prokaryote within anothe r host-prokaryote. (I) Mitochondria spo:cialize
in the oxidation of 3-carbon organic acids (the Krebs cycle). providing an immediately
availahle energy supply in the form of ATP. (2) P lastids may contain photosynthetic
pigments and enzymes (chloroplasts). or may store food. Many of us are convi nced that








w ,/ "


,, ,







1 , 1,


I, ,,I



~ , .- --, ,,-














Fig. 1. 1 Relationships of the iving Kingdoms.



.'.- "



mitOChondria. p!astids and eyen (3) nage lla were once r"'' e-living prokaryOkS. which
were e ngulfed and co-opted during the evolution of the eukaryotie cdl to ~come specialized and efficie nt components of the ncw. more sophisticated syStem.
EUlcaryotic cells also have their DNA organ ized into a number of discre tc chromosomes, which are found inside a nucleus which is surrounded by a membrane. Cell divi_
sion in eukaryote5 involves a complex process called mitosis. The nuclcar membrane
breaks down. a mitotic spind le of microtubules develops, and the chromosomes are
duplicated. Then the daughter chromosomes separate and are pulled to opposite poles by
the contracting spindle fibres. Each set of chromosomes then becomes enclosed by a ncw
nuclear membrane. and the cell finally divides into two.
Prokaryotic cclls have only a single. usually circular chromosome. and do not
undergo mitosis. They usually divide by a much si mpler process called bin3ry nssion.
Mitosis, with ils very accurate duplication and sharing of the genetic material. seems to
have been a C'l'lIcial invention. Only eukaryotic cells. with their precisely regulated genetic mechanisms. apparently had the potential!() evolve into more complex, multicellular organisms in which cells are organized into different tissues and organs. All prokaryotes are still microbes.
Now look at the Kingdom diagram again. The Archaebacteria and the Eu bacteria
are prokaryotes. lbe eukaryotes encompass the Other five Kingdoms, and it is in th ese
other Kingdoms that the dazzling e\'Olutionary explosion o f new taxa has occurred. The
diagram shows five eukaryote Kingdoms: Protozoa, Chromista, Plan tae. Animalia and
The e;ttplosion of eukaryote evol ution was made possible by. among other things. a
modified form of mitosis called me iosis or reduction division. In many organisms this
produces special sex cel!s called gametes. Each of these sex cells ha$ a single SCI of
chromosomes (w~ say that the gametes are haploid). When two gametes from compatible
parent organisms fuse. the resulting cel! (the zygote) has two sets o f chromosomes (we call
lhis condition diplo id). In plants and animals. zygotes develop into diploid, multic<;.ilular
organisms. but in most fungi the vegelative phase is always haploid. so meiosis must take
place in the zygote. Whether meiosis happens in the zygotc. or at the other end of the life
cycle, during the formation of gametes, it is responsible for the reassortment of the genetic
infonnation buill into the chromosomes.
New fcatures are constantly being added to the pool of genetic material by the
process of mutatio n. but sexuuI reproduction is the mechanism by which this pool is
recombined each generation in most eukaryotic organisms. producing an endless supply
o f variation upon which the processes of natural selection can work. This is one of the key
sec rets of eukaryote diversity.
The radiation of the twO unicellular Kingdoms (Protozoo and Ch romista) show)
how the evolution of the cukaryotic ee l! expanded life's horizons. But the full potential of
the new teamwork - J can it that, since sever.ll prokaryotes eooperate to make one functional eukaryotic eell- was not real ized until cells. as well as cen components. began to
cooperate. When organisms became multicellular. different cells could assume different .
specialized functions. This division of labour eventually led to the development of tissues and organs, and ultimately permitted the evolution of complex beings like our
selves, beings with almost infinitely expan ded capabilities (both wonderful and terrible).
Three new multicellular Kingdoms arose. exemplifying three different ways oflifc.
~Iu!ticellular organisms which could pho tosynthesize - make their own food from simple
inorganic precursors - were eaten by other multicellular organisms that lac ked this talent.
and both were recycled after death by a third group. These groups we calJ produce rs,
consumers and decomposers - the plants, the animals and the fungi. We rerognize about


9 phyla of plants, about 32 phyla of animals. and 5 phyla of fungi (2 chromistan and 3
'The world being what it is, the picture is not as simple as we might like. Some of the
divergent paths of evolution have come together again, almost as they did at the birth of
the eukaryotes, and many organisms that seem unitary are, in fact, partnerships or even
consonia. Lichens, for example, always incorporate both an al ga (e ukaryotic or prokary
otic) and a fungus.
Howcan fungi fit into two Kingdoms? !be answer lies in the way we derme the tenn
fungus (plural: fungi). Fungi are eukaryotk heterotrophic, abso rpth'c organisms that
develop a rather diffusc, branched, tubular body and reproduce by means of spores.
This describes not a single ph)'logenetic liDe, but rather a way of life shared by organisms
of different evolutionary bac kgrounds. We recogni~e throm lstan fungi as well as
eumycotan fungi .
If you find this strange, consider the 'algae' for a mome nt - they include represen
tativc5 of three Kingdoms: eubacterial prok:aryoles (the blue-green cyanobacte ria),
chromiSlans (brown algae, diatoms. etc.) and plantae (green algae). Both algae and fungi
are defined functionnlly or ecologically, rather than phylogenetically.
At this point it beromes clear that this book does not, as its title implies, deal
exclusively with the fifth Kingdom, Eumycota, but also discusses some elements of Kingdom Chromista. But these latter are relatively minor players in the biosphere when compared with the huge numbers and biomasS of the Eumycota.

Biological Classification
The first part of this book deals with the classification of the fungi. You can eer'
tainly ignore chnpters 2-7, nnd mo"e quiddy to the more aecessible and, to many people,
mon: interesting ch;!pters later in the book which deal with the many ways in which fungi
imlXlct on human exiStence. Hov,-ever, I don', think I am overstating the case if I say that
unless you understand something about how the main groups of funSi differ in morphology and behaviour. you will not be able to make much sense of Ihe more 'relevant'
sections of the book. If you can develop a son of 'cognitive map' of the main classes.
recognizing them on sighl, and undcrs(~nding the unique abilities of each. you will find
the study of fungi - mycology - infinitely mon: rewarding.

Biological Nomenclature
Every species of living organism is a collection of individuals which are very
similar (genctically. if not always in appearance), and each species has a unique name
made up of twO wOrds, which may actually be from the ancient Latin lex.icon, but are far
mon: often new, ps~udo-Latin words coined for the occasion. This two-epithet name is Ihe
bi nomial. You and ( belong to the speeies Homo Sllpiens. The supcnnarket mushroom
belongs to the species Agaricus bnmnesctns. In each case the first of these two Latin
words is the gene ric name or epithet (this places the organism in a genus. a collection of
simil:lr andlor related spe<;ies). The second Latin word is the epithet applied to one particul:lf spceies of the genus. But notice thallhe name of the species always consists of
both epithets together. This is because only the two-word combination is aClUally unique
to that species. The generic epithet is shared by all Olher species in th;!! genus. The same
species epithet may also be applicd to species in other genera (for example. many Canadian spring flowers, though belonging to diffcrent genera, have the same species epithet.
canadensis. as does the national animal of Canada. the beaver), So remember that only the
IWO epithets together - the binomial - properly specify a species. Homo sapienl is the
only extant species in the genus Homo, but most genera contain more than one species.


:lnd some, for example the mushroom genus Cortinarius, are made up of hundreds of
For purposes of classification (which is actually a method of inform:ltion storage
and retrieval), related genera are grouped into ramilies, families are grouped into orders.
orders into classes, dasses into phyla, and phyla into Kingdoms. Here is a sample of how
an organism is classified in this hiera rchical (boxes within boltes) system. Note that the
binomial is in italics, as it is in most scientific publications, while the names of
higher-ranking tlUa (families. orders, ctc.) are not in italics. If you refer to a binomial in
writing, it should be underlined, to show that it would be printed in il:llics.
Kingdom: EUMYCafA
Phylum: Dikaryomycota
Subphylum: Basidiomycotina
Class: Holobasidiomycctes
Order. Agaricales
Genus: Agaricus
Species: Agaricus brunllcsulls - the edible (supermarket) mushroom.
Why do we use this binomi:li nomenclature, which is so unfamiliar to the man-()rwoman-in -the-street? Why nOt use common names wherever they exist? For three good
(I) the common names of many organisms differ from country to country.
and even from district to district;
(2) the same common name is sometimes applied to different organismsfor example, the British, North American and Auslralian "Robins";
(3) common names can be downright misleading: Irish moss is a red alga.
Spanish moss is a flowering plant. clubmoss is a fern ally, and Il!indeer
moss is a lichen,
Let's face it, common n:lmes are too urm:liable and confusing to be of any use to
scientists. who rely heavily on international.communication and cooperation. Please take
the time to learn the proper scientific namts of the more important organisms you encounter in thcse pages. !fyou eve r want to know more about any ofthtm. you'll find that their
binomials are the key to almost everything that has been wrinen about them.
Bul why Latin or pseudo-Latin binomials?" I can hear you saying plaintivt1y.
That's easy too:
(I) Latin is officially a dead language. so al though scientists do coin new
\'\'Ords. the grammar, vocabulilJ)' and usage will change much more slowly
than those of all living languages. In a changing world, we need the
relative slability of Latin for our scientific names.
(2) The use of Latin for names and diagnoses of all new uua also means
that no one can be offended by being forced to use someone else's
language. Lalin has again become a useful international standard.

Biodive rsity
Different strokes for different folks. For some people, place names are evocalive,
calling up vivid memories of past e.~periences. For me it is the names of organisms I have
seen that bring back those experiences. Melrvsideros exu/sa conjures up Christmas in
Auckland. New Zealand, where the red flowers of this tree adorn beaches in December.
Pro/tO. c)"IIaroide5 lakes me back to the am;u:ingly rich Fynbos plant communicy ifI South

Africa, where this Oamboyant shrub flouri shes, and has been adopted as the nati~nal
Oower. Amphiprion places me on the Barrier Reef in Australi ... where these agi le Imle
damsel fish with blue-white stripes live unscathed among lhe tenwcles of lMge sea anemo-nes. Such organisms and the communities and ec~ystems of whic~ they are P:uu. are ~e
real reasons I leave home. I hope that some of you will also come to think ufthe hlodlver"Slty
you encounter as a measure of your quality of life.
Biodiversity is one of the buzz-words of the nineties, and I for one hope that it will
continue to be a Dewsmaker in the new millennium. Biologists know from the earliest
years of their ttaining that the Eanh is blessed with an amazing number of differeD! Ihing
things. As you have just read. systematists have tried to catalogue and describe all these
riches. but with widely varying degrees of success. We know practically all the birds, and
almost all the mammals, that inhabit the eanh. But we know only a small fraction of the
ntthropods and fungi. How can I make those two statements 50 confidently? Because
although there are many omithologists and mnmmalogists scouring the globe for new
taxa, they rarely find any. At the other end of the scale, entomologists and mycologists
find new taxa every day. They have so far described approximately a million insects and
some where between 70,000 and 100,000 fungi. but it is obvious to the professionals who
work in these areas that huge numbers of both groups have not yet been descri bed. I began
my mycological career examining the sequence of fu ngi involved in the slow decomposition of Scots pine (Pin/IS s}'/Ies/ris) needles. Almost immediately I found several microscopic fungi which turned out to be new to science. and I had the privilege of deSCribing
thcse fungi (You can see some of them in chapter II of the CD-ROM). Since I movep to
Vancouver Island. off th e west coast of Canada, in 1994, I have seen many mushroo ms that
could not be identified using the e)l;isting literature. I am convinced th at many of these
fungi are actually undescribed.
How many fungi are wailing to be disCQ\ercd? D:lvid Hawksworth came up with an
ingenious ans"'cr a few years ago. Noting that Britain is among the most intensively
in\estigated areas on Eanh for plants and for fungi. he pointed out that almost all the
Oowcring plants in Britain are known. and that there are about 2,000 species. Although
the fungi of Britain are definitely not as full y known. since new ones are still being
described, abum 12.000 species have been recorded there. This gives a ratio of abuut si)l;
fungi to each plant species. Extnlpolating (perhaps rather ambitiously) from Britain to the
entire globe. Hav,-ksworth suggested that since there appear to be about 250.000 species
of Oowering planl.S in the world, there are probably sb: times as m~ny fungi - about
1.500.000 fungi, in facl. Even if this figure is an over-estim:lte. and there are onl) half a
milli on fungi, we have still described only 20% of the total. and a huge task lies before us.
But if we accept this figure as a workiny approxima tion (and no one has yet come up
with a different formula), it brings us to a realization that about two centuries of mycology
have so far succeeded in describ ing only about 6-7% of the world's rnycota - a pretly
shocking Slate of affairs. Over the years I have been involyed in describi ng probably three
hundred fungal ta.t a. and have now basically run out of steam in this area of mywlogy.
But e,en if all the mycologists alive today were to publish 100 spa:ies apiece, they would
still manlge to describe only about 300.000 taxa. So it is a multi-generatio[ task.
The preceding discussion assumes a steady state in whi ch no species are added, and
none subtracted. from the global total. But we know that this is not t.he else. New species
are arising con~tantly. albe it at an unknown fate. as results of the combined effects of
selection pressure and genc tic recombination. Our own specics. by sticking its fingers
into every existi ng niche and ecosystem, as well as creating new ones. is undoubtedly
providing the fungi wi th new challenges at every tum, and they are surely responding to
those challenges by sp;twning ne w taxa.

KINGUQillS, t: LASSIl''1CA nUN "/<;0 tUum VI::KSITY 7

Fig 1.2 Dr. 8obMurphy, with a flTe-belied toad from
Vietnam-protection for f~

But now we come to the tragic bit.

Human activities afe undoubtedly driving
some fungi inlO extinction. We don't Know
which orhow many are being lost, and it is
absurd for anyone to suggest that we are
losing two species each week or twenty
each day. Infonnation on extinctions is extremely hard to obtain: How can you tell
when a pa rticular microscopic fungus,
which can be detected onl y by culturing
the soil, or a macros<:opic fungus tMt may
fruit only once in 20 years, has finall y succumbed'! Nevertheless. we have good reason to suspect that these things are happening. For exampl e, the huge fruit bodies of Bridgl"opo ru s (O xyp orus)
nobilissimus. a polypo re that grows on ly
in o ld-growth forests o n the wesl coost of
NorthAmerica (see chapter 5). are seen less
and Ics~ frequently, and (a long with the
forests in which it Ih'es) this species may
certai nly be considered endang ered.

But o ne of our problems in North America is that we do not have exte nsive records
of the myCOtll from the past - a base-line with which present-day comparisons can be
made. Fortunately, so me European countries, with centuries of datil collec tion to dr,lw
upon, have tx:en ab le to document the decline in num bers of mDny fu ngi. and hllVe
published what they call Red Lists, Thes.: listS highlight the increasing rarity of many
fungi. and the appa~nt disappearance of somc,
So what doc s a fire-bellied toad from North Vietnam have to do with prese rving
fungal diversity? Re3d on... Dr. Bob Murphy. Director of Ihe Royal Ontario MU$Cum's
Centre fo r Biodiversity and Conservation Biology. reports in Ihe Globl" and Mail for Jllly
12th, 1999 that he has JUS! retumed from collecting herpeti les (amphibia and reptiles) in
the North Vietnam ra inforest. His comments about his animals are worth repeating here.
"BeeaU!;e th ey're beautiful, aesthetic ally appealing. wonderful animals, you can get them
protected. If you can get them protected. you protect the forest. If you protect the forest,
you pr(){ecl everything that's there, l"S{Hci(1Uy tire fUngi (my italics), which are producing
the majority of new pharmaceuticals that are coming out:' You will find an echo of that
statement in chapter 24, in the discussion of antibi otics, immunosuppressants and other
fungal metabolites.
So ou r efforts to collect (md describe the world's myeota need to be redoubled. As
you will learn from many of the other chapters in this book, and perhaps mOSt accessibly
fromchapter24. many fungi eonfe r e normous be nefits on Mank ind_ I am nOt just referring
to tbe producers of ant ibiotics such as pe nicill in and imm unos up pressant s like
e)'elosporine. but also to the myriad species which recycle organ ic matter. especially
plant debris. and to the others that establish obligate mUlualistic symbioses with many of
ou r most imponant plants.
This awareness of our ignorance has led 10 proposals 10 compile whDt are call ed
"All-Taxa Biodh'ersily lOHmtories" Of "ATBT" for sho rt, A meeting [ 0 discuss such an
ATBI for a forested area in COSta Rica came up with a fi gu re of 520 million for the fUllgi
alone. Although the Costa Rican venture didn 't ny, it spawned a margi nall y less ambi -



tious projel:t for the Great Smoky Mountains National Park in Tennessee. Setting other
organisms aside, it has been estimated thai there are 20,000 fungi in the Park, of which
only 2,250 have so far been described, (Hey, that's more than 10%, 50 we are already ahead
of the game.) A two-year pilot project aimed al refining sampling methods and data
protocols was begun in M~h 1999. and mycologists everywhere will be watching with
in terest (or being co-opted) as this unfolds. To learn more about this project. visil the web
site hltp:J/www,disco'

Web Sites and Further Reading on

Classification and Biodiversity
http://ph ylogeny.a ri zona.ed uJlreeJphyl ogeny.html contains information
about the ph ylogenetic relationships and dlara<:teri stics of nrganisms,
to link biological information available on the internet in the form of a
phylogenetic navigator.}msubbio.hlm? rf=ma& COB",home &
TMog =15251]25924 750&1'tli n t= lS251325924750 has pages on
http://teclnnic.lIationalgeographic.coml2000IbiodiHrsity/ has pages and
maps that document loss of biodiversity (though nO! in fungi).
Crowson. R.A. (1970) C lass ifi cation and Biology. Heinemann, London.
Jaques. HE (1946) Living Things: Ho w 10 Know Th em. Wm.c. Brown,
Marguli s, L and R. Guerrero (1991 ) Kingdoms in turmoil. New Scientist. 23
March 1991 , 46-50.
Marguli s, Land K.Y. Schwartz (1982) Five Kingdoms. Freeman, San Fr~n
Pauerson and Sogin ( 1992) in The Ori gin and Evolution o f Prokaryotic
and Eukaryotlc Cells. (eds.) Hartman and Matsumo.
Ross, H.H. (1974) Biological Systematics. Addison Wesley. Reading .
Weese, C.R.. O. Kandler and M.L. Whcelis ( I990) Towards a natural system of
organisms: Proposal for the domains AKhaea. Bacteria. and Eucarya.
P n>Cet!dings or the National Academy of Science 87:4576-4579 .


A Mixed Bag:
Protozoan 'Pseudofungi'
(the so-called "Slime Moulds" Phyla MYXOSTELlDA, DICTYOSTELIDA,
Chromistan Fungi
Eumycotan Fungi (Phylum CHYTRIDIOMYCOTA)

Firsl let me elaborate a little on the definition of fungi given earlier. Fung.i..~jJelher


cell ulose, and with in this wall the cytoplasm and nuclei live and move. protected from the
o utside world, bu t able to explore small areas of it inside their apically extending, microscopic. hyphal tunnels, and much larger areas by means of their OetaChable r~roducti\'e
units called s pores.
But before I discuss real fungi. four "outsider" phyla must be mentioned. These are
the so-called ,.


I .
t of as fungi,
are still
with in some
curtent mycological literoturc. this is at least phy logenetically incorrect. Here's why. The

assimilative or somatic phases of three of these four groups are basically amoeboid: none
of the four ever produces hyp hae (a diagnostic feature of most true fungi), and the assimilative plasmodia have no cell walls. The names currently applied to some of these groups
an: mi~ing, in that they imply a fungal nature, so in three cases I have supplied DeW
names renect;'ng their non-fungal affiliations. I hope you will agree with me .a~r yOU
have read the thumbnail sketches below and compared them with my later descnpllons of

the waH-possessing hyphal fungi. These phyla are included in some mycology courses
because some of them (particularly My~ostelida) tend to tum up when we look for fungi.
And if mycologists, who have historically looked after them, ilbandon them, which other
group of organismic biologist~ will agree to add these organisms to their already crowded
course schedules?


This is the only one of these four non-fungal phyla you are likely to find if you go
out looking for fungi in autumn.
somatic or assimilative phase of the

pets, crawling around

slowly pulsating plasmodium will

dramatically into a
duster of stalked, dry sporangia full
formatio n involves
redllction division (meiosis). so when
germinates to release a cdl that
> may be either amoeboid or bifJage\!ate, this cell can act as a gam'ete. Fusion of IWO
'?;C11Q;. cumpalible gamet~s produces a diploid zygole_~hich can Ihen fuse or aggregate with
I . . " other zygot~s. begm 10 feed. andevenmal1y grow mto a plasmQcliuni once more. A typical
~ w.;;.Q; r
mymsfelid life cyc1\? is shown in Fig. 2.1.




ge''''i nation

Fig~ 2.1

MyxosteUda: Me cycle of StemQn;/is fusca.

A l\IlX ED BAG 11

.., ,~~ vidual amoebae which feed by ingesting bacteria , The reproductive phase begins when
t t ~ the amoebae begin 10 secrete cyclic adenosine mooophosphate (cAMP), a son of phewt,
!!lone which cau~ the anlOt:;.~ t~ be..!!lutually attracted. They stream together and form
aggregations called pseudoplasmodia or :&l!J::f (these differ from lltte plasmodia in that
each amoeba retains its cell membrane). Each slug crawls around until dry conditions
prompt it to undergo differentiation, heaping itself up and eventually fOrming a Smlcture
called a sorocarp...which has a slim cellulosic stalk and an expanded head comaining
spores. Dictyosteiium has been used as an experimental organism by many sciemists
because it provides a simple system for studying differentiation. (Fig. 2.2)

(. \.;


.y ......


..... r'


'~ 1





The colourlcs:; colorue$ of U:tbYri~11t

fa cause a.,wasting dise:lsc of eel grass (Zosfem,



one of the few marine flowering plant~). e s'j,t;;-dlc-shaped. naked cells of rne....co1ony-J
live and move entirely ~thil!.a networ of narrow, tubular, polysaccharide sheathS which
they themselves secrete. They release biflagellate gametes, and the zygOie divides mitotically to generate a new colony, whose cells are presumable diploid. Most orner members
oflhis group are also marine. parasitizing algae. (Fig. 2.3)
("(" ~


J~ ~b ~ "iE:!
~ 2
11-'; ~~ \, "/

:1:r .. 1/




~ "C~~1"'~
~ ---"'~.
-'<),<:, "'" 0



Fig. 2.2 Dictyoste&da: life c~1e of Diclyos lelium djscoideum.










Phylum PlASMODI OPHORIDA (formerly



cabbage (Brassica oluacea). Inside, they grow into multinucleate
primary plasmodia. These eventually develop II wall and divide internally into uninucleate se<:ondary sporangia. These germinate, releasing four secondary. biflagellate z~pores
which leave the host. These may also act a.~ gametes. fusing in pairs, but soon-infe<:t a root
again, developing within host cells into mu ltinudeate secondary plasmodia. At marority,
these can. cleave into uninucleate cysts, each containing a single spore, which can persist
in the soil for many years. ThIs parasite stimulates the cabbage roots to become grossly
swollen, a serious diseas'e' co ndi tion known as "club roo!." (Fig. 2.4)

"Real Fungi

The four groups just outlined are nOI fungi. Every other organism dealt with in this
book is II fungus.
As I mentioned in chapter I. what lILe call "fungi::.share many morphologica1..aru!
behavioural similarities in their ~milath-.e..p.base, buUb:ey.-do...not.ha.'iC. a _unifonn &!<. It now s~iiiSobvious that they have evolved from at least \WO ances;;;;"'"" . can produce cells that swim hy means of one or twO very fine
whiplike extensions
I flagell a (rather like the tails of sperms). T hree phy la Hyphochytriomycota, O om ycot:l and C hytridlomycota - fall into this category. Molecular evidence tells us that they are members of two different Kingdoms, the first two
being Chromistan in origin, the last (despite ils Oagc:Uars: phase) ElImYCQlao The other'
two main-line, largely terrestrial fungal phyla never have moiilc: cells. ami they _ the
(). Zygomycota and Dl kllryomyt:ot:1 - make up the rest of Kingdom Eumycota~thollgh
only the Dikaryomycota produce highly_diff!.rentiated, multiccJlufllf'reproductive struc\ you will sec.
Before I introduce you to the three flagellate phyla, a few words about flagella
(singul ar: flagellum). These are very long, narrow organelles. essentially contractile ex~
tensions of a cell. which have the ability to beat. or make whip-like motions. Th is beating
confers roolility on the cell: flagella move the cell about in water, giving it the ability to
swim up chemical gradients (that is, 10 move from a lower concenu'l.Iion of a substance
toward a higher concenlrlltion), such as those which lead toward a sexual paMer or a
suitable host organism.
"".YJ\ .n(f



c{:l.' q. 1

Fig. 2.3labyrinlhulida: Labyrinthu/il.



The amazing thing about flage!la is that wherever we find them among e~ar)'otic
organisms, they have esse ntially the same fine Structure: along the shaft of the fl~gellum
run 9 pairs of peripheral microt\lbules and 2 central microtubu!es - the 9 + 2 "Pauem.
Each microtubule is buill from II protein called tubulin, its subunits arranged in 13 vertical staclcs (count them in Fig. 2.5) around a hollow centre.

" picture ofa transverse section of a flagellum (which is about one-sixth [0.17J of
a micron thick) would look more or less the same whether the flagellum came from one of
the simple fungi discussed here, or from a protozoan such as Poromot!cium (which has lots
of short flagella called cilia allover the outside of the cell).


from II unicellular or

colonial green alga, a sea gooseberry (a Ctenophore) whi ch bas plales of cilia that beat in
rhythm and move the whole macroscopic organism, or from the spenn (male gamete) of a
brown alga, 11 sea urchin, a moss, a (ern, or a human. You see, all eukaryOles really are

-- -y- .
../ - ', '

. ~ e<


{nucl ......1:>. ) __

..... .-,.cIe stage


""'0" '1

IN 711 AOOT ~ ...\II

Fig. 2.4 Plasmod"fOPhorida: life cycle of P/;umod;ophora br",ssicae.


U FP" . CC~


Fig. 2.5 - Transverse sect ion of a typical
9.2 microtubule flagelum(diameter
about 170nanometres)

Kingdom Eumycota, Phylum 1: CHYTRIDIOMYCOTA

The somatic phases of the microscopic chytridiomycetes vary widcly inflPpearallee, but when they undergo asexual reproduction, most produce zoospores ~l!1a single,
backwardly dirccted,JWll! lasb flagellum. I will discuss members of four orders: the
Chytridiales, Spizellomyeelales, BlastocladiaJcs, arld J\'Iulloblepbaridales_ Although
these orders were formerly separated on the morphology of their microscopic thall i, we
now know that this is too variable to be reliable.
Emphasis has switched to ultrastructural features of the zoospore, some of which are
illustrated in Fig 2.6. Unfortunately. although con~er'iative, and therefore taxonomically
valuable, these characters can be seen only in the transmission electron microscope after
elaborate preparative techriiques. Fortunately. you can sec enough of an Allomyces
zoospore under the light microscope (using phase contrast optics) to identify the phylum
(though somo: members of this phylum recently discovered in the rumen of large herbivorollS mamma!> have man y flagel!a on each cell.)
Orders Chytridiales ond Spizeltorn ycctales. These orders look very alike under the
light microscope. and it takes an expert to tell them apart _However, most Chytridiaks arc
aqu~tiC', while most Spizo:lIomycctales live in soil. Until important,differenq:s were found
illth~ ultrastructure of their zoospores (Fig. 2.6), the two orders were considered to be one.
These simple fungi do not produce hyphae. They are often parasitic, and their assjmilativ~ thalills often consists of a single cell. This cell is either: (1) entirely converted into a
reproductive sporangillm (th" holo.ql1])ic mode, Fig. 2.7B) as in Olpidium b'assicae. t)[
(2) differ~ llliated into assimilative rhizoids and a sporangium (the euca rpi c mode, Fig.
~2. 7A). as in Chylridium lagenaria or Spizellomyces prmctatu-~. Other chytrids have a more
extensive system of rhizoids, called a rhizorn yceUum. which may nourish several sporan gia. as in ChrdochYlrium (Fig. 2.7C). W~ describe this multi~porangial condi tion as pnlyce nt ric to differentiate it from the monocent ric form~ just mentioned, which produce
only a sin gle sporangium. The difference between rhizoids and rhizomycclium is that
rhizoids generally have no nuclei in th"m. and are usually less than a millimetre long.
whik rhizomyc elia contain nuclei and can be much more extensive.

You might be interested in the activities of some of the members ofmcs<: two orders
including the fungi just named. The holocarpic Olpidium brassicae does not itself caus~
much damage to plunt roots, but is the vector of some n:lsty pl:lnt viru ses. The eucarpic
Sphellomycts puncUllus and Chylridillm Illgenoria paras itize polle n grains. The poly_
centric Cladoclrylrium is saprobic, growing on decaying aquatic vegetation. At least one
chytrid is II seriouS problem for fanners: Synchylr;um endobiolicum causes wandisease of
potato. This fungus produces dark brown, cauliflower like growths on the tubers. and a
catastrophic reduction in yield. Fortun ately. although the pathogen is widespread in
Europe, and has spread to Newfoundland, resistant varieties of potato help to keep the
disease und er control. Other microscopic chytrid~ parasitize algae, and can be so numerous as to Cause epidemics which sign ificantl y. if temporarily. reduce primary production
in lakes.



Fig. 2.6 Litrastructll"e of f~1 zoospores: er. endoplasrric retict.Un; F, fIagel.m; G, goIgi apparatus;
K, knetosome; L. ipid; M, milOChorrlion; m, microbody; rm. mastigooeme; mt, rricrotul::Ues; N,
rncleus; NC, nuclear cap (rbosomes); nFe - l1OI"I--ti.n:tioJlal centrioles; Nu, rudooIus; R, ~;
Ro. rootlet; Rv, nroposome; SO, striated cisco
-r.:i51S ~:::l y"~JJ.!)oV)

" ...,.J- rv\.Q



The Frog Probl em ...

Most recently, a eucarpic chytrid has been found attacking amphibia in many part
of the worlq. It has been associated with significant die-ofTs of frogs in Australia, Central
America, and at !he National Zoo io Washington, D.C., U.S.A. The condition has been
quite reason ably called " chytridiomycosls' since no other organisms are yct known to be
involved. The fungus lives inside epidellllal cells nnd causes thickening of the skin which
may interfere with oormal respiration (frogs hreathe partly through their skins). Its zoospores
have ultrastructural characters (the kind that can be seen only under an electron microscope) that put it into a new genus, BlIIrachochytrium. Joyce Longcore, the chytrid taxonomist who detenni ned this, published a short ankle in iruxu/um, the newsletter of the
Mycological Sodety of America for October 19%, 'and gave illustrations of both the
eucarpic thaUu s and the zoospores. The paper deSRibing !he new genus appeared in
Mycologia in April of 1999, and the full reference is given at the end of this chapter.

B: O/pldlum

c: cr.dochytrlum



Fig. 2.7 Types of thali and reproductive strucllres among the Orytriciorrrytota. A:. eucarpic thaLs
of Spiullom)ces p uncta /us lSpil:eIorn).tales) in pine polen; B: noIocarpic thallus of Olp/dium
b raukae (Chytridiales) in cell of cabbage root; C: poIycenlrk tha~us of C/adochylrium
(Chytrio::iales); D: stages of oogamous reproductkln i1 Monobll'pharis polymorpha


A i'lUXED B.\G 17

No one knows why this fungus would suddenly begin killing frogs in places as
diverse as Au stralia and P:mama. The fu ngus may have been tra!l5poncd to these places
only recently - perhaps even on the boots or equipment of re~archers studying the
d isappearance of frogs. Or the fu ngus may have been present for a long time but frogs are
now succumbing because their immune systems have been impaired by recent environ
mental changes. One obvious change is increased ultraviolet light. which is known 10
damage immune sys tems of animals. Recently, chlorinated chemicals released by hu
mans have auacked the ozone layer in the upper atmosphere. allowing 10% more UfV
light 10 reach the Earth's surface. Industrial chemicals may also be danlaging the frogs'
immune systems. Retinoids are under suspicion because they eaw;e binh defects in many
animals, including frogs and humans. Accu tane. used to treat acne. is a retinoid known to
cause binh defects in humans. U you are interested in pursuing this topic, I M1ggest you
search for more infonnation on the internet: check out the archives of Rachel, an internet
environmental magazine.
Sexual reproduction in chytrids and Spizellomycetales needs to be reexamined: it
used to be assumed that any zoospore with twO flagella, and evely resting spore. resulted
from nuclear fusion. Now we know that some biflagellate zoospores originate by incomple te differentiation of cytoplasm during zoospore formation. and that many resting spores
are just thickwalled asexual sporangia which can survive dry periods.
Order Blas todadi alcs. Here the thallus has both broad true hyphae 3nd narrow
rhizoids. Allomyas orbuSCllllls, whose life cycle is illusll":lted in Fig. 2.8. exhibits what
we call alternation o r genera tions - a rotation between haploid and diploid thalli.
Haploid Ihalli produce gametes in $pedalized gamt tangia. while diploid thalli produce
flagellate zoospores and resting sporangia. In AI/omyce.l the gametes come in two sizes,'a
condition called a nisogamy. The general principle underlying anisogamy is division of
labour: the smaller. more mobile game te (which we can now think of as male) ac tively
see ks out the larger, less mobile (female) gamete, which has sacrificed some speed in order
to carry enough food to give the next generation a good stan. In ,l,/lomyces arbflsculus.
bo th kinds of gamete arc formed on the same hapl oid thallus. The colourless female
gametangia are Ixlme at the lips of hyphal branches. with the orange male gametangia
immediately below.
Zygotes develop into diploid thalli which bear two kinds of sporangia. thin-walled
and thi ck-walled. The nucl ei of thinw a!led sporangia undergo repeated mitosis and
produce mi lospores. which in this case 3fe diploid, uniflagellate zoospores that can establish new diploid thalli. The other kind of re productive structures. resistnnt sporangia.
shown on the right side of the diagmm, are thickwalled, brown. and can survi'>e for up to
30 years. E~'entually, some environmelllal stimulus trigge rs reduction division (m.:iosis)
in these sporangia. and the resultant haploiil meiospores are liber:.lted and develop inlo
sexualthaUi . Coelomomyces is another genus of the BlastOCladiales in which some spe
cies arc obligate parasi tes of mosquito I3rvae, and attempts are being made to use them in
biological control of Ihesc in~1S (see chapter 14).
Orde r Monoblcpharldalcs. MOll oblephar;$ polymorphu (Figs. 2.6. 2.7). which is
found on twigs of bin:h, ash, elm or oak submerged in slightly alh.!!"e freshwater pools,
is the first fungus we have met that has gone all the way to complete se.,u~1 differentiation
of gametes. The male gamete is ffi()tile (a speno). but the female (an egg) is not. This style
of sexuality is called oogllmy. Sperms fonn in gametangi~ called antheridia. while eggs
develop in oogonia, which are found on the same hypha just below the antheridia.
Spenos are ofte n released before the adjacent oogonium is ripe. This mny be a
mechanism for avoiding selffertilization. and ensuring oulbreeding (calle4 hetcrolhal
!ism in fungi). After the egg has been fenitized. the resulting zygote becomes amoeboid .


moves 01,11 01110 the top of the oogonium. arid encysts, developing a thick wall. Meiosis
probably occurs when this resting spore gemtinates. produci ng a genn tube (another
name for a first hypha).
Ahhoogh we Cbytridiomycota vary in so many things: in the morphology of their
assimilative phase, in their pauems of selluality. and in their adoption of parasitic o r
saprobic lifestyles; most of !hem have mOlile spores (zoospores or gametes), wjlh one
flagellum al the back (posteriorly uniflagellate - the cell swims li ke a spenn), and their
eel! waUs. like those of the other, more comple ... , eumycotan fungi, are largely made of
c hitin (8 polysaccharide very sintiJar to the stuff of which insect exoskeletons ate made).

They synthesize lysine by the same pathway (see chapter 9), and the more advanced

of the group produce troe hyphae. The Chytridiomycota apparently represent

modem survival of the ancestral line that evolved into the eumycolan fungi.


, ~~




Fig. 2.8 BbsIOCLxiaJe!.: liie cycle of A IIQmyces arbusculus.

- ...

('1 "-t,) ,.'- .~ . ~ ,

' ,-





Some new and different Chytridiomycetes!

lust to spoil our unitary picrure of the chytridiomycetes, in 1975 Orpin diSCovered
some new and very different chytridiomycetous fungi living in the f\lnlCnS of large herbivorous m:unmals, These fungi, mos.tly species of NeocallimastiT, were obligate1y anaerobic. They resembled then- aerobic relatives in many ways. but had no mitochondria, and
often had multiflagellate zoospores. Fifteen species of anaerobic chytrids had been descrilxd by 1994. They produce rhlzomycelia I>.hlch efficiently penetrate plant material,
and have enzymes that break down ceHulose more effectively than the cellulases of the
mould Trichodeww (see chapler 14 pan 3. and chapter 24).

Kingdom Chromista, Phylum 1: HYPHOCHYTRIOMYCOTA

This group is like the chytridiomycetes in many ways: they live in fresh water or
soil; they can be parasites or saprobes; they may be holocarpic or eucarpic, the laner kind
having assimilati\'c rhiwids; the sporan;;ia release uniflagellate zoospores. So why aren't
they chytridiomycetes? A single ch:lr.l~ter: ,visible under the light microscope gave the
original clue.. and was soon supplemented by sc\'eral ultrastructural features acce~'Sible
only to the electron miCl'OSC()pe {Fig. 2,6).l1JC 'visible' feature co~h3yiour of

al\\ revealed by the

h fla!:elJum is smooth
(a whiplash flagellum). while in the hyphoc hytrids the axis of th e flagellum bears many
fine laleral filaments, called mastigonemes, thaI give it the name IinscJ flugellum. These
may ap~ar 10 be insignificant differences, but bio!og,i s~~ consider the numbers and kinds
of flJ;;ella on zoospores to be an e," rcmely cQns~n' J1ive char:leter- one likely 10 remain
unchanged over vas(stretchcs of time, perhaps even hundrcds of millions of years, This
make~ it 3n important indicator, whic h is amply confirmed by the ultrastructural differences illustrllled above, and juslifies the recognilion of Phylum Hyphochytriomycola..
There arc few well,documented spedes in Ihis phylum, but H}phochylrium call:rwidl"s is
common in soil, and is often (like the chytrid~, Spizellomycl"s and Chylridium) found in
pollell when this;s added to soil as 'bait' in lite laboratory, This species may be of some
importance in the natural biological control of piOn! pathoge nic Oomyceles (see below),
by parasitizing their oospores, 1\0 hyphochytrid hos yet been seen 10 reproduce sexually.

Kingdom Chromista, Phylum 2: OOMYCOTA

lIaving just read about the millllte but bosic differences between the two previous
groups, you won't be surprised 10 learn thai similar inconspicuous features di~tinguish
the oorn),cetcs, our last and mOSt important group of chromistan fungi,
Basic feat ures ( I) Oom)'cClou,~ 7.00spores have two flagella : one tinsel one whiplash (Fig, 2.9A). and these arise from the side oflheccl1. rather than:lI the front orlhe rear,
as in other groups, The zoospores swim with their tinsci llagcllum pointing forward. while
thc whiplash l1agellulll is dire<:l~ backward ,
(2) Unli ke the nu dei ofal! true fUllgi. Iho><: ill assimilat ive hyphae of oomycetes art:
diploid, and
(3) the walls of Ihe hyphae usually contain a cellulose-like material (a poorly erystall ized hexose polymer), though this makes up only a fractio[l of the cell wull. and chili n
h~s also been fou[ld in some oornycctes, All of these characters separ~te them from the
eumycotan fungi. But the feature that gives th~ group its name is its oo!;!lmous ~.::xual
reproouction. lind the facllhal each zygote develops illto a thick-wa11cd. ~rsistent o-o;<;pore


(Fig. 2.10 A.B) Note, howe\"er, that fungal oogamy is not unique to the Oomycetessome Chyuidiomycetes such as Mvnoblepharis do it, too.
Chytridiomycetes and Hyphochytriomycetes are often extremely inconspicuous.
as befits organisms that can devOie an (albeit brief) lifetime to e;w;ploiting a single p<llJen
grain. Oomycetes. though they also include some holocarpic and eucarpic unicells. often
produce c;w;lensivc hyphal networks (mycelia). These fungi, covering a dead fish Iil:.e a
Whitish fur coat, or devastating crops such as grapes, hops, lettuce, cabbage, radishes,
potatoes and tobacco. have spawned a number of common names - water moulds lind
white r usts, downy mildews and damping orr. We' ll tal:.e a 1001:. at some e;w;amples.
Order Saprolegnlales. The wate r mould, Saprolegnia parasitica, attacKs fish and
their eggs. After establishing itself, the fungus reproduces aseJlually. The tips of the normally non -septate hyphae beeome modified into long mitosporangia (Fig. 2.9A) delimited by a cross-wall al the base. These ase;w;ual sporangia release biflagellate zoospores,
often called swarm spores which swim actively for a while, then encyst: this means that

. . _e



D: AI~ugO -

1>0" Of SO ""

Fog. 2.9 Asexual reprod.Ktion in Oomyco ta. A: Saproiegriales; BD: Peronospofales.

they Stop swimming and develop a thick wall. later, they genninate again as secondary
zoospores which. if they are lucky. will find a new substrate and deve lop into new assimilative thalli. 'This process of encystment. followed by a repetition of germination, is a
strategy that gives the spores a second chance at finding food if they aren't so lucky when
first released.
Many Saprolegnia and Achlya species form compatible anthe ridia and oogonia on
the same mycelium. which means th at they are hom othalii c. S ince the assimi lative thallus is diploid, meiosis must take place inside the gametangia. E.lch globose oogonium
contains several eggs (Fig. 2. lOA). A nu mber of antheridia may grow toward and touch a
single oogonium. penetrating its wall at pre-formed thin spots and sendi ng in fertilization tubes which deliver the male nuc lei to the eggs. Fenilization is more reliable because
neither gamete is exposed to the vagaries of a free-swirruning existence. The whole
double life cyc le is illustrated in Fig. 2.11.
The zygotes develop thick, resistant walls and obviously function as survival spores
th nt can live through Such catastrophes as the drying up of the pond or stream. Homothnllie species ha ve lost the enhanced variation provided by o utbreeding, but they still
benefit from the thick-walled resting oospores produced by the sexual cycle.
Order Peronos porales, Many members of th is order arc ob ligately parasi tic on
higher plants. In some cases they cause epidemics that dev astate imponant crops. The
build-up of these epidemics is made possible: (t) by our need to grow dense stands of
single plant species (c rops), and (2) by aerial transmission o f me rungi, which have evolved
airbome mitosporangia (Fig. 2.9 B.C) Noto that these are often wrongly called conidia:
they are analogous but not homologous to those spores (whic h are disc ussed under the
Phy lum Dikaryomycota). Dogonia are also fonned, each contai ning a single egg (Fig.
2.10 B). Sexual reproduction is usually homOlhallic (the antheridium arises from the
same thallus as the oogonium).
We will examine
representatives of five ge nera from three Frunilies, Pythincene
(Pyllrium, Phy /()phrhora) . P e r o no s porllccu e (Pu() n()s p ora, Plasm()para), and
Alhuginaceae (Albugo).
Damping-orT disease of seedli ngs (Pylhirlm - Pythiaceae)
Th is is a soil-bome disease, so ilS causal agents. species o f Pythillm, have no need
for airbome sporangia, since they persist saprobically in most solts, and spread by zoospores
during weI condi tions. When thesc motile cells find young pl:llllS. they cause infections

-owFig. 2.10 Se)(ual reproduction in Oornycota. A: Saprolegriales; B: Peronosporales..

which release toxins and also produce a pectinase enzyme which dissolves the middle
lamella that glues plant cells together. Seedlings of many plants collapse rapidly when
this disease strikes at the base of their delicate shoots. Damping-off is, unhappily, familiar
to gardeners who try to get a head stan on the growing sea.>on by germinating seeds
indoors. The disease can be controlled by using heat-sterilized soil, by dusting seeds with
Benomyl (a very safe fungicide - see chapter 13), or by watering seedlings with other
fungicides such as Zineb or No-damp. The complete life cycle of Pythium is illuscraled in
Fig. 2.12.









Fig. 2.11 Saprolegniales: life cycle of Sapro!egnia.


A !\llX ED BAG ' 23

Late blight or potato (PhYlOphlitoro - Pythbccac).

In the mid-nineteenth century, a NorthAmerican oomycete caused havoc in Europe.
Unintelllionally imponed to Ireland and reintroduced to a suscepti ble host from which il
had been separated 250 years earlier. Phytophlhora injl!'J lanJ wiped out the Irish potato
crop in the damp. cool s ummers of Ihe yem 1845-1 847, causing widespread famine in
thaI poor, one-crop econo my. At fi rst, the disease was not aUributcd 10 the fu ngus. but 10
an e;(cess of water in the plants, or even 10 the effects of the newly introduced Sleam
locomotives. However, the Reverend M.J. Berkeley, Englancts leading mycologist, drew
sporangiophores emerging from the potato !ea\cs, and correctly concluded that the fungU$ eau.~c d the disease. His contemporaries eventual!y admitted that hc w~!S right. and this
episode led to the fO!.1nding of the discipline now known as Plant P~thology.



spo rangium



oogoniu m


.. /

6 ..'. i



Fig. 2. 12 Peronosporales: lifecyde of Py thium.




The ravages of potato blight contributed to a million deaths, and drovc millions
more toemigrate from Ireland. Ten ye;:m; after the first epidemic, the population of Ireland
had crashed from 8 million to 4 million. Contemporary pictures from the umdon Jllus
Ira/cd Nc"'s convey some of the misery caused by the recurring epidemics. Ragged and
starving peasant girls gleaned desperately in the fields for anything edible, and whole
families Were forced to leave their homcs forever. Some died. Many sailed for North
America, but 187 doubly unfortunate souls were shipwrec ked and drowned off Forillon
National Park near the tip ofth<: Gas~ Peni nsula, Quebec - in sight of the promised land.
There is a fine web site on tbe potato famine at htt p:/hass un.vassar.edul-sUaylor/
FA.MINE with many contemporary illustrations.
Until 1976 this hetcrothallie pathogen (e)[cept in its homeland, Mexico) was ase)[ual,
representing only one of the two mating types. In that dry year. many crop failure s led to
importation of potatoes that carried the other matin g type with them. It has also been
suggested that new genotypes were spread in ~d tubers. in tomato tissues. and even in
tropical storm systems. However it came about, new sexual populations have certainly
supplanted the older lI.>;ClIual and have led to a resurgence of the disease. which
now costs the U.s. alone about 53 billion per year in auempts al control by spraying
fungicide~, by trying to breed resi stant varieties of potato, etc.
The airborne sporangia of the potato blight fUngus are c1e:lrly an efficient shon-range
dispers:almechanism, but humans were JUSt as dearly the long-range ve<:tors of this disease. POtato blight i~ still a threat, though it can be control1ed by: (I) spraying with
fungicide at times carefully chosen by plant pathologists (nowadays with the aid of
spechtl blight-forecasting computer, (2) destroy ing infected foliage before
har.... est. and (3) planting disease-resistant seed potatoes.
[n addition to its most infamous spct:ies, the genus Phylopluhoru contains about 60
other species. Some of them are also. as one might suspect, serious plant pathogens.
PhytopirlllOf(I sojOl! plagues soybean farmcrs in North America. Phyt()phlllOf(I megakal)"ll
attacks cacao trees in West Africa. A hybrid between P. cambivom and P.frugariae has
killed about 10% oflhe aldcr trees (Alnus spp.) in Britain and is now spreading to France.
Holland. Sweden. Gennany and Austria. Ph)"tophlhom cimwmomi is destroying Jarmh
(Eucalyptus) forest and other natural ecosystems in western Australia, cQrk oak forcsts in
Spain, and is a serious problem for grower.>of avocados. pineapples and ericaceous shrubs
elsewhere in the lIorid. No wonder this genus pml'ides work for hundreds of plant p~
Ihologis\s and mycolog ists lliorldwide.
Downy m ilde w d ise~s (Plasmapara. Penmospora - Peronosporaceae)
Thc downy mil dews include blue mould of tobacco and downy mildcw of grape.
Since thcse diseases have historic or economic import3nce. I" lItel1 you something about
them. In this group the mitospol""Jngia are no longer unspeci:l.1ized hyphal tips. but are
borne on highly differentiated. branc hed. 3crial sporangiophores. The sporangi:t don ' t
just release WOSpores but are themselves set free and blown or splashed away. The sporan
gia of PerrmQspom genninate b)' producing a hypha, though those of mOSt o ther members
of the grou p still release motile zoospores.
Downy mi1d~w of Gra pe (Plasmoparu - Peronosporoceae)
P/llsmopara ,;ricola. an oomycete native to America, causes downy mildew of
gr<lpcs. It can be found attacking wild grapes evcry summer. But because it evoh'ed along
with its Nonh American host. a biological balance has been strock, and the wild llilis
species aren't seriously damaged. When this fungus wa~ accidentally introduced to Europe in the 1870s, it was a different story. The French grape vines (Vitis villifera) had no
re~istance tothe Ilt" palhogen. and were quickly devastated. FQttunately for the oenophiles

of the world, the: concoction of Bordeaux Mixture. olleofthe world's first practical fungicides, by a university professor(yes, we profs do occasi onall y have good ideas!) saved the
day. The rather strange story behind this invention is told in chapter 13.
The life cycle of Plo.smoparo is illustrated in Fig. 2.13. Look at this set of diagrams
carduUy, and decide at which stage you think it would be moSt vulnerable to chemical
att3i: k (Here's a clue - the answer begins with 7.. . ).


Blue mould of Tobacco (PerorlOspora - Pcronosporac~ae)

fo,ly last example of a downy mildew fungus is Pcrrmo.f[XJra rabacin(l, which causes
bl ue mou ld of tobacco. TItis disease was first recorded in Ontario in 1938, was epidentic
in 1945- 1947, and had not been seen since 1966. But in 1979, seedlings infC1:ted with the
pathogen were imported to Canada from the U.S., escaping deteCtion at the border. The
weather that year favoured the development and spr~ad of the fungus. and a huge -scale

F!8. 2. 13 Peronosporales: He cycle of Pla smapara vitico/a.

epidemic ensued. About 30% of the OnLlrio crop. wonh $100 million, wa. lost. BI",e
mould helped 10 put the Ontario tobacco industry 011 a slippery slope, and the decline in
tob3o acreage is still contin",ing, though it is now driven by changing societal auitudes
toward smoking. Pemnospom once again became a !iCrious problem (3 coffin nail ?) for
Omario tobacco growers in 1997.
WlUl e rus t disease or crucifers (Albugo - Albtiginaceae)
This disease allack..s cabbage, radish, etc. - all members of the family Brass icaceae
_ and is caused by Albugo candida, which produces extensive white blisters on leaves
and stems. These unique blisters contain innumerable unicellular mitosporangia devel
oping in chains f;om the tips of shon. tightl y packed sporangiophore; (Fig. 2.9 D). When
the host epidermis bursts, the sporangia are wind or rainsplash dispersed to other host
plants. where each CilIl germinate 10 release eight bit1.agellate zoospores. Oogonia de
velop later. inside the host stem Of leaves, and sexual reproduction is usually heterolhal
lie, or OIItbreeding.



Further Reading and Web sites

Barr. D.1.S. ( 1990) Phylum Chylridiomycota. pp. 454466 (in) Ha nd book or P rotoclista
(Eds.) L ~-Iargulis, J.O . Corliss. M . Melkonian and OJ. Chapman. Jones and Bnrtletl.
Buczac ki , S.T. (Ed.) (1983) Zoosporic Pilint P ath oge ns, a Modem Perspective. Aca
demic Press, New York.
Dick. M.W. ( 1990) Phylum Oomycota. pp. 661685 (in) H andbook ofProtOCliSla (Eds.) L.
Marguli s. J.O. Corliss, M . Melkoniiln and 0.1. Chapman. Jooes and B.mlel1, Boston.
Erwin. D.C. & O.K. Ribiero (1 996) P!Jytop/'thom d~ases worid"ide. APS Pres.s. St. Paul.
Fuller. M.S. ( 1990) Phylum Hyphochyt riomycota. pp. 380 387 (i n) Hlln dbook o f
Protoctista (Eds.) L. Margulis,
Corl iu. M. Me(konian and DJ. Chapman. Jones
and B.mlelt. Boston.
Fulle r. M.S. and A. Jaworski (Eds.) (1987) Zoos poric Fun gi in Teaching and Research.
Southeastern Publishing Co.. Athtns.

t o.

Karling. J.s. (1977) Chylridiomycetarum Iconographia. Cmmer, Vaduz.

Large. r:..c. (1962) The Advance or lhc Fungi. Dover, New York.
Longcore. J.E., A.P. Pessier and D.K. NiChols (1999) Balrac/'()c!Jyrrillnl detldrobmidis
gen. ~t sp. nov.. a chytrid pathogenic to nmphibioris. i>,'Iyco logia 91: 219 227.
lI-l arguli s. L.. J.O. Corliss, M. Melkonian and DJ. ChJpman (Eds.) ( 199{ '-I andbook of
PrOIQC lista. JOlles and B.mlett. Boston.
~I oore .

R. T. (2000) l\-Iyrological dispatches [abou l Phytophrlwm].l\l ycologist 14:93

Sl'=.... F.K. ( 1960) Aquatic Pbycomyce tes. 2nd BIn. University of Michigan Press. An n
S~nc:~r. D./l.I. (Ed.) ( 1981) The Downy i\l ildews. Academic Press, New York.
Webster. J. (1980) In[~oduction 10 Fungi. 2nd Edn. Cambridge Uni"ersity Press. Clm
http://dogwood.botany.uga,edulzoos puricfungil i5 a website dedic ated to "Zoosporic
fungi 0 11 line"
http://vassu n.\"assar.e dul-stmylo r/FAl\I INE cove rsthe Irish potato famine in detai l.

Eumycotan Fungi - the mainstream

Phyla (2) ZYGOMYCOTA and

Kingdom Eumyc0I3 is made up of three phyla, Chytridiomycota, Zygomycol3 and

Dik aryomycota. These, and particul~rly the third one. far outnumber the chromi stan fungi

in species diversity. We already know about 100,000 cumycotan fungi. and it is obvious
to those of uS who work with them that these arc just the tip o f the iceberg. We esti mate
that there nre ...."Cll over a million species wa iting to be found and described. Hu ndn:ds of
new fungal taxa an: described c"cry year. For eumplc, in 1990. Rafael Cast:ll'leda and I

described 14 new genera and 40 new species of microscopic moulds from dead leaves of
Cuban rninfurest plants. This wealth of species is a measure of fungal succe ss in eYolu~
tio nary terms, just as the existence of millions of species of insec ts tells us that they. too,
are winners (though their total biomass is f:tr less than that of th e fungi), Before we look at
the eumycotan fungi in detail. it is worth enquiring into the reasons for their success,
E:trlier. I introduced the idea that 1he numbl.-r. ki nd and arrJngemenl of motility
organelles (flagella) found in the chromiSlan (Oornycota. Hyphochytriomycota) and
some eumycolan fungi (Chytridiomycota) are very basic, highly co nserved featurcs. As a
corollary of Ihis, the absence of motile eelJ~ from the life cycle of most eumycotan fun gi
must al so be considered important. Th is seems to reflect a radical shift in evolutionary
dim:tion, It shows very clearly that most true fungi are h.::lsically te rrestrial (landlubbe~). and must have been so for a long time (evcn in geological tenns). l-'Iany more
ecological Riches and substrates arc available on land than in the water. and the challeng~s of sur"\"iv~1 and di spersal are very di fferent.
fun gi are beterot(op-.We which mean s that th ey dee;nd on energy-ricb carbolL.sompounds manufactured by othe r organisms. But this doesn' t ~m to have been a
serious disadvantage. Fu ngi have e\'ol\'ed e nzymes that can digest some extremely JOugh
substr.l\es. Chitin (arthropod exoskeletons). keflltU;J (mammalian and avian skin. hair,
hom and Feathers), cellulose (most plant debris - the largest reservoir of biological
materi al) and Ilgnin (a major constituent of wood) nou rish mJny fungi. thougb we must
.keep in mind that cellulose and lignin remain com pletely unavailable to almost all animals (except with the collaboratio n of microbial sy mbionlS). The unusual ability of somc
saprobic fungi to exploit cell ulose and lignin gives them almost exclusive access to the
massi\'e quant ities of plant debris produced every year, and may well make them .the
world's number onc r~yclers. Only man-made plastics arc. perhaps unfortunately. lm-


mune to tIleir aLiacks, wroch means that we, not tile fungi, must take respon~ity for
recycling these substances.
l . ~~
The fungal colony (Fi g 3.1), with its strong. watefii1Qw. chitinous hyphae, its ri chl y
branched growth pallern. the repertoire of digestive enzymes it can secrete at its everincreasing number of growing tips, and the hydrostatic pressures it can bring to bear, is
ideally suited for actively penetrating. explori ng and exploiting solid substrates in a
manner that the bacteria, chief competitors of the fungi in the recycling business, cannot
match. (flow many hyphal ti ps do you think there are in Fig. 3. 1, an illustration of a very
young colony? 1761 294? 338? 502? - the answer is 388, and this numlxr will double
every hour or two.) If a fungus is growing in liquid culture or in a solid substrate and
produci ng a spherical colony. the rate of increase is many times faster, and the finil
number is astronomical.
The non-motile microscopic spores of eumycotan fungi. which come in a dazzling
array of forms (Fig. 3.2) to fit specific functions, are often produced very quicJil,y. (in a
matter of days or e ~'en hours after the initial colonization of the substrate). and in enormous numbers. They are dispersed by wind, by water, or by animal vectors, and they can
often survive long periods. sometimes even yean, of unfavourable conditions such as
freezing , starvation or desiccation (which means drying Out, and is speUed with one ' 5'
and two 'cs). Like bacteria. fungal spores are everywhere, especially in the soil (in astro-

Fig. 3. 1 Young colony of Phycomyces arisWlg from a mitospore.l'-Iote lhefarge number of hyphal





1 '/


->I "9

\I~ ""

nomic n umbers) and in the air we breathe (sometimes up 1010.000 in a cubic metre). If
you are curious about the ways in which we describe and name these spores, zip off 10
chapter 4 and find out.
Fungi have learned 10 cope with environmental extremes. They can grow at temperatures as low as _5Celsius and as high as 6OCelsius. They include the most xerotolerant
organisms known: some moulds will grow at the amazingly low wate r activity of 0.65
(most plants wilt permanently at a water activity of 0.98). Other IT\Qulds grow in oxygen
eoncentrations as low as 0.2% (air contains 20% oxygen). Cenain fungi can grow under
extremely add cond itions (pH I): others can tolerate alkalinity up to pH 9. These topics
are covered in more detail in chapters 9 (Fungal Physiology) and 20 (Food Spoilage by
Fungi and its Prevention).

- t 'f
As I have already noted. the s3probic funal are recydcq parex.cellenc.e. but they are
; !) also among the world's greatest opportunists, and don't restrict their attentions to natIJ-

1'-Ii i

~ ~

fabric. paper and paint, or almost any other kind of organic matter. Some of their metabol ~( lites (m ycolo:\:i ns) are extremely dangerous - even carcinogenic - if they Contaminate
.'~ ~ ~ ~ (ch apter 2 1 - M ycotoxins in Food and Feed). And parasitic fungi cauS!: the majority

%: '


raUy occurring dead wood and leaves. Wherever there is a Imce of moisture, their omnipresent spores will germinate. and the hyphae arising from them will allac!; food and

~i~ '"

~ t~ c-

00 .


! \. r:

X'YJ \




'"-'" "L



F!&. 3.2 Diversity of spo!"es amongEum~otan fungi.

of serious plant discases (chapter 12 - Fungal Plant Pathology in Agricultu re and forestry), as well as some of animals and people (chapter 23 - Medical Mycology).
Fortun:Ue!y. there is a brighter side to fungal intervention in human affairs: we have
hamessed the biochemical virtuosity of the saprobic fungi in the production of beer. wine,
bread. some gourmet cheeses. my sauce, some antibiotics and immunosuppressants, organic acids, and many other useful chemicals. Fungi are even being used to convert plant
waste into high-protein animal feed. We ourselves eat a number of the large. spore-producing stnJctures developed by fungi: mushrooms, chamerelles, morel~ and tnJff1es are
aJl familiar to devotees of French cuisine. who prize them for their unique flavours. Some
of the parasitiC fonus are now being recruited to attack insects, weeds and other fungi
which threaten our welfare (chapter 14). And fungi in intimate, obligatory association
with the rooLS of almost all higher plants (forming mycorrhizasl. silently, invisibly and
influenti3.l1y perpetuate one of the world's oldest and mOSt successful fonns of mutua lis tic
symbiosis (chapter 17).

Phylum 2 - ZYGOMYCOTA - Conjugating Fungi

Class Zygomycetes - orders Mucorales, Entomophthorales,
Kickxellales, Glomales, and Class Trichomycetes
The second eumycotan phylum is the Zygomycota. This phylum contains twO
dasses. class Z~'gomycetes and class Trichomycetes. Since most Trichom)lcete~ Me
~rasiJes or r;Oromcn5a\s insid~ !he guLS of li\'in&...Wb(Q~s, they are only a fQ:9tnote.
albeit a f3.scinating one. to this chapter.

Zygospor,lIIgia. The name of the class is derived from the way in which its members
reproduce sc l>ually by the physicaJ. blending - fusion or ronjugation - of morphologically
similar gametangia to fonn ijl'gos'ji'6ran-gmiil(the teleomorphic phase). 'Zygos' is Greek
for a yoke orjoining. The gametangia arise from hyphae ora single mycelium in homoth allie SIXcicS. or from diff~rent bm sexually compatible mycelia in heterothalli c species.
Zygosporangin usually d~velop thic k walls, ~nd ~ct as r~sting spores.
The four diagrams in Fig. 3.3 show how a zygosporangium develops. When compatible mycelia of Phycom)'cts blllktsluallus meet, inqjvidual hyphae establish intima~
S0(l!(lC t. deydopjpg fing er- ljke o!!lSWWlhs and seeming to grapple wilh One anotbs;r...o.
This lets them el>change chemical signals ",hich establish that they are iltQeed sexually
compatible. Then Ihe two hyphae grow apart again. only to loop back. swelling as they
approach each other. and finally m~ting head-on. They have become gametangia. w~ich
fu se when their tips tooch. Note that there isn'l any SCl>ual differentiation in size or shape
hen:: since we can't call them male and female, we simply label the mycelia '+' and '-'
After the walls bern'ccn the twO gametangial tips have broken down and their multinucleate contems have mixed, the miJ;.(ure is quickly isolated by two septa, one at each side.
and the p~ircd-off nuclei fuse. The structure is now called a zygosporangium, and it develops
a thick and often ornamented wall. even while still supported on either side by the former
gametangia. which are now calle-d suspensors. Although the two slI.'lpeI1llors are now just
empty append:lgc.", they make it easy to recognize a zygosporangium when you sec one .


.." ';




Anamorphs. You won'toften see zygosporangia in field collections, though I sometimes find a homothallic species of Syzygires producing them profusely as it parasitizcs
ovcr-mature wild mushrooms. But asexual or anamorphic phascs of zygomycetes are
easy to find on mouldy bread or peaches, or on horsc dung. A number of examples are
illumated in Figs. 3.4 and 3.6.
Collect some fresh horse dUng. keep it in a damp chamber, and look at it through a
dissecting microscope, or even a hand lens, every day. You should be able to follow a
sequence of specialized coprophilous fungi - and the first to develop will probably be
the spectacular anamorph of Pi/abO/liS (Fig. 3.6), which is discussed below and in chaptcr
11. The non-motile ase:>:ual mitospores llre usually fonned inside mitosporangia borne at
the tips of specialized sporangiophores. Zygomycetous cel! walls are mainly of chitio and
the nudei in their vegetative hyphae are haploid. Now for a taxonomic survey of the
phylum and its two classcs.

anMto mosis

Fig. 3.3 Development of zygosporangium (teleomorph) in Phycomyces blakesleeanus



Class ZYGOMYCETES: 7 orders, 30 families, 125

genera, almost 900 species.
I will introduce you 10 four of these orders: !he Muoorn1es, E nlomo phlh ora les.
Ki ckxellales and Gl omaJ es. The affi nities of the Glomales are SliII uncertain. since they
almosl never reproduce sexually. but the mUlualistic symbiotic relationships they establish inside the roots of most higher plan ts (perhaps as many as 300,000 plant species!) are
so imponant thai these take up half of chapler 17, I recently re ad the manusc ript of an



, !


BI~ k fS!N Ir lspo r~





Fig. 3.4 Anamorphs in the Zygomycota.. AO: MucOfales; E,F: Kickxelales.




unp ublishcd paper which places thc Glom al es in a new phylum ten tat ively called
Symbiomycetes. We shall sec ...
I) Orde r M ucorales. 13 families, 56 gcnera, 300 s~ie5. This order includes all
the common saprobic zygomycetes. Here belong the ubiquitous bread mould. Rhizopus
sr%nijer (fig. 3.4 A). and theequally common genus Mucor. Each globose mitosporangium
of these fungi contains hundreds of nonmotile. asexual spores, and these sporangia are
produced at the ends of tal! . stout, simple or branched hyphae called spornn 2io phores.
The trademark o f the family ~Iuooraceae is a swollen eJl:tension of the sporangiophore called a colum ell a (Fi g. 3.4 A and D). wh ich protrudes into the sporangium, and
often persists afte r the delicate outer skin or pcridium of the sporangium has disappeared
and the spomngiospores have been dispened Other families often ha ve fewer spores per
sporangium, and their sporangia have no col umell~.

Thamllidiwn <!legans (Thamnidiaceae) (Fig. 3.4 D ) seems to compromise. [ts tall

sporangiophores bave one large, terminal, columellate sporangium. but lower on the stalk
there are branches which fork repe atedl y in a dichotomous manner, the fi nal branchlets
cnding in tiny mitosporangia (sporangioles) which contain only a few spores. The reduc
tiooist tendency is also evident in Helicostylum (Thamnidiaceae) (ill ustrated on the C DROM), wh ic h ha s 1020 spores per s poran giu m , and in B la kesl eo lrispora
(Choanephoraceae) (Fig. 3.4 8), which has only three spores per sporangium. This trend
reaches its logical conclusion in Omninghnmdlo (Cunninghamellaceae) (Fig. 3.4 C),
which has only one spore per mitosporangium. and in which the walls of spore and
sporangium appear to have fused. Now the whole mitosporangium becomes detached and
acts as a dispersal unit.
Although tygomycetes can go through cycle after cycle - spore, mycelium, sporan gium, spor~ - producing only the annm or ph, they sometimes fo rm se.w~1
zygospomngia (the te leomorph). perhaps as a survival ~h~nism. perhaps for the ben
efits of genelic ;ecombination, or pernaps just because compatible strains have met.
The anamorph.teleomorph alternation is diagrammed in Fig. 3.5 for one of the most
common and successful members of the Mucorales, RhiJPpus sroi()l1ijer (Mucoraceae).
Note that when the zygosporangium gcmlinates. it produces a mitosporangium rath er
th an a germ lube,
Zygosporangia vary in mioor way s from one genus to another. and among families
ami orders, but they are generally Mher sim ilar (Figs 3.3. 3.5. 3.6 D and F): if they are
present. they are the easiest way to tell if a fUngus is a tygomycete.
By contrast, the anamorphs of zygomycetes - mitosporangia and the structures on
which thcy :lr~ borne - have evolved some amazing and biZ:IrTe adaptations . This contraSt
between teleomorphic constancy and anamorphic diversity is presumably the result of
diffcring evolutionary pres.ures. longterm survival, one of the main obje<:tives of the
teleomorph, is presumably beSt ensured by suuctu res with minimal surface are a and thi ck.
protective walls. Dispersal, the main purpose of anamorphs, can be achieved in many
wa)'s. let's look at tltree of the more speda1il.ed zygomycetOU$ anamorphs.
PilohoIlIs cryswllilills (Fig. 3.6 AD) is an atyp ical but fascinating ,oprophilous
{dung' inhabiting) member of the order Mucor~les . It grows very rapidly, and is one of the
finl fungi to fruit in the extended succession (h.:1.\ occurs On dung (see chapter II fOf a
det~iled e~pose of this succession). Its unbranched sporangiophore$ are 24 cm tall. and
have a unique explosive dispcnal mechanism.
The whole sporangiophore is a single large cell . Beneath thc b lack apical
mito,porangium is a lensli ke s ubsporangi al ves icle. with a lightsensi tive 'retina' at ils
base th3t controls the growth of the sporangiophore very precisely (Figs. 3_6 BC), aiming


it acc urately tOward any lighl roun.:e. tn a word. it is phototropic. The generation of
osmotically aClive compounds inside this gi1ml cell causes pressure in the sporangiophore and the subsporangial vesicle 10 build up until it is over 100 pounds per square inch
(7 kilograms per square centimetre). This eventually causes the vesicle to ellplode. hurling the black sporangium away to a distance of up 10 2 metres. directly toward the li~t.
The mucilaginous contents of the subsporangial vesicle go with the sporangium, and
glue it to whatever it lands on. Can you explain why P i/ooo/ros needs such a specialized
mechanism for spore dispersal: such a powerful r;annon. su r;arefully aimed11I you can't
fi gure it 01,11. you r;an find the answer in r;hnpter 11.
Note that the originality of Piioho/u$ eXtends only to the behaviour of its anamorph
- th e teleomorph (the zygosporangiurn. shown in Fig. 3.6 D) is fairly conventional.
2) O rd er Entomophthorales. As the name implies. these fungi often attack insects.
EmomophthoTa muscae infects, and eventually kills, houseflies. Dying flies. their bodies

riddl,d by 'h'

r",,,, ,,",Uy =wl '010 "

p."d '''''''OM - I fi,d ,",m

--.".. .".".. 0
O::J 0'
& 00

0 0





,r. /


Fig. 3.5 Mucorales: ife cydeof Rh ;zop us sto/onffer.

{ 'ow.,


and on the growing tips of shrubs in my garden - where the fungal infection bursts
through the insects' exoskeleton and produces tightiy-packed masses of sporangiophores
(Fig. 3.6 E).
Each sporangiophore bears ooe unicellular, sticky mitosponmgium that is shot av,."llY at
marurity. When the fly dies on a window, this barrage produces a whitish halo of mitosporangia
on the glass. These sporangia can infect other unsuspecting flies that come to pay their last
respects. As you may already have guessed, species of Enrorrwphthom arc being investigated
for their potential use in biological control of insect pests (see chapter 14).
Note again that the zygosporangia of Entomophthora, though developing in an
unusual way, by the fusion of hyphal bodies .t he fly, are still recognizable as
zygosporangia (Fig. 3.6 F).
3) Order Kiehellales (Named after a mycologist called Kickx). Members of this
order are atypical of the Zygomycetes in that they often have regularly septate hyphae.
Their teleomorphs arc unremarkable, but they develop seme of the most complex anamorphs
known (Fig. 3.4 E,F). I have found Coemansia (Fig. 3.4 E) on bat dung from acave , Its tall
sporangiophore beaN; many fertile side branches called sporocladiu, Each of these produces a row of lateral cells called pseudophialides (true phial ides are discussed in chapter
4) . Finally, from the apex of each pseudophialide aris es an elongate, one-spored
milosporangium (a sporangio\e).

Fig. 3.6 AD: PilvbQ/U5 (Mucora les). A: habit of sporangiophores (anamorphJ on dung: be~ded
appearance is caused by condensation droplets; B,(: action of subsporangial vesicle and retlflal area III
phototropism; 0: zygosporangium (teleomorph). E,F: Entomophthora (Entomophtoo.:a.les). E: .
section through the Jnamorph sporlbting on a fly; F: zygosporangium (teleomorph) arising by fuslOrl
of hyphal bodies.



That'S complex enough, but it looks simple beside Spirodactylon (Fig. 3.4 F). This,
surely the most el~borate of all zygomycetous anamo'llhs, produces a tall, branched
sporangiophore that is repeatedly tlu:own into tight coils. Within these coils arise the
sporocladia, which bear pseudopitiaiides, and these in tum bear one spored sporangioks.
It is hard to imagine why this strange configurotion might have evoh'ed, until one
learns th:u the fungus grows on mouse and ral dung. Coprophilous fungi have various
highly evolved str.l.tegies for getting back inside the gut of the animals that produce their
prefcfTed substrate. This isn't tOO difficult for genera like Pi/abo/us, that grow on herbi
vore dung, since all they have to do is get their spores onto the animal 's food, which is all
around. Bul rats and mice are not herbivores, and it is essentially impossible for the
fungus tu ensure that its spores will be present on their food. The only alternative (as 1 see
il) is to anach spores to the animal ilseIf, in tIN: hope that they will be ingested during
grooming activities. Rats and mice are creatures of habit. using wel1 -trodden paths each
day. Along tbese trails they deposit dung. and there, later, the coils of Spirodactylon
become entangled in their hair. Only Ihe zygosporangia of tbe KKkxellales convince us
that these strange fungi are ind~d zygomycetes.
4) O rd er G lomales. These soil-inhabiting fungi were placed in the Zygomycota
only tenwtively, since almost none of lhem fonn zygosporangia. Nevenheless, they are
extremely important, because their hyphae enter the li ving rOOt cells of perhaps 90% of
all higher plants and establish with them obligate mutualistic symbioses called arb~ular
myc or rhbas (Ai\I) or end omyco rrh h:as. These are illustrated and discussed in detail in
chapter 17.
AM fungi won't grow in axenic culture: Ihey must be assochllcd wilh a plant root.
Their gene rally very large and thick-walled resting spores are common in most soils, and
are stimulated to genninate by the prollimity of plant roolS (almost any plant will do,
b;:cause these fungi have such wid.:: host-ranges).
Their usually nOn-septate hyphae spread through [he soil and enter living roots,
'where they dewlop st ructures tbat are diagnostic of the order: intrac.::llular, finely
branched_ tree-li ke arbuscules (Fig. 17_3) which are the interface across which the fungus
ellchanges mineral nutrients, especially phosphorus. for photosynthales (sugllr.!. etc.)
provided by the plant. Many of the Glomales produce both arbuscules and lipid-filled
structures called l'~sicles or intra ma tri cal spores inside plant rootS.
The soil-inhabiting myc.::lium is very efficient at mobilising insoluble phosphorus
and lrans localing (moving) it to the plant. Since phosphorus is often the limiting nutrient
for plant growth, A.t\1 fungi help planls to thrive in poor soils. These fungi are therefore
vital in many natural habitats. and of great potential value in agriculture_ Again, for
details consult chapter 17.

Class TRICHOM YCETES: 4 orders, 7 families, 48 genera,

almost 200 species.
This eccentric group of fungi Jive almost exclusively auached to the lining of the
guts of living anhropod~. which is why you won' t run into them very often. But they are
uamples of Ihe opponunism displayed by fungi. and the determination shown by my cologists in winkling OUI fungi wherever they are 10 be found. Bob Lichtwardt's 1986
book gives a fine account of thi s offbeat group.
A plate (Fig. 3.7) of phase-contrast photomicrographs by Rich:mi Benjamin (from
''The Whole fungus" - see reference below) shows the characteristic structures of some
Trichomyceles. Top left (A) arc developing trichospores of Smiufum. Top right (B) are
trichospores of Slachylina showi ng the hair-like appendages that give them their name.


Bottom left (C) is a trichospore of Smilfium.
Bottom centre (D) is a devel oping zygospore of Trichorygospora . and bottom
right (E) a released. mature zygospore with
a roaar and a bunch of hair-like appeud ages below il. Only this l:lSt structu re (look
at the conical ~suspensors:' top and bottom) places the Trichomycetes in phylum
Zygomycota, since otherwise the group
does not closely resemble the Zygo

fig 3.7 Representative5 of Class

TrichomYCC1CS - see text for explanations.

Further Reading about Phylum Zygomycota

Benjamin. R. K. (1959) The merosporangifero us Mucorales. Aliso 4:321-453.
Benjamin. R.K.'( 1919) Zygomycetes and their spores. pp. 573621 (in) The Whole Fungus. Vol. 2. (Ed.) B. Kendrick. Naliou:..] Museums ofC:..nad:... Onaw:...
BClltivenga. S. P. ( 1998) Ecology and c"olulion of arbuscular mycorrhizal fun gi.
I\Icnvainea 13: 30-39.
Cerda-Olmedo. E. and E.D. lepson (Eds.) (1981) PhycolII)"ces. Cold Spring Harbor. N. Y.
Ful kr. t>,I.S. (Ed.) (1978) Lower Fungi in the Laboratory. IXpl. of Botany. Uni\". of
Ingold. C.T. ( 1978) The Biology or Mucor and its Allies. Edward Arnold. London.
Kendrick. 8. and S.M. Berch (1985) Mycorrhizac; applications in agriculture and forestry. pp. 109- 152 (in) Compreh ensive Biotechnology. Vol. 3. (Ed.) C. Robinson.
PerganBOn .()~foni.

Lichtwardl_ R.W. (1986) The Trichomyeetes. SpringerVeriag. New York.

Monon. J. B. and G.L. Benny (1990) Re"ised classification of arbuscul~r
fllllgi (ZYl;:Omycetes); a new order. Glomales, two new suborders. Glominene and
Gigas porineae. and two new families. Aellulosporaecae and Gigasporaeeae. with an
emendation of Glomaceae. :\Iycota.'(on 37: 411 -491 .
(). Donnell. K.L. (1919) Zygomycetes In Cultu~. Depmment of Botany. Univcrsity of
Georgia. Athens.
Brum!rett, M .. L. Melville and l. Peterson (Eds.) {I99n Practical Methods In l\Iyeor
rhixa Resea rt h. Mycol ogue Publ.. 8727 Lochsidc Dr. Sidney. BC. V8l 1MB.

Canada. [CD-ROI\.IJ
Zycha. H.. R. Siepm:mn and G. Linnemann (1969) i\iueoralt'5. Eine Bescltreih ung aller
Gatlungc n undArten dieser PiI7.gru ppe. Cmmer. Lehre.



Subphylum 1 - ASCOMYCOTINA: , ~,..Q~,~
the Ascomycetes
q.Ji" . S"



Zygomycetes, the subjects of chapter 3. are terrestrial fungi: there's 00 doubt about
that. But they thrive and sporulate only in damp places where the atmosphere is more or
less satural~d with moisture:. For eumple, Rhi~opu!i slO/onifu will colonize the moist
interior of a loaf of bread, but won't produce its characteristic sporangiophores and
mitosporangi a on the outside of the bread unless the surrounding atmosphere is humid. If
we pel'$uade the fungus 10 sporulate by keeping the loaf in a damp chamber (a plastic bag
cont3ining a few drops of wale r will do) and then take it out of the bag. the sporangiaphares will quickly collapse.
Hyphae of mOSl zygomycetes are wide, thin-walled, and coenocytie - continuous
tubes with no cross-walls. Hyphne of phylum Dikaryomycota (Ascomycetes plus Basidi
omycetes) are nnrrower. Hyphae average nbout S microns in width. but in aggregate they
aTe ,"cry long (sometimes kil ometres per gram of soil).lhtY_lU"e also.sep ta.te -they' have
crosswalls called septa at regular intervals. These min inture bulkheads give the hyphae
Some physical rigidi ty. andlimit loss of cytoplasm if the hyphal wall is ruptured. As a
result. we find that ctikaryomycota can grow in a wide range of conditions: for example,
they can often spread and fruit in drier situations than zygomycetes could tolerate. Some
dikaryomycolan anamorphs (especially coelomytttes) grow in dead leaVe!; and stems of
desert plants. and some moulds are th e most drought tolerant of all organisms. able to
grow at water acti vities below 0.70 (for example, on jams, salt fish and Other substrates of
extremely bigh osmotic pressure - see chapter 20).
While many zygomycetes can assimilate only 'accessible' substrates like sugars
and SlaKh, ascomycetes can oflen exploit cellulose. and many basidiomycetes can digest
both cellulose and lignin, carbon sources th at are available to rem arkably fe w other
organisms. Though fungi cannot fix atmospheric nitrogen (this talen! seems 10 be restricted to the prokaryotes), dikaryomycotan fungi can use many different forms of combined nitrogen: some ascomycetes eve n specialize in metabolizing the protein keratin.

which is the main component of hair and skin. In case you were wondering if membe~ of
this groop constitute a health hazard - they do.
Some other orde~ of ascomycetes are obligate parasites of plants. Remember the
'dow ny mildews' caused by oomycetes? There are also plant di seases called
mildews' that we caused by ascomycetes. The similariry o f tellllinqlogy is unfortunate,
but try to remember the difference, because although the groups of fungi involved are
both obligately biotrophic, the diseases are different in many important ways. such as
host ranges and methods of control. This is just one example of how Wonomy has
practical implications (see chapter 12).
Thousands of basidiomycetes, and a quite a fe w ascomycetes, establish intimate
mutualistic symbioses (mycorrhizas) with the roots of treeS, especially conifers (see chap. ter 17). Nearly 18,000 ascomycetes, and a few basidiomycetes, have dome sticated algae.
thus becoming lichens, which can live in some of the world' s harshest climates and
colonize the barest and mOSI inhospitable substrates (see chapter 7). Some dikatyomycotan
fungi have even re-entcred the water and, lacking motile cells, have evolved Olher mechanisms, such as long appendages, to aid spore dispersal. Dikaryolllycotan fungi range from
unspecialized, almost omnivorous saprobcs, 10 fungi so specialized and ecologically
demanding that they are found only on one particular Icg of one spec ies of insccL Some
dikaryomycotan fruit bodies are microscopic (as in many ascomycetes), but often (especially among the basidiomycetes) they are large and complex, and most of the common
names appl ied to fungi rerer to the visible Ic:leomorphs o f basidiomycetes. and in a few
cases, ascomycetes. You may already be acquai nted with some of these; I will introduce
you to many more in the pages ahead.
_ ',A(,.e I"'\~_

:w... .

51 EO ['\..

;9'~t.,.O . -


Fig. 4.1 Diagnostic chart of pl-tfIa, and the subphyla and classes of Dbryomycota.



Characteristics of Teleomorphs..

Most dikaryomycotan fungi share a number of imponant features - (I) chitinous

cell walls; (1) hyphae with regular cross-walls called sepia (centrally perforated to allow
mo,'ement of cylOplasm, and som~ti mes nu clei, between compartments) (note that many
yeasts are unicellular, so don't produce hyph~); (3) the ability of sommic, assimilntivc
hy ph:te to fu se with one another (an35 tomosis) and to exchange nuclei; and (4) the
o<xurrence in their life cycles (or at leasl in Ihase which produce a teleamorph) of a
unique nuclear phenomenon called the dikaryon , After sexually computible nudci from
different mycelia ha"e been brought together by anastomosis, they pair off, but don', fuse
immediately to fonn a diploid zygote, Instead, they go on div iding synchronously to
populate what are called dikaryotic hyphae, in which each compartment has two sexually
compatible haploid nuclei. Oh yes, thcy do fuse eventually, but not before some remarkable develop mentS have taken place, and in basidiOln}'cetes, perhap~ not for years, Read

If ascomycetes and basidiomycetes share all these trungs, how do they differ? Actually, in muny ways, and with experience it's usually casy to Icllibeirsexual fructifications
ap3rt with thr n:lked eye, But their microscopic, uni cellular mriosporangia are most
diagnostic of all (compare the subphylum diagram~ in Fig, 4.1 and Fig, 5.2 on p. 80).
The meiosporangia of a$Com),cctes are asci (singul:u, ascus), They are cylindrical
or s~c -l ike and ~t maturity u~uall: contain eight haploid spores (ascospo~) which are
e.' pelled into 'he air through the top of the :lSCU.".
The meiosporangia of basidiomycetes are basidia (singular, basidium): they usually have four liny projections call~ ste rigma ta , each bearing a haploid spore (basid
lospore) which i~ shot ~way indi\'idu~ lIy at maturity.
The formation of asci or basidia marks th ~ cnd of the dikaryophase: the paired
nuclti h:lve fused and the resulting zygotc has undergone meiosis (a nd a mitosis in
ns,'omycetrs) to produce eight haplnid a~cospores or four haploid basidiospores, Compare the two sets of diagram s in Figure 5.2, and n()lC how similar the developmental
proces..~es are until the final Mages,

Teleomorph life cycle

.'\ow let's e,t;.amine the se,t;.ual (1~l com orp hic) pm of the ascomycete life cycle from
the beginning, When an asco~pore genninates, it establishes a haploid mycelium. In
heterOlh:ll1ic ascomycet~s, thi.~ can"t undergo sexual reproduction until it mtcts another
compatible haploid mycelium. When thi s rare event tuk es pla~'e, the fungus cleverly
m:uimiles the ensuing polential for genetic rCCQmbination. One would expect a single
sexual fusi on , resulting in a single lyg Ote. But mOSt ascomycetes interP'Olalc a
dikllfyo phasc, during which the number of pain of compatible nuclei is multiplied. often
enormou~ly" as dikary()\ic hyphae Coften called ascogenous hyphae, as in Fig. 4,2) grow
and bran,h within a mass of monok:ll)'utic (haploid) Ii."sue which is the fnlmework of the
fruit body (the ascoma). Eventually, the ultim ate branches of the dikaryut ic hypffilc" of
which there may be millions in larger ascornata, rench their ord~ined positions in Ihe
future hymenium and the long--dd:lyed sexual fusions take place, lltc grnome is reshumed during the ensuing meiosi5 m each ascus (this gcnetic recombination is due to
crossing-o,"cr, which is cxplained in chapter to), Each meiosis will produce a som e wh ~t
differ~nt =angement of the gcnom~, In thi s way the product$ of a single hyphal encoun ter an:: first mulliplied; Ihen, on top of tha!. the reshuffling of genes inherent in meiosis
generltes a lot of genctic divers;I}, Not only IS the dikaryon itself an unusual phenom-



enon. but during the d ikaryophase an effectively diploid mycelium is growing within ..
and drawing nouri shment from. the haploid ascoma tissue. This phenomenon has intcre~t.
ing paI:llleJs in the red algae, though molecular evidence doesn' t support II d ose relation
ship between the two groups (both lack motile gametes and app!':ar to have simply hit
upon the same solution to the probkm jX>SCd by the rarity of sexual enCQUnters).
Aseospores are not motile, in the sense of sclf-prop!':lling, but most ascomycetes
nevertheless send their as~ospores off with a burs! of kinetic energy. The ascus is a tiny
spore-gun, which worb by build ing up internal pre ss ure, th en rel easing it through the tip.
Thejob of most asci is to get !Mir ascospores into the turbu lent airflow aoove the ascoma.
Matu re asci of the dung-inhabitingAscobollls (Fig. 4 .2) project above the hymenium and
point toward the light before discharging their spores. In this way they ensure that the
spores will not run into any obstacles on their upward flight (see chapter 8).


QO'''''O"U' ;

FI. 4.2 Teleomorphic cycle of anapothcd.llascomycete, AscoboluJ (Pt-zizalesJ (see text for h.


Four Kinds of Ascoma


, 0,(;(;11

. .


The multicell ular scructures (ascomata) that produce the

and act as the platforms from which the spores are launched, come in four main de-;j~ sectional views of
which are shown in Fig. 4.3.
(I ) Apothecial Ascomata allow many asci to discharge simultaneously because the
entire fertile 1a)' or h)'menium is exposed..
(2) Perlthecial Ascomata have a narrow opening which permits discharge of only
one ascus, or a few asci. al a time. as do
(3) PseudolbeciaJ Ascomata (different development, different asci).



--- -


,'I f _


, If _ _

Fig. 4.3 Teleomorphs: asci, ascophore and sectional views of ascomata.

(4) Clclstothedal As.::omata lade an opening entirely. This usually indicates that
the asci are spherical, u in!hesc iIIustratioos. and no longer shOO! their spores: the fungus
has evolved another dispersal sttategy. That may have happened because the fungus fruilS
in a confined space (for ex.ample, under bark, or below the surface of the ground) where
airbome dispersal cannot operate. We often find that the s~ of such fungi aredisperscd
by animals.

Four'Kinds of Ascus
Before we go on to explore the many orders of ascomycetes, we mUSt lake II. closer
look at the ascus ilSelf. All asci are nOI the same. There are four flavours (Fig. 4.3) :
(1) UnltunicateOpe rcuJate Asci which have II. single wall with a builtin lid or
operculum at the tip - at maturity this pops open so that the spores can be ejected.
Unitunicate-operculate asci are found only in apothecial ascomata.
(2) Unitunicate-Inopen.: ula te Asci which have 110 operculum. but have a special
elastic ring mechanism built inlO their tip. This is a pre-set pressure release valve. or sphincter. and the ring eventually stretches momentarily, or turns inside out, to let the spores shoot
through. Such inopereu late asci are found in perithecial and some apothedal ascom.ata.
(3) Proto tunicateAsci which have no active spore-shooting mechanism. These asci
are usually more or less spherical, and are found in cleiSlOthecial (occasionally peritheeia]). and by pogeous (underground) ascomata. Sometimes the waU of this kind of ascus
dissolves at marurity and releases the ascospores, which can then ooze, rather than be
shot, out of the ascoma; or they may wait inside until it decays or is ruptured. These asci
are often called prototunicate. Yet perhaps because they are found in sever.ll otherwise
rather diffe rent ordert. il seems likely th.1t they represent a Sf("oruiary condition. and have
evolved seveml times from unitunicate a<;ci (as they clearly did in the trumes - Tuberaccae
in thi s chapter).
(4) BilunicateAsci which have adouble wall. A thin. inextensible outer wall covert
a thick, elastic inner willI. At maturity the thin outer wall splits. and the thick inner wall
absorbs water and expands upward. carrying the ascospores with it This ' Jac k-in-a-box'
design allows the ascus 10 stretch up into the neck of the ascoma 10 expel ilS spores. The
bitunicate ascus is so different from the unituni cate ascus that we assume they diverged a
long time ago.
In many unitunicate ascomycetes. the peritheeial ascoma develops only after the
,cxual stimulus, so that the asci can grow into an actively enlarging cavity. In man y
bitunicate ascomycetes, ferti lization doesn't happen until after a solid primordium or
stroma has developed. so room has to be made for the asci by dissolving away exisling
tissue. In some cases the asci themselves do the job, but in others it is carried out by
special sterile hyphae (pseudoparnphysc.s) iIowing down from the upper layer of the
stroma; the asc i then grow up between them. Remember th at pseudol:hecial ascomata
always produce bitunicnte asci.

Many Kinds of Anamorph
Here is a mantra to begin with - say it until you know it:
Telw morph
(the whole fungus) = (asexual reproduction) + (sexu al reproduction)
In any modem consideration of the Ascomycetes. we cannot ignore their asexual
reproductive phases, many of which are called moulds:You already know that zygomycetes
have diverse asexual phases. So you won't be surprised to discover that many asca-


mycetcs have co mparable asexual (anamorphic) phases during which they rcproduce
rapidly, and often relatively cheaply, by means of mitospores called conidia.
The asexual ly reproducing phase of Ihe ascomycete life cycle wa.~ more Of" less ignored for many yean in favour of teleomorph srudies. But when we consider tiutt the anamoIph
is an important (andsome~ Ihe only) phenotypic expression of many ascomycete genotypes, we realize that it has much to tell us. Besides, one can get DNA and RNA from
anamorphs just as ea~ily a.~ from teleomo rphs, so we are beginning to understand the relationships of an.:unorphs bener. even in many ca.<.es wbere flO teleomorph is known.
Though they play essent ially the same role in the life cycle, the anamorphs of
ascomycetes differ from those of zygomycetes in two very important respects:
(A) While zygomycete mitospores commonly originate by rrce-cell ronna tion inside a sporangi um. many spores cleaving from a single mass of cytoplasm, the mitospores
(conidia ) of aswmycetes are basically modified bits of hyphae, either budded out as a
new structure, or converted from a whole existing cdl.
(B) In zygomycetes, anamorph a[ld leleomorph often occur together (especially in
homOtllaltic species) and always share the same binomial. In ascomycetes. anamorph and
teleomorph often develop at different times, and on different SUbstrates. Each phase has
often been collected in Iota! ignorance of the e:ljsten ce of the other, and because of this.
the International Code of Botanical Nomenclature maintains that it is legal 10 give them
separate binomials - a useful option. but (me gi ving rise to a great deal of confusion in
some studenl.'i' minds (How can one organism have two names?)
Several thousand ~namorph-telcomorph connections have now been established in
the ascomycetes. YOli can now find them at this web site:
h t t p:JI"'.....'" .biology. ua l berta.calj bn:usl 01 ana Ideo/alia td. h t m1
These represent on ly a smail proportion of the tO(;l1 number of Ia.~a, either of anamorphs
or reicomorphs (we know ubout 30,OOOof each). Be>:ause annmorphs so often occur alone.
il is still nOilllalllnd ~cccpted practice to use separate binomials for them, as you will see.
N~vertheles s. ! find it complctely unacceptable to talk about con id ial funl:!i. as many
ot her le~t~ do, as if Ihey constituted a sepa!1lte major hi gh -level tax on called th e
Deutcromycotina.' Th is ignores bOlh the evidence that thcy are all <:xpn:ssions of
dikaryomycotan genomes. and th e th ousands of contlec!ions that have already been
established with telcomorphs (and the number grows every )'eat).
Of abo ut 30,000 known llscomycetcs. 5,000 hal'e so far been connected to tM-ir
anamorphs. \\~hat about the many thou sa nds of conidial (anamorphic) fungi that arc still
'orphans'? I lhin k there is good reason In belie\'e that many of them have given up sex
altogethe r. and become 'anomorphie-holomorphs: though they seem to have retained
some genetic flexibility by: (a) having more than one kind of nucleus in the ir mycelia
(heterokaryosis) as iI re su lt of occasional hyphal fusions (anasto moses): (b) S()rn<:timc.~
undergoing a comple:\: pa rasexual process involving rare somatic dip!oidization. mit otic
crossing-over. and finally a return to the haploid condi tion (this process is more fully
explai ned in chap ter 10).
It turns out that the conidial fungi are a mixed bag. Although most of them arc (or
were) part of life cycles. others arc (Of were) connectcd with basidiomy~tes .
Despite this mixed ancestry. we have h~d to sct up a single classification for all of them.
because it is often impossible to tell, just by looking at them. in whic h subph>'l um the
co nnecti on lies. Unfonunately. our ~cheme for cla.o;sifying the anamorphs has so fur been
able to make lillIe refercnce to teleomo rph s, for severa! reasons: (I) tdeomorph s are
known for only 10- 15% of anamorphic species; (2) members of ....hat seems to be a single
anamorph genus lOa)' hnve teleomorphs in lIlany different holomorph genera (even from
different orders). This must be due to convergent emlution among ana morphs: (3)

anamorphs belonging to several different anamorph genera can have sexual phases in a
single holomorph genus. This must be due to radi3tive evolution among anamorphs. So
our attempts to classify anamorphs have concentrated on: (A) their mitospores (collidia) ..
(B) the diverse stroctures (conid iogenous cells. conidiophores and conidiomnta) which
bear them, (C) the ways in which the mitospores develop (conldiogencsis). and, more
rceeotly (D) molecular te<:hniques, which are now helping us to elucidate their relation

Morpho logy of Anamorphs

There are about 2.000describcd genera of conidial fungi, and almost 30,000 described
species, and these numbers are increasing rapidly. The fint really useful classification of
dikaryomycotan anamocphs. established in the late nineteenth century, was based on mature
morphology. The princi pal characteristics uscd were: (1) colour. septlltion and shape of conidia:
(2) conidiophore 3ggn:gatiOIl, Of lack of it: (3) the production of conidia in enclosed SlrUCrures
or the absence of such enclosure. These chamcters are illustrated in Fig. 4.4.

The division of anllmorphs inlo two large groups is informal, is based on charncter
(3 ) above, and is really JUSt for convenience. The easiest decision to make is usually
whether a conidial fungus is a hyphomycete or a coelomycete. You can recognize a
hyphomyccte because its conidiophores can be single or aggregated in various ways, but
are n~ver enclosed within a covered conidioma. Coelomycetes form their conidia in
initially enc losed conidiomala, which usually devclop just beneath Ih~ surface of their
plant substrate. I am not going to discuss coelomycetes in detail (though there are thO\.l sands of them, and they cause many important diseases of crop planl~) . but I must mention
a few basic facts.

Coelomycetes : ;: covered or ostiol ate conidiomata

A covered con idioma is called an aee n 'ular conid ioma or acervulus (Fig. 4.4).
This may develop at various depths within the host: it can be subeuti,'uI3 r (covered only
by the host cuticle): intraepidcrmal (arising within the cells of thc epidermis. as in the
diagram): SUbepidermal, as in the phmomierograph below: or developing beneath severa!
layers of host c<:l1s. Under th is roof of host mat~rial. funl;al hyph~e aggregute and fonn a
fl~t fcrtile layer o f short conidiophores that produce many conidia (shown in a vertical
section). The pre%urc of accumulating conidia, and often of accessory mucilage. eventually splils the hosl epidennis and allows the conidia to escape.
At the other e nd of the spectrum is the flJsk-shaped. ostio13te py eni dial eonidloma
or pycnidiuffi, ~cn in vertical section, in which the fungus itself pwvides the enclosing
wall. and conidla eventually ooze out through n nnrrow ~pical 051101c.
Hyphomycctes = exposed conidiophores or conidiomata. Among the hyphomycete:s,
conidiophores arc usually soli tary. though they sOllleti mes form columnar aggregations
called sy nn c m a lal conidiomata. or cushion-shaped mas ses called s po rodoe hial
conidiomata (all shown in Fig. 4.4).

Conidium morphology
Presence or absence of pigment is important. as ru-e shape and septatiOfl. "There are seven
shape and septation C<ltegQries. (Fig. 4.4) (A) commonest of all are singl~~elled amcrospores.
(B) the addition of one crosswnllmakes tlltm didymosporcs. (C) conidia curved through
more than a half-cirele. or coiled in two or three dimensions. are called hdicospores.
(0) those with several conspicuous. radi~!ing ,um.<; orother projections are c311ed sUlurospores.
(E) septa running two ways. like the me:shcs of a 1b.'I, or like the mortnJ layers of a brick wall ..
identify diclyospores. (F) twO or more transverse septa. arranged like the rungs of a ladder.

characterize phragmospores. (G) Finally, those which arc Ioog and thin (more 1han15 times
as long as !hey are wide), are called scoleeo:spo res (which means worm-like').

Con idiogenesis (mitospore development)

More recently. it was d iscovered mal conidial fungi use a number of different techniques to produce thcir spores. Sioce these often represent genuine 'embryological' differences, they have become important characters in OUT da~sification . Spores which look
alike often develop in different ways.
We begin by checking an anamorph to see which of two basic patterns of development _ blastic or mallic - it exhibits (Fig 4,5 A,B):
In blastic conidiogcnesis (Fig. 4. 5 A), the young conidium is recO"Jlizable before it
is cui off by a cross-wall (this is an extension of the idea of cells 'budding ').






Fig. 4.4 Anamorphs: corda, conidophores and cooiciomala.




In thallie conidiogcnesis (Fig. 4.5 B), the cross-wall is laid down before differentia_
tion of the conidium begins.
Ripe conidia may also be liberated in two different ways, described as schizolylic
and rhexolytie dehiscence. In schizolytic dehiscence (Fig. 4.5 C), the halves of a double
septum at the base of the conidium split apart by the breakdown of a kind of middle
lamella. In rhexolytie dehisce nce (Fig. 4.5 0), the outer wall of a cell beneath or between
conidia breaks down or ruptures. We will examine ten different kinds of conidium development: se ven blastic (Fig. 4.6), and three thallic (Fig. 4.8).

Type I: blastic-acropetal conidiogenesis

The Monilia anamorph of Moni/inia fructicola (Unitunicatae- lnop erculatae:
Leotiales), Ihe brown rot fungus of peach and other slOne fruits (see chapter 12), and the
Cladosporium anamorph of Mycosphaerella rassiana (Bitunicatae: Dothidealcs), a common mould on decaying organic matter (and in the air), both produce conidia in chains by
apical budding. The youngest conidium is at the tip of the chain. The chain branches
when two buds, rather than one, develop on the conidium at the tip of the chain (this
conidium may then be called a ramoconidium). This is clearly just a modified fonn of
hypha] growth. (Fig. 4.6)


c : schizolytic .tces.<iGn

Fig. 4.5 Basicmodes of conklium development and release.


Type II: blastic.synchronous conldiosenesis

The hyphomycetes BOlry/is and Gona/obalr)"um produce many conidia synchro
nously on a swollen cell: Gon(lfoholrY"1/l goes on to form acropetal chains of secondary
conidi:!. while 80/Tylis does DOt. (Fig. 4 .6)
Type Ill: blastlc.sympodial conidiogenesis
In species of Bemn'l!Tia. insect pmhogens now being used in biological control of
potatO ~t1e, the n:lrTOW tlpe~ of the oonidiogenous cell e~ten ds sympodially; each new
apex becomes con"ert~d into a blastic conidium, then the ne~t ape~ grows OUi from
behind ami to one side of it. The more conidi a are produced, the longe r the conidiogenous
cell becomes. Allhou~h LLplOgTaphium anamorphs of Ophio.\fQftW (Prototunicatae:
OphiOSloma ta!cs) have ~ingle co ni diophores. these have comp le~ heads with several tiers
of supporting cells (metulae), the ultimate (){\eS bearing many syrnpodially extending

Gon.W,olf yum

' "~~';\ I"Pi'~

'[i (l:






Frg. 4.& RepreseotJtive <ir1.1mo<phs with b/c1StK: coricflOgenesis.




conidiogenous cells, and innumerable conidia accumulate in a slimy head. These spores
are insect-dispersed. Bo.sifimbria lteleolTJOrph unknown). which is common on horse dung,
has simpl e conidiophores that elongate sympodia1\y during conidiation. (Fig 4.6)
Type IV: blaslic-annellidic or blaSlic-percurrenl conidioge nesls
In the SpiWcata anamorph of Venn/ria il1(leqllalis, the apple scab fungus . e~e h
~ceding coni diu m leaves a ring-Like scar, an anncllation. around the c:onidiogenous cell.
",hicb then grows on through the scar ('pereurrentl}") to produce the next conidium.
Conidiogenous cells that have produced seven spores bear seven annular scars - hence
the name anndlidic. Scoplilariopsis(Fig_ 4.6. 4.7 A) has s.cvcraJ annellidic conidiogellOus
cells on each branched conidiopho~ . upl(lgraphium conidiophores may h~ve many
such cells at their a~.\ (Fig. 4.6).
II h3s =ntly been confirmed that some individual annmorpbscan be both annellidic
and sympodiaL J'll give you tWo examples of how this knowledge may cbange our classification. When it was thought, not many years ngo. thatcon id ioge ne sis in tbe synnemam l
anamorphs of Ophiosta11W species was either exclusi\<ely sympodial o r e xclusively
percurrent. they were segregated into two anamorph genera (PesQlUm and Grophill1>!).
Now it has be<::n shown tbat both kinds of conidiogenesis can occ:ur on the same conidiopho re, they are being united a,gain in the older genus, Grapltiutrl. In exactLy the same way,
some complex mononematour; anamorphs of Op/lw.flOml! species were segrcgnted into
the 'exclusively sympodial' \ lmicic/tuiid/a (which I monographcd) and the 'exclusively
~rcurre nt' uprogmphium, but are now united under the olde r name, LeplOgraphilllll.
Type V: blastic-phialidic co nidi ogenesis
Many common moulds produce conidia in rapid succession from the open en d of
spedul conidiogenOIlS cells called phiulides. Common genera such as PellicilliwlI, As
persill1ll3nd eha/am arc 311 phialidic (Fi g. 4.6). Many plant pathogenic hyphomycetes.
such as F u),/Irill'" ami VerlicilliUm, both causing serious wilt diseases of crop plants. also
produce phialides _ Pmicil/;wlI and Aspersilllls are dry- spored. Fusarium. Verticil/ium
and Stadl)'bolrys ha 'c slimy spores. Phialidic ontogeny is basically rluher similar to type
IV - percurrenl.
Most phialides don't change in length while producing many successive conidia,
though mony wall layers build up inside the open end of the cell (Fig. 4.7 B), This
accumolation of wall layers may ",,-elllually plug th<:: opening. ;Ind in phi31ides to whicb
this happens there is a tendency to produce sy mpodial extensions tbat develop new fertile
apertures . Such phialides are calkd polyphlalides sine.: th ey have mo re [b~n one
co nidiogenous locus.
Type VI: blastic-retrogressive c onidiogenesis
In Basipt lOspora (<I the rmotolerant fUl1gu~ use d in Indonesia in the preparation of a
led food colou ri ng ), a conidium forms at the tip of the rel atively undifferentiated
conid iogenous hypha and is delimited by a cross-wall; then a short zone of the hypha just
\)clow tne conidium balloons out to produc.: the second conid ium. Aft~ r this bas bee n
delimit~d by a septum, the next segm~lIt of the hypha and blows oul, a nd 50
on. As the ch"in of con idia elong ates. the conidiogcnous hypha becomes ,honer. Si milar
development occurs in Tricholh<,cium and C/(li/ooou),lIm, but this is an unusliol kind of
con idi ogenesis. (Fig. 4.7 C)
Type VII: basiluxic conidioge nesis
In the Oidium anamorph of Erpipht gmmittis . \\ hit ish chaills of conidio (the ' po wdery mildew') COyer the host le3ws. Each chain consists of a graded series of gradually


maturing conidia, the oldest at the tip, the youngest barely differentiated from the hyphal
cell just below it. New material is added at the base of the chain in a fonn of intercalary
growth, arising from a sometimes swollen mother cell which appears to be a highly modifiedphialide. (Fig 4.19)

Type VIII: thallic-arthric conidiogenesis

In the Georrichum anamorphs of Dipodll$cUS spp. ($ accbaromycetes), an assimila tive bypha stops growing. then becomes divided up into short lengths by irregularly
arising septa_These are double septa which split apart sehizolyticaUy to give a 'chain' of
short cylindrical 'fission arthroconidia' th at disarticulates and appears jointed (hence
'arthric ')_ In Oidiodendron (Fig. 4 .8 A ), a common soil mould, the branches of an often



_IH i_

8: blastic-pI"oial idic



C : llIa>tic-r.'IDg,essjve

Fig. 4.7 Analysis of threelnodes of blasticcooidiogenesis.


tree-li ke eonidiophore disaI1ieulate into ronidia, ul timately leaving only the denuded
' trunk: (the stipe). Many basidiomycetes also produee thallic-arthric eonidia.

Type IX: alternate thallic-arthrlc conidia

In CQremilllia (Fig. 4.8 B) some hyphal cells degenerate to rele ase the intervening
cells as 'alte rnate anhroconidia:

A: OIdIodmdron - !halicanhrio;

'LI ~:..!
! ' ~'.J!"
t.... t .' .
. .!
"I'. , .
:.... ~ ~ ,14


...~, . " ! l ~ .~
'., , .,1 ~:';

- r- '




', 1' J.# ,

) / .r. , . '. . . . .

'. .


.. I !'...

.. , :. 1,;
.. .


. i

,! ;;.... .


8: CoremJella - lII.. nate~hric:


Frg.4.8 Deveklpmental analyses of thallicconidiogenesis.



Type X: t hallic-solitary conidiogenesis

The Micrrnp<>n,m anamorphs of NanniuJa (prototunicatae: Onygenales) (fig. 4.8
C). which can digest keratin an d cau,e skin diseases in humans (see chapter 23). deve lop
single. large. thalli e ph ragmospores at the ends o f hyphae. These conidia are liberated
rheJ\.Olytically. as the final diagram shows.
One of the earliest klnds of 'deve\opn1Cmal' infonnati on was the observation that
some moulds produced conidia in chains. while othefli did not. But looklng back o,'er the
various kinds of conidiogenesis I have justdescribcd. we find no fewer than seven w:l>'s in
which look-alike ;chains' of conidia can develop. These are seven good reasons wh ): we
no longer rely on mature morphology alone to establish our classification of conidial

Import ance of Conidial Anamorphs

Why is it imponam to be able to identify conidial fu ngi'! Some of them lilcml1y
grow on you. The most p['(:valent fungal diseases of humans (mycoses) are causcd by
conidial fungi. Various superficial mycoses, rungi ng from ringworm of the scalp, through
jock itch (more vulgarly known as crotch-rot) to athlete 's fOOl, are tauscd by ker:llinatlacklng spedes of M icrosponlm. EpidumophylQII. and TrichophYl/)n (see chapter 23),
When I tompiled the fungi tausing imponanl plant d iseases. I found that 62 were
conidial fungi (hy.,phomycetes an d codomycetes). as compared to III from all other
fungal groups combined. One of the most serious outbreaks of plant disease in recent
years was the southe rn corn blight. callsed by Ol'eclislera (Hdmil/lhosporillm) maydis. the
anamorph of Coclilio/H)/"s heleroslrop/ws ( Bit unicatae: Doth ideaies), which devastaled
the U.s. corn crop in 1970, The special 'Texas male sterile' struin oreorn btcoming \\ ide ly
used for seed at thai time was highly susceptible to the fungus, which produces a toxin
that disrupts mcmhr:ules. especially mose of the mitochondria, reducing the production
of ATP. The tox in also reduces photosynthesis: it inhibits uptake of potassium by the
guard ce ll s of the stomates, causing the stomales to close and thereby rtducing the im~ke
of carbon dioxide. Southe rn corn bligh t was brought under control by changing the strain
of seed com used by grov.ers, Plant diseases are covered in more detail in chapter 12.
Cellulolytic hyphomycetes cause blue st3in and soft rot of wood, discolour:ltion
and loss of stren gth of couon materi31s (the phialidic S lachybolrys is panicul:u-ly troublesome in the tropics), and moulding of almost ::l.Ily damp organ ic substrate. Sradlyboll)'s
c/Ulr/a rWII is u common fung us growing on paper (such as th ~t cove ring gypsum \\'311board) in dam p buildin.:;s, and is now regarded in some quaners as a serious threat to
hum3n health,
Many mou lds spoil food in storuge (and in your refrigerator), Food spoi lage i (he
subje~l of chapter 20,
Worse yet. AspergilIlIsj/avIIs grows on peDn ut S and many other subs trates, producing a nlycoto;.;i n called a lla to:>o: in, which contaminates food and causes li ve r damage ~I'cn
at \'cT) low ~On<.:entrationS. It is the mo~t potent carcinogen (cancer-inducing) subswnce
known. The subjo:ct of my~oto.tins is explored more fully in chapter 21,

F"s(lrillm gramineorum. growing on feed rom. produces another

mycoto~in .

zearalcnOlle. which is a steroid, and causes ccs trogeni c synd rome - vaginal and recta!
prolap,~c - in young fem ale pigs. Many other rn~cotoxin s ha ve been di scove red in rece nt
.years, They are potential thre3ts to human and animal health of wh ich W~ are only now
becoming fully aware, and they h3\'C neccssi t::ued the development of new technique s for
toxi n monitoring and new programs for plant protection and food storage,


On the positive side. hyphomyeetous and coelomycetous anamorphs are among the
prime coloni~ers and decomposers of plam debri s, playing a vital role in the carbon and
nitrogcn cycles _Hyphomycctes dominate the soil mycota in most forests . Thc economy
of many streams is based on the dead leaves of land-based plants. These are colonizcd by
aquatic hyphomycetes, which usually form tetnnadiate (four-anned) conidia. and are
tolerant of low temperatures so can grow during the wimer and el'en under ice. These
fungi make the dead leaves much more palatable and nutritious for the various detrltivorou$
invertebrates which eat them. and thus the fungi act as vital intermediaries in energy now
in northern stream systemS, The terrcstrial and aquatic ecology of conidial fungi is C.tplored in chapte r II.
Some soil-inhabiting hyphomycetous anamorphs have evolved specialized traps
with wh ich they catch small animals - ncmatodes. rotifers. tardigrades, amoebae and even
springtails. These truly predatory fungi can be visited in chapter 15,
Conidial fungi are nOt just OIlt there doing their own thing, We have also learned to
exploit some of them for our own purposes. The en~ymes of Pellicillium camember/ii
produce the soft. smooth texture of Camembert and Bri.;. cheeses. Penicillium Toqu efonii
puts that inimitable zippy navour in blue chee~s such as Roquefort. Danish Blue. Sliiton
and Gorgonzola. Now [here's e\'en Cambo~ola, which blends the buttery texture of
Camembert with the assertive na YO\.lr of Gorgon~ola. AspugillllsoryZl/e is used in the Far
East to tum soya protein into such delicacies as soy sauce (or ils sweet Indonesian v:IIiant.
Kct-jap. the word which became Ketchup in English) (see chapter 19). Other anamorphs
are also exploited in the ori Cnl tO prepare a variety of 'fermclll<::d foods: and at least onc.
a species of FIIS{lrium. is now mass-cultured to produce food for people. Finally. despite
the insidious threat of mycoto~ins. secondary ITl<ilabolill:s of moulds have come 10 pla~
important roles on thc human for example. a substance which gave Plmicillium
chrysogenum an edge over competing bacteria in the natural habitat became one of our
must potent weapons agaio>t bacteria! disease - penicillin.
CycJnspnrine. a s~condary metaboliLc: isolated from the mould To/yp0c/I1I/i1l1lJ
";':1'11111. is the most effeclive and least [oxic immunosu ppresS!lnt yet discovered. It ha,
enormously impru\"ed the success rate of organ transplant operations by pre~-enting recipienlS' immune systems from rejecting the impl:mt. but not lea\ing them totally dc
fenseless against infe<:tion. This subst:tllce or ilS dcrivatives also hold out some hope for
treatment of severe autoim mune diseases such as juveniie diabetes. rheumatoid anhriti , .
multipl e sclerosis. myasthenia grav is, aplastic anaemia. Addison'S disease. Hashimoto's
thyroiditi~ , and systemic lupus eryth emat osu~. See chapter 24 for a more dtailed discu s
sion of the cyciosporine phenomenon.
In addit ion. conidial anamOfPhs can now be g.;.neticaily transformed to act as hosts
fOf ,'eetors carrying multiple copies of genes from othereul::aryOtic organisms (including
humans). and have already becn persuaded to express and secrete a num~r of euhryOlic
gene products. including insulin, human growth factor, hum an tissue plasminogen activator (used to dissolve blood clots). bovine chymosin (an e nzyme used in cheese-rna\.;ing). and amylDse and cellulase enzymes (sec chapters 10.24). Obviously. the biotednological potential of the moulds is tremendous.

A Survey of As co myceto us Holomorphs

Now to put anamorph and tekumorph together, and tall:: nbou! the whole fungus
(the holomo rph). If you have any querieS about ~namorph-teleomorph conncctions in
ascomyceteS. there is now a web site at which you can look them up. The URL is http://
........w.hi ology. ualberta.calj bn.u.Slo/analel eo/a nat el. html Emer Pezi::.a (a common cup
fungus ho10morph) and sec how many different anamorph connections you ["l:trie,e. Try


(a hyphoruycetous anamorph with single, genernlized phlalides) and see

how many holomorphs come up. Why do you th ink there are so many"?
I wHi "riefly survey the more important orders of Ascomycetes, linking thedifferent
life-forms together in as many cases as possible. Although 45 orders of ascomycetes (qui te
a few of them almost entirel y lichenized) were recogni zed in one recent classification,
you may be relieved to discover that I will show examples of. and provide a key 10, only
17 (mainly non-lichenized ones - some of the lichenized orders are listed in cbapter 7).
Here they are in order of appearance:
Taphri nales
Elaphomycetales Leotiales
Ophiostom atales
Sphaeriale s
Rhytismatalcs Laboulbeniales
C lavicipitales Dothideales

A CfI!tnOnilU/I

(I) Order Taphrinales: 9 genera, 120 species. This is an ou tlying group which
causes seriou.~ diseases of some plants in the Rosaceae (e.g. Taphrjrw defonnans causing
peach leaf curl) and the Amenlifene (e.g. Taph rina populina on poplar). Fig. 4.9 shows
T!Jphrina defonnan5 attacking :I peach leaf. Le aves become thid:ened, distorted and
often yellow or midish incolour.1ltis fungus has four unique or unusual fearures: {A)"The
assimilative mycelium is dilcary(){ie ~ this would immediately distinguish it from most
otber ascomycetes (and indeed questions about the taxonomic positioo of thi s
order). (8) It produces an exposed layer of asci on the surface of the host leaf (Fig. 4.9).
Since there is no surrounding or supporting fungal tissue, there is nothing we could ,all
an ascoma. (C) The ascospores often bud in a rather yeast-like manner. even while still
inside the ascus. (D) When the asci open to re lease their spores. they tend to split across
the tip, rother than around it (Fig. 4.9), so they are not like the rest ofthc operculate group
~com!XU"e them with the asci of the Pezirules, the nex t order. As yOt! may ha'e guessed by
now. thi s group sits uneasily among the other ascomycetes. and one eminent authority
grouped the Taphrina!cs wi th the smut fungi (see order Ustiiaginales in chapter 5); both
are yeast-like whe n grown in axenic culture. Compare its features for YOlIr:se!f with some
of the orders that follow.

~a k ld


""""P"'" ,

asO on

~acI1 ~a!


Fig. 4.9 Taptwmles: Taphrina deformans.



Series Unitunicatae-Operculatae

(2) Order Pw zales: ISO genera. 900 species. The ' operculate d bcomytetts' we'll look at 7 of the 13 families currcntly rccognited.
a) Family Pezizaceae. Classic 'cupfungi' producing apothecia\ as~omata that are
usually shaped more like saucers or goblets, usually without stalks, and found growing on
wood, dung or soil. They vary so much in colour, tc:<turc and ornamentation thaI most
discornyccte specialists split the Pezizaceae into several tri~s or even families. Their asci
have adiagnostlc pop-open lid or operculum (Figs. 4.3, 4.10 B). and the tips of the asci are
amyloid (sometimes e:<prcsscd as ,> or in Europe as J' - this means giving a blue, starchlike reaction in an iodine solution known as Melzer' S reagent). A small species of Peziza
(Fig. 4.10 8) often crops up on soil in greenhouses. frequently preceded by its blasticsynchrol"lQus Chromelosporium anamorph (Fig.4. IOA). Largcr species of Peuza, producing thin. rather brittle apotheda\ ascomata several centimetreS across, wilh light bro"'n or
Qrange hymenia. can ~ found on the ground in spring and fall. The c:<posed hymeni um
of each of these ascomata contains millions of asci. and if you rmd a ripe specimen and

.",, -



G ;so...-.l_$pO<ft

Fog. 4. 10 Representative Peziza~5 (Ul'litl.ricatacOpercL4atael.


blow on it. you can somelirnt~ provoke II massive s)'nchronized ~pore-shooting in whi\:h
the thou sands of simult.aneously ex~lled spores look like a puff of smoke.
b) Family Sarcosom:Uaceae. Wood-inhabiting fungi with apotheaa that are often
stalked, Idatively tough. and brightly coloured. The asci are sub-(lpercuiale. and nonamyloid. The scariet cups of SarcQsc),pha coccillcn, growing from buried hcmlock
branches, brighten up the early spring in eastern Canadian woodlands. The brightly
coloured. stalked apothecia of Cookeina are II. common $ight in the Neottopics, and may
provide a camouflaged perch for the tiny but equally colourful poison arrow frog. as one
Nmiona/ Geographic cover showed.
c) Fancily O! ideace~e. Scmel/jllin sculellal(1. its ora nge apothecia rimmed wilh
dark hairs (which give it the name 'eye-lash fungus' Fig. 4.10 D), and prodUCing nonamyloid asci. is one of the commonest cup-fungi. growing on rotten wood. AnamOlJlhs
don't seem 10 be produced in this famil).

Fig_4.11 Suggested evoIutio rklfY seq.Jence from epigeous to hypogeous Peziza les.


Some genera. such as Cl'l1l'G (Fig. 1.. II). produce cl osed but hollow allCOmata. Th~
asci are cylindrical or clavate, and are arrang~d in a flat hymenium lining the aseoma, but
they do not shOOt their spores. These apparentl y contr.ldictory features show that nwm_
bers o f Ihis family are becoming sequestrate (meaning Ihal their fTllit bodies do not Ukr '
ate spores at mawrity) and hypogeous (" hich means thaI they produce their aseomata
un<krground ). AnQ{her n1<'mberofthis family, Geopom (Fig. 4 .1 1), is also .>equestmt<: and
hypocous. but now the air space inside the frui t body is much less than in CtII~a: anOlh ~r
~Iep on the way to becoming a truftle (see Fig. 4 .1 I and Family Tuberaceae). This evolu
tionary process is diagrammatically illustrated in Fig. 4.11 . The founh and final step sees
Ihe e limination of air spaces allOgether. and is a solid truffle of the 'genus Tuber. Family
Tuberoceae - see (g) below.
Evol ution toward the seques trate am! hypogeo us condi tion is not reStricted to the
Otideaceae. but can also be secn ope rating in several other families of the opercu lare
d ) Family AIICobolaceae. StudenlS who have followed the succession of fUll gal
fructifications appe aring on horse dung will be familiar with the two mOSt important
genera of this large ly coprophilo u$ family - AS"obolus and Slleeoboilis. Both produce
minute, trans!ucent apothecia (see n under the dissecting mi cfOlICope. Fig. 4.\0 C). The
dark dots are mature asci. which are broad. and projCl:t from the h)'OM'!nium when mature.
so that their lips may orie nt themselves {O point toward the light. The aseOSporcs have a
purple or brown outer wallla)cr. Ascoboll,s (Fig. 4.10 C), like most other a'lComycetes.
shoots ascospore s individually. San'QbolllS atypicall y sticks all eight ascospores to
gether in a bundle, and Ihey are expelled as a sin;le projectile, whic h gives them extra
range. I havcn'l personally seen any anamorphs in this family. though a few are known.
e) Family Hel\'ellaceae . These mostly spri nSfruiting fun;! have large and unusu
ally con figured apothecial ascOmata. All are Sialked, wilh beige to brow n. hymeni umcovered caps. fhl vdla specie~ (Fig. 4.\0 E) have a drooping flap on either side. and for
that reason are callcd s:ldd le funs:i.
The ascomata of Gyromiu"U species aT:: among the I~esl ascomycete fructifications.
and some specie~ contain the lo xin gyromitrin . a prccursor of the deadly
monomethylhydrazine. By causing ~om~ fatal poLo;onings. the spring -fruiting Gyrom ilw
e.,clllellla (Fig. 22. 1 D) has earn ed it s place in cMpter 22 on poisonous mushrooms. It is vital
for morel-huntcrs to bo:: able to distingui,h Ihe convolutoo head of Gyromill"ll. the fal.>e
morel. from the ridged and pitied htad of the delicious tTlle morel (Fig. 22.1 C - sec below)
Family Morchcllacea~. While C)fVm;lra. ab(}\'e. is one of the few lethally (Oxic
fungi. its com;in Mordlella. th e Inle morel (Fig. 22 .1 CJ. i.1 one of tho: fine ,t of nil edible
fungi. Species of M orchella have n broad. hollow stJlk. and a pined and ridged. spongelike, nlOre or less conical or ellipMlid~1 head. Since Ihe hymenium doesn't cover the ridges.
il sce m~ lik.<: ly th aI a morel is a compound ascoma. each pit repreo;cnting an individual
apothecium. The anamorph of the mOl"C I is a blastic-symp<XIial hyphom}'crt~. COSlallliliella .
which I have Often found growing on soil by trails in Algonquin Park. Ontari o. in the fall.
/l- Iorels have a brQ;,d geographic ran~e. bUI arc common in relatively few arca5, of
which Mich igan is perhaps the best-kno\\'n_ People thron g to Ihe woods in (l.hy 10 hunt
thiS elusive delicacy. and Boyne Cily hold ~ an annual morelhunting champiom;hip.
When Dutch elm disease was killing mill ions of el m trees. morels sometimes fru it~d
profusely around re~~ntly d~ad trees. In recent )'enrs they have a!so heen collcct~d in
large numbers on burned-ovcr areas of weslcm forest~. 1'>'!orels are discus~ed a) a delicacy
in chapter 18. JUSI to confuse the issuc a linle. a sec-ond genus of Morchcllaceae. Vapa.
also fruils in May. Species of \?rpi' aren-I to~ic. but neitho:r arc they good to cal. The
wrinkled thimble-cap, Vl'Ipa bolumi(."ll . looks like a morel, but it is C:iSy to tell the differ-

eroce by bisecting the fruit bodies. While the cap and stalk of the tNe morels are fumly
united, the cap of Velpa is attached only at the apex. In addition. the stipe of Verpa is
'stuffed' with conony mycelium, while those of Morchella are completely hollow.
(g) Family Tuberaceae - the troilles. Here, the evolutionary process still active in
the Otideaceae has run its course. The ascomata are sequestrate, hypogcous and solid (no
air spaces any more - as you can see in the bisected specimen of Tuber aeslivum in Fig.
4.10 F, which a truille dog brought to me at Scheggino in Italy). The asci of Imilles.
produced in a highly convoluted hymenium, ~ rounded and thin-walled (Fig. 4.10 G)
with no trace of an operculum or other shooting mechanism, and usually contain only 13 spores. The ascospores of truffles have complex, highly ornamented walls. They come
in two basic patterns - spiny and lacunose (Fig. 4.10 G). Only by examining a series of
microscopic characters, and considering some intennediate fonns that trace the probable
course of evolution in the group (Fig. 4.11) can we tell that these fungi ~ related to the
'operculate discomycetes:
Although it doesn't make taxonomy any easier, we must now logically place thesc
hypogeous (underground) families wilh their epigcous (above-ground) forebear.; in the
order Pezizales. The hypogeous habit has necessitated the evolution of new methods for
passive spore dispersal, in which some agency other than the fungus supplies the energy
for dispersal. Members of the Tubcraceae, especially species of the genus Tuber (the true
lr1Jffles). have achieved this by developing what ean only be called fascinating smells.
These odours are released when the ascospores are mature, and lead many mammals
unerringly to the ascomata, whieh they unearth and consume, subsequently depo~iting
the still-viable spores elsewhere. Tuber melanosporum, the black diamond, Queen or
Perigord truffle of Fn:nch gastronomy, is dependent not only on mammalian vectors but
also on the roots of oak and haze lnut trees, with which it establishes a symbiotic
edomycorrhizal relationship (see chapter 17). Tuber melano$porum and TI,ber magna
rum are. respectively, the blac k and white tromes of French and Italian haute cuisine,
perhaps the most highly esteemed (and certainly the most expensive) of all edible fu ngi .
and so are discussed in ddail in chapter 18.
(3) Order Elaphomycetalcs: I genus, 20 spec ies. At firs t sight, the
ascomata of Elaphomyces look Just like truffks; and they 're even called 'deer tmilles ' .
But they have no hymenium - the basically spherical, non-shooting asci are produced
randomly throughout the interior of the ascoma. Elaphomyces no longer offers much in


fig . ".12 Unitunicate.inoperc ulate asci. A: Nectria (Hypo<::realesl; 8: Sordaria lSordaria!es); C:

Melanconis lDia portha!es); D: Claviceps (Ciavicipitaies); E: Microg/osslJm (amyloid ring,
Leotia les), f: R05ellinia (amylorct ring, SphaerialesJ; G: Lecanora (Lecanorales).



the way of visual dues about its possible epigeous ancestors, so only mo!etular techniquts can help us decide its relationships.

Series Unitunicatae-Inoperculatae
Although none have lids (opeKula), the asci of this group are not as uniform in
appearance or structure as we might like (Fig. 4.12). Most have thickened walls al their
tips. pierced by a fine pore. Inside the apices. many have diagnostic sphincter-like rings.
which control the expulsion of the spores. Some of those rings are a myloid OT l ' (they
stain blu e in iodine). others don't react wi th iodine and are called chltinoid. Some asci
don 't have rings at all, and in one such order-the lithenized Lecanoral cs (4 .12 G) - the
Bscal apex is extremely thick and pierced by a narrow canal. The troe relationships among
these orde rs have yet to be full y worked out.
(4) O rder Sphaeriales: 225 genera, 1.300 species. Man y members of this order
produte dark, brill Ie, globose to pe:t.r-shaped individual per:ithecial ascomata with prominent ostioles (narrow apical openings) (Fig. 4.13 A, B). Others have many perithecial
cavities immersed in a single stroma to form a compoond fructification (Figs. 4. 13 C, D).
The asc i often have an apical ring or sphincter, whith is usually, though not always,
amyloid (stains blue in iodine). Thread-like, sterile elements called paraphyses are present
between the asci in the hymenium of some members. but absent from others. Ascosporc~
can be light or dark, simple or septate. with or without germ pore or slit. sometimes witb
gelatinous sheaths or appendages.
The ~ompound fructification of Xy/arja. a common wood-inhabiting genus (Fig .
4.13 C). has hundreds of pcrithecial ascomat a just below the surface Each perithecium
contains many asci. The asci are inopeKulate. with an amyloid apical ring and contain
eight darkly pigmented. asymmetrical spores. These spores will eventually be shot OUI
through the narrow ostiole.
This order also includes such pathogens as Hypoxylon pruirla/um, which causes
poplar canker, a disease that kills milliOllS oftrccs every year. The extensive. more or less
elliptical cankers develop groups of pcrithecial :!$Comara after the tree cambium has bet:n
killcd .
(5) Order Sordariales: 5 families. 75 genera, 6OOspecies. This is agenernlly saprobic
group producing solitary perithecial ascomata. and found on dung or decaying plant
remains. Their asci sometimes have non.amyloid apical sphinctcrs. and sometimes lack
any apica l apparatus. Scveral members of this order are important tools in fungal genetic~
and biochemistry. First and foremost is NCllrospora. which has justifiably been called the
'Drosophila of the fungus world'. It was on Ncurospora CTaSJa that the science ofhapJoid
genetics was founded. The uses of NClIroSporo. and Sordnria mutantS are explored in
chapter 10. Many species of Sordari(l and PQdospor(J. (Fig. 4.13 A) fruit on herbivore
dung. and shoot their ascospores from perithecial ascomata whose necks are phototropic
(poim to,,-ard the light). Different members of the genus Podos{JQm. which has over 100
spedes. have 4, 8, 16, 32. 64. 128. 256, 5 12, 1,024 Of 2,~8 ascospores per ascus. The
\'arlOUS rombinations of tubular and gelati nou. ascospore appendages in Potk>spora not
only help in species identification. but also Slick the spores to &!'Iss after they hU"e been
shot away from the dung on which the a5Comata develop. Somc species of Podospora
have Phialophora anamorphs (Fig. 4 .J3 A). Choe/Qmium (Fig. 4 . 13 B) is un important
cellulolytic genu s that damages fabrics and paper. especially in the tcopic s. II differs from
most other Sordariali:s in that its asci, though cylindrica l, deliquesce or autolyse at maturity. Sin~e they don'l shoot their spores. thcy have no apical ring mechanism. and the
mucilaginous. lemon-shaped ascospores ooze out of the ascoma into a charncteristic mass
of toiled or dichotomously branched hairs that dcvelop on the 101' of the ascoma. Dis



petsal must be b)' rIIin or arthropods. Chaewmiunt has BQtT),otYichufJI anamorphs (Fig.
4.13 B). Neums{'QT(i has Chrysoni/ia allamorphs.
(6) Order Diatl')'pales: 20 genera. 125 species. The bark on dead branc he~ of tree,
often devdops eruptions that mark the extensive immtrs4:d strOmata (compound ascomata)
and the grouped ostioles of sueh common genera as Dia/rype (Fig. 4.13 D) and QI/memorill.
Diatrypaienn asci have a tiny amyloid apical ring, and the ascospores, also vel)' small , ore
characteristically sausage-shaped (allantoid).
(7) Order Hypocrealcs: 80 genera, 550 species. This order is recognized by its
brigbtly coloured, simple or compound, peritbecial ascomala _ usu~lJy yellow. orange or
red - wbich are fleshy or waxy in lexrure. and usually bome on supporting layers of
mycelium (s l.lbicuJu) or in stromata. Four genera are especially well-known:
(a) Nee/ria (Fig. 4_ 14) often has bright red, superficial peri thecia (right) contai ning
two-celled (di dymOSporouS) ascospores. Some species couse cankers and diebac ks of

-.- -



t . <''00'&

8. CI...._ (~")

"flood ucorn...

trees. N((tria sensu laID has a "arieLy of conidial anamorphs (Fig. 4.(5), bUI all of them arc
phi::tlidic. The crumpent sporodochill of one commonl y encoumcred anamorph.
Tuben:1l10ria (Fig. 4.14 ). cause a condition known as coral spot. As you can see in Fig.
4. 14, the TIlIU'n:1l1aria anamorph oftcn grows beside the dark red NtCiria ~ritheeial
a.o;comata. It is interesting and a little unusual to see both phcnm}'pic expressions of the
g~!lOme being produced simultaneously. HOI'/eve r, the most economically important of
the nectriaceous lInamorphs are cenain Fusarium species (Fig. 4.1 5. 15.2. 21 . I 8). ITl.lny
of which cause destructive wilt diseases of higher plants or produce mycOlOxins.
(b) Gibherella also has Fusarium anamo rph s. A member of thi s genus causes a
dise::tse of rice called 'foolish seedling' in which secdling~ grow too rapidly and conse
quent!y fall over. The active principlc. a plant growth honnone called gibberellic acid.
has bee n extracted and is !lOW widely used to stimulate plant growth.
(c) H)"poll1)"ce.i laClijluurum is an orange fungus which parasitizes the agaric (mush
room) gene ra wC/arius and Russufa, producing a layer of tissue that completely covel"';
the gills and suppn:sses their development. then developing thousands of bright orange-

.. otf.e

~ ..

..", 06ocf>rOl


... ~ ",,!&IodH


TU~rcUIMfll aoarroorpl"l

F.g. 4.14 H)"poct'ealK Neclria cinnabarina <and its Tubercu/aria <lnamorph.




IT ,..o.'oow.

n __ """""

i/ '\

Fig. 4.15 HypocrroJes.: anamorphs of Nee!,;a sensu lata Arrc'J.Ns inc5cate possble i'les of


red perithecial ascom ata all over thc surface of the host. The Hypomyces completely
envelops the aborted mushroom and its colour gives the host-parasite combination the
name 'lobster fungus'. Strangely enough. this monstrosity is edible, though 1 regret to
have 10 tell you that it does notlaSte like the divine crustacean. Hypomyus has extremely
characte ristic spindle-shaped, two-celled. colourless ascospores. The anamorphs of
ffypomycts species belong to the hyphomycete genus CladobOlr)"um. which has an unusual blastic-retrogressive method of fonnins conidia.
(d) Hypocrea forms fleshy stromata on wood. The dark spots on these strom~ta arc
the ostioles of the embedded perithecial cavities. 1be teleomorph of Hypocrea, though
not recorded far less oflen than ils green-spored. phialidic anarnorph. Trichodemra (Fig. 14.3) which. because il is a broad-spectrum mycoparasite and produces
ceHulases and antibiotics. is one of the mo st important moulds in forest soils. It is now
being exploited in biolosical co ntrol of pathoge nic fungi (sec chapter 14) and in the
proouction of enzymes which can convert cellulnse to glucose (chapter 24).
(8) O rder Diaporl halt.'5: 90 genera. SOO species. Here several beaked. perithedoid
ascomat(J. are immersed in a single Stroma (a.'i in DiaporlM impuIsa. Fi8. 4.16).
Paraphyses are often absent; and the asci. which have an amyloid apical ring. become free
inside Ihe ascoma and then autolyze. This rather paradoxical situation suggests that
evolution is in active progress here. Two important genera stand OUl. Cryphonec rria
(Endorhia) parasWca causes chestnu t blight. which almost extinguished an important
species of NorthAmeric an tree in about SO years: you can read the full story in chapter 12.
Because of this near-extinction, you will probably nm be able 10 find speci mens of
Cryphoneclrio, but another member of this order. Gaeumannqmyus gramirtis. which
causes 'whi teheads' or 'lake-all' of wheat, is common. It rots the fOOlS of afflicted plants
and so causes premature drying OUl of the plant, sometimes reducing yields to zero.
(9) Order Leolia les: 13 families. 400 ge nera. 2.000 species. The ' inop('fculale
disl,:omyceles.' The apothecial ascomata are superficially similar to those of the Pezizales,
bul the asci are inoperculate. and usually have amyloid apical rings. This suggests to me

that the two major kinds of apolhecial ascomata arc examples of parallel or convergent
evolution. Several of Ihc families in this order are common and well -known. so four of
them are dealt with below.
(a) Family Sclerotiniaceae. As the name implies, Ihese fungi often fonn sclerotia.
which may be solid masses of fungal tissue. or may be of mixed origin - fungal hyphae
riddling a mummified host such as a peach, plum or cherry. or a catkin. Having ovef\\.in
tered in this guise, they germinate in spring and use the stored energy to produce slalked
apotbecial ascomata (Fig. 4.17 A). Ascospores, the primary inoculum, are shol when the
hosl is in flower. and gain entrance through the Sligma. The anamorphs are generally
responsible for sccondary dispersal during the growing season, and some cause serious
planl diseases. For example, Ihe soft brown rot of peaches (Fig. 4. 17 A) and chcrries is
produced by a Monilia anamorph of Monilinia . The beige or greyish powder on the
surface of Ihe peach and the cherry are made up of bran ched chains of conidia. The longer
I leave Ihe ripe cherries on my cherry Iree. the more oflhcm will succumb 10 the Moniiinia
sofl brown rot. as the conidia being produced on one cherry infecl others (see chapter 12).
Anolher Monilinia produces spur blight of wild cherry, killing back young shoots and
forming new conidia on the leaves.
Many members of this family have distinctive anamorphs . while the teleomorphs
are rdatively uniform . So some of the genera erected for the teleomorphs have rather
atypically been distinguished by characters of their anamorphs - and even named after
them . So we have Sclaa/illia with Sclerotium (sclerotial) anamorphs, Moni/inia with
Monilia anamorphs (blastic -acropetal), Botrya/inio with BorT)tis anamorphs (blaslic
synchronous). and Sireptotinia with Srreplobolrys anamorphs (blastic~sympodial).

Sclerotium . Monilia and Botrytis cause several serious plant diseases - grey mould
of strawberry is caused by Botrytis cinerea (chapter 12). but when BOlrytis grows on
overripe grapes in certain areas of France. Germany, Hungary. and South Africa it is called
the 'noble rot' in several langu ages ('pourrilUrc noblc ' , ' edclfaulc') becaus.c the small
quantities of sweet dessert winc that can be made from such shrivelled grapes have intense
and exquisite Oavour, and can be sold for very high prices. Find out what a boule of
Chateau d 'Y quem sauternes from France (or a 'Trockenbeerenauslese' from Germany)
costs at your local wine store: be prepared for a shock. The full story can be found in
chapter 19.
(b) Family Ph acidiaceae. Somc Phacidium spp. cause snow blight diseases of coni
fers. If we look roore closely, we will see that this family is not typical of discomycetous
fungi in general , sincc the ascomata develop inside host tissue and are at first covered by
a thick roof of dark fungal tissue (Fig. 4 . 17 D). But at maturity th e roof ,plilS open and
apical ring



immersed perithecia

Fig. 4.16 Diaporthale,: Diapo rthe impulsa.

exposes the hymenium. 111C apical ring in the asci is amyloid W). Comp:m:: thi s family
with Order 10, Rhytismatales. below.... How do these orders differ? Phacidium has
coclomycetous anamorphs: those of pathogenic species such as P. coni/erar"," belong to
ApOSlrI.useria. while those of saprobic species li ke f'. beru/inlllli belong to Ceurhospora
(Fig. 4.1 7 D).
(c) family Geoglossaceae -literall y earth-tongues _ produce unusual stalked,
somewhat flattened and tongue-like aSCOm3ta which emuge from the ground (Fi. 4. 17
B). The hymenium doesn't line a cup or saucer. bUI co'ers Ihe convex upper surface of lhe
aswma, which is fleshy and yeUow in Spa/hl//aria, tough and black in Microg/o$SWII and
Geag/o!iJum. If you squash a tiny piece of the hymc nium of a mature Geog/O.'SHIII a.>coma.
you will see the asci, each of which con tains a bundle of eight long, parallel.
phragmosepuuc brown ascospores (Fig. 4.1 7 B).


.,., PlOCIt

~.ti ....

.... P!'C_
In.nti"ll on

corui., n. lIn

c."mo."",. "'.me'l'"

Fig. 4. 17 Repre:;entative 'inoperculJte di>comycctes: A: Monilinia and its Monilia ar"\J.morph; 8:

Ceoglossum; C: Le olia: D: Ph;)ddjunl and its Ceuthosp ora anamorph.

(d) Family Leotiaccac comaiM more typical 'discom)cetc.' ~uch as 8i.!porcllll.
which produces those small ycllo'" discoid apotheda so CQmmon on fallen, decorticated
tree-trunks, while Chforociboria. also fairly tommoll. stains wood green and fomlS small
green 3lX'1hecia. Less typical are the Spectacul:lr ascomat:l of uo/ia (Fig. ~ .17 C): these
are much larger; stalkM. jelly-like. and have convex fertile heads. a beautiful velvety
green in uotia ~iscosa. in conlrast with its vivid yell()\O. sti~. AnOlher rather spcct.:lCuhr
member of this order is Btl/garia inqllinalls. found on wood of deciduous trees. The
clustered apotheciaJ ascomat" h"ve "rubbery texture. and the hymenium is jet black.
(e) Fumily Dennateaceae includes Diplocarpon rowe (whi ch. with its MarSS/Jllina
anamorph. causes bluck spot of roses) and a cornman but interesting fungu~. TnJ(ilUa
j!ideo/a, that fruits on the upper surt'ace of dead leaves of holly (f/ex ) in my garden. Its
ascomata have a hinged lid. which opens when thc leaf is kept in a dump chamber.
( 10) Order Rhytismatales: 70 genera. 400 species. The thOSt: of the
Phaddiaccae. develop irnmcr!.Cd in host tissue or a fung~l stroma. .... hich ultimately ruptures 10 exposc the hymenium. The asci often have apical rings, but these are small and
chitil}()id (do nO! Slain blue in iodine). The aseospores ~re usually long and thin. and have
a slimy sheath (absent in the Phacidi:lCcae). The gcnus Lophodl'rmillm is sometimes
endophytic :lr\d asymptomatic in pine needles fOl" much of ilS life. but c\'entually fruits
after the needles die (see chapter 11). Rh)"lisma acerililim cau~s 'tar spot" of red maplc
leaves in eastern North America. Rhyrisma p""cralllm produces ~ simi13r syndrome on
big-leaf maple in westcrn l\orth Americ~. but the small. Individual aseomata do not fuse .
( 11) Order Cla vid pitalcs: 27 genera. 270 species. This order comprises a group of
high ly evolved and sophisticated. obligutely parasitic fungi with: (a) frequcmly ~talked.
all-fungal stroma!a (Fig. 4.18 B.C.D.E). (b) long asci without apical rings, but with thick_
ened tips (Fig. 4.18 F). and (c) long. Thread-like asco~pores thm in some taxa rr~gtii1fnt at
or following release. ( Fig. -1.18 F). Three bizarre and spectacular genera. Cltll"kt>ps.
Cord)"C(ps and !:.p ichl.u.
gh'e us a snapshOi of this fascinating order.
(a) Claviups pllrpurea (Fig. 4.18 AC)diseharges ilS ascospores when ilS main host.
rye. is in flower. and infection Illkes pla~"C through the stigma. As the infection progresses.
the fungus lakes over thc food being channeled imo seed-production by the host. The
ovarian tissues are repl aced by a mycelial mat that prod uces rm.$ses of conidia of the
Spilact/ia anarnorph in a sweet,smelling neCI~r. In sects nre attractcd 10 tht: nectar, and
spread the conidia tn other host phmts. The m)'cclial mal haraens and becomes a purpli~h
sdcro tium - the ergot - which r~p1a~'es the grai n (Fig . -l.18 Al.


I have foulla very large ergots on 1)"111]($ mollis,

a largc gra~s that grows ;!long the

shore in the Pacific Northw~st. The largest ergot is 4 cm long ana almo~t5rnm wide. The,;.:
sderotia fall to the gwund in autumn. overwinter. ana g~nninme the following spring,
each producing scve-ral stalked slwmata (Fig. 4.1& B. C). Each stroma has a spocrical head
"'ithin ,,hich many pcrithe.:ia de"elop ju~t below thc surface. Each ]X'rilhecial cavit)"
contains many asci. each with eight extremely long ascosporcs.
Because this fungus has a small larget, the stigma of the rye flo"'cr. which is avail nble only during a narro ..... time-w; ndo", ~nd because spores reach it only by chancc. the
fungus must dispcr;c a large number of aSCO$pores in a short time. A rough e;rlcubtion
suggests th~t a single ergot can give rise to 5 stromata. and each of th Ose may contain 100
pcrithecial ca"ities. each cavity with 50 asci, and each ascus producing 8 ascospores: a
towl of 5 x 100 x 50 x 8 ::: 200,000 propagules per ergo!.
If the sclerotia are a,cidentally co ns umed by cank. or if ryc bread made from ergoty
rye is e~ten by humans. a large number of alkaloids founa in lhe ergot cause a form of
poisoning knO"'n as ergotism. Of. more picturesquely, SI. Anthony's Fire. Human vktims


hallucinate and fee! that they are burning (see chapter 21 for a fuHer account of
this mycotoxicosis). The alkaloids ergotamine and ergotaline cause contractions of the
smooth muscles, and the ensuing restriction of the peripheral blood supply can lead to
gangrene and even death. SI. Anthony's Fire was fairly common in the Middle Ages, and
sporadic outbreaks occurred until recently_ Ergot, the only fungal structure in the British
Phannacopoeia Codex. has been used in obstetrics both to induce childbinh and to
control post-parruml bleeding. Another species of Claviceps broughtlhe germs renewed
fame, or perhaps I should say notoriety, as the prime source of LSD (lysergic acid diethylamide), one of the most powerful psychedelic drugs (it is a hundred times more potent
than psilocybin, the active ingredie nt of ' magic' mushrooms).
(b) CQrdyceps species (Fig. 4.18 D-F) are bizarre: they generally parasitize insttts
or spiders, or hypogeous (underground) fungi, aod their large stromata spring up directly

L~ po<\O?I ",.n



ElophamycfS {no<ll

Fig. 4.18 Representative Cbvidpitales. AC: C/aviceps; D-F: Cordyceps.


from their victims. These perithecial stromata arising from an insect larva or pupa are
known as "vegetable caterpillars," in recognition of the fact that they always incorporate
elements from more than one kingdom. These strange 'two Kingdom' structures are used
in traditional Chinese medicine as a treatment for "general debility after illness, weakness, spitting of blood caused by TE ... chronic coughing and asthma ... night sweating
... anaemia ... malignant tumour."
As mentioned, a few species of Cordyceps don't pick on arthropods, but cannibalistically attack another fungus. Actually, it's even another ascomycete - the underground
deer uuffle (Elaphomyccs). The large, stalked Hroma of the Cordyceps can be seen
emerging from the host troffle in Fig. 4.1 8 E. Every September for many years, during a
mycology field course I taught, we found Cordyceps parasitizing Elaplromyces along one
of the hiking trails in Algonquin Park, Ontario. Once one of the students had spotted the
club-shaped stroma of the parasite, excitement ensued as we dug down, following the
yellow rhizomorphs of the fungus , UUlil we finally excavated the host. This fmd was often
dubbed _ and with good rcason - 'fungus of the day,' though perhaps that title should
have been pluralized.
Cordyceps, which must infect target organisms that are clearly far scarcer than rye
flowers, goes a big step funher than Claviceps in the multiplication of spores. Each of the
8 long ascospores breaks up into about 100 partsporos, often while still in the ascus (Fig.
4.18 F). I estimate that the usually single large stroma produced by this genus from its
fungal or insect host may bear as many as 800 perlthecial ascomata , each containing at
least 100 asci, each ascus containing 8 spores, and each of them fragmenting into 100
part-spores, for a total of800)( 100)( 8)( 100:; 64.000,000 propagules: sixty-four million
spores from a single stroma.
Many of the anamorphs of the Clavicipitales are in the genus Acremonium, with
simple, tapered phialides, but in 1996 Cordyceps $lIbsess;Us was discovered to be the
holomorph of TolY[Jodadillm ni\"~um (as T. inj1anun) . So what , you might say, until you
realized that Tolypoc/adillm inj1alwn is the fungus that produces the medically important,
selective immunosuppressant Cydosporine. which has made the organ transplant revolution possible. For the story of that amazing phannaccutical, see chapter 24.
(c) Epichloc causes 'choke' disease of grasses. A grass called Glyceria normally produces open, nodding inflorescences. When Epiclrloif attacks , the energy for the inflorescences is stolen by the fungus and used to produce creamy yellow perithecial stromata, each
incorporating many peritheda, that surround the stalk of the now sterile grass. In.a recently
discovered twist to thi!; story, this apparently damaging parasilic fungus has been found to
have a mutual istic symbiosis with the grass. The simple, phialidic anamorph of Epichloif
(which used 10 be calledAcremon;um, but has recently been segregated into a new anamorph
genus, Neoryplrodium), grows systemically throughout the grass plant withollt producing
any disease symptoms, and actually protects the grass from herbivores by producing a
virulent neurotoxin. A more detai led discussion of this relationship is given in chapter 2 1.
(\2) Order Erysiphales: 28 genera. 100 species. All members of this order are
obligate parasites on leaves and fruits of higher plants, causing diseases called powdery
mildews. These fungi have superficial mycelium which extracts nourishment from the
host plant through specialized hyph ae that penetrate the epidennal cells of the host and
develop special absorbing organs called haustoria (Fig. 4.19). You should have no diffiClllty spotting a few powdery mildews in sununer because their whitish co lonie, growing
on living leaves are unlike anything else. In dry sununers they are particularly common
on gra,s in shady parts of lawns, on squash plants (cucurbits), on perennial Phlox, on
Ainus rugos a, and many other angiosperms. Basauxic chains of conidia of the Oidillm
anamorph (Fig. 4.19), whose powdery, whitish appearance gives these disca,es their name,


Key to Some Common Genera of Erysiphulcs

Ap(X'ndage type

One ascus (X'r


"lore cha n one ascus per


Appendages like assimilative hyphae



Appendages dichotomously branched

at end



Appen!bgcs curled at end


Appen!bges needle-shaped. with

bulbous base


arise from the mycelium in carly summer. Airborne conidia spread the disease from plan!
to plant. and are later succeeded by dark -coloured ascomma which mature slow ly in fall.
and release ascospores the following spring. This orde r well over 1.000 higher
planl species. and the powdery mildews of gl'3pes, hops, gooseberries and cereals are
eeonomically important diseases_
The generic COncepls in this order are unusually straighlforward and easy to appl)'.
since they depend on two major features of the a~oma: (I) the number of asci within it.
and (2) the kind of (lppendage growing out from it (fig. 4. 19). In one way. the ErysiphaJcs
arc the anti thesis of Lhe Sclerotiniaccae. Thel1;). the anamorph s were far more distintti'e
and diverse than th e lekomorphs; here , the reverse is true. Most anamorphs of the
Erysipbales beloltg to tbe hypbomycete genus Oidilllll. Althou gh Ihe order Erysiphalcs is
~ery easy to charactcrizc and reeognilc, its sy~tClllatic jX.Isition is comro\ er.;iaL Some
mycologists insbt Chat its asci are bituilica ce. which would place it alongside the
Dothidca!cs (see below). but many mycologists do nO{ accept this. and place the order
among the unirunicatt: ascomycetes. The asci are sometimes ralher Lhick-walled. but one
of the world experts on the group, Dr. Zheng Ru-yong of Beijing. tell s me that she has seen
dislinctive inner and outer wall layers only in an un described taxon frorn Tibet. and has
never seen the "Jack-in-a box" mechani sm so typical of the bitunic:lIae. The usci seem to
have neither an o~rculum nor an apical ring apparatus_ This information, plus their
strange arrangements for dispersal and dehiscence (see chapwr 8). cheir unique basau",ic
anamorphs. and their obligatdy para5itic )'et slrange1y superficial lifestyle. make them a
rather peri phera.l (though important and interesting) groLp.
A!der le3\' oflen bear extensive colonies of PhyllaCli/!ia. Under the dissecting
microscope you can see ascomata with unique appo::ndage.> (Fig. 4.19). The basal bulbs of
the appendages develop Ilrst, then the needl e- like extension, grow OUI. At ITIJturi(y. these
~pp<;:ndages aJj b.:nd downwnrd in unison ,111d lever the uscoma off the leaf surface, br~Jkin !!
its conneclions with the mycelium. it is then free 10 be blown or splashed away. becoming
attached LO a new ~uhstrntc by an Jpical blob of mu<:il~ge seneted by specialized hyphae.
Par.Jdoxic~ll)'. this leaves the ao;ci. which are designed to shOO( their spores, facing down
w:lTd. The final chaplcris written when Ihe ascoma splits around thecquatorat J builtin line
of ".'cakness. and hlngo:s open so that thc sjX.Ires can finally be ,hot away. (Fig. 1l.3).

Series Prototunicatae
In (hc following fOllr orders, the walls of the asci break down when the a,cosporcs
mature, and therefore the SjX.Ires cannot be forcibly ejected. This has led to (he evolution
of new ways of dispersing the spores.


(3) Order Ou) gcmlies: 40 genera. 120 species. Here bf.,long some unusual fungi
which cause skin diseases in people. and can digest hair. bom and feather - all be<:luse
they have lhe unusual abil ity to metabolize the resistant protein. KeraTin,
The Family Anhnxlerm.:ltaceaeconlairu; the genera Arrhrodum(l (wilh anamorphs in
Tridwphyum) and Nanniz;:i(l (anamorphs in Microsporum). the infamous d ermatophytl'S
which cause superficial mycoses ranging from the inappropriately named ringworm orlhe
scalp to another misnomer. athlete's foot (you cenainly don't need to be athletic to catch it)
- see chapler 23. Other members of the Ollygenales can degrade cellulosc, and yet OIhers
are coprophiJous (dung-inhabiting), They all produce ascomat a, but although thcse are
theoretically cieistOlheeial. their walls may be very loos ely woven. and in some lhe ascospores can simpl y full out lhrough the gaps. The asci are always more or Jess spherical,
never shoot their spores. and tend to break down at m:lrnrily. Because of my earlier conclu
sion that asci evolved as sporeshooting devices, I assume that lhe ascoma and asci in the
Onygcnales are reduced forms, sim plified during evolution from an earlier spore-shooting
design. The a~comala often bf.,ar Jtighly Charac:tcriMic coiled or branched appendag~ th~t

ftg. 4, 19 Reptesentatr.oe Erysiphales.


can make identification easy - if the teleomorph is present The ascomata of various genera
are illustrated in Fig. 4.20 under 'peridia and appendages'.
If you isolate dermatophytes in pure culture, the y mayor may not produce
tekomorphs. But they will develop characteristic thallie conidial anamorphs (Fig. 4.20).
Sometimes these produce small, thallic-arthric conidia (Chr)'sosporium or A/albranchca),
sometimes large, spindle-shaped. transversely septate, solitary thanic conidia (Trichophyton or Microsporum), and sometimes the same culture will produce both kinds of
conidia. When a fungus has two or more different anamorphs, thes e are called
synanamorphs. The three most important anamorph genera of dennatophytes are Epidermophyton, Microsporum and Trichophyton. Of these. Epidermophyton has no known
te!eomorph, nine species of Microsponun have telcomorphs in Nanniuia, and se .... en
species of Trichophyton have teleomorphs in Arthrodemw .







-~ ----....
---...-.--- -.

.... .


...... ......


0"""" ...

----- --. ........



Fig. 4.20 Famfties of the Onygenales.

:~ UP ~. CCiil'
~"<,; 3:::3 LIOTECA


(14) Order Euroti a les: 50 genera, 140 species, This largely cleistothecial ordcr
contains the teleomorphs of some of the most successful of all conidial fungi - the common green and blue moulds of the hyphomycetc gcncra Penicilii"m and Aspergillus,
Aspergillus conidiophores have characteristic apical vesicles (Fig, 4.21 A); thosc of Penicillium are brush -like (Fig. 4.6). These ubiquitous and almost omnivorous anarnorphs are
blastic-phialidic, and produce masses of dry, wind-dispersed conidia. These moulds aren't
just extremely successful, they are of considerable importance to us because they produce
antibiotics and mycotoxins, and cause a 101 of food spoilage. Species of Aspergillus have
teleomorphs in Eurolium (a section through a c!eistothecial ascoma is shown in Fig. 4.21
A) or Emericella . while many penicillia have teleomorphs in the rathcr similar T(!laromyces
or Eupellicillium. Thc c\eistothecial ascomata ofthc teleomorphs have impenneable walls
one or more cells thick. The asci (Fig. 4.21 A) are scattered throughoUlthe cavity of the
ascoma (i.e., never in a hymenium); they are spherical, thin-walled, and break down when
thc spores mature. The ascospores often have a pulley-wheel shape. Again, it is thought
that these fungi are 'reduced' derivatives of spore-shooting ancestors.
(15) Order Ophiostomatales: 15 gene ..!, 130 species. The ascomata of this order
generally have long, tubular necks, with the ostiole at the tip (Fig. 4.21 B). The asci are
not arranged in a hymcnium, and autolyse early. The spores ooze out of the ostiole and
form a slimy droplet that is supported hy a ring of specialized, hair-like hyphae at the top
of the neck. These fungi often fruit in bark beetle tunnels, and the elevated spore drop has
e volved to ensure that the beetle carries spores with it when it flies offin search of another
tree. The most important genera in this order are OphioslOma and Cem/ocys/is (although
it is now understood that thc two genera are not closely related. and shonld perhaps be in
diffcrent Orders - sec Wingfield et a1. (Eds.) 1993)_Ophiostoma IIlmi (Fig 4.21 B) causes
Dutch elm dise ase, which was introduced into thc U.S. in 1930, to Canada in 1944, has
since spread right acro>s the con tinent, and has much more than decimated Ihe American
elm. This beetle-transmincd fungus has a Graphium anamorph that produc es many tall,
synnematal conidiomata (Fig . 4.21 B) each bearing a slimy droplet of conidia at its tip. In
producing this stalked spore drop, the anamorph is completely analogous to the
teleomorph; both are trying to ensure that bee tles don't leave home without them.

' . ~"" '/i.",,

Fig. 4.21 Protottmicatae. A: Eurotiales; B: Oph iostomatales.


O<>h"""''''' .....

CeralocySlis jagacearwn and itS Chara", qu(!rcina phi~lidic :mamorph are the
cause of another widespread and serious tree disease. oak wi lt. The tdeomorphs of
Ophiostomn and CerolOC)'slis are very similar, but the genera are easily distinguished by
their anamorphs: the Chalara anamorphs of Cer(llQC)'Stis have solitary phialides with
long, mbular coHarettes. and form long. cylindrical conidia (Fig. 4.6): OphioslOma has
se\'eral different anamorphs, none of them anything like Chala",_
(16) Order Lahoulbenlales: 75 genera, L700 species. (Fig. 4.22). This group i, so
distinct fTOm the other ascomycetes that some ~ople put it in a se parate Class.
Laboulbeniomycetcs. While thai might be justifiable. it wO\lld also complicate our clas
sification and make life a little mOle difficult for you. So. having noted the possibility of
suc h ele\,ned status, I will press on. All 1.700 known species are invariably found at
tached to the exoskeleton of insects. or occasionally millipedes and mites. Thc dewlapmcnt of SligmalQm},ces baerii. which is found on houseflies. is followed in fig . 4.22 C An
as(osporc becomes !mached to lhe animal. gcnn inat.:s, and sends a foot inlO lhe exoskel
eton to absorb nutricnts. Although haustoria may penetrate as far as the epid~rmal cells.
Ih~re is never any real invasion of host tissues. Thc ascospore develops a median septum.

F.g. 4.22 LabotJ:Jeni.llcs.


and the upper cell become. differentiated into II male organ, with several phialidc-likc
cells that produce sperm:uia, The lower cell then develops an ascogonium with a trichogyne. which is fcnilized by the spcrmatia. Several asci then develop from the ascogonium, and cve ntually deliquesce. The mature ascoma is spine-like, projecting from the
extenor of the host, and can be seen with a hand-len$. Other genera exhibit the same b~sic
features (Corl!lhrom}'c~J, Fig. 4.22A, and HI'Jperomy(cs. Fig. 4.22 B).

The Laboolbcniales apparently don' t produce anamorphs. $0 arc presumably spread

from animal to animal by adhesive ascospores during mating of the hosts, or when insects
form dense swalTlls. Thi s goes some way toward explaining the almost incredible sitespecificity of many Laboulbeniales. Various species arc restricted to one pan of the in~ct.
forcxample, onc sideofa panicular left limb: oreven tOOllCseX ofthcir host. though mo.'\
species arc not quile so limited.

Series Bitunicatae
These all produce biwnicate asci. (Again. if you don't remember what these
look. back. at Fig. 4.3).

Fig. 4.2 3 Repre>erltative Dothideales (BitLricatael.


. "'""-.




(17) Order Dothideales: 50 families, 650 gene,.!, 6,300 species. This is an extremely large and diverse order, which will obviously need 10 be subdivided when its
taxonomy is better understood; I will mention only one or two conunon examples.
(a) Family Venturiaceae. Venturia inaequalis causes apple scab, an economically
important disease. You'll find the Spi/oca ea pomi hyphomycctous anamorph causing
large brownish spots on the leaves and disfiguring blacldsh scabs on the fruit. It produces
its blastic-annellidic conidiogenous cclls (Fig. 4.23 A _ you can see the rings clearly) and
obclavate conidia on those spots and scabs. But you won ' t find the teleomorph during the
growing season. Its psel.ldothecial ascomata (seen in section in Fig. 4.23 A) develop
slowly in the dead apple leaves over the winter, and the ascospores are shot in spring when
the susceptible young leaves appear.
Apiosporina morbosa causes the extremely common and disfiguring black knot of
some rosaceous trees. especially wild cherry and damson plum, its pseudothecial ascomata
developing on conspicuous black fungal stromata: you shouldn't have too much trouble
spotting these on wild cherry trees. lbis fungus damaged and disfigured my damson
plum tree despite my best efforts at control.
(b) Family Pleosporaccac. Pleospora herbarum is common on dead herbaceous
stems, and has anamorphs in the hyphomycete genera Stemphylium and Alternaria (the
fonner shown in Fig. 4.23 B).Asco,pores and conidia in this genus are both dictyoseptate.
Phragmoseptate or dictyoseptate ascospores are common in the Dothideaks; in fact, if a
fungus has ascospores of this kind, the odds arc about 9 tol that it is a member of the
Dothideales. Coelomycetous anamorphs are also conunon in the bitunicatae.
(e) Family Botryosphaeriacea e. Guignardia aesculi and its Phyllosticta
coelomycetous anamorph cause a leaf scorch of Aesculus (horse-chestnut. buckeye) that
defo!iat~s many ornamental horse -chestnut trees in eastern Canada a month or so before
they would nonnally lose their leaves. It doesn't kill the trees, but it is extremely unsightly and significantly shortens the trees' growing season. Horse-chestnuts on Vancouver
Island aren't affected: perhaps the disease has not yet reached the west coast.
(d) Family Capnodiaceac. Commonly known as 'sooty moulds,' these fungi grow
on the sugary excreta of various insects such as mealy bugs and scale insects. I have found
blankcts of their thick black mycelia covering the trunks and leaves of southern bcech
(Nolhofagus) in the forests of South Island, New Zealand. The black. feathery branches of
the numerous anamorphs are easily scen by the naked eye.
Now I will provide a dichotomous key to lie 17 orders just discussed. But you will
see at the very beginning of the key that this chaptcr has by no means dealt with all fungi
that produce asci. Many thousands of fungi are always found in intimate relationships
with algae, and are called lichens (chapter 7). Many more never produce ascomata, often
have unicellular thalli. and are chemically rather different from other ascus-producing
fungi. These are known as yeasts (sec chapter 6). [have treated yeasts and lichens se parately because each group is phylogenetica!ly diverse, and includes non-ascomycetous
fungi (notably basidiomycetes).


No ascoma produced, asci solitary. in chains, or in layer
onhosl ...................................................... ..................... .......... 2
Ascoma produced (open or closed,
cpigeolls or hypogeou s) ....................... ........ ............................ . 3
2 Hyphae oftell absent; ascus -like mciosporangia free or
produced Oil indi vidual hyphae ................................. ............... (yeasts: chapter 6)


2 Hyph ae always present; a.o;ci borne in a
naked layer on the surface of the host plant ,............................ Taphrina les
] Thallus containing algal cells or filaments .............................. (lichens: chapter 7)
3 Thallus without algae ............................................................... 4
4 Ascus wall thick, with two functionally
different layers (BitUllicatae) .................................................... Dolhid eaIes
4 Ascus waU trun, functionally single-layered.
lysing at or before maturity in some orders ........................... _.. 5
5 Ascus wall lysing before spore maturity; ascospores not
forcibly discharged (Prototuni catae) ................ ............... ......... 6
5 Ascus wall persistent; ascospores forcibly
discharged except in hypogeous fonns (Unitunicatae) ............ 9
6 Assimilati\'e hyphae absent; ascornata on exterior of insects.
appearing as spine like outgrowths .......................................... Laboulheniales
6 Assimilative hyphae wcll--<leveloped. immersed or
superficial ...... __ _.__ ._ .. _.................. ,.... ,......................................... 7
1 Ascornata usually with ostiole: asci lysing early ..................... OphioSlomatales
1 Ascomata dosed (deistothecial). occasionally ostiolate;
asci spherical, randomly arranged within the ascoma .............. 8
8 Ascomalal peridium complete; ascus wall lysing just before
maturity; anamorphs usually blastic-phialidic .... ..................... Eu roti ales
8 Pcridium oftcn loosely woven. wilh characteristic
appendages; anamorphs thallic ................................................ OnygenAles
9 Asci opening by circular lid (operculate), or with trun apex;
ascomata apothecial or hypogeous ........................................... 10
9 Asci opening by apical pore or canal, with apical sphincter
or thick apex (inoperculate); ascomata perithecial
or apothecial ................................................ "" .......................... II
9 Asci withom lid or sphincter; ascomata c losed; obligate
planl parasites with superficial assimilative hyphae ................ Erys iphal es
10 ASl.:om~ta apothecial or hypogeolls: asci in hymenium ......... .. Pezlzales
10 Asco mata closed, hypogcous; asci random ............ .................. Elaphomycetales
11 Mature ascomata have an e:O:pDSed hymenium ................. _....... 12
11 Mature ascomata perithecial (closed but with ostiole) ............. 13



apical sphincter blueing in iodine (amy loid) ...........

nonamyloid sphinctcr ............. .,............................. _.
apical sphirn:ter amyloid (blueing in iodine) ......... _.
non-amyloid ring, or ring absent ..............................

14 Ascomata compound. perithecia radially arranged within a

black stroma; a.scospores sausage-shaped (allantoid) ...............
14 Ascomma single, or compound in a Stroma:
nscosporcs nOl sausage-shaped ............... ..................................
15 Ascornata single ............................. ., .................... .....................
IS Ascomala grouped in a stroma or on a subicular layer .............


:. , .... '\,0 ~

... -



. . .)

Dia trypaJes
So rd.llrial es

16 CH:\.I'1ER F OU R
often stalked: asci long. n:urow, lacking sphincter,
but apex thi ck. with pore: ascospores long and thread- like.
often fragmeDting at maturity: all obligatel),
..... ........ ...... .. Cl avicipilales
parasitic (on plants. arthropods or fungi) ...
16 Stroma never stalked: asci and aseospores not as above .......... 17
17 Ascomota compound. perithecia immersed, with long neck
or beak: asci with apical ring but lysing ................................... Di3()Ort haies


t 7 Perithecia not beaked. often brightly coloured. embedded

in a Stroma. or ~uperficia1 on a subiculum: asci not lysing ...... Hypocr eales

Furthe r Reading on Ascomycetes and their Anamorphs

(Hyphomyceles and Coelomycetesl
AnI. JA. von (1981) The Geller-I of Fungi S porulating In Pu reCull uf'l'. Cramer. Vaduz.
Arx. J.A. \'on and E. MijJler( 1975) A reevaluat ion of the bilunicute ascomycetes with keys
to f"milie s and genera. Studies in Mycology 9: 159 pp. Centraalbureau \'oor
Schimmclcultures. 6 aam.
Burron. GL (1968) T he Gene ra or Hyp homyce tes from SolI. WiltialI15 and Wil kins.
Breitenbach. J. and F. )(r'Jnzlin (1984) Fungi ofSw ltler land. Vol. I Ascomycetes. Verlag
~1)'kologia. Lucerne.
C:.umich~<::L J.W.. B. Kendrick. l.L. Conners and L Sigler (1980) Ge n~"'J ofH~l)homycctes.
Unh'ersil), of Albena Press. Edmonton.
Cok, G .T. and B. Kcn(jrick (Eds.) (198 1) molo~ o f Conidia l Fu ngi. (2 Vols.)Aca(jtmic
Press. New York.
Colc. G.T. an(j R.A. Samson (1979) Pa tte r ns of De" cioprn cnt in Conidial Fungi. Pitman,
Den ni s. RoW.G. ( 1968 ) Bri tis h Ascorny~elcs . 2nd Edn . Cramer, Lehre.
])omsch. K.H .. W. GanlSandT H. Anderson ( 1980) Compend ium of Soit Fungi. Vo!s. I &
2. Aca(jcmic Prcs~ , London.

Ellis. M.B. (1971) Demati acoous lIyphomycctes. Commonwealth 1'>lycolog ical

J n~ti

lu tC. Kew.
El1i5. 1'>1.8. (1976) 1\ lo re Inmatiaceous H )'ph om~'ecte.~. Commonwealth Mycol ogical
Institute. Kew.
Ellis. M.8. and J.P_ Ellis (1985) :'I lict'ofungi o n Land prant~. An Id ent ifi cation Hand book. Croom Helm. London.
Ellis, 1'> 1.B. and J.P. Ellis ( 1988) :\'Ikro fu ngi on ~ lisceIl3 ncousSuhst ...J tes. An Identificatloll Han dbook . Croom He lm. ull1don.
Hawkswonh. D.L . P.M. Kirk, B.C. SUlton and O. M. Pegler (1995) Dic tionary of the
Fungi. Sih Edn. CAB 1n1Crnali(mal, Wallin gford.
Hughes, S.1. (1976) Soot)' moulds. l\ l ycolOf;ia 68: 693-820.
K~n .

J.. R. Summerbell. L Sigler. S. Krajll cn and G. Ln nd (1997) Laborato ry H:mtlbook

or Dermalop hy tes. Star Publkations.

Kend rick. B. (Ed.) (1979) Th e W hole F UIl IlUS. (Vols. 1 & 2). National Museums of Canada.


LuttreJ!. E.S. (1967 reprint) Taxonomy of th e Pyrenomycetes. BibJioth ~ea Mycologica

Vol. 6. Cramer. Lehre.
Nag Raj. T.R. (1993) Coclomyce!Ous Anamorphs with Appendage. Bearing Conidia.
Mycologue Publications, 8727 Lochside Dr.; Sidney. B.C., VE L I ME Canada
Nag Raj. T.R.. G. Morgan .Jone~ et aL (197 2--1 982) leo nes gene rum cOl'lomycetum. Fascicles IXl[l. Departmcnt of Biology. University of Waterloo.
Seaver. EJ. (1978 reprint) North American CupFungi - Openula tes. Lubrechl and
Cramer. Monlice!1o. N.Y.
Seaver. EJ. (1978 reprint) North American Cupfungl - Inoperculat es. l ubrecht and
Cramer. Mon ticello. N.V.
Si..."3lICS3II. A. ( 1984) The Bilu nicate A.scomycetes and thei r Annmorphs. Cramer. Vaduz.
Sutton. R C. (198 0) The Coelom ycetes. Commonwealth Mycological Instit ute. Kew.
Wingfield. MJ .. K.A. Seifert and J. F. Web!xr(Ed$.) (1993) CeralQcyslis and Ophiostoma,
Taxonomy, Ecology and Pathog~nkity. APS Press, 51. Paul. Mn.
lng. J .. X. Mao. Q. Ma. Y. ZJng and H. Wen (1987) Icons of M edicinal Fungi from
China. Sdence Press. Bdjing.
Zh~ng. Royong ( 1935) Genera of the Erysiphaceae. !'.Iycota)(on 22: 209263.
lutp;lIwww. botany.u R esea r chLabs/!.. l al lochLa h/ l\'fa lloch/ l\ lou ld s!
!\Iou lds.h tml is a website devoted to isolation and identification of moulds.


Subphylum 2 - Basidiomycotina:
the Basidiomycetes


With tht: Ascomycetes under your belt. you should now find it easier to cope with the
other half of Phylum DikaryomyCQIa. Subpilylum Basidiomyootina has many important

fe:uures in common with the AS(;om)'cotina: (1) haploid lIudei in 5Om3!ic hyphae; (2)
chitinous hyphal v.w]s; (3) regularly sepia!!: hyphae; (4) presence of central pores piercing
the septa; (5) !he potential for somalic, assimilath'c hyphae 10 anastomose; (6) the produc-

tion of complex and often m3Cf05Copic sexual fruit bodies; (7) the presence of a dikaryophase
in the life cycle (e.lcept in some anamorphic holomofphs): (8) a specialized mechAnism for
launching the tociospores into the air: (9) proouchon of a conidial anamorph by many

species. Make no mistake. ascomycetes and basidiomycetes evolved from 0 common stock.
Yet they are usually relatively easy 10 tell apart , macroscopi cal!y, microscopically
and ultrastrocturaHy, because it is probably a long time , even in geological tenns, since they
evolved apart , 5 0 we can expect to find a lot of differences as well, Here are some of them,
A) Walls: The wall s of ascomycete hyphae aTe basically two-layered, those o f basidiomycete hyphae are multi-layered, Don't worry about this, because it can be determined only with me transmission electron microscope,
B) Se pta (cross walls): DikaryomyCOIan hyphae are regularly septate, but the stlUCture of the septal pore in different c:lassesofthe Iw05ubphyla differs, as you can see in Fig,
5. 1. The differences are importllnl, bul can usually be seen only wilh the electron microscope. Ascomycete sepia (Fig. 5.1 A) are pierced by a simple, central porc, wilh a round
' Vo r oni n body hovering on each side, ready to plug the pore if the hypha is damaged.
Septa of class SacchaTcmycetes (many yeasts and related fungi that fonn ascus-like
mciosporangia; sec chapter 6). are often perforated by many mlcropo r cs (Fig. 5.1 B). In
dasses Holobasidiomycctes (mushrooms. brac ket fungi, etc.) and Phragmobasidiomycetes
(jell y fungi) the se pta have a central barrelshaped structure called a dolipo r~ covered on
both sides by a cap of membralle called a parenthesome (Fig. 5.1 C). The septal poTe of
the rust fungi (atypical basidiomyootilla placed in class Teiiomycetes), is simpler. but is



often blocked by a pulleywh1 occlusion (Fig. 5.1 0). Both basidiomycotan pore mechanisms sm to prevent the migration of nuclei from cell to cell; the importance of this will
soon become clear - read 00.
C) TIle Dikaryophase. In, anastomosis of somatic hyphae may eStablish a heterokaryon (a hypha containing more man one ki nd of nucleus), but doesn't
usually initiate the dikaryophase. This is restricted 10 the special system of ascog<:nous
hyphae arising from the ascogonium within the ascoma. But when monokaryotic basidiomyCtle hyphae anastomose, they may, if they are of compatible mating types, be establishing the dikaryophase. which can then grow for months or years before indul ging in
any ovenly sex ual behaviour. To put it in Ii nutshell: ascomycetous telcomorphs have a
restn'cted dikaryo phase, basidiomycetes often have an ex/ended di karyop hase, and
even their anamorphsean be dikaryotic, a phenomenon not found among the ascomycetes.
0 ) C lamp connections. In both groups the dikaryophase comes to an end in the
hymenium of the teleomorph.ln many ascomycetes, al this point, each aseogeoous hypha
develops a reflexed tip called a srozier. which allows the two nuclei of the d ikaryon to




Hotot>asKliom ycet9s
& p l'u"agmobasic!iomycet9s

Fig. 5.1 Types of sepIa typical of various fungal


divide simultan eous ly. one in the hypha. one in thc hook of the crozi er. in such a way that
Ihe subsequentl y delimited ascus mother cell comes to contain a eomp~tib[e p.:lir of
nuclei (Fig. 5.2 A). In ascom ycetes. tbis phenomenon is generally restricted to the hyme nlum. but in many basidiomycetes. similar bypasses are found. not just allhe base of the
basidium. but al every septum In the dikaryophllSl!:. In basidiomycetes. they are called
clam p conn ttt ioflS. and their development is shown in Fig. 5.2 B. If a septate. som~tic
hypha has regular clamp eonnectiol1~. like those in the phase contrast picture (above.
right) it must be that of a dikary{){ic basidiomycete. If clamps are absent. the hyph ae could
still be those of a dikarymic basidiomycctc (many of the mushrooms called boletes have
no clamps on their hyphae), but they could equally be those of a monokaryutic basidi
omyccte. or of an ascomycete, or even those of a zygomycete. since members of Ihe Order
Kicbellales have regularly septate hyphae.
E) Basidia. This is perhaps the most basic difference and one of the easiest to see.
Whik the me iospores of a:s<:omycete~ are developed inside meiosporangia called asci
(Fig. 5.2 A, Fig. 4 .3). those ofbasidiomycctes are fonned outside specialized meiosporangia
called basidia (Fig. 5.1 B). Nudear fusion aud the subsequent meiosis bappen inside th"
cell. but the spores blow out lil<:e tiny balloons at the ends of four tiny tapered outgrowths
called ste rigma llt.
[n most ba~idiomycctcs. the se spores are then actively cxpelled from the ir percher
(Fig 5.3). But remembe r that just ~s in the a:s<:omycetes. there is a Significant minority 0
basidiom ycetes ",,hieh de\elop basidia. but have lost the spore.shooting mechanism.
The,," we call seques tra te. ~ausc the mature bJsidiospores are kept in side the basidioma
(which m~y simply remain dOiSed. or may develop underground). ~ing released l:lter in
a variety of ways. some of which in\olve animal veclOrs. as wc shall sec.




I \ \
\" \.-:,. \

".1 !::J.



~ ! .I
~\ ~\




1 i

" ~,V~ ~:



to '"

I '

& ~



'''' m....,...


8 ..-.:Io\ienoo...

. ~&,
, ;


W ti 1!

, \



\i' j (fjf




r,:, 1




Fig. 5. 2 Cornp.1rison of a~(U~and hasidun development (set! text).

4 ~ >OQ. " _

' I




You may be relieved to learn that you don't have 10 !learch for any of Ihe~ microscopic and submicro~opi~ features to recognize a basidiomycete when you see one. The
reason for that is thaI many diagnostic fealures arc visible 10 the naked eye. What else do
you know that looks like a mushroom ? It is unique. The sam.! is true of most Other
basidiomycele fru clil'ications. You com e to r.!cogni 7.e cernin basidiomycete mycelia on
sight after a while, wilhout even using a h~nd lens, be<:ause they tend 10 form delicate but
visible fan li ke arrangements on decaying wood. If you can alread)' recognize mush
rooms, brac ket fungi. puffballs. earthstan;. bird's-nes l fungi and stinkhoms, you're well
on the way to b.::ing able 10 tcll almost any ba~idiom)'ccte from an as.;omycete (and from
any other fungus).
I recognizc three classes within lhe Subph ylum Ba~idiomyeolina. These are the
Holobasidiomycetes. the Phragmobasidiom:.cetes. and Ih~ Teliomycetes. The first class
includes all the common names just mentioned. The second includes many jelly fungi.
and the third comprises the rust and S!1lU! fungi. We'lI vi,it them in rum.

Class Holobasidiomycetes
All basidiomycet<)s with holohasidia - those that arc not subdivided by septa belong here. This is the kind ofbJsidium illustrated ubove. bel.:llU'C it is the kin d found in
most basidiomycetes. Again. the presence or absence of cross-walls is a microscopic
chura~ter tha! is ofte n difficuh to see. And again. there are macroscopic features that
enable us to recognize 99% of all holobasidiomy~tcs as belonging to this class. If you
don' t hove these femurc s at your fi ngertip5 a lready. ti me spe nt looking al the various
illustrations in thi s text. and at one of the beautifully illustrated field guides lisled III the
endofthis chapter. will pay off handsomely when ),OU go outdn<m to lool:.for the.~ fUngi.
Its nOt that holobasidiomycctes are all the ~ame : in fac t. they present a dn7.ziing di vCllSjt y
of fonn lmd function. But .... hi'! most hoJobasidiomycctes dcvclop ch~r.tcteristic fleshy_
corky or woody basidiomat!l~ tho~ of phragmobasidiom}cete~ (\\hich have b asidia
sudividcd by septa) (Ire often gelatinous. ~nd tcliomycetes ha,'e nothing you eQuId CJII a
Scp::mlte frui t body. merel)" fonning pustules on thcir Ii'ing hOSK And in ld iomyceles.
toc basidia develop directly from a specialiZed resting sporc called a tdiospore.
Th e Holobasid iomycetes comprise tWO highly interrdatt:d se ries. called
Hym~llomyce t~e and Gnsleromycetae. Most Hymcnomycett:~ shoot their bJ:;idiosro re~
actively from hymenia that are exposed al maturity (G<lSleroulycetes do not). Basi diospor;:s which are to b.:: forcibly dis.;harged (ballistospores) blowout at an angle to the
fine Sterigma that btears them : in other words Ihey are asymmetrically moullIed, or offse!.
as can bte seen in Figs. 5.2 B. 5.4 B and 5.10. JUSI before d\~harge. a droplet of fluid,
enclosed within a membrane. appean at one side of the spore b::tSe, and within seconds Ihe
spore is ~hot away. A minutc quantity of mannitol and he.\0se sugars is secreted from a
small area at lhe base of the spore. forming a hygroscopi c spot on wh ich woter cUlldcllse;;
from the saturated air 'iullounding the bJ~idium. The droplet th~n coalesces instantaneously with a film of wat<,r on the $urf:l<'e of the spore, as in Fig. 5.3, call5ing a rapid
displacement of the sporc's cenlre of gravit,'. Thi~ rcdistribution of ma ss is opposed by the
sterigma whi ch is under high turgor pressure. As ~ result. Ihe spore imm~diately breaks its
fragile conneetion with the sterigma ~nd shoots away with ,'t:ry high initial acre!er.uion,
though it doesn't go very far. The mechanism has been describ.::d as a surface tcnsion
catapult. ft is fascinating IMt esselllial!y the samc mechani sm is found in the bas idia of
mushrooms, jelly fungi. ruSt fungland some ye~sts. II is a HfOng argument for the monoph~'ly of 'he Basid iomycetes.
If you want to follow the extended trail of experiment (tnd observatiun that led to
the \.Current CXpIUn:ltion. I recomm~ nd that you read Mon~y. KP. (1998) ' More g 's than the

Space Shuttle: ballistospore discharge' Mycologia 90: 547-558. There is also new evidence that some mushrooms chill their fruit bodies by evaporative cooling. This enhances condensation on theiT spores, which apparently need a layer of free water if the
shooting mechanism just described is to work [see Husher et aI. (1999) 'Evaporative
cooling of mushrooms' Mycologia 91: 351 -35 2)
Gasteromycetes, if they have bymenia, don't expose them when the spores are
mature; the spores ~ symmetrically placed on the sterigmata, and are never actively shot
away. I believe that the basidium originally evolved as a spore-shooting mechanism, but
that for various ecological reasons, which we will explore, it has on many separate occasions lost that function. So our assumption is that the various kinds of gasteromycete have
emerged independently. on many occasions, from among the Holobasidiomycetes.
Oberwinkler, an authority on the classification of the Basidiomyce te~ has recognized
nineteen Orders of Holobasidiomycetes, but I will discuss only ten (and give a key to
them later). Why the difference? He subdivides what I cal! thc Order Aphyllophorales
(bracket fungi and relatives) into si)"; Orders, what I call the Agaricales (mushrooms) into
three , and recognizes one or two obscure Orders I did not feel it essential to enumerate
here (Only if you become a professional mycologist will you have 10 think about the
possibility that there may indeed be nineteen Orders of Holobasidiomycetes!) First, two
'outlier' or atypical Orders:
I) Order Exobasidiales: 10 genera, 67 species. This Order is atypical in much the
same way that the Taphrinales was atypical of the ascomycetes. Unli ke most other
holobasidiomycetes, Exobasidium doesn't produce a fruit body (a basidioma) - just a
whitish layer of basidia on the surface of the host plant. The host in this case is a member
of the Ericaceae. Other E)";oba~idiaJes occur on members of the family Commelinaceae.
Ex()hasidillm produces symptoms like those caused by the Taphrinales - excessive growth
of the leaf tissu es, and disturbances in photosynthesis that often cause the leaves to turn
n::d. This has led to speculationJhat these two Orders represent some kind of connection
between the subphy la.
(2) Order Oacrymyeetales: I! genera, 72 species_ These are all 'jelly fungi: again
atypical of the elass. that grow on rotting wood. Their gelatinous, yellow basidiomata are
common and conspicuous in wet weather, but shrivel up and almost disappear in dry
periods. The basidiomnta of Dacrymyces are irregular to the point of 5hapelessness, and
look like those of some Phragmobasidiomycetes (the real jelly fungi) - a quick look at the
basidia (Fig. 5.'4 B) will settle the issue. Basidia of Phragmobasidiomycetes are septate.
but dacrymycetalean b~sidia are not. They have a unique appearaoce: we call them tun,


Fig 5.3. Current explanation 01 basidiospore discharge mechanism, from N.P. Money, 1998.



ing fork basidia because they develop two long arms that grow up to the surface o f the
jelly, where their basidiospore s are produced and shot away. The basidiospores arc a1so
unusual in becoming multisep tate (phragmosepta\e) after liberation. The gelatinou~ fruit
body of Dacrymyces plays a double role in that it often produces an unnamed tha llie arthric conid ial anamorph (Fig. 5.4 A) before the basidia deve lop. The ba.~idioma of
Guepjnjopsis is more shapely than DacrymyCt!s. and a translucent gold in colour. On the
west coast it is common on rotting branches in fall.
(3) Order Aphyllophoral es: 4OOgenera. 1,200 species. 'This isone of the larger and
more poorly defined grouP$ ofhymenomycetes. and one of the most diverse. Its name can
be translated as'without gills,' and it seerns to be designed as a catch-all for hymenomycetes
that don'l fit into the fourth Order. the Agaricales, which hou ses the mushrooms with gills
or fleshy rubes . So the AphyUophorales currently embraces eight families with conspicuous but different basidiomata - the dub and coral fungi, the tooth fungi, the chanterelles
and the horn of ph:my_ the dry rot fungi, the paint fungi, the 'split-gilts,'and the bracket
fungi. Mos t are saprobic on wood, and while they do us the favour of scavenging On fallen
branches or logs and recycling the nutrients in these, they are equal ly at home attacking
either the structural timbers of our houses. if we allow these 10 become damp. or the wood
and roots of living trees. A few are ectomycorrhizal (see chapter 17). This Order is almost
certainly heterogeneous_ and will evemually be split up.
a) Family Coniciaceae. The basidiomata are o ften effuse or resupinate (spread out).
on the surface of decayin g wood . The hymenium may be smooth. wrinkled or toothed.
and the b~sidiospores arc smooth in outline, colourless or pale. and non-amyloid. ,
The members of this family are sometimes called 'paint fungi.' The spread-out
basidioma of Aleurodiscus fUnjcillatlu even has the cracks you associate with old paint.
Remember thai even though it looks simple. a paint fu ngus may have a complex internal
struclUre . ltS microscopic structure is often intricate. The basal tissue is usually comJXIsed
of only one kind of hypha. and is thus described as monomitic. but in so me taxa the fruit

A . .... amo rph

F.g. 5.4 Dacrymyceta!es: Dacr ymyccs stillatu5.



~!l 1 6L!OI eCtl


bodies are di.mitic, with thin-walled generative h>-phae and thick-walled skeletal hyphae
(Fig 5.6). The hymenium may also in~orporate specialized aeet.sot)" ste rile hyphae (e.g.
crystal-encrusted cystidia (Fig 5.5A) Sl.I<:h as those in Am)"/osle1tmn, which also has what
is known as a ' thickening' hymenium that produces successive crops of basidia). These
are fungi that richly repay microscopiC study. Despite this, relatively few mycologists
ha\'c tangled with them, though my mentor, Lue!la Wcresub (\\hose memory I sci!! trea sure. though she died in 1979). was one of them.
Anamorphs of th is group of fungi may be Iha!1ic-anhric conidia produced when
clamped hyphae disarticulate at the septa. as in the OSleomorpha anamorph ofTrechispora.
or more specialized con idiophorcs producing blastic-sympodial conidia, as in the unnamed anamorph of SiSIQrrtma (see Kendrick and Watling 1979).
b) Family Thelcphoraceae. These are like the Corticiaceae in many ways, but most
fruit on the ground rather th an on wood. The basidioma may be resupinate (spread OUI) or
fan-like or stalked. and the hymenium may be smooth. warty or toothed. The basid-




, ),


. ,-


fig. 5.5 Represel1lillive Aphytophorilles.




iospores are irregular in shape, ornamented, brown to colourless, and nonamyloid. The
dark tissue give~ a green reaction with KOH (10% aqueous potassium hydroxide) _
Thdepllora terresfris (Fi g. 5. 5 B), with brown. fibrous. vase-shaped basidiom~!a and a
smooth hymenium. often establishes mycorrhizal relationships .... ilb young oonifers in
tree nurseries (see chaph:r 17).
e) Family Clavariaeeae. Club and cora! fungi. Arising from the ground or from
wood, the erect, beige, yellow, while or purple busidiom:ua may be unbranched and clubshaped, as in ClamrimfelphU$ (Fig 5.5 E), clustered. as in C/(IIaria and CI(IIulinupsis. or
repeatedly branched and coral1oid. as in Ramana (Fig 5.5 E). Th ey are monomitic or
dirnitic. The hymcnium covers the uppe r pan of the basidiOffiatil.. and is no! put OUI of
action by repeated wetting, as those of most other hymenomycetes would be. Basidiospores are colou rless. smooth, and non-am>loid.
d) Family Canthare!laceae. The basidiomata are monomitic (coostructe<! from a
single kind of hypha) and arise from the ground. They may be yellow. stalked and ra!h~r
mushroom-like. as in Camharellu$ cibar;us (the 'chanterdlc' or 'pfifferlingc: Fig. 5.5 D),
though the hymeniurn is thrown into thick, fleshy folds which only sup,;,rlicially resemble
gills. The cap of the more deli~ate (bu t still edible) Can lharellus 1:,b(U!Ofl/l;.\ is umbihcute (that is. it has a central. navdlikt depression). Basidiomata may also be: large and
highly convoluted. as in lhe edible Spumssis. the cauliflower fungus. which can actually
be much brger than any cauliflower I've ever seen. The edible 'hom of pknty,' CmltrdlU5.
is often almost black, and has a rather smooth hymenium. Gcmplws looks rather chanteIelie-like, but is nOt edible, The bas idi ospores of !he Ca nth JrelJacca~ ure smooth.
colourless and non-amyloid.
e) Family Coniophoraceae. Thll monomi!ic basi diomata usually appear on wOPd.
and the hymenium can be: smooth. toOthed. folded or tubulate. That of Serpula laCT)"IJiJJs,
the dry rot fungus, is d impled . The basidiospores are smooth, bro" nand double-wall:d.
Sapl/fa and Coniop/lOnl (the ce llar fungus) cause scrious rots of strt!~t urallimbc: r.;. and
Serpu/a can e\'en grow through brick wallS to find suitable substrate_
f) Family Hydnace~"" Th e tooth fungi (Fi g 5. 5 C). The hymenium covcrs tupcring
tceth that point vertically downward. like miniature stalactites_ The basilliomata may ~
ra!h~f irregulur and e)(centric, as in H(ricillllJ erinacells (the wood urchin. which froits on
the sid~ of trees) and Heridmn coral/oidu. or very mushroom-jik. as in D~nlinllln
( Hydnum) relxmdmn. the edible 'heds-ehog mushroom' or s,,eeHooth: Aurisco/piulil
I"II/gare, a dcJ:cat~ mem~r of th~ Hydnaceae with a lon g stipe al\d an e ,centri c cap. frUl t~
on decaying Douglas fir cones. 1'.hny corky or "oody spccie~ of H:.dnellum gro" Oil the
f(lrest floor. ufte n developin:; around and engulfing ccnifer necdle~ and twigs Sarcodmi
i, large, wi th a scaly cap 3011 a dark stipe. The spores o f thi $ family are imooth, colou rless.
and nonamyluid.
) Family S<:hi zophylbceae. The common (amI therefore succe"ful) Schiwphyll"",

commune ( Fig. 5.5 F), often seen on dead branches. looks like an agaric without 3 Sialk.
but is Ie;' !!y 0 compound fructification, in wh ich tll ~ inroned cdg~ ~ of contiguous cupu
!at~ i).asidiomuta give it its mislead ing common naln.:, split gill: This sp..'Ci.:s is easil~
grown in culture, and is a popular subj~ct for gnetic rcse3rch.

h) rami!y Polyporaceac. The bracket oTshclffung i_ These are fr~quentl)' dil'ided up

into !;e'eral f;:tmilies by modem aUlhor5 (see discussion of generic CQncepls, below). The
ba~idiomata usuall y ari~ c on wood. and may persist for seyera l years. Th;: undersid~ of the
fruit body is generally riddled with thousands of poro!s. the openings of ~erticaltubes
which are lined with a basidial hymenium. Since the pores may be a couplc of centimetres
d~ep. this is u very efficient W:ly of increasing hym~nial area. Larger spedes with peren

nial f\\lit bodies also add a new layer of tubes each year and may eventually become
almost a metre across, so spore production may reach astronomical numbers,
Bridgeopoms (Oxypon/s) nobilissimus is a rare and threatened species found only
in oldgrowth forests of the Pacific Northwest. United States law now mandates that 240
hectares (600 acres) of forest must remain undisturbed around each known site of this
fungu>, Progress! A basidioma of this species was fonnedy noted in the Guinness Book of
Records as the world's largest fungal fruit body, but it has now been supplanted by a
specimen of Rigidoporus u/mnrius that is still growing actively at teew, England, Po/ypoms
squamosus, the Dryad's saddle, is 'easily recognized by the conspicuous scales on the
upper surface of it> fruit body and its relatively soft texture. Fornes fomenrarius has very
tough, hoof-,haped basidiomata. A few polypores, such as Laeliporus sulphureus, which
produces spectacular orange and yellow fruit bodies on fallen trees, are soft enough when
young to be eaten (conunon name: Chicken-of-the-Woods), though they should be avoided
if the substrate is Eucalyp/!ls. Albmrellus ovinus is another unusual polypore which looks
very like an agaric, grows on the ground, and has soft flesh. The pores are very narrow and
shallow. Heteroba.lidion annosum is highly pathogenic to many conifers, and causes
serious root-rots. I have seen a forest clearing produced by this fungus: it had killed
represematives of fourteen different conifers, many of them introduced species. PipIOporu,~
b,m.!inuJ, on the other hand , kills ouly birch trees. Tmmetes versicolor (often called the
turkey tail) is one of the smaller and most conunon saprobic polypores.
Like many other fungi, polypores often have anamorphs (see Kendrick and Watling
1979), though these may be very inconspicuous. Heterobasidion annosum has a
hyphomycetons anamorph in the genus Spiniger, which forms many conidia synchronously on an apical vesicle. The Ptychogaster anamorph of Trameles fOnTIS altemateanhric conidia (to review conidium deYe\opmcm, return to chapler 4).
Many polypores, e.g. Poria, Po/yporu$, and Ganoderma, may not kill trees, Ihey
cause serious decays of both standing and structural timber. These rots cost us many
millions of doll ars every year. The general division here is into brown rots, where only the
cellulose is digested. and white rots, where both ceUl.llose and lignin are metabolized.
Collricia cillnamomea, a centrally stalked, ground-fruiting polyp<Jre. is atypical in being
ectomycorrhizal (see chapter 17)
The generic concepts among thc polypores have changed a lot in recent years as a
resuh of extensive anatomical and enzymological research. and identification is rather
difficult for the amateur. How do we ddine genera in the Polyporaceae?
To the uninitiated, most polYp<Jres tend to appear rather similar - a bracket-shaped
excrescence on a branch or trunk of a tree. Most of the bracket fungi were at one time put
into the genus PolYPoTHs_ No more! Mycologists now recognize almost 100 genera of
bracket fungi. Why has this plethora of names becn imroduced? It is because a 101 of new
microscopic and biochemical characters have been recogni7.ed (which certainly doesn ' t
make life easier for the student). These characteristics arc as follows:
(I) The kind of hyphal system. All fungal fruit bodies arc built up of hyphae, but
those of poly pores can have as many as three different major kinds of interwo,'en hyphae,
and are calkd monomitic, dimitic or trimitic, according to whether they haye one. two or
three major hypha! systems _Monomitic fruit bodies are made up of what we call generatiye hyphae, which arc septate, can be thick- or thin-walled. and mayor may not have
clamps. Mosl such sp<::cies are rebtively soft in texture (e _g., the white cheese polyporc,
Tyromy(u chioneus). Dimitic busidiomala have two hyphal systems, the generative being supplemented by either thick-walled, non-septate skeletal hyphae which give
basidiomata a hard. tough texture (e.g., the artist's conk, Ganoderma applanal"",), or by
thin-wall ed, highly branched binding hyphae (e ,g" the sulphur shelf. LaetiporuJ






sulphureIIS). Trimitic basidiomata are composed of generalive hyphae. plus skele tal
hyphae, plus binding hyphae (e.g., the turkey lail. Tramell'S versicolor) (Fig. S.6 - afte r
HJ. Hudson, Fungal Biology)
(2) The kinds of digcslin or degrndalh'e enzymcs produM by the fu ngus. Brown
rot fungi digest cellulose bUI IK)llignin. White I"Q( fungi digest lignin. but tend to leave
some cellulose. Mycorrhizal fungi may not degrade wood .11 aIL
(3) The septation of the generative hyphae, In some species they are simple septate, while in olhers they are regularly damped.
(4) The kinds of cystidia produced, and th eir origin.
(S) The reaction of basldios pores with Melzer's reagent (they are amyloid [stain
blue) in BOlldaruwia, dextrinoid [slain brown] in Perenniporia).
(6) The size, shape, ornamen tati on and watls of basidiospores (spores h~ve a
troncate base and a double wall in Ganodenna, are minutely spiny in Ht/trolxuidion).
Perh~ps the best keys a\'ailable are \0 be found in the two-volume NOr/h Americoll
Polypores by Gilbertson and Ryvarden (1986,1987; Funginora. Oslo). but many mush.

1___ Generative hypha

___ Skeletal hypha

_ _ Bind ing hypha

10p.m I

Fig. 5.6. Diagram of trlTitic hyphae (after H.~ Hodson, FlIgillBiOOgy, 1986).

(iJ u~PECel

room field guidl:s also contain relatively good co'<ernge of polyporcs, and if you incluck
these persistent (ungi among your collections, you will come home with something inleresting at any time of year - eyen in the depths of winter, or the dri~st month of summ~T_

Agarica les and Gasteromycetes

4) Orde r AgariClIles: 300 gener:!. more than 10.000 specks. This Order bring~ (0gcthM" the most familiar of all fungi, the soealled mllshmoms and toadstoob. Since no
two people agrc~ 011 the preci5~ dividing line between these two categorics. it is better to
call them all agarics. the term used by the knowledgeable. among whom you should soon
be numbered if you are receptive to the material in thi s section.
Compared to polypores. agarics are relatively ephemeral. the basidiomata persisting for anything from a few hours to a few weeks, depending on the species. They occur
seasonally. fruit ing mainly in laiC summer or fall, thoogh on the west COOSt of North
America they can be found in almost any month of the year. The Mycological Society of
Son Francisco holds its annunl Mushroom Fair in December. when agarics are only memories in :'>1inne5ot3 3nd Manitob3.
Agaric fruit bodies arise fmm an extensive, perennial mycdiurn which r~ mifies .
in,isible to the eye, through soil, plant debri s or wOOf.!. gathering energy for th3t once-ayear (or Qnce-e \"cry-se.vcral-ycars) splurge. Some fairy rings (which are fe3ily enormous,
radi~ll)" exte ndi ng fun g~ l colonies) arc estimated 10 be over 400 ye~rs old. and h~'e
presum3bly produced noshes of b3sidiomata in many of those >ears. A single colony of
Armilfari<l os[oym: growing in the forests of wc,tem North Am erica has been found to
co~er 600 hectares, and 10 h3' e biomass exceeding that of 3 blue whale. Such colonies arc
prob~bly at kast 1,000 years old.
Most agarics are either sap robic. exploiting dead org3nic maHer. or
l'l:lomyeorrhi7,al. establishing mutualistic symbioses with th e roolS of woody plants.
~~p.:ciall y conifus of the economicall y importont family Pin3ceae. Thb explains why
woodlallds arc often such cxcel1ent place~ to look for :l3ries. A detai led discussioll of tlh>
cctomycorrhizal relationship is given in chapter 17. Only a few genera. such ,IS Armillaria,
arc p~[~sitic. and even lh~t notorious genus (see ForCSI Pathology in chapter 12) is sometime, ~!probie _
:'>!ost agarics share the same basic design (F ig. 5.7 A-D). There is a e<:ntTal. venleal
stalk or stipe. with a horiZOnt311y spreading C.:lp or pileuli 3tthe top_ The underside of thc
<;ap usually bears delicme. radia lly arrangcd. verti cal plaws called gills or tatncll~ e .
thou::;h some h3'e vertiClll fleshy tubes inslead. The hymenium CO'CIS both sides of each
gill. or hnes eoch tube. B.:I;;i d io~pores arc launched from the basidia. drop through Ih~
space XI" ~en lldjacent gills, and enter the more turbutenl oUI~ide air whil'h carries Ihem
3\\'3). In so me genera. forex3mplc Am(lnita. the dcveloping basidiom3 is totally enclosed
within a mcmbmnous univeTs:d "eil. rem3in $ of whkh can be seen on the m3ture. e.\pall(kd .:I.:;;aric in the form of a she;l1h or ,oha aTOlJod the base oftbe supe. and spots. warts
or patche. 011 th~ ,ap. Thae may also he a partia l H~il connecting the stipe nnd (hc edge
of the CJp in young spccim~ns. c!!closillg ;md protecting !he de,-eloping gills. This. too.
m.:l) remaIn o n the stipe of the m3(Ure, exp3ndcd agaric as a mCJlltw.lnous r ing or anllulus
(as in AIIUlll iw lint! AgaI"iClJ,). or ns a filamentous, cobwebby veil or corti!!a (as in
Corl;""riIlS). A fc\.\ ag3r1<::S have both ring and voka: !>Ome olhers ha'e ooly one of these
fC:lllIrC" and the majority ha\"e neither.
Agarics are complex. rather variable structures. nnd have many other laxonomiC3liy
valuable features. The che<: k:- list given below includes mJOY (thou gh nOI nearly al1) of
them. ~nd show s the kinds of information we need to coll~ct in order to clas.sify thc
thou53J\ds of different agarics. If you arc going 10 m<lke 3 serious stab at it. you could do


worse than photocopy the chart on page 90-91 and fi ll in as many of the blanks as )'ou can
before going to the books. or to 3 mushroom identification software program such a~
If you 11)' to fi nd :lll of th ose characters in a number of agarics (admilledly a counsel
of perfcction). yoil willieam 3 tremendous amount abom them, In fact. you C:ln usu:llly
idemify them 10 ge nus wi th a sm:lU fraction of those c haracters. lhdugh getti ng the m to
species will probably call for muc h more information. If you read "",hat follows. in which
I introduce you to representatives of si~teen fami lies. you will sec which or the characters
m"ntioncd above arc the most important in se parating them.
a) Family Agruic:lceae. The genus AgariClu (Fig. 5.7 B). to wh ich the supermarkct
mushroom belongs. (I) has a ring. (2) lacks a vulva (that is. it has a partial ,'ei! blll no
universal ve il), (3) its gills are no t attached to the stipe (they arc described as free). and (4)
its spore prinl is dark. Other members of the fami ly such as Ullcoagari"IIS may h:lve spore
prinl~ of different colours. but they are never rusty brown or cinnamon. Leuco(:lgaricus
IIIHltim's. whic h ;s common on law ns. is all aU-while or c re<lmcolollred :lgaric wlth a ri ng.
but no vol va. 11 has an uncomfortable resemblance to th~ deadly poisonous Amauila
I"iro.w, so although it is no! dangerous (edible to some. a gal;tric irritantl00lhcrs). [always

'~ --1

S_ Ap ......

'Fig. 5.7 Ag,lricales.

C, Copt/tWS


D: Bolo/us



Locaflty:_ _ _ _ __ __ _ __

~ IDate:'

_ _ _

Habitat notes:
sol t ype
soil pH:_
vegetationalcommunity:_ _ _ __ _ __ _ __


solitary / in troops / in rings / on ground / on wood / on living tree/other

(Photograph, draw or preferably paint general view and vertical section of fruil-body)
CAP (PILEUS): Diameter: (range) _ - _ em
Shape: convex / bell-shaped / conical/ umbonate / flat / depressed / umbilicate /
(whenmature) _ _
funnel -shaped/cylindrical {when you ng)

Surface colour: when imma"t~":",===::-;0,when mn~"~":,.,===__

when wet_
when dry_
Surface texture (circle oneor more): dry / moist/ greasy / viscid / glutinous/ peeling
easily /smooth / ma tt / polished / irregularly roughened / downy / zoned / velvety /
scaly / splitting / shaggy / with valva fragments

Margin: (choose one or more) regular / wavy / upcurved /incurved/ smooth / rough /
furrowed/ striate / split / shaggy! with veil fragments
(c hoose as appropriate) remote / fre e / adnate! adnexed / sinuate I decurrent /
crowded/ distant / forked / anastomosing
Easily sep<lrable from the cap-tissue: Yes/No
thick / thin
consistency: brittle / pliable / fleshy / waxy
Colour: when immature
atmaturity_~~-,Number of different giD lengths (series) _ or number of tube layers _
Obvious featuresof ginedge, tube-edge, e.g., colour (esp. if different from rest, i.e,
marginate); outline - smooth I jagged _ _ __ _
central! offcentre! absent / hollow / solid! sluffed (with cottony mycelium) /
tapering upward / equal (not tapering) / rooting
Dimensions: length (range) _ -_ thickness _ - _
Colour: when immature

at maturity' _ _ _~

Consistency: fleshy / stringy /britt le / cartilaginous{flexible} /Ieathery (tough) /

Surface: fibrillose / dry! viscid/ scaly! smooth
Characters of stipe base (e.g., swollen, rooting, etc.},,______ _ _


VOL V A, if present: sheathing stem base I scurfy rings
RING, if present: single I double I membranous I filamentous I persistent I fugacious I
moveable I thick I thin I apical! median I hanging (skirt-like)
FLESH: colou-: inside cap: when wet
when dry
insidestipe: whenwet
Colour changes when exposed to air:
Milk -~ke latex: presentl absent
Colour when exudedl-====~':fter exposlXee:'0~':;'':::===
Smel beforecuttr,g _
after cutting
Colour: in mass (spore print)_ _ __ _

Shape: spherical I ovoid I elongate I angular I clXved : size range _ -_

~ ~ -_


OrnameotaliOll: none I warty I r()lJl(.!ed I pointed (spiny)I ridged I striate I net-&ke

Sizeandshapeof germ-pore, if present _ __ __ _ _ _

Iodine reaction of spores: blue-black to dark violet (amyloid) I red-purple (dextrinoid) /

yelow-brown or brown (nOll-amyloid)
BASIDIA: length:width ralio - less than 4: 1 I more than 5: 1
runber of sterigmata_

CAP TRAMA: typesof cenpresent _ _ _ _ _ _ _ _ __

GilL-TISSUE (TRAMA): type and arrangement of cetlsbetween adjacent hymenial
faces: divergent/ paralellconvergentfl1terwoven
(These tramal characters are not easy to observe, but jf gins are sandwiched
between two microscope slides placed at right -angles to DOe another and s6ced
with a new razor blade, the resulting sections can be revealing_)
CAP-SURFACE (P ILEIPELLlS): cells of outer layer: filamentous I rounded
SPECIALIZED STERILE CELLS - CYSTIDIA: present on: ~-face I gil-edge I cap l stipe
Shape: fiform I cyrl!ldrical I clavate I ventricose I branched (sketch here)
Size_- _ , _ -_


thick-waned! thin-waned I colourless I pigmented

other feat l.XS;_ __ __ __

~ U ~P EC C~

~B I 8 L! 'JT E CA


advise people agaiMt making a mcal of it. Up/ora dypeolaria has a scaly cap and a ring.
both typic al of the genus. Macrolepiora rachodes is a much larger, edible species. Again,
note the large cap scales and the conspicuous ring. This species was placed in vpiora
until rentl y. Endoprychum is a scquestr.ue derivath'e of Agaricus. The gill cavity never
opens. and the gills themselves are convoluted and spongy - a totally inappropriate
configuration for dropping spores into the air.
b) Family Amanit:l~~ae. All members of the genus Amaniw (Fig 5.7 A) have (I)
wbite spore prints, and all ha\'e (2) a universal "eil and (3) a partial ,'eiL MOSt therefore
have a ring and a volva at maturity, as in Amanila calyptra . However. these generali zations camouflage ~ lot of vari abi lity, especially in the vol va. (4) The gill tramR is divergent (Fig. 5.7 E). (5) the gills are often. but not always, free (not auachcd to the sti pe). In
some species. e,g., Am(lJlila muscaria, at maturity the vol,'a is reduced 10 scurfy rings
around the base ortbe stipe. Howevcr. the upper part of the univc rsal veil oftcn bn=ah up
into SPOB, warts or patches on the cap as the frui t body cxpands. These are an excellent
due to the prior existence of a univcrsal yeil. and are partic ularly obvious in AmlJnita
mrlscaria. In Amoniuriuiwi Honncrly placed in me genus Atn<1niIOpsis) the ring is essenti31ly absent. The volva is conspicuous. but splits cleanly and so does not leave patches
on the cap.
Becausc some AmaniIG species an:: dcadly poisonous (see ehapter22). the genus has
",,-en made me cover of 'Scientific American: and mushroom huntcrs (especially those
pllnning to eat what they collect) should always make sure they get to the base of the
stipe of any agaric they pick. so they ca n see whether or not there 'S u volva. Th e 'destroying angcl,' AnI/mila l'iIVsa, is pure white. with ring. conspicuous volya and even a wbitc
spore print. But this species. like A.fuim. does nOI have spots (p.ltches of universal veil)
on the cap. Like most other mem bers of the famj!y, thi s lethal species (see chapter 22) is
ectomycorrhi zal. and so [nllts on ly n",~r tree species with whic h it i, symbiotic (see
ch3ptcr 17).
Temrilotn)'Cts. a saprobic genus. is involved in anO(her !tind of mutualistic symbiosis: with mound-building termites in Afri ca and Asi a. a relationship discussed in chaptcr
16. Irs frui t bodies arc al so widely eaten - sec c hapter 18.
c) Family Bolbitiaceae. Basidiornata of the genus Balbi/ius are small and ephemeral. since their tissucs autol yze (sc lf-digesl) at maturity. (I) The surface layer of the cap
(the pileipcllis) is epithelial (the cells are swo!len. and don't appear filamcntous). (2) The
spore print is ochr;rceous to ru sty brown. and (3 ) the spores havc a gcnn pore. Representath~ genera are A,~fOC}'be, Bol/Jilills. and Cl)nocybe. CQ',oc),be fillJris contains deadl)'
am~toxins (sec chapter 22).
In addition to nonnat ag~ricoid species. the Bolbitiaceae has sequestrat~ members
\\ ith b;rsidia thaL don' t shoot their spo re~. Th e genu~ Guslroc)'be st iII looks like an agaric.
but its spores are symmetrically mountcd. its C,IP does not ope n. and it has a habit of
falling over as soon as it comes up. The~c fealllre5 show that it is e'-en now acti,'ely
",\ol\;ng. and that its spores are not wimldispased.
d) Famil)' Copri naceae, This fami ly also has ( I) a pileipellis ofswol1cn cells. but (1)
th: ba~idio$pores are usually black and smooth. and (3) have a genu pore. :Vkmbers of the
ad'~n~d genr.:s Coprinus h:tve weed-like vigour and opportun ism. pionecring tho: exp~vit.:ltion of such habi tats as recently di sturbed ground and dung, The be,t-known species. Cop rimlS COIII(l/US (Fig, 5,6 C). the 'shugg)' man e' or 'shaggy ink cap,' has a co mplex
SCt of physical arrangements and 3. precisely timed o;cquel\Ce of events during spore liberation th~t make it one oftb.- most advanced of all agarics. It is ediblc. but only when young.
"hen thc gills are still white. Later they tum redbrown. then bI~cI::. an d melt away from
bo1!om to top. This behaviour is described in detail in chapte r 8. Capri" us arramClIIll rius


is anomer edible species. but il musl nO! be washed down with alcohol. The reason for this
prohibition is exphined in chapter 22.
Coprinus plicatilis is one of many small, delica te specics. some of which gro",'
specifically on dung . More details about fungi that specialize in e:<pioiting this subs trate
can be found in chapler 11. I h:l.Vc ~en a sequestrate member of Ihis family. Pwaxis,
fruiting in desertS on three contirw:nts. II looks very like Copril/us comalUS. with black
spores: but it ha.s no Tecogniable gills and doesn't autolyze. The spore mass is dry and
dispc::rses only when the fruit body disintegrates. Though some taxonomists erected a
special Gasteromycete Order for Podaxis and similar fungi, ! treat it as a sequestrate
member of the Coprinaceae. with an appropriate common name 'the desen shaggy mane.'
It simplifies life to do this. and [belie" e it also emphasizes the U"\Ie relationships of these
e) Family Coninari aceae. Here (I) the cells of the pileipellis are fiiamentous, neWT
swollen. and (2) th~ basidiospores are rusty brown and often (3) roughwalled. Coninarill$,
Cll/edllG, Gymllop i/lIs, Hebeloma. lnocybe and RQ~ites are representative genera. The
besl known ge nus is Corlilwrill.!. often ca~ily rccogniz~d at Ihe generic level by its
unusual partial veil. which is called a cortina (cunain) - numerous indiv idual fil amems
streIch between the stipc:: and the edge of the pileus as it c)(pands. After the cortina ruptures. the filamenrs can often be seen on the stipe. usually coloured brown by spores that
have fallen on them. Cortinarills is a ~'ery large and div~rse g.::nus, with perhaps 2.00Cl
species, most or all of whkh are ectomycoIThiza!. Identification to spedes is usually
almost impossibk. because !h~ necessary monographs have not yet been published. In
fact. COrrillGriliS is so large and unwieldy that it is now generally subdivided intO seven
groups. more or Ie~s as follows:
(I) 1o.lembers of Subgenus Coninaril<$ have warty spores, ,ystidia. and the.:fruit

bodies are oftcn s~lurat~d with a purple pigment that is differcnt from the pigments found
in the other groups. Only a few species afe now placed her~. bll\ tb~se indlldc the ",eU
known Cortillari." via!a,e/lS.
(2) Members of Subgenus My.wdllm h<lve a slimy cup and a slimy stipe.
(3) 1o.1embe.s of Subgenus Phiegl1lacillm ha\'e a slimy cap, a <.Iry sfipe and a bulbous
(4) ,\-!em bers of Subgenus Tdamoll;a have a dry. hygrophanous cap. and the ,ap
tissue blackens in KOH.
(5) Members of Subgenus Lepmcybe have n dry, non-hygrophanous cop. and luck
anthraqulnonc pigmcnrs. All de~dly poisonous cortinarii arc membo:rs of this subgenus.
(6) 1o.lembers of Subgenus Dennocybe ha ve dry caps. and are saturated with waler
soluble nnlllrllquinonc pigments - the gills are especially brightly pigmented.
(7) 1o.1embers of Subgenus SI!T;C<!ocybe have dry caps with a silky .urface. and 3rc
non-hyg rophanous. They are often difficu lt to separate from the Tc \amon ias.
Some species of Corlill(lr;u.! subgenus Leprocybe are insidiou$ly poisonous because Ihey contain tfu? lox;n orellanine. You C:ln read the rather horrible details in chapter
22. Many H(/)e/OIr.n species afe tctomycoIThiza1. Gaierilla aumml/ali:; is a smull but
deadly poisonous. amatoxin-containing species Ihat grows on rOUcn \\'ood in Norlh
Amenca. Mo~a species of the ectom ycorrhi zal Inocybe are also poisonous because they
cQntain mtlscarin~ . ond GYlliliopilus specwbiliJ' sometimcs contains the halludnogen
psilocJbln (seechaplcr22). But at ]cast one meml>cr of the Coninarlaceae, RO~;leSCllperat(l,
is a well-known and highly regarded edible (sec ,hapter 18). CrepidO/lls is atypical: il is
one of a fairly small num ber of asymmetrical or fan-shaped agaric~ in which the cap is
laterally attached to Ihe substrate and has liule or no SlipI.'.

Some members of the Coninariaceae have become sequestrate. The genus
Thaxluvgasler closely resembles Conioorius in many ways, but its cap never expands,
and its gills have become so convoluted thai even if they were 10 be exposed, they cou ld
not successfully drop many spores into the air. I have often found a beautiful purple
species of 17raxterogasrer in the Southern beecb (Norlw/ngus) forests of New Zealand. A
brown species of Tha:rrerogaster Ihat I also found in New Zealand had even lost its
ellternal slipe, and looked rather like a puffball, though a vertical section of the froil body
revealed a central column of stipe tissue - the transformation slill isn't comp lele. The
stal ked_ brown-capped ThaxlerogQSlu pinsue occurs in wes tern Nonh America.
HymenoglU/u is another sequestrate derivative of the Cortinariaceae.
Family Entoloma~. ( I) The spore print is pink to salmon-coloured. and (2)
individual spores are e:ureme1y angular or sometimes longirudina11y ridged; (3) the gills
are altached to the stipe. En/oloma, Nolaneo., Lepfonio. and Cli/opi/us are representative
genera of this mainly terrl colous (grou nd-fruiting) family. Most species of the mycorrhizal g~nus Ellloloma contain gastro-intestinal irritants, and some can cause serious
poisoning. Ellt%ma abortil"llm is a common specics in whlch nonnal fruit bodies are
ofte n accompan ied by lumpy, rounded. misshapen ones. We now know Ihal the latter are
being anackcd by anl)(her agaric, Am/illaria mellea (fricbolomataceae), whose basidia
can be found in them. Theeasily recognized parasitized basidiomata are edible. El1lolo11UJ
has gi"en rise to a sequestrat~ offshoot, Richonitlla, whose basidiospores are angular.
clIactly li ke those of Entaloma, and unerringly reveal the evolutionary origin of this
seq ucm:uc fonn.
g} Family Pluteaceae. (I) The spore print is pink, like that of the Ento lom ataceae.
but (2) the spores are ellipsoidal and smooth, (3) the gills are free (not attached to the
stipe). and (4) the gill tissue or Irama is convergent. The lign icolous (wood-inhabiting)
genus PIUleus has 100 species. of which P/llleus crrvinus may be the most common.
Pcmaps the easiest way to make an unequivocal i<kntification of this species is to squash
a tiny pl~ce of a gill un<kr a coverslip on a 3 x \" glass slide, and eumine it under a
micror.cope. This should reveal what wc call 'comute cystidia,' large cells bearing apical
homlike projections that are unique to the gills of Plllltus ctnoinu.!. They are one of the
excellent reason s that those studying mushrooms should get hold of a microscope if at all
possible: il can sometimes mill identification really easy.
Voll"uriel/a "O/I'lIcea, the straw mushroom. though not nalive to North America. is
the Ixst-known member of the genus. since it is widely cultivated in the Far East (see
chapter 18). NellI time you eat mushrooms 11.1 a Chinese restaurant., see if they belong to
this sptcies - you can easily spot the persistent volva almost enclosing the whole
basidioma. I got some living speci mens of thi s fungus from a mushroom grower in Java,
and later watched them optn and make a profuse pink spore print.
h) Family Hygroplloraceae. (I)The basidia arc long, (2) the spore print is white. and
(3) the gill lrama is div\!rgent or parallel. Species of Hygrocybe. the most common and
conspicuous gellus. have parallel gill trama (Fig. 5.7F). are usually ye llow, orange or red.
and haw a very charactcristic ""uy, tr.mslucent appearance. Species of Hygrophorus. {hc
other ~enus of the family, have divergent gill trama (Fig. 5.7E). often have a partial veil.
and are white. grey or brown. (Divergent gill trama '" Hygrophorus. parallel gill trama '"


i) Family Strophariaceae. A saprobic family that contains many 'magic' mushrooms.

(I) The spores are purple-blaekor brown. (2) are smooth-walled and (3) have a germ pore;
(4) the pileipellis is filamentous; (5) the gills are attached to the stipe and (5) often bear
accessory cells called chrysocyst idia. which have contents thai stain yellow in alkali.




Some species of Psilocy/n (e.g., P. culnnse) and Stropharia Cootain the hallucinogen psilocybin, and the flesh of such spedes often tums blue when bruised. It is easy to
grow Psilocybecubense in culture, but for some peculiar reason possession of psilocybincontaining species is illegal. This topic is explored further in chapter 22. The nonhallucinogenic gcnera Pholio/a and H)'phowma usually fruit on wood. Sequestratc derivatives of the Strophariaceae found in New Zt~land and Australia are placed in the genus
j) Family Tricholoma[aceae. This is the largest and most diverse family of agarics,
with o 75 genera. It is not a 'natural' fanlily. and is now in the p~ss of being subdi
vided. so we can make only a few generalizations about il. (I) The spores are white to pink
in mass, and (2) have no germ pore; (3) Ihe gill trama is parallel, and (4) the gills are
attached to the stipe. Not a particularly encouraging ..... ay [0 define a family.
A variety of genera are mentioned below in alphabetic order:
Armilfarin mellta. the so-called honey mushroom. can be a dangerous tree pathogen. though what used to be thought of as a single species is now known to comprise
several distilKt taxa - for eumpk, the co mmon Armillaria of the west coast of North
America is Armillaria os/Oyae. one genel of which extends over 600 hectares.
Armillaria mel/ea produces characteris tic blackish mycelial st rands called
rhizomorphs under the bark of afrected treeS. Conthnrellula umbonala has unusua l but
highly char.:ICteristic fotting gills. Calalhelasma is a genus of l!U"ge mycorrhi7..a1 agarics
wilh a conspicuous and persistent ring. This genus resembles the much-sought-after pine
mus hroom (Tricholoma magnil'ela"') but lacks its penetrating spicy odour, and is. nOt
regarded as edible. C/itocybe davipeJ has decurrent gills and a swollen stipe base. ClilOCybe
dea/baw contains the toxin muscarine (!;Ce chapter 22). Col/ybia has a somewhat confused generic concept. The basidiomata of the type species and a few other species are
very small and arise from sclerotia. as in Co/l)"bia cookei. which grows on dead ag::uics,
and Collybia tuberosa, whose sderotia resemble apple seeds. Coi/ybia racemosa, another
small species, produces a most unusu al Sc/erosrilbmn syn nem ~tul anamorph along the
stipe which sometimes forgets to develop acap. Larger species. such as Collybia mamlara.
have diagnostic brown-staining propensities. but such spedes are now being moved to
other genera. A good web site dealing with this genus is:
htt p://www.nybg.orgfbscllreslcollcolintro. htm l
Flwnmufilla I'eiuriptl. the 'velvel stalk: is a wood-inhabiting species that often
fruit s in winter. (t is al so grown in cul tivation. and etloMed basidiomata wilh tiny caps are
marketed as 'enoki- take ' (see chapter 18), Laccaria /accala is a very common mycorrhilal agaric which has unusual globose or ellipsoidal, spiny. amyloid basidiospores.
There is an excellent onlinc key to species of Laccaria at:
http://wvt.....,fmn h,orgfcandrlbotanylbota ny_sitesl1ungi/index.html
upisra m.da is a common spedes which is also a choice edible. despite its rather
unappetizing lilac to pu rplish colour. Lyophylllllll decastes is widely euten. but does not
agree with some people. Marasmill.1 oreades is the edible fairy ring mushroom commonly
found in pastures. M)"una leaiana is an unusually large and brighily coloured representative of this saprobic genus which has marginate gills (the edges are a different colour
from the rest of the gill). In this case the vivid ornnge colour at the edge of the gill is
proouced by a concentration of cystidia with orange COnlenls. NyclOlis a.lleropirQrtl parasitiles Lacrarills. Although the Nycraiis looks like a mushroom. its eap often becomes
almost entirely convened into conidia. so it is efrectively an anamorph. Xeromphalina
campant lla is a very small saprobic species that fruits profusely on decaying tree stumps.
Xerula radicata (formerly Col/)"bia. formerly Oudtmansiella) represents a modem trend

96 CH,\PTER fiVE
10 break up the Tricholomal:lceae into smaller families. II is placed in Ihe recently-proj.l'OSed family Xerulaceae. One of the mysteries attached to the Tricholomataceae is that
despite the very large number of ta",a it encompas$.CS. only twO sequestrate forms alt
known: HJllnmrgiunJ and Podolrydnangium. both of which arose from Lacc<lria. Compare thai with ,"'hal happened in the ne",l family, where sequestrate genera outnumber
those that shoot their spores.
k) Family RU5sulaceae. An almost emirely ectomyrorrhizal group, with flesh that is
distinctively brittle due to the presence of groups of unique. turgid, spherical, thi n-walled
cells called sp haerocys l~. Some ta:>;onomists think these fu ngi are sufficiently different
from other agarics to give them the rank of Ordcr (Russulales).
The spores are also unique in having elaborate omamcm':llion of ridges and warts.
Thisomamenlation. but not the rest of the spore wall, stains darkly (usually blue-blac k) in
~ofel zer's reagent. This is known as the am yloid (or starch-like) reaction. Thc spore print of
the RUS5uiaceae is white. cream or yellow.
The family Russu laceae contains two large epigeous agaric genera, Russula and
Lactarius. and 5i:\: much less common ~cqucstrate derivatives (which don't shoot their
sporcs, and so don ' t give spore printS). Allhough RUSJu/a and Luctarills are similar in
many respectS, they are easily distinguished by the presence of a milky late:>; in LoClariu$
('milky caps'). and by the absence of late:\: and thc bright colour of the pi lcu.~ in mOSl
species of Russula. Russula vircsccns is widely eatCn in Chin:l. though only Rusmla
ruarnpclina. with its shrim p-like flavou r, is widely eaten in ;-':onh Amcrica.
A sectio n through a spec ies of the sequestrate ,'r/acowanirtl re" ea ls a reduced stipe.
and shows that the gills are distorted and clearly not the vertical plates of tissue s~n in
troe Ru ssulas. Nevcrthe less, the spores of Mt.lC()Wallires have amyloid ornamentat io n and
are clea rly rus~ ubc eous . Russula has giv cn rise to IWO s~paratc sequestratc lincs.
M"':owanirn - Gynmom)"ces and Elasm()m)"ce.' - Mancllia. Both invo!\lC an agaricoid and
a hypog~ou s form, and both reta in m icro- amltomic~1 cha racters. like sphaerocysts and
amyloid spore o rnamentation. that give su rprising proof of [heir origin in Ru,uula.
AI! species of Lactarius bleed some ki nd oflale:\: when damaged, givi ng them the ir
common name of mil ky-caps. rhe highly appropriate Latin nJllle also eon"eys this message. The latex unequivocally separates Luctari"s from RUHllla _ Luc/arius dtliciQSUS
broi~s green. but has orange latex which OUi wh~n the basidio mu L'i damaJ;ed _The
late", in wcrarius vinace,miftscen.! is especially conce ntrated just above the gills. and
although whi tish wh... n it emerges, becomes yellow after a few secondS.
From Ll,cUlriu.1 have evolved two sequcstmte gcncra: Arc,mgdit /l(l (~ti!l mushroom-like [agoricoid). bllt with a cap that encloses the gills. and n<HI-shooting basidia),
and L-1/<"vIllYccs (wh ich has become hypogeous and tfUme-like). All three genem produce latex.
I) Family Boletaceae. Some mycologists consider this group sufficiently distinct
from the other agaric s \0 meri t its own Order. Boletalcs. I prefer to keep these mu~hroom
li ke organisms wi th in thc Agaricaics (con"eniently r.:d ucing [he number of Order.; you
need to mcmori le). BoletI'S, as they are usually called. afC often large. solid agarics, "'ilh
the h>'me niu m lining 0 laycr of vcni cal fleshy tubi:s that (diag nostically) can be easily
separated from thc nc.'ih of the ca p. The often swollen stipe freq uentl y has nct-like or
" 'arty ornamentation (Fig. 5.7 D). and somdimes a pan ial veil. The sporc~ are elongated.
and yellow ish-brown in mass. The re arc no cla mp connections 011 the hyph ae. Most
boletes are t<:tomycorrhizal.
Bo/n'f$ tdu/iJ- is the famous edible 'Steinpilz' or 'ccp' of Europe, and fonuna[el y
also occurs in Nonh America. [t is cither a rather variable spedes. or more probably a




spc!cies /;ompkx. Many other boletes are also eatcn. though specie, with ornnge or reddish pore-muuths, like thuse of S o/ellis frosti i, -SO/eIllS sa/anas. and many other speci~>.
mUSt be avoided. Those whose flesh turns blue when bru ised should also tu~ted with
caution_ Ty/opi/us fel/ells is visually spectacular. but gastronomically a bust. It often
occurs in liUge numbers under conifers. raising the expt:Clat;Ons of the onlooker. but
hopes iUe dashed when the pink tube mouths are secn. and we realize that we ha\'c found
the biuer boletc.'
The blue-staining Gasrrobo/e/'IS is alleged to be a sequestrate deriv;:u he of 8 01 etu~. though it is SOmetimes placed in the Xerocomac~a~. Suil/us spraguei demonstrak s
the panial veil that is found in many species of this genus, as does SuiIllIS gre.-il/ei. Mony
species of Suillus alSO ha,"e viscid caps. TnmcocQ/llmella . which has a "estigial stipe. and
Rhitopogon. whic h does nut, arc seq uestrate. hypogeous offshoots of SlIilIl'S. Like the
pare nt ge nus. th ey are important e<:tomycorrh ilal panner~ o f COnifers in west~m North
America. RhitopogQn porksii. a very commOn western species. has a spongy. lacunosc
basidioma. The spores. howeycr. ~ just like those of 11 Suillus. and DNA studies ha,'e
established that RlrhfJpogou is very closely related to S"i/l"s .
m) Famil y Gornphidiaccae. This mycorrhilul family has (I) viscid caps. (2) decurrent gills (not tubes). (3) a dark grey to brown ish-black spon: prin t und (4) microscopic
struclllre that shows it is closely related to the Bolela<:eac:. Gomphidilts haS \\ hitc flesh;
that of ChfrJQgompJms i5 pin!:: to orange. Sequestrnte fOIms have arisen from both gcnern.
This family is common in western ~onh America, much Ie,s so in the ~a5t.
n) family Gyrodontaceae. This family superficially resembles the

ll ol~I;lceac.


(I) the lubes are shallow and not easily detached: (2) thc spore print is yellowish or
olivaceoos brown: (3) the spores are subgloOOsc to ellipsoid: and (4) the h ~phae have
clamp conne<:tions. Fuscoboferinus. Boferinm, Gyrodon and G}"ropomf are represema

Ilve ge nera.
0) Family Paxillaceae. Like the Gom phidiaceae. this mycorrhizol f~mily II) has
gills. nOlIllI1e-S. but (2) the gills are easily separated from the flesh of the cap. (3) The gi n
trama is divergent and gelalini1.ed. (4) The spore print is brown or "hite. and (5) the spore~
are ovoid to elli(}Soid. The common species. Paxill/l.~ ""'o/mus, i~ a s)' mbiom of cQnifer;.
and is easi ly rccogni1.ed by it, inrolled cap margin. its decurren t gi!l$ and the brown stain,
th at appear after it has b.:en handled. Hygmpltoropsis alium/i(lC(I is kn own as the '1~1bc
ch:mtcrclle. It has conspicuously forking gills.

p) Family Strobilomycelaceae. The cap of Simbiloinyces jloccopus is (l) greyish

b13ck, (2) with large. shaggy scales, and (3) the tubes are grey, turning reddi,h ",hen
bruised. (4) The spore print is black. and (5) the spores arc omamem~d with:1 network of
ridges. The genus DO/dellils ilppcars to have given rise to no fewer than four sequcs trnk
fOl1l1s: ;1usrrogalllieria. Cham(/lli.tiCi. Gall/iula and ProlOgClurieria.
If you wanl to know more about the Slr3nge and fas<:inatin; sequestf"Jte agarics ~
taxa derived from no fewer than founee n famili es o f agarics - which no long~r shoot thei r
spores. you CJn rend two papc rs dealing with this iss ue: Kendrick, 5 . (1 994) E, olution ;n
action: from mushrooms to truffles. Mdil'ainea 11: 34-38 (pan I) and 39-47 (p~n 2).

In 1989 Canada joined the many countries that have issued stamps depicting
macrofungi. producing hand some (if slightly stylized) stamps of CI(lnt/ino{J.~is fusiform;'.
flo/elUs mirabi/is, Caltllwrel/'lS cinnabarimlS lInd .Morchella esculmra. (I ha\"~ been
trying to get th e Canadian pOSt oflice to bring out some Stamps on moulds. thus far
without success. despitc the important roles tho::se fungi playas producers of penidllin.
griseofulvin. cyclospori ne. an ato~in. etc.)

The foregoing is no more than a gesture sketch of the world of the agarics_ If you
want to learn more about what many people consider the most fascinating of all fungi. you
must buy or borrow one of the field guides listed under 'Further Reading' at the end of this
chapter. The large tome by Ren~ Pomerleau has all the minutiae a Northeasterner needs
(though the colour illustrations are poor). but the pocket-sized Audubon Guide by Lincoff.
though less detailed. covers the whole continent and can go anywhere with you. "The
larger-fannal Mushrooms of North Amuica by Roger Phillips. published in 1991, h.;J.s
over 1,000 colour photographs. and includes many more species of. for eump!e,
Coninarius (93}.Amanita (41). Lacfarius (64) and Russula (8 I). than other guides. Mush
rooms DemYSlified by Arora, though oriented toward western North America, is a mine of
useful and often amusing information for all mushroom-fanciers; it also covers a wide
range of taJla (even dealing with many sequeStrate forms). The Ntw Savory lVild Mush
room has CllcclIent colour photographs. hul is mainly uscfullo those in !he Pacific Nonhwest. The latest addition 10 these field guides is Fungi of Easum Canada and rhl!- NonhI!astem United Slall!S by George Barron. It covers over 600 species of fungi and is illustrated with more than 650 photographs.
In addition to agaric s, these books cover the more conspicuous Gasteromycetes.
Ascomycetes and Aphyl1ophorales. Some of the larger and more difficult genera caU for
separate keys, and those [0 the northeastern species of Russula by Kibby and FallO are
excellent eumples. "Malclunaker" is a new. profusely illustrated synoptic key [0 2.000
mushrooms on CD-ROM (see Bibliography at the end of this chapter).

Series Gasteromycetes
Althoogh many kinds of sequestrate fuogi can be traced to their agaricoid origin.
many others probably evolved so long ago that i[ is no longer possible to trace their
ancestr), with any degree of certainly. For these. which we call Gasteromy~etes. we ha\'e
erC(;ted special Orders, based on the mode of passive spore dispersal iDlO which mey have
evol ved. I think you will agree that if these groups have any agaric ancestry, it is well
concealed. All have non-shooting holobasidia.
Umnoperdon. a minute floating g~teromyccte. occurs in woodland ponds. Its basidia are produced inside a tiny, entirely closed. hollow basidioma. so there II.w ld be no
point in the spores being forcibly silO! from the basid ium. The non-shQO{ing nature of the
basidium is apparent from the symmetrical way in which me spores are mounted on the
sterigmata (remcmber that typical shooting basidia have their spores asymmetrically
mounted as an integral part ohhe shooting me~hanism)_ Fig. 5.8 AE shows non.shooting
basidia of a range of gasteromycetes.
(5) Order Sclerodennatales: I I genera. 38 species. The 'earthballs' (as opposed 10
puffballs'). Here the spore mass (gleba) has small spore-rontaining cavities (locul!1S)
wilh no real hymenium, ,md is powdery at maturity. with no true stipe or capillitia!
thread.,. In the com mon genus Sclcrodenn{1 the spore mass is blackish at maturity. and the
basidioma has no ostiole.
The separate locules are clearly visible in Pisolirhus linC/orills (Fig. 5.8 F). which is
perhaps the mosI famous of all fungi, since il helpscooifers andeucal)'ptS
[0 thrive on panicularly unfavourable si[cs. It has been the subject of many research
projects. as you will read in chap[cr 17. I have found this fungus fruiting at various places
in North America,Australia and South Africa. The basidiomata are often lumpy and almost
shopeless. and it is sometimes called the ugliest fungus in the world. despite its cllcellent
qualities as a mycorrhizal symbiont. Mature fruit bodies hove becn collected as a source
of spore inoculum aod. as I have seen, can also be used in a hot-weather version of a
snowball fight.



Sphaerobo/us stellatus, of the atypical family Sphaerobolaceae, has a sixlayered

peridi ... m . At maturity, the innermost layer and pan of the third layer liquefy, and the
second layer takes up the free .... ater. eventually evening suddenly and throwing the gleb:!
up 10 sill metre$ toward the light. These are the only g~teromycetes in which a form of
active spore di spersal has been reevolved. But notice that evolution did not reverse it$elf
- the odds against that ever happening are astronomical. and I know of no documented
(6) Order Mela n,ogastrales: 9 genera, 46 species. A completely hypogeous group.
in which the gleba has many loeules with no true hymenium, and whose contents are
mucilaginous at maturity. Locules are separated by distinct white septa. Basidiospores are
symmetrical and have a fairly broad anaciurn:nt SCM, both signs that they are not rn;:thely
shot: away from the basidia. Me/unogasl er and uUCQgasfer are representatl\'c genera.

B. CHI/rum


A. H~""g..
( ........... tal.


c SeW_ _



,..::-:l" ',:'

. '.-:






Fig. 5.8 HoIobasidom)'l":etes which lack active spore <ischarge. A: Agaticaies; ~H,t L)'I":operdales;
C,F: Sderodermalales; D,G: T~ostomalales; E: Phallales.


(7) Order Tulostomatal('s: 9 genera and 75 species of smlked puffballs. with dry.
powdery gleba. TU/o$toma looks a bit like a rabbit pell~t on a stal k, but has a bu ill-in
ostiole (Fig. 5.8 G). Cu/os/omQ has a ge latinous stipe and a most peculiar stell:lt.: ostiolc
rimmed with red pigment-the only puffball that WCQP; lipstick. I first saw this fungus in
New Zealand. but have found si milar species in the Carolinas.
(8) Order L~'cop('rdale5 : 26 genera. 260 species. These are the common and wellknown pu rtbaJl s and eanhs tars, with powdery glebas. Though most are saprob ic in soil
and on rotten wood, some may be In contrast to the Sderodermatales.
the glebal ,avilies are lined by a hymenium wh en young. The mature spore mass is
usu:llly kh:lki---coloured :lnd milled with capi11itial filaments. The peridium has [\\-'0 or
more l:lyers. and usually develop> an apical Qstiole. The papery inncr peridium can be
compressed by raindrops. expelling air and spores Ihrou gh the OSliole. L)"CQptrdon (Fig.
5.8 H) is the best-known genus, to which most common puffballs ~Iong. ul/Ige rm rlnnia
(fonncrly Coh'(lIia ) gig(lrIleo is thc giant puftball. Before the spore mass (g leb:l) malures.
and while tile imerior looks like white II\aM;hmaUow. thi s fungus is often collected :lnd
emen. A C:lnadial1 specimen collected in 1987 held the world record I1l1til 2000 for the
largest edible funglls - 2.6-t metres in circumfercllCe and weighing 22 kg.
GeaSlmm species (Fig. 5. 8 l) are known as carthstars. In this genus the thick OUler
pcridium spli ts stellately as it dries out. and the Sl:gments fold back in order to raise the
gl eba. in its inner. papery pcridium, above the dC:ld leaves that might otherwi se preve nt
the puffball l1lechanism fTom wo rking.
(9) Order Nidulariales: 5 genera, 60 species. These are the bird's nest fun gi. in
wh kh the ba~idioma has be:cn modified to be<;;ome a splashcup spore dipersal mecha
ni sm. The basidiospore mass. or gl eba, is divided up among ;.everal indiv idu al 'egg,'
(morc formally. pcridioles). The kineti c energy of rnindrops is focused :lnd rcnttted by
the funnelshaped b:lsidioma. and the rebounding water carri es the pcridiolc~ with it.
Crw;ibil/ulli. Cyoliws. Nidu/(1 ;lnu Nidillaria arc represcntotive genera.
In C'ymilus (Fig. 5.9 A) the pcridioles nre atlll.chcd to the wull of the basidio m~ by a
long thread. most of wh ich is folded up inside the stipe of the peridio lc. When the peridio1c
is ~plashed out. the thread unwinds rapidly. mtil ing behind. At the e nd of the thread is a
sticky blob which acts to anchor the pcridi o1c to wholever it strikes.
(I OJ Orde r Phallo. lcs: 25 genern.45 species. These :lre the st inkhom~ ..... hose spore,
are di~pcfSed by nni mal vectors. The gkba is slimy and re all y do.::s smcll bad, so it auraet,
flies .... hieh wallow in the mess, eating some spores and carrying others away on their fut.
Althou gh two well-known ~tinkhoms. representing the ge nera Ph(ll/II.! nn d Milfillllol. are
fairl ~ common in NonhAmctica. the most bizorre genera are commoner in Austrol:lsia and
the tTOpics. All stinl.:hom~ de~"Clop in a gd:Uinous matrill wtthin a membranous 'egg shdl" or peridiu nl. but when thcy 'h3tch: their mature fruit bodies can be: strikingly
Pll<IllljS (Fig. 5.9 D) and M ul;,W$ (Fig. 5.9 B) hnve the simplest morphology: the
stipe elonsatcs rnpidly, can:ying their respectively th imble-shaped and conical heads
(of\~n called receptacl es). into lhe air. whcr~ they can relea~c Iheir effiuviu m and :lttraet
thc nies more easily. Europe:lns h3~'C sufficient knowledge of these fungi 10 enjoy cartoon; of lh~m. Nonh Ame ric ans. 10 whom th.:y nre les, f~miliar. look al such artwork
a~kance .

The genus Dict)"lIphora (whose na me means 'nel-beare r') docs ind~ed have a vi sually striking lacy skirt h:lnging below Ihe n:ceptac1e. My guess is that this is 3 landing
platfonn for flies qucuing up for a sample of gleba. InAni/umlS (Fig. 5.9 C). the gleba is al
fi ~l central in the egg. LIter the spore mass covers the inner side of seve ral IX:topus-Jike


arms. In CIllIhru$ (Fig. 5.9 F) the arms remain fused. and in some species ronn an open
lanice. again with the gleba on the inside. Astroi (Fig. 5.9 E) is ~ urely one of the mo,t
numboy~nt members of a truly spectacular Order. Bright orange-red extensions of its
receptacle radiale OUt like the petals of a flower. and also look rather like meat, providing
a d iverse range of visual as well as olfactory clues to would-be vectors, which can be
drawn from among the meat-ealcrs (e.g. wasps). the nect~r-eaters (e.g. butterflies) and the
visitors to excreta. H)"sierangiwn is hypogeous, so the gelatinous layer found in most
Phallales is nOt welldeveloped, and there is no dramatic ruptu re of the peridium at maturity. But the affinities of this ~lusive sequestrate genus with the otherwi.o;e e;(hibitionis.
tic Phallalcs are accepted.

. ....
B Mul/I>UJ


Fig. 5.9 GMtefomycetes. A: Nkliariales; BF: PhaIJIes.

CI~ lhtu~


Classes Phragmobasidiomycetes and Teliomycetes

The twO remaining classes in the: subphylum BasidiomyWlina are very different
One is of no (or very liule) economic imponance, the other causes many serious crop
diseases. Both have basidia that are divided into four compartments by septa, each eom~
partment giving rise to a single basidiospore. In Class Phragmobasidiomycetes, the basidia are borne on some kind of basidioma, but in Class Tcliomycetes. they arise from
overv.intering spores. Members of these two Classes often have the ability (I) to fonn
secondary spores from their primary spores: (2) andlor 10 produce yeast-like cells. Most
Holobasidiomycetes can do neither of these things (but see p. 114).

Class Phragmobasidiomycetes
This group contains four Orders: Tremellales, Auricularialcs. Scptobasidiales and
Tulasndlales, which ali have basidia subdivided by septa.
I) Order Tremell ales: TIlese are jelly fungi generally found on dead wood. Long
considered harmless saprobes, they have re.:ently been unmasked as vicious mycoparasites
of other woodinhabiting fungi. The basidia (Fig. 5.iOA) aR: often described as 'erueiately
septate: being \'Crtically divided into four compartments. Each of these develops a long
outgrowth that extends to the surlace of the: gelatinous matrix and produces a ballistospore.
The most ro:ent interpretation of these 'basidia' is that the \'ertical septation separates the
nuclei into four cells that can be called basidiospores, and that the long 'epibasidia'
which grow up to the surface of the jelly are actually germ tubes. This would mean that the
'basidiospores' arc actually secondary spores, results of a form of 'germination by repetition: a phenomenon so common in the phragmobas idiomycetes that it is often used as a
diagnostic character.
The basidiomataofTremel/a areoften irregularly shaped (fig. 5. lOA). Otherrepresent:u;\"e genera are Ph/ogioris, the rather attractive scoop-shaped 'apricot jelly,' and
Tremel/adon. But in Pseudohydnum, convergent evolution has produced a form reminiscent of certain holobasid iomycetes. Pseudohydnum has its hymenium on downward
pointing teeth like those of the Hydnaceae (AphyIJophorales). but the rubbery tel<.ture of
its b~idiotna. and the cruciately septate basidia, give the game away - it is undoubtedly
a membt:r of the Tremellales.
(2) Order Au ricula ria les: j genera. 16 species. Members of this Ordcr are easi ly
identified by their gelatinous. ear- like basidiomata arising from wood (Fig. S.IO B). The
e longated basidia an:: di vided by transverse septa. and each of the four compartments
dC"clops a slender tubular outgrowth that produces a basidiospore when it reaches the
surface of the gelatinous matrix. The Chinese call members of the genus Aurit'ularia
'cloud ears' or 'tree ears,' and use them in cooking. largely fortheir interesting texture. We
have recently discovercd that th~ y comain a substance which reduces the clotting propensities of blood. and so may offer some protection against heart attacks.
(3) Order S~ pto hasldiales: 2 genera, 175 species. mostly in &pwbasidium (Fig.
5.11 A). This Order also has transverse ly septate basidia, but its basidiomat3 are 110t
gelatinous. and it parasitizes scale insects. These do not die. but become sterile. They are
buri.-d in a weft of fungal hyphae that produces basidia on its surface and provides shelter
for other healthy scales.

Order Tul as nellales: This small Order is interesting to us mostly because it has
yet another variation on lhe phragmobasidium. In TU/(Isnel/(I the four deve loping sterig
mata swell up and each becomes separated from the body of the basidium by a secondary
septu~ (Fig. 5.11 B)


Class Teliomycetss

1.9. orrf'li}-

This group comprises two distantly related Orders, Uredinales and Ustilaginales,
which produce no basidiomata and have simple septal pores with pulleywhcd occlusions
(Fig, 5.1 D) rather than !he doliporcs chilftlCterislic of most other basidiomycetes.
(I) Order Uredinalcs: 164 genera, 7.000 species (3,000 in one genus - Puccinia) .
The rust fungi are all obligately biotrophic on vascu lar plants and often have very narrow
host ranges. being restricted 10 a single family. a single genus, or c,'cn a single species.
Although they have obviously ~volved with !heir OOslS for millions of years and don't
usually kill them. rust fungi can severely reduce yields of our domesticated plants, par
ticularly the cereals on which wc are so dependent. The rust fungi produce basidia from
overwintering spores (teliospores), so they don't form basidiomata. But they do produce
no fewer than five different kinds of spore, each specialized for a particular step or phase
in the life cycle, And they often alternate between two hoStS , which lend to be from
tu}(onomically distant groups, This is important information, because as you will sce in
chapter 12. our efforts to control many diseases of our food crops depend on our knowl



. . -\1
Fig, 5, 10


A: Tremelales; 6: miculariales.


'.''?" - ."",,,,...

r.,... 1> 113 ; I~ SG~

fj::!; :::

- --

.". ' -' '


edge of the life history of the pathogens. Tn any case . the~e most comple)( of all fungal
cycles are intrinsically fascinating .

PlicciniG graminiJ subspecies Ir/tici. the fungus causing black Stem ruSt of wheat ,
can e)(emplify mllcFOCyclic, heteroecio us rust:; (those produci ng all five spore fonn> and
moving back and forward between two differ"'nt hostS). The different stages of the li fe
c>'cle are shown in Fi g. 5.12. Basidiospores, ....-hi eh are of + an d - m ari ng types. land on a
young leaf of barberry (BtrberiJ) in spring. and initialc localized monokaryOlic infectio ns. The hyphae arc intercellul ar. but they seo d haustoria into host cells to absorb food_
Soon. these monokaryotic mycelia develop tiny flask-shaped spe rmagoniA (stage 0) in
the upper lay ers of the lea f. They produce only small brown spots and don ' t do any
si gnificant damage to the barberry. Each sperm~gon;um forms innumerable liny spcrm D.tla which ooze OU I in a sweet-smelling neclllJ. A tuft of rec:tpth t hr ph ne also grows out
from the oeck of each spennagonium. Insects are attracted by the nectar. amI walk or fly
from o ne ~penn agonium to another. unwittingly transferring spe-rmatia o f each mating
type 10 recepl;~'e hyph ae of the Olher type. This process, wh ich is somewhat analogous to
pollination. initiates Ihe di karyoph ase . The dikaryotilation spreads to the lower ~urfacc


o U$tila;o

E rWe!l.l

a TulUMlla

F!S. 5.11 Phragmobasidiomycetes and Teliom}'Cetes. A:.Sep tobasidiJles; B: Tulasnellales; C:

Uteclio<lles; O.E; Ustiaginales.


of thc barberry leaf. where the fungus has alre ady produccd the pri mordi a of cup-like
structures called uecia (stage I) - two are shown in this r.ection_
The flower-like aec la burst through the host epidermis, and liberate dikaryotic
aeclospo res - but these spores can' t infe<:t the barberry. Only if they land on a wheat plant
(Triticum ) can they establish new dikaryotic infections_That is why I e~ll them ' transfa
spores.' The dikaryotie mycelia in the wheat plant SOOII produce uredi nia _ pustules of
reddish-brown. dikaryoti.; uredin iospo res (sum mer spores - stage II) -which aga in bum
through the host epidemlis and are wind-d isperst:d to olher wheat plants_
Note thai the urediniospores arc unicellular and rather thick-walled. but have distinct equatorial germ pores. The many new infeclioa~ generated by the5e spores soon
produce further inoculum. and waves of uredi niospores, borne on the prevailing winds,
cause the mass ive epidemics of wheat ruSt that periodically sweep North America.
Toward the end of summer. these sam e pustules switch over to producing another
kind of spore, the dark. two-celled. thick-walled telios pores (winter spores - stage 1lI).
Each cell of the telio~pofC is binucleate at first. but karyogamy soon occurs and th e
spores ovc rwintc r in the genuinely di ploid or zygotic condition. In spring. each cell
germinates and gives rise (0 a short hypha which Ix:comes a trans\'ersc1y septate basidiu m
(Fig. 5. 1 I C) (rother like those of the Auricularink s and Septobasidiales). Each cell develops a short sterigma wh ich in turn bears a basidiospore (stage IV). These are borne asy m



rKO~ 'V. '>'PM'!

5";0 IV

Frg. 5.12 Urc<finJles: life cycle of Puccini" graminis.

5~ .O


metricaHy, and are shot away in typi cal basidiomycete manner. They must land on a
barberry leaf if the cycle is to continue.
Some rust fungi don't produce all five spore fonns. and are described as microcydk
Some complete their cycle on a single host, and are called autoeciolls. Puccinia poa!!n!!mora/is, a nonnaUy heteroecious rust fungus, persists in the Canadian arctic through
the ability of its urediniospores to overwinter. It never forms tdiospores, and so needs no
alternate host Some tropical rust fungi don't form teliospores either, but in this case it is
because there is no need for an overwintering spore,
Stage I (aecia) and stage II (uredinia) may be regarded as the two asexually
reproductive stages (anamorphs) of a rust fungus, Stage III, the teliospore, is regarded as
the sexual state or teleomorph, so the host on which these spores develop is called the
primary host. In the case of Puccinia graminis subspecies Irilici, wheat (Triticum,
Poaceae, Monocots) is the primary host, and barberry (Bl!fberis, Berberidaeeae, Dieots)
the altenlate host.
Because of the threat they pose to our food supplies, the cereal rusts have been
intensively studied. and they have repaid that scrutiny with a rich harvest of taxonomic
and genetic information. The species Puccinia graminis attacks many different grasses,
Several subspecies have been recogn ized by their apparem restriction to individual grass
genera, e,g, P. gramillis ssp, avenae on oats (Avella), P. graminis ssp, lwrdei on barley
(Hordeum), and, of course, P. graminis ssp. trilici on wheat (TririCllm), Each of these
subspecies is subdivided into many physiological races which differ in their ability to
att:lck specified commercial varieties of the host genus, Puccinia graminis ssp, rririe! has
over200 such races, and new ones arc di scovered ever)' year, Wheat breeders have to work
hard to stay one jllmp ahead of the pathogcn_ Breeding of resistant plants is discussed in
chapter 12,
Some heteroecious rusts move between angiosperm and gymnospenn hosts, and
sometimes it is the alternate host, mther than the primary host, that is economically
important. Gymnosporallgium is an. interesting heteroecious rust. On.e of its hosts is a
rosaceous plant like pear. It produces spennagonia on the upper side of the leaves, These
lilxrate both nectar, to attract arthropods, and spennatia (non -motile, but effectively male
gametes) which the visiting animals transfer to spermagonia of the opposite mating type,
whereupon dikaryotization happens , Al'ter dikaryotization, the fungus goes on to produce its aecia on the same lesion, but on the other side 0f the leaf. On another rosaceous
_host. serviceberry (Amelallchier), it produces aecia on the hypertrophied fruit. The aeciospores can infect only the other host, a conifer such as juniper (Juniperus), on which
the spectacular gelatinous lelial horns are produced (these are obvious only during wet
A similar alternation happens in the genus Crol1llrtium, Cronartium ribico/a (blister rust of white pine) produces its spcrnmtia ami aeciospo res on five-needled white pines
(eastern whi te pine, Pinus strobus, and western white pine, Pinus monlico/a), and its
urediniospores and tdiospores on wild curran! (Ribes) _The aecial hosts of Cronartillnl
comandra!! (Comandra blister mst), are two- and three-needled pines, including Pinus
ponderosu (ponderosa pine), and Pinus contorta var_/arifolia (lodgepole pine), The teliul
hosts are the herbs California comandra (ConwnJra umbelll(l var, californica) and Basta,d to~dflax (Comllndra lh'ida), The name of Ihesc diseases, 'bliSler rust,' refers 10 the
conspicuous aecia, and it is Ihe perennial aecial cankers on the pines that gradually
spread and often eventually girdle nnd kill the tree, Cronartiumfusifonne, another blister
rust, alternates between various southern pines (on which it dewlops its aceia) and oaks
(Quercus spp). Chrysomyxa arctostap/lyU moves between black spruce (Picea mariana),


on which it produces its accia. and ArctQstaphylos, an ericaccous shrub on which il
produces its lelia.
The genus PhrogmidiulII commonly occurs on members of the Rosaceae, I found a
telia! specimen in the garden, on one o f my wife's precious roses. She w:.s not impressed.
Howevcr, I was noslalgic about it. because the flIS! microscopic fungus I ever collected.
way back in the 1950s. was a Phragmidium producing dustcrs of its dark. stalked.
phragmosporous teliospores 00 blackberry leaves. When I mounted the spores I immedi
ately assu med it was a dark- spored hyphomycete (see chapter 4a). I can't remember who
dis(lbused me of this notion. but if you get Ihe Class and Order right . this is one of the
easiest rusts to identify. The teliospores from our rose leaf had a distinct. though colourless,
sta lk, si)!; darkly pigmcnted cells. a nd an apical spine. These characters and its host preference identified it as Phragmidium muetvnawm , which is the conunonest of the nine
species that occur on roses. These tcliospores are big, as fungal spores go: the body of the
spore is about 77 microns long.
Some rusts fungi are systemic. spread ing throughout the ir hOSt plants before sporulating. This means that the sudden eruption of uredinia all o\'(:r the leaves can be rather
spectacular. In Java I foundcoff~ leaves infected with the infamous coffee rust, H(mifaea
vas/a/ri:!o which causes defoliation of the coffee plants. It was the in\'lSion of this rust
fungus that caused Sri Lanka (fonnerly called Ceylon) to abandon coffee as its prime crop,
and make the radical shift to growing - and exporting - tea.
(2) Order Ustilaginales: 60 genera. 1.000 species (300 in USliiago). Like the rust
fungi, the smut fungi are all parasites of vascular plants. and produce basidiospores. on
tr:lOsversely septate basidia arising from ove""'intering tcliospores. But the tWO groups
differ in many respects, as Table 5.1 shows.
a) Family Ustilaginaceae. In this group the teliospore is karyologi cally equivalent
to that of a rust fungus. so the shan hypha arising from a germinating tcliospore of
Ustilago becomes 3-scptatc. and buds off a yeastli ke basidiospore from tach compartment (Fig. 5.11 0 ). Compatible ele ments soon fuse to restore the dikaryon.ln homothallic
species this can rather conveniently involve basidiospores from the same b:.sidium, or a
basid iospore can fuse with a cell of the basidium, or t.....o cells of the same basid ium may
fuse. or teliospores may germinate and fonn a mycelium between whose h)'pllae fusions
can occur. Many smut fungi. however. are heterothaHic. so fusions must be between cens
o f different and compatible parents.
The tcliospore.~ of Ulti/(Iga via/acea are present on the seeds of its host. Silene
(Caryophy llaceae), and gemlinatc when the seeds do. After the dikaryotization process
desc ribed above, the newly dikaryolic mycelium infects the seedling. Although the myceli um becomes sy~temic, spreading throughout the host. it incitcs no pathological symptoms until the flowers develop. The n the pollen is replaced by a mass of dikaryotie
mycel ium. which eventually disartic ulates inlO teliospores. The disease is called anther
Many other smuts are also organ-speeific: in com smut, caused by Ustilagomaydis.
some or all kernels are replaced by grossly swollen masses of black teliospores.ln onion
smut, caused by Urocysris cepu/(Ie, the tcliospores develop in the bulb, Note thaI the
organ attacked (and often replaced) by SmUt fungi is always one into ... 'hieh the plant
directs high-energy resources - anthers. seeds, bulbs. Sinee human s are often interested in
the host storage organs as sources of food. it may not be too surprising that frust ratio n at
the appare nt loss of that food led people to sample the fungus instead. As ~ou can rcad in
chaptcr 18, at least two smuts are widely eaten: the black spore masses of tom smut
(Ustilago maydis) are regarded as a delicacy in Mexico. and VIlilago tsculenw. which
causes hypcnrophy in the sIems of wild rice, is widely eaten in China.


Table 5.1 Differences between Rust IUld Smut Funj,,>1


Ustilagina lcs

I) Tdiospores terminal

Tel iosporcs inte rcal ary

2) Basidiospores 4. shot from

BasidiOSpore number variable,

sterigmata. not discharged

3) Spcrmagonia produced ( sex



organs )

No sex organs, any

can fu se

4) Clamp connections absent

G amp coonections common

5) Often requi re 2 hosts

Never require 2 host:;

6) Oblig:uely biotrophie

Facultali\-ely biotrophie. yeast like in culture



usually iOCllli zed

8) To:>liospores in telial

son, location

9) Auack ferm. gy mnosperms and



CQrnpatible cells

Infections usually syste mic

Teliospores replacc host orod'", c.g., ovary,
Anac k only angiosperms

b) Family Tilletiaceae. Here, events are phys ically more compressed: karyogamy.
rn.:iosis and mitosis all happen inside the leliospore. Wh ~n this germinates, the resulting
basid ium produces a cl uster o f s lender. parallel basidiosporcs from ils apo:>x (Fig. 5.11 El
These soo n copu lmc in pairs to rc~!O rc tho:> dikaryon. Tillnia caries . the cause of ' bunt' or
s:inkin g smut of wheat. is Just as im port ant an eco nomi c problem as ste m rust. btc~use il
has so f~r proved impossible to breed strnins of wheat resistant to this fungus.
No w I' ll wrap this long chapter up wi th a key to the more common Orders ofbasidiomycet~s . If you ' ll read through it. it will hel p you to rec~ p the major characte ristics I
h~ve shown you in the te xt ao.d pictures above.
No basidioma: basidia solitary (free),
o r On ind i"idual hy phae .............................. ......... (see yeasts)
No bnsidiomu: basi di a arisi ng fro m
restio.g sporc..~ (class Te liomycelcs) ...................... 2
;\0 basid ioma: basidia in a layer On
sl,Irfa<:e of host plan t ........_-. .................................. E:l:obasid ialcs
B ~si dioma prod l.lced .. .... ... ...... ..... ,.. .......... ...... .... 3








'Smut' fungi; ~utoeeious, basidiospores

not discharged, damps common, resting
spores intercalary; grow in culture ...... _...... ,........ Ustilaginales
'Rust' fungi; often heteroecious,
basidiospores disch arged, clamps absent,
resting spores terminal, oblig~tely biotrophic .... Urcd inales
B~sidia .... enieally or transversely septate
(cl ass Phragmobasidiomycetes) ................... ,....... 4
Basidia not divided by septa
(class Holobasidiomyectes) ____ .. -..-. .................... 5
Basidia divided venically into 4; each with
a long apical extension, bearing
one spore (jelly fungi)_ .. _______ -. __ ___ .. _____ .. ............ Tremellalcs
Basidia divided transversely into 4;
euch cell with a lateral outgrowth beari ng
one spore (ear fungi) .,......... ,..............
_.. ___ ... Auriculariales
Basidiospores obliquely attached to
sterigmma; hymenium exposed at
maturity and spores forci bly discharged
(give spore pri nt) (series Hymenomycet ae) ..... ... 6
Basidiospores symmetrically attached
to sterigmata. or steri gmata absent, spores
not discharged (no spore pri m) (sequ,"strate '
Agaricales and series Gasteromycct ae) ....
___ .. 8
Basidia sknder, with I\~O long extensions
(tuning fork basid ia) (jelly fung i) .......... ___ ..... Oacrymycetales
Basidia usually with 4 short sterigmata,
no long extensions .......
.. ....... __ ___ .
.. ...... 7
Hymenium covering ve rti call y orie nted,
radially arranged lamellae or lin ing
v<!rtically oriented fleshy tuhcs
(agarics and bole l ~S) ... ... .............. ... ..
Hymcnium in other conligurations __ __ __ ........... ,.. , Aphyllophorales
Basidiomo. agaricoid. but not releasing
spo re s; or micro -anatomical features
establishing relationships to agarics
or boletes _...... ,............ ,.. ,....... .
,..... ,..... scquestrateAgaricales
No clear derivation from Agaricnles or
other groups (series Gastc romycetae) ______ .. .......... 9
Ba~idiospor<! m~ss (gleba) sl imy,
stinking, exposed on receptacle
(stinkhoms. etc ) _
............... _'- ___ ____ ... ...... ... ... Phallales
Gleba nOI slimy and evil -smelling __ ................... 10
G leb~ enclosed in several small, separnte
peridioles; basidiomata tough and deeply
funne l-shaped or c up-shaped
(bird 's nest fungi)
.. ... Nidulariales
NOI us abo" e ..................... ___ _______ .
.. ! 1




Spore mass powdery. drab or khaki

coloured, peridium 2-layered, inner
peridium papery, usually with ostiole
(puffballs) ... ,............ ........ ......................... ....... 12
Spore mass dark, peridium 1layered,
thick. no ostiole (earthballs) .............................. Sclcrodermatales
Basidiomata more or less sessile
or stalk nO! distinct ............................
Basidiomata prominently stalked " ."

.. ............ Lycoperdales
............. Tulostomatales

Further Reading on Basidiomycetes

Arora, D. (1986) Mushrooms Demyslified. 2nd Edn. Ten Speed Press, Berkeley.
Bandoni, R.I. (1987) Taxonomic overview of the Tremdlales. pp. 87-110 (in) The Expanding Realm of Yeast-like Fungi. (Eds.) G.S. de Hoog, M.Th. Smith andA.C.M.
Weijman. Centraalbureau voor Schimme!cultures. Baam.
Barron. GL (1999) )<"ungi ofEaslem Canada and the Northeastern United States. Lone
Pine. Edmonton.
Breitenbach, 1. and F. Kranzlin (1986) Fungi of Switzerland. VoL 2: Non-gilled Basidi
omycetes. Verlag Mykologia, Lucerne.
Breitenbach, 1. and F. Kran zlin (1991) Fungi nf Switzerland. Vol. 3: Bolete, and Agarics
Part I. Verlag Mykologia, Lucerne.
Breitenbach. J. and F. Krlinzlin.( 1995) Fungi of Switzerland. Vol. 4: Agarics Part 2. Verlag
l>lykologia, Lucerne.
Coker, W.e. and Couch, J.N. (1928) Gasteromycetes of the Eastern Uni ted States and
Canada. Un iversity of North Carolina Press, Chapel Hil l.
Corner. E.J.H. (1950) A l\Ionograph of Clava ria and Allied Genera. Annals of Botany
Memoi~ 1.
Corner. E.1.H. (1968) A i\-tonograph of Cantharclloid Fungi. Oxford Un iversity Prcss,
Comer, E.1.H. ( 1970) Supplement to a Monognlph of Cla~'aria and Allied Genera. Bcihcftc
1\ova Hedwigia 33 .
Com:h. J.N. (1938) The GenusSeptobasidiIlm. Unive~ity of North Carolina Press, Chapel
Cummins. G.B. and Y. Hiratsuka (1983) Illustrated Genera of Rust Fungi. (revised Edn.)
American Phytopathological Society. Minneapolis.
Eriksson. J. K. Hjorts1am and L. Ryvard.:n (1973-8 1) The Corticiaeeae of North Europe.
Vo ls. 1-6. Fungiflora. Oslo.
Fischer. G.W. ( 1953) Manua l of the North American Smut Fungi. Ronald, New York.
Jahn, H. (1979) Pilze die an Holz wachsen. Busse. Herford.
Ken drick. B. (2000) The )<' ifth Kingdom on CD-RO ~ I , Version 2.0. Mycologue , 8727
Lochside Drive. Sidney. BC. Canada V8L IM8
Kendric k. B. and R. Watling. (1979) Mitospores in Basidiomycetes. pp.473-545 in The
Whole Fungus. Vol. 2. Nat. Mus. Canada, Ottawa (now available on ly from
l\Iyeologue. 8727 Lochside Dr., Sidn ey. Be. Canada V8L IMS.)


Kibby, G, and R. Fallo (1990) Keys to the species of Russula in northeastern North
America. 3rd Edn. Kibby Fatto Enterpri se~ , 1187 Millstone River Rd., Somerville,
N.J 08876.
LincofC G.H. ( 1981) The Audubon Society Field G lIide to NOl"th Amedcan Mushrooms.
Knopf. New York.
McKenny, M., D.E. Stuntz and J. Ammirati (1987) The New Savory 'Vild Mushroom 3rd
Edn. University ofWa~hington Press. Seaule.
Moser. M. (1983) Keys to Agarics and Boleti (Polyporalcs, Boleta1es, Agaricalcs,
Russulales). Roger Phillips. London.
Oberwinkier, F. (1982) The significance of the morphology of the basidium in the phylog eny of basidiomycetes. pp. 935 (in) Basidium and Basidiocarp. (Eds.) K. Wells
and EK. Wells. Springer-Verlag, New York.
Petersen, R.H. (Ed.) (J971) Evolution in tbe Higher Basidiomycetes. University of Tennessee Press, Knoxville.
Phillips, R. (1991) Mushrooms of North America. Phillips, Little. Brown & Co., Boston.
Pomerleau, R.(1980) Flore des Champignons au Quebec. Les Editions La Presse, Ottawa.
Ramsboltom, J. (1953) Mushrooms and Toadstools. Collins. London.
Reijnders, A.EM . (1963) Les Problemes du Developpement des Carpophores des
Agaricales et de Quelques Voisins. Junk. The Hague.
Singer, R. (! 975) The Agaricales in Modern Taxonomy. 2nd Edn. Cmmer. Weinheim.
Smith. A.H. and H.D. Thiers (! 97 1) The Boletes of Michigan. University of Michigan
Pres~, Ann Arbor.
Ziller. W.G. (1974) The Tree Rusts of West em Canada. Infonnation Canada, Ottawa. Mushrooms of the San Francisco area.
hltp: II I bsci I res /col/colintro.html. All about the genus Collybia.
http; l/www.fmn /caudr / botany/botany_sites/fungi I index.hlml. A key to the
agaric genus Laccaria.
Th;;: "Matchmaker" visual basic program by Ian and Eli Gibson contains descri ptions of over 2.000 species of gilled mushrooms, 680 of them linked \0 1,269 colour
photographs. A series of menu screens permit entry of characters and subsequent searches
for matches. The program thus offers a synoptic key for mushroom identification. There
are also 773 colour photographs of 399 non-gilled taxa. This program is available on CDROM with The FiJll! Kingdom, from Mycologue Publications (see


Yeasts - Polyphyletic Fungi

Everyo ne knows the word 'yeast: but vcry few people have m(II;1I idea what a yeast
really I$. and fewer still are aware thaI the name is applied [0 organ iSIll5 of very different

origins. You arc about to join Ihat eli te group. The word 'yeasf has been wid ely illt~r
preted in terms of morphology alone. but as you will see. th~lt is si mplLuic. and 1 fOnTIS are
develo~ in many di fferent groups of fungi, from Zy~omycele5 to BlISid iomycclcs (with
r... pre~ en tativc fo rms in all three major subgroups - Holobasidiomyceles ,
Phragmobasidiomycetcs and Teliomycetes). Cu rrently. about 700 species of yeast ~ are
knov.-n. distributed IImong about 100 genera.
Y~ast> arc moslly (b ut not all) unicellular orga nism s. some Qf which arc useful to us
bec;\u,e they 'r~i5C' bre:ld, put the alcohol in beer (left) and wine . and are~, high-protein
food supplement as ..... ell a~ a rich source o f B vitamins. But the re is much more to them
than th;).t. ;md th~y have a darker side: some are implicated in food spoi lage. A few yeasts.
such a5. Candida Illbicans (Fig. 6.2 C). cause potcntiall y s('rious disease.~ of humans .
i\!lh<.Juh )e~sts;).rc still oft~n characterited as si ngle -celled fungi that \11.1 not produce
hyphae. C(Jndida und qu ite a few o ther yeaS ts cl early produce hyph ae. as well as what we
call 'yeast ' cellS. The yeasl cells of Candid" are !>.asicall y ooni\lia. and develop in what we
"o uid call bh ~ticacropctal' branche\l chai ns.
B<'tause o f their economic and med ical importance. there was a need to identify
micro>copitally simil:tr but physiologic~lly different yeast~. So zymologim (yeast C;<p.?rts) ~cveloped a ta>;.onom ic scheme based on physiological lests such as the ability o f
)CaSb to ferment or assimilate D. "ariety of sugars, thei r nitrogen and " itumin requirements. antibiotic resistan!;e. elC. More recently. sophisti cat<,d tcchniques stich as magnet ic r~son ance analysis o f ce ll wall compone nts. elec trophoretic enlymc analysis . eyto
chrome ~pectrophotometric analy~is. serologic:!l tests. DNA reassociation. and O;":A!>.aM:
compo 'itio n. have all ix:cn pressed into .>ervice in the <;e ar~h fnr u~cfu l t~>;.ono rn i c cl1 aw~
ters in YCJSIl;.
One as.sumption underlying much of this activity wa ~ th~t yeaSts had relativdy few
morph olog ical characters to wurk on. It W~<; thought that yeil~ts reproduced by one o f two
proce~,es. which " <'re s.implistica ll y called 'budding or ' fission: But yeasts do in fact
exhibit morphologica] and d-:ve]opmcntal f<'atures whosc significance hus o oly rece ntly
bee n appre ciated. Th ese chawc ters cven offer clu ~s to !h~ un de rlY1fl;,! phylogenetic
di'"Crsit~ or the group. We now think of <Issimilati,e yellSt cells as essentially conid ia. and
have identified sc"nal diff~re nt kiTld" llf co nidi ogcncsis amo ng thcm. as Fig 6.1 .~ h ows.
:>.bny yeast s (about 600 species in 22 genera) nc"er d.:vdop a telcomorph. and aTe es~n
tially conidial fungi.
,\l u ltiblCr~1 budding )e asts bud from many d iftercnt points on the cell. produci ng

only one daught er cell (conidium) from each site. and 1<'~l'ing many scars (Sllccharomy-


ce" -

Fig 6.1 A), What havc commonly been called apiculate , bipolar buddin g ycnsts
have lon g cells Ihtu bud re~aledly each end. c~tending percuuently in the proc~s.s
(e.g. Sacclraromycodel - Fig, 6.1 C. lower di~gram). Cells or what ha\'e been inaccuTOtely tcrmed ' fission' yeastS also extcnd percurrenlly. but 011 a much broader base (e.g.
Sci1izCJS(lcchar<)nl),Ctl - Fig. 6.1 C. upper diagram), Sume hyphal yea.m produce !hallienrthric conidia (Geolrichmn - Fig. 6.1 E). 3a~idiom}ce!oos yeasts may be blaslie-s)'mpodial (Cryptococcus - Fig, 6.1 B) or bla~tic-phial idic (Rhodll/onda :md Sporob%mycts
- Fig. 6.1 D). Somc of these unicel]ular nnamorplls can switch in to the tekom orphic
mode , and produce stnlcrures that would appear 10 place them among the Dikary ornycotn.
though sine<: sex invoh'es fusion of individual cells to form a zygote. thcre is no d ikaryon .
Yeast phases of smu l fungi do, howeyer. have a dikaryopha sc.
Some yeasts form endogenous me iospores inside meiosp orUlIg ia Ihul arc
karyologietilly exactly compal'1lble with asci (scverol such meio~porangia, most comaining foor spores. are visible in Fig. 6.2 A). Ihoogh the wall chemistry (a good indicator of



v ~E?


Fig r),l Corxiogeoesis in yeasts (compare with figs. 4.54.8)



phylogeny) is somewhat different from that of Ascomycetes, and they are never produced
on or in a fruit body (ascoma).
The ability of some yeasts to produce hyphae is emphasized in Fig. 6.2.
S(lccharomycopsis (Fig. 6.2 A) produces Candida anamorpbs. Dipoda.lcus (Fig. 6.2 B)
produces a Geotric!lIlm anamol1lh. shown here beside the meiosporangium.
Other yeasts are Basidiomycetes. Some of these (e.g. Spvrob%mycu - Fig. 6.2 F)
even produce exogenous spores borne asynunctrically on poinled outgrowths ofthe cell:
these spores are forcibly discharged, and the mechanism involved is obviously that of the
basidium. Some, which produce hyphae, even make clamp connections (Fig. 6.2 D).
Others, such as Cryptococcus, produce blastic-phialidic (Fig.6.l D - ccntre) or blasticsympodial (Fig. 6. I B) conidia.
Tooutlinc the full taxonomic diversity of yeasts. I must also add that when members
of the Ustilaginales (Tcliomycetes) or Taphril\3les (Ascomycetes) are grown in axenic
culture, they become yeast-like. Basidios~ of Tremdlales germinate 10 produce a
haploid yeast phase. Sever.u fungal pathogens of humans. while filamentous in culture.
ace yeast- like when growing inside 1.1$ (e.g. HiSlOpiasm(l capsula/um . Blastomyces
demtati/idis - see chapter 23). Finally, a few fu ngi such as Mucor roJlxii (Zygomycetes)
can be changed from a hyphal to a yeast-like morphology. oc vice versa. by varying levels
of carbon dioxide Of" of various nutrients.
So 'yeast' morphology is sometimes a response to environmental factors such as
osmotic stress. a response that has evolved many times in different groups (just as the
lichenization process [chapter 7] and the change from agaric to sequestrate derivative
[chapter 51 have occurred many times). As a final twist to this tale, mycologists have
discovercd that some fungi which consistently produce hyphae (e.g. Arlh f(xucus, AxhbY(J,
Candida, Crtbrolhuium , Dipodascus, Erem olhuium. Gu illiulllonditlla.
S(lcclulromycopsix). are closely related to the unicellular yeasts. This conclusion is based
on four kind s of evidence: ( I) even in hyphal fomt>. there is n~ver a dikaryophase; (2)
they produce a~cus-like meiosporangi~ in isolation, or singly, in clusters. Or in chains, on
individuJI somatic hyphae. but never in any ):;jnd of ascoma; (2) their cell walls contain
l ~ss chitin and more mannan than those of regular ascomycetes; (3) some of them produce
yeast-like anamol1lhs; (4) some ofthem have many extremely narrow mlc ropores piere
ing each septu m. rather than a single central pore. These features. among others. argue for
the recognition of the 'ascus'-fonning yeasts as a group distinct from the ascomycctes
pro~r. J (reat them as a separate class.
Class Saccharomycctcs. Representative genera are DipodascHs with GeOfrichwl1
anamorphs. Hallstniosporu with Kloeckera anamol1lhs. and Sacchorom)'copsis with C(Jn
dida anamorphs. CUlldida a/hicuns. ",hieh produces aerial hyphae (fig. 6.2 C). and whose
teloomol1lh (if any exists) is unknown, causes ca ndidiasis. a disease ",'hich affects mucouS
membranes in various parts of the body. or may evcn become systemic. This is more ful1y
discussed in chapter 23.
The Geo/richum anamorph of Dipod<lsCliS produces hyphae whi ch break up into
thaUic-arthric conidia. but since this is a yeast. there arc subtle differe nces between th is
a nd, for e.>;amplc, the many basidiomycetous anamorphs that abo produce thaUie-anhric
conidia. Wall chemistry is diffe~nt and the septa have many micropores rather than the
single. central septal pore of most othe r hyphal fungi.
Class Holob:l~idiom ycetes (in part). A second. very different group of yeasts have
chitinmannan walls which also contain some xylose or fucose (both absent from the
Saccharomycetes). The anamorpbs in this group also lIave two modes of con idiogenesis.
Mosl are blaslie-sympodiaJ (e.g. the Cf)ptoco<:cus anamorphs of Filobasfdiellu). Others

are blastic-phialidic (e.g. Cryptococcus anamorphs of Filobruidillm). The teleomorphs,
where these are known. produce clamp connections and basidium-like strucrures. The
holomorphs are placed in the family Filobasidiaceae, and reg:ll'ded as belonging to the
holobasidiomycetous order Aphyllophorales. Cryptococcus lleojOntlOIlS, the anamorph
of Filobosidiello Ileofomums, causes a potentially serious lung disease, cryplococcosis,
which is further discussed in chapter 23. Some other genera, such as Pha/fia and Bul/era,
are known only as anamorpbs. And although the tdcomorph of Trichosporon. if one
exists. is unknown, this anamorphic yeast probably belongs here, because iUl hyphae
have dolipore septa (Fig. 6.2 E). As the diagram shows. this genus forms conidia
sympodially, and the hyphae also tend to break up into thallic-arthrk conidia.
Clllss Thliomycetes (in part). The third group are called the red yeasts, because they
cootain carOtenoid.> (though some spedes of Cryptococcus and Phaffia al so produce
these compounds). Rhod%ru/a, which produces pinkish or reddish colonies, forms blaslic-phialidic conidia from the attenuated ends of the yeast cells. SptJrobolomyce.t cells
(Fig. 6.2 F) devclop sterigmata from which asymmetrically borne s?Ores are forcibly
ejected. A se ries of such balliSlospores is formed by sympodiaJ extension of the sterigma.
Note that although the spore-shooting technique being employed here is that of the
basidium. the spores being formed are asexual mitospOles (conidia). Yeasts of this group
sometimes produce a teleomorph: a chlamydospore-like teliospore, which genninalcs to


,hlr"'ortl>rlc """"""' m





S~,.j>(r l omyc..

FIS. 6.2 Some I.IlI.ISUiII ~asts. AC: Saccharornycetes; D.E: HoIobasi<ion:etes; F: Teiomycetes.


fonn an oUlgrowth fTOm whose tip mciosporic ballisiospores are formed and discharg~d.
The red yeasts are now considered to belong in Of ncar the ord<!r Ustilag inales of the clas,
Teli omycetes (e. g. Aes.wsporoll and 5poridiobolm wilh 5porobolomycn anamo'1lhs;
Rhodosporidium \\ ith RhodOloru/(I anamorph$).
The following brief labl e gives examples of anamorphs and holomo'1lhs in each of
the three main groups of yeasls;







5accl1(! rom)"copsis





Filobas idiaeeae




Filo b(lsididl(l

Cryp l(JCOccus

USlil agi nale.'i









i\lajor group
SacCh llTOm}cetes



11 is now possible!O differe nt iale basidiomycelOus yeaSIS from saccharomycetes

by staining with bufkred dinzonium blue B. But in order 10 id cruify )'Cilsts to ge nus and
sp..~ks. one now has tochcck such features :IS: (I) the minimum. optimum. and maximum
temperatures for growth an d sporu lation: (2) gro\\th in '. he pre>ence of .<;o me t()xi (; ~om
pounds; (3) o, mot olc r~n~e (growth in high s ug~ r or salt concerllrations); H) cell morpho]
O<"!Y and method of conidiogcnesis.
YeaSlS hayc always been import.lnt to us. primarily us the producers {) f bread and
alcohol. which is stilt despile l"Omp.!lilion from oth er fungal mellboliles. and despite its
manifest dang~ rs . ou r mos t walely used and nccepted .~oc ial drug. Accounts of th~ in
volvement of yeasts in human affairs can be found in chapt~rs 10 (Fungal genetics). 18
(Fungi !IS food). 19 (Fungi in food processing). and 23 (Medical m),cology).

Furthe r Reading o n Yea sts

Arx. I .A . von (1979) rl"Op~gation in tile yeaStS and >e ast !ike fungi. pp. 555-57 1 (in)
The W hol e FlIn:;us. Vol. 2 (Ed. B. Kendrick). " mion:!1l'.luseum\ofCanada. O uawa.
Arx. 1.A. von ( 1980) A mycolo:;ist"s \"i~w of yeast.>. pp. 536 1 (in) ij iuJogy a nd Ac llvi
lies ofYe:llit5. (Eds. F.A. Skinner. M. Pas5more and R.R. Da'enport).t\cademic Press,
Arx.l. ,\ . von ( 1981) Systematics of conidial yeum. pp. 85-96 (i n) Biology (If Con idia l
FlI n~i. Vol. 1 (Eds. G.T. Col~ & B. Kendrick). Academic Press. Ne .... York .

YEASTS ' 117

Arx, J .A. von. L. Rodrigues de M i,""nda. MT Smith and D. YalTQW (1977) The Genera
OfYeaSlS and the Yeast-like Fungi. Studies in i\IycolQgy 14. Centraalburuu voor
Schimmelcultures. Baarn.
de Hoog . G,S., /l.I .Th. Smith and AC.M. Weijrnan (198 7) 1111~ E)(p~nding Rtnlm of
Yeast-like Fungi. Stud ies In Mycology 30. Cemraalbureau VOOT ,xhimrneltultUfeS,

Kurtzman, c.P. and 1.W. Fell (Eds.) (1997) The Yeasts -9 Ta'\:onomic S tudy. 4th Edn.
Elsevier Stience Inc., New York andAmSlerdnm. fA comprchen,i\'e treatment by 38
Sumson, R.A ., E,S. van Rec:nen- Hoekstra (wi th 12 others) (1988) In trodu ction 10 Food Borne Fungi. 3rd Edn. Centraalbureau voor Schimmeicullures, 8 :1am.
Skinner, F.A., S.M. Passmore and R.R. Davenport (Eds.) (1980) Biology a nd Acthilles
of Yeasts. Academic Press, New York.


lichens - Dual (or even triple)


Lichens are among the toughes t macroscopic organisms: What other group can
grow on bare roc k:, in exposed silUations subjected 10 extremes of temperature. radiat ion
and desiccation, from hot deserts to the arctic, from the seashore to the highest mou ntains
(lichens are found at over 7,000 metres on Mount Everest)? As you can sec on the CDROM versiOn of thi s, the rocky cliffs along the nonh shore of Lake Superior are
covered with lichens. So is the ground in tbe forest near Scheffcrville in northern Quebec.
So is the bark of a tree at Dingo Beach in Quecnsbnd, Australia. The intertidal lOne is
another tough neighbou rhood, and the rocks just above high tide are ex posed to desiccation, salt sproy, rain, sun and frost, often in rapid succession. Yet many rocks along the east
and WC:>I cOOSLSofNorth America are cooted with a black lichen called Vurucaria. Simple
lichen associations also grow beneath the surfaces of rocks in the Nam ib desert of south
em Afric a. Thcy wi!! grow wherever the air is clean.

Anatomy: Lichen = Fungus


W11 at is thc lichens' secret? They are dual organis ms. Each lichen combines the
talents and strengths of a fungus (the mycohi ont) with those o f at Ieasl one kind of alga
(the phycobiont). The fungus obtains water and minerals. builds a complex thallus. and
produces sexual and asexual reproductive st ructures. TIle alga lives a nd photosynthe
si ~es within the fun gal thall us, and although algae constitute only 5- 10% of the total
biomass of lichens, usu:llly conce ntrated in 0. zone just below the upper surface of the
thallus. they supply energyrich carbon compounds to the entire organism.
In nature. nO{ one of the 15.00020.000 (ully lidtcnized fungi (almost a fifth of all
known fungi. and 40% of all ascomycetes) is ever found without its domesticuted alga.
though mOSt of th e algae can lead indepe ndent existences, and many of the fung i ha ve
bee n grown in a.'l:enic culture. The degree to which the association has led to physical, as
opposed to physiological, integration varies. In the si mplest case. that o f the amazing
cryptocndolitbic associations of fungi and alg!}C recently discovered beneath the surface
of sandstone in the dcserts of Antarcti ca and of Namibia. there are no speci al dual Stro,
tures. There are a few 'filamentous' lichens. in which the algal fi laments de tennine the
form of the association. BUI almost all lichens are at least 95% fungus. and so the fungus
dctermines the shape of the emire organisllL
Figure 7.1 M shows a section through part of a lichen thallus. Jl,1ost of the thallus is
clearly made up of fungal hyph ae. Those composing the uppe r and lower surface are
dcnsely aggregated. forming protective cortical laycl"$. Inside the thallus there is more
room. and the rollnd algal cells sit j ust below the upper cortex, surrounded by fungal

11 8

hyphae. In fac t. the fungus has effectively ,\:aptured' the alga. and the relationship is one
of c)Ilptoitation or balanced parasitism rather than of mutualistie symbiosis. since about
5O'ib of the food synthesized by the alga is pirated by the fungal hyphae. which fonn tight
little cages around the algal cells (Fig. 7.1 L).

The photobionts
Althwgh there are about 500 genera of lichens and up to 20.000 species, these are
al! associated with only 25 genera of eUKaryotic green algae and 15 genera of prokaryotic
blue-green algae (Cyanobacteria). About 80% of lichens contain unicellular green alga~
(most of them contain the unicellular green alga Trebollxia, which has nOt been found
free -livi ng). about 10% cenlain filamentous green algae, and about 10% contain
cyanobac teria. The phycobionts of more than 90% of all lichens are drawn from only
three genera: two green algae. the unicellular Trebow:ia and the filamentous Tnmlepohlia,
and tnc filamentous cyanobacterium, N05tOC. So lichen taxonomy has little to do with


Figure 7.1 Lichens. A,B cruslose thali; C,D fOOse thalli; E squamulose thalus: F-H fruticose
thali, note5qJarTllJles at base of podetio..rn inH; I thalus reieasng5OTe<ia; J coraloid isicia; K
cymical isicia; l idlen synthesis, rrebouxiJ being enveloped by its mycobiol'lt; M \I.S.
d:scoichen tlYough apotllCcial <&oma.



algae - it is essentiolly fungal ta:<.onomy. and the names given to lichens are always
those of the funltal component. or mycobiont.
About 500 lichens with green phycobionts have ar~as on or in their thu!li which
comain blue-green algae instead. These anomalous. often wun-like. areas are c.:llled
cephalodia. Three-pan lichens are found in such common genera as l.obaria, Pe!ligera.
Pu:nlocyph ellaria and Sricia. In lichens cOllloining green algae, the carbohydrates
(pholOsynthates) that mO~'e ii:om alga to fungus are sugar alcohols: in lichens containing
cyanobacteria, glucose migrates to the fungus. We do not yet know how the fungus
control5 this transfer. Cyanobacteria have the usefu l ability 10 fi:<. almospheric nitrogen,
and some ofthis is also IXlSscd on to Ihe fungus.

The myco bionts

We know belw~n 15,000 and 20,CX)(} Iichcni zed fungi. About 10,000 produce only
tdeomorphic (sc:<.ual) fructifications, lI.'hile !he rest produce conidial anamorphs as wcll.
and the~ are .j.() genera of lichens which produce on!)' an:unorphs or are sterile (most of Ihese
gro .... on !eavc, in BrJzil). Over 98 % of alilichcnized fungi are ;\scomycetes, but the re are a
fc .... lichenized basidiomycetes, one of which is shown on the cover of this book.

Morphology - thallus types: crustose, foliose,

fruti cose, squamulose, leprose
:>'IU5t lichens are what we call 'd iscol ich ens: since their fungal fructifications are
apothec ial ascomata. /cmudop/li/a t ricetorom is n bit of a mouthful. but il is the name of
an ea5i1), recognized lichen which grows as a layer on the surface of roltcn wood. The
th:;tUus is bluish-green, while the SCAttered apotl1eial ascom:;ttA rue pink. Lealllorn X) lophila
proJu,e) e\ongal~d whitish thal!i embedded in the Sllrface layer of many of the larger
dec orticated logs tllat have wash ed up alung Ihc beach bdow my house. hs aputhccial
ascomala afe a deep red with a whitish margin , Cutuplaea produces brilliant orange
apothccial ascomala on findy lobed orange thalli that grow u\er rock surfaces. Purmeiia
produ,es grey 10 grun lobed Ihalli lhal often form bTge circular colonies on rocks. [ts
apolh~dJI ascomat:l, are brownish cups conCentrDled toward the ce ntre of the colo ny.
u/i:ariil columbiana i, an upothccial li<:hen that grows on dead branches of trees in
westcrn Nonh America. It has a delicately brunched. bright yellow, lacy thallus bearing
bro\\" apolhecial ascomata. The fine. brunched. }'ellm.-green th ~lIus of U$U~fl hangs
down HI strands from tree brunches, and may bear small apolheda. We need to categoriL<:
the~~ \~ry diffcrcnt thJlli, at !cast for lhe sake of comm unkat ion an(! convenicnce.
Of the lichens just mcntion~d. lcllladophi/(1 il!ld LecwlOl'a arc closely pressed to, or
even embedded in. Iheir substratc. and are tcrmed Cf ustose (Fig, 1,1 A. 8). Calap/,,!u and
Panu/i" are attached to the subslr.lte by thread like rhizincs produced from their lowt"r
cor.!~. and arc (at least in throry) separJble from thdr substrate. Thdr lobed appearance
ghc, suc h thJlli the nam e foliose (Fig. 7.1 C. D). Lerhmia and U~'l1ra grow ~way from
their substr~tcs ~I\d often branch r~pe~tedl y: th~y ~Ire called fru ticl)se (which means bush 1ik~ :l:1d has nothing 10 do with fruit )(Fig. 7.1 F-H ). A fourth kind of thallus is c:<'cillplified
b~ !I1:my species of C/"dQllia. wh iCh are basically made up of many small upturned scales.
somttimes derived from thecr<icking and frugment.:llionof acruSlose thallus. This kind of
thallu s, ofl~n found on soil. is calkd ~q uam u lose (F ig. 7.1 E). SpeCies of Claril)lIia are
UI1U'lJu! in that they often have dimorphic thaUi. with ~qlJamlJlcs on the substrate. and
uJlri,ght, sometimes br.lnched fruticose structures called podeli~. which frequently bear
RproduClive organs - apothecial ascom:l1a. pycnidia\ conidiomata and c,'en soredia
(see below). The fifth and last ki nd of thallus is the Icp ro;;e. in which thc entire thallus is
mao: up of loose, powdery, sorcdia-like materi al.


Sexual reproduction

most lichens. asdiscussed abovc. art apothecial. some. such as l'ern/clITia.

produc<: flask-shaped perith<:da (sec chapter 4), and some , like Raced/a, Pyre/I Ilia 3nd
Arthonj(I, have pseudotheda containing bitunicalc asci (c hapter 4 again). Some. like
l.Lproria. never reproduce sexually. About 20 lichens jnvoh 'c basidiomycetes. Perhaps
the most common is Omphalino eriecfOm ll!, shown on the coverofthis book. in which the
mycobiom is (as the name implies) a smalll(garic.

lichen asci and ascospores

Lichen a,c; tend to m~!Ure ler)' slowly. since tile energy to produce them is capIUr~d slowly by the algae. At any given time, relmively few of the asci in a lichen
hymcnium will be ripe. and the kind of 'puffing' so orten cen in free-l iving apothecial
fungi like Pc:J~a never happens in lichens. Some lichen asci are unitunicateinor<'TC ulatc.
others are bitunicate. Some of th ose are oflhe 'jack-in-a-box' kind we have already se~ n
in the Dothideales (chapter 4): but others. especially in lhe very b rge order Lccanoralcs
(which has nearly 6.000 spedes). have a diff('rent kind of billinicat<! asc i thai spl it at Ihe
tip, after which part of the inner wail sometimcs emerge s_ Such asci are called, rather
c lumsily in my opini on. archlleasceo us. There is speculation (ha t they may represent the
ancestors of today's 'jad.-in'lhe-bo,,' bitunic<lte asci. and bal'C survived in lichens bt:cause tile shooting of ascospores isn', as \'i131 to them as it is to nonlieheniz~d asromycctes.
Lkhen ascospores vary \lide1y in morphology. [n Penu.f(lrio there is one large
ascospore per ascus . In Acarospom there may be up to 100 spores ~r as(:u~, A,cmpores
m~y be ameros porous (singlc-celled). didymosporous (twocel led) or diclyoSporolis (nl~ny
cclkd). and as me ntion(d. they rip<;:n ,"cry slo,,ly. only a few being mat ure al nny given

Asexual and somatic reproduc tion

Although the obvious frui ting ~truclUres of moSt lichelU are the fungal tekomorph.
m:my lichens also produce p ycnidial a n omor phs, whil;h can bt: seen around the edg(s of
C{"'!OIlia fl)'xidara p(xktia as small dark dots. ~'I:my lichens also produce specialized
's,omatic propagules: In sume. Ihe upper su rface o f Ih~ th\lllus ruptures. e"posing a
poy,dery mass o f pro~g ules called sorcdia. which arc sm31l sroups o f cells en
tangled in fungal hyphae _ Sometimes the entire thallus is basicaily powdery (lepra>e).
Ano ther kind of asexual reprodu ~tion involve, small. [jnger-lik~ or branched structures
calkd i'M ia. which grO"' up from the thall us. then break off. Some rcpres.:mmi\'es of
certain genera produce only isidlo. olbers only soredia. Lichcn~ that reproduce ase)(u~lIy
are k~ ~ llkely to form .l;;COmala.

the mOSt common accC5sQry struc tures are the podet ia of such squamulose
genera as Cladollill. Thesc arc large. upright. often branched Structures which generally
ha,-e onc or more apothecium like cups at the top. These may in fad become s ingl ~ red
apotheda, as in Cindonj" COCci/em , or they may bear smaller. variously col()ufcd apot h~
~cia around the rim. or they may ha"e tiny anamorphic, flaskshap.:d pycnidill.l e<>nidiomat:t
arouad the edge, as in CladO/Iia p,I'xidafll. The surface of the podetium may also be
covered with powdt:ry sorcdia.

Taxonomic groupings
Although thae arc twelve almost entirely li chenized orders of ascomycete s. ond
four more with some hchenized members. I 3m goin g: to men tion only eight of the !;Irg(f
or more common orders.

( I) Order Arthoniales: 17 genera, 650 species. with green algae as phycobionts.
Thalli mostly crustose. with apolhecioid or lirellate (long and narrow) ascomata, producing bitunie~te asci.
(2) Orde r Graprudales: 30 genera. 1,700 species, with green phyeobionts. Thalli
crustose, with apotbecioid or lirellate ascomala. containing unitunicate-inoperculate asci
y,. ith a thickened apex rather like that of the Clavicipitalcs.
(3) Order Leeanorales: 300 genera, 5.700 species. with green phycobionts. Crus
lose, squamulose, foliose or frulicose Ih:l.lli. with apothecioid ascomata producing
archaellSceous asci (primitively bitunicate?) This huge order is home to many of our
commonest lichen genera - Ciadonia (includ ing 'reindeer moss; C. rangiferina. and
'British soldier: C. coccinea), H)pogymnia. I.etharia . Panne/io, and Umbilica r/a ('rock

(4) Order Opegraphales: 35 gencra, 900 species. with green phycobionts. Thalli
are crustose or fruticose, with apothecioid or lirellate asc:ornala, and bilunicate asc i.
(5) Order Peltigerales: 18 genero, 600 species. usually with blue-green phycobionts.
Foliose malli wim apothecioid ascoma!a producing archaeasccous asci.
(6) Order Pyrenul<lIes: 35 genera, !.ISO species. with green phycobion!s. r-,'Iainly
crustos.e, wilh pseudothecial ascomata containing bitunicate asci.
(7) Orde r Teloschislales: ! I genera, 600 sJ)C'cies. with green phycobionls. The
thalli are of all four main types, bearing apothedoid a~omala with Z1rchaeasceous asci.
and also producing pycnidial anamorphs.
(8) Order Vcrrucariales: 25 gener~, 700 species, with green phycobionts. Usually
crustose. rock-inhabiting lichens wi th pseudothecial ascomata and bitunicate asci.
The discipline of !ichenology has until fairly recently been conducted OUlside the
mainstream of mycology, because the dual organisms vcereconsidered so radically different from non-licheni zed fungi in nutrition. ecology and li fespan. Bm it is being increasingly ~alized that me life processes of lichens. including their biotrophic nu uition. ue
nOt rellily alie n to those of many other fungi. and we can anticipate increased integration
of this large minority group. as specialistS in Ii chenized and non-1icnenizcd fungi exchange infommtion and ideas. At least OfIe important refcTence work, the Dictionary of
tile Fungi. now covers both groups.

Identification of lichens
Lichens produce abolll230 unique compou nds which arc called 'lichen substanccs:
These are mainly weak phenolic acids. derivatives of orcinol or bela-orcinol. They include depsides, depsidones. and dibenzonfuran derivati\es such as usnic acid, which has
antibio tic properties. The indicalor, litmus, is obtained from depside-containing lichens.
Some of these unique lichen substances are routinely used to identify the genera ::md
species that produce them. KC)'s 10 lichens often call forchemicalteslS with 10% aqueous
potassium hydroxide (KOH). chlorhle bleach (el) and 5% alcoholic pa raphe nylenedi
amine (PPD). These. when applied in various sequences. combine with depsides and
dep.idones to gh'e characteristic yellow. orange or red colour reactions. Professional
lichenologi,ls can't stop al this level: accurate identification of many Hchens calls for
more refined techniques. ( I) RecrystaUilDti on of lichen substances: these are first leached
out of the thalli by aceton<:. th<:n redissolved in 3 glyceri ne/alcohol mix with some water.
orthoto!uidinc, anilinc or quinoline added. Heating causes recrystallizntion. gene rating
characteristic shapes, and colours observed under UN. More precise identification can be
anained by resorting to: (2) paper chro"!:l.lography, or (3) thin layer thrnmatogr:l.phy
(These procedures are necessitated by the existence of a5 many as six 'chemica! stra.ins

within some lichen spedes. These may look ell3ctly alike, hut their chemistry diffcrs, and
though they often have different distributions, these frequcntly over!~p), (4) DNA analysis, of various types.

lichen synthesis
The very exiStence of the slowly developing lichen ascospores is something of a
puzzlc. because when they are eventually released, no algal cells go with them . This
means that if the ascoslX'res are to establish a new generation of lich ells, they must
encounter an appropriate alga, and this in turn implies that lichens must be constantly
resynthesized in nature. The only problem with th is was that for many yean; all our best
effortS to synthesizc lichens from their component fungi and algae failed. Only relatively
recently was the trick finally mastered. It involvcs having each of the prospective partne rs
in a thoroughly debilitated condi tion. Only then. it seems, will the fungus literally embrace the alga, and only then will the alga permit itself to be co-opted without making the
ultimate prOl:est.
In a successful synthesis, the fungal hyph ae grow around each algal eel! and produce a ppressoria on its surface. Ii appears that, once the alga is in this situation, its
physiology is subtly altered. While it more or less normally, it becomes very
'leaky: losing large quant itie s of soluble carbohydrates. Trebou:Iio leaks ribitol.
Tnnrepohfio leaks erythritol. and Nostoc leaks glucose. All of these are quickly absorbed
by the fungus, and convened into typical fungal carbohydrates such as trehalose. This is
interesting in vicw of recellt work sugge >ri ng that high levels of this sugar are one of t):le
sccrets o f surviving cxtreme desiccation

Growth rate and longevity

Sincc the sustaining alga usuall y makes up no more than 5-10% of the thallus, and
since lichclls ill exposed situ ations will be dried out during much of the year, it is apparent
that we can' t cxpect lichens to grow very fast. And in facI, they dont. since 1-4 mm per
year is a respectablc ralc for many li chens, though some grow faster and some muchslower
than that. Their tough, resistant thalli, and their ability to sit out dry or cold conditions,
resuming metabolism quic kly when wetted, seem to have conferred on them great longevity: some liche n colonies arc reputed to be 4 ,500 years old, giving the ancient bristlecone
pines (Pinus aris/a/a) of the Wh ite Mountains in California some inconspicuous competition for the title 'World's o ldest li ving thing.' This represents an amazing change from
the discomycetes, with their ephemeral fruiting bodics.

After taking colony mcasurements on many gravestones. which were, of course,
dated, Iichenologists were able to calculate past growth rates. This enabled them. for
example. to help glaciologists determine how long it has been sin~ panicular rock faces
emerged from under the ice of retreating glaciers.

lichens and air pollution

Lichens can tell even urbanites something impo"ant about their habitat. Since
lichens have no roots or other specialized absorptive organs, and since they often live in
soil-less habitats. they are dependent on the rain to bring them mineral nutrients. As we
know. the rain over much of eastern Nonh America contains dissolved potlutants especially sulphur dioxide as sulphurous acid. Lichens are CJltremcly susceptible to the
deleterious effects of acid rain, and /T\3J\y cities are essentially lichen dese"s. Fish, u~s.

li chens: all are like the canaries that miners used to take down the pit - ultra,en,iliye
indicators of dangers 10 our, elves and to the entire biosphere.
As a footnote to this chapter. I Fed I must mention the case of the bitunicate ascomycete. Mycosphaerella ascopfJyl/i and its host. the brown marine alga, Ascophyllum
11odOSllm (an inhabitant of the Atlantic ocean). Aseomata of Mycosphaerella are invariably found embedd~d in the tha llus of Ascophyllum. Since th~ fungus is always present.
this may indicate a kind of reversed lichenization, with the alga providing the thallu,. and
the fungus some ki nd of growth substances (or perhaps it is just a universally d istributed
pnmsite - no one has yet done the research necessary 10 establish the facts) .

Lichen phylogeny and evolution

Unlike many other grou ps, lichens have no common ancestor: only a wid ely shared
symbio~ic proces> that has arisen time and time again as a result of natural affinit y, opportunity. or need. The polyphyletic nature of li chens has been conclusively demonstrat ed
wilh molecular techniques. The lichen, are really a nutritional. rathcr than a taxonorruc.
Since the basidioma of Omphalina aiee/on"" does not contain algal cell" and
since other species of Omphalina are not licheniz~d . we think that this one is still evolving into th e lic hen co nd ition. Other fungi may be evolving away from the lichen state.
These could include non-lichenized mcmbers of the Lecanorales and Arthoniales.
It has been suggested that if life were to be found on another planet. it might well be
liche n-like. I consider this to be unlikely. because the existence of lichens depends on the
previous existence of the two founding races - fungi and algae _ neithe r of which is
an) thing hke as tough as the lichen association. If conditions on other planets arc as
n~sty as we suspect. we should look in the Ar~haeb~cteria for the ki nd of l ife - foml~ that
might be found .

Furth er Reading about Lichens

Ahmadjian. V. and M.E. Hale (Eds_l (1973) The Lich ens. Academic Press. New York.
Ahmadjian. V. and J.B . Jacobs ( 1981) Relationship between fungus and alga in the lichen
C/m/oaia cri.~Ia/el!a. Nature 289: 169- 171.
Br()(lo. tNt. (198 I) Lichens of the Ottawa Region. S}"llogeus 29. National Mw;eums of
Canado. Ottawa.

B.W., M.S. Baddeley and D.L. Hawksworth (1 973 ) Air Pollu tion and Lichens.
Athlone Press, Un iversity of Lond on. London.
FrieJllnnn. E.!. (1982) Endolith ic microorganisms in the Antarcti ~ cold desert. Science
215: 1045-1053.

Hak . I\I.E. (1983) The Biolog,Y of Lichens. 3n:1 Edn. Edward Arnold. London.
Hale. \I.E . ( 1979) Ho w to Kn Oll" the Lichens. 2nd &In. Wm . Brown. Dubuque.
Ha\\ksworth. D.L. and OJ. Hill (1984) Th e Lichen-Forming Fungi. Blackie, G lasgow.
Ha\\ksworth. D.L. and F. Rose (1976) Lich ens as Pollution i\-1onitors. Studies in Biolog)
1\0. 66. Edw~rd Arnold. London.
Hawk,v,orth. D.L. (1988) The variety of fungal -algal symbioses. their evolutio nary significance. and the nature o f lichens. Botanical Journal of the Linnaean Society
96: 3-20
Hawksworth. D.L. (1988) Coevolution of fungi with algae and cyanobacteria in liche n
symbioses. pp. 125-148 (in) Coevolution or Fuog i with Plan ts and Animals. (Eds.)
K.A. Pirozynski and D.L. Hnwksworth. Academic Press, Lon don.

Kendrick. B. (1991) Fungal symbiosis and evolutionary innovations. pp. 249261 (in)
Symbiosis :is II Source of Evolutionary Inno vati on. (Eds.) L. Margulis and R.
Fester. MIT hess. Cambridge.
Richardson. D.H.S. (1975) The Vanishing Lichens. Their history. biology and importance. David & Charles. Newton Abbot.
Richardson. D.H-S. (1992) Pollution Monitoring with Li<:hens. Naturalists' Handbook
19. Richmond PubL Co.. Slough.
Seaward, M.RD. (1977) Lichen Ecol ogy. Academic Press, London.
Smith, D.C. (1973) The Lichen Symb iosis. Oxford University Press, OXford.
Smith, D.C. (1978) \Vhat can lichens tell us abuut real fungi') i'lIycologia 70: 9 15-934.
Viu. D.H .. J.E. Marsh and RB. Bovey (1 988 ) Mosses, Lichens an d Fe rns of Northwest
North America. 296 pp. Lone Pine, Edmonton.
Vobis. G. and D.L. Hawksworth (1981) Conidial Lichen -Fomlin g Fung i. Pp. 245-273 (in)
Biology of Conidial Fungi (Vol 1). (Eds.) G.T. Cole and B. Kendrick. Academic
Press, New York. is a co mprehensiyc and beautifully illustrated web sile
explores many aspects of lichens and thcir ecology.





Spore Dispersal in FungiAirborne Spores and Allergy

Fungi cannot walk or run, but some can swim, most can soar, a few can jump, and
some must be carried. From your rcading of the taxonomic survey in this book, you can
probably put a few names in each of the categories I have just mentioned. At the beginning of the book, when I was defining the word 'fungus' I concentrated on the unusual
somatic morphology and the heterotrophic, osmotrophic nutrition shared by most fungi.
But P<'rhaps I did not place enough emphasis on one of the main rcaSDns for Ihe success of
the fungi: their abili ty to produce and disperse vaS! numbers of tiny, but often highly
characteristic and spec ialized, spores. By sheer fecundity the fungi make sure Ihm, whenever and wherever a new food substrate becomes available. they will be on hand to exploit
it. "'Ian y fungi are cosmopolitan - you could find them almost anywhere in the world.
Thc air we bre athe sometimes contains more Ihan 10,000 spores per cubic metre. The soil
contains astronomical numbers of spores, wait ing for food. Why are there so many? How
did they get there? What significance do these numbers hold for us? This chapler will try
to answer those questions.

Chemotaxis - swim for it!

The taxono mic survey recogn.ized five Phyla of fungi. Each oflhese has solved the
problems of dispersal in its own way, though some methods of dispersal have been invented more than once, and sometimes the parallelisms are striking, as yOll will sec. The
Phyla Chytridiomycota. Hyphochytriomycota and OomycOla are basically aquatic , so
their spores are often equipped with flagella.
In the Chytridiomycetes eac h zoospore has one backwardly-directed whiplash flagellum. and it swims like a spenn. In the Hyphochytriomycetes, the single tinsel flagellum is forwardly directed. In the Oomycetes, each zoospore has two flagella. on c whiplash
and one tinsel. These zoospores, once liberated from their mitosporangia. may embark on.
a random search for a new substrate, in which case their chances of survival aren't good;
more [O!1unate spores are given a chance to llse a Spe<:ial talent they possess for ascending
a chemical gradient toward a food substrate. For example. th~ zoospores of Pythium and
Phyrophlhora. many species of which parasitize the roots of plants, fiod their hosts by
tracing the source of thc sugars and other chemicals that leak out of root cells. Some



chytrids that attack nematodes detcct and swim toward substances emanating from the
bodily orifices of the worms. TIlls process is called chemotaxis (see also cbapter 15).

Airborne Sporangia and where they got to

Some oomycetes have become parasites of the aerial parts of plants (remember the
downy mildews in chapter 2). Hopping from one plant to another is no job for a spore Iha!"s
designed to swim. In response to this selection pressure, two completely new structures, the
aerial sporangiophore and the detachable, "\\inddispersed mitosporangium, evolved,
apparently in tandem. And they have changed the biological history of the planet.
The microscopic sporangia of downy mildews develop at the tips of sporangiophore branches, have a very narrow attachment to the cell thai produces them, and are


Fig. 8.1 Spread of Phytophthora inicstans. A: in eastern North America 1843-1845. B: m Europe
during 1845.

easily disloosed by wind or rain. Landing by chance on an other leaf. those of mo~t
spedes re,-en to their ancestral behaviour. and require the pn:sence of a film of free water
so thaI they can release motile, bifiageUate zoo.pores which swim off to infect the plant.
usually entering through the Stomales. In a few of the most highly evolved oomycetes.
members offarnily Peronosporoceae. the airborne sponlngia produce a germ rube . The;e
fungi appear to be cutting their last link with the aqUJtic life of their ancestors.
As I mentiono:<i in chapter 2, the human species is probably the most impon:ml
vector for many fungi. One imponant example of this is the oomycete Phyrophlhr)f(l
ilifes/(Jl1s, which causes late blight of potato. Human tran<,QCe::mic commerce inadvertently carried Ihis Central American fungus to nonheastern Nonh America in 1843, and to
Europe in 1845. I say 'inadvertently' because at that time no one even knew the fungus
existed. or what it was capable of. The maps reproduced here (Fig. 8.1) show how, after
th:se introductions, it~ natural spread proceeded. Airborne sporallgia were obviously a
successful invention.
The structures associated with selmaJ reproduction in :lYgomy~tes are very conser'ative. Zygosporangia are basically tiny, look-alike. thick-walled, resistant capsule, designed to survive hard times. But in a few case, they may also ha"e some adaptltions for
dispersaL The antler-like outgrowth s of the suspensors in Ph)"com)"cts blakesleeal!llS
mlke the "Whole structure a 'micro-bulT' that could be unknowingly picked up and carried
lway by a passing arthropod.

Non-motile Sporangiospores
Zygomycetous Anamorphs
When wc look at the lMmorphs of zygomycet~ s. we find a bewildering diversity of
form and function. We can di stinguish four mai n kinds of di spersal mechanism. and
s~\~r.ll sub-categories.
(I) Large. spherical , columellatc rnitosporungia each containing hundreds or thous.::.nds of spores (Fig. 3.4 A). But the generally similar form of these spor.mgia is not
rdkc\~d in their dispersal techniques. (A) In some c)(umplcs the spores are produced in a
slimy malri.~ . This may be SUlTQunded (i) by a thin but persistent membranc (peridium). as
in Phycr)mYCt.f l1il<:IIS. or (ii) by an equally thin membrane that dissol \'es and e:c.poscs the
~pore drop. In many J//lcor species Ihe e.\ posed mucilage imbi~s water and swells to
S<!'eral tillle~ its origir.a1 silc, often supported by a collar-like remnant of the peridium.
Thi. is a mlkcd spor~ drop. and is often an adaptation for di,persal by small animal
\C Cto~. (B) In othe rcas ~s th e ~po re ~ are dry. so th:\t when the pcridium rupture s. they can
blo ..... awuy on the wind. e.g. Rhhopru siolorlifer. (e ) In the third group, the spore m:lloS is
"iolentl}" d ischarged. This technique has been evolved by onl y on~ gentlS of Z)'gom;.cctes, Pilo/m/m (Fig. 3.6 A-C). a specialized inhabitant of the dung of herb ivorous
m~;nmals. In order to sur. ive, (his fungus mUSt gel its spares away from the dung and 01110
th~ prospective diet of the animal concerned. The subsporanginl vesicle of this fun gus
ruplllre<; when internal pressure rc~ches about seven atmospheres. and e~pds th~ spore
mas~ to adislanceofup to two metres - far eoollgh to gct it away from e\'cn an elephant's
hug~ <J~posi\.

(2) Small. b "-)pored sporangia (sometimes called s porangioles). In such puta-

ti,d> intermediale genera as Thumnidium (Fig. 3.4 D) Io.rge and small ~porangia coc .~ist.
The ~ m:\ll sporangi a ofte n break off und are wind dispersed. wh Ile the large sporangia
remain in place and act as slimy spore drops. T/!Qlflllidium is unusual in this two-pronged
allocation of reprodocth'e resources. Hdicoslylum produces mul!ipl~ sporan gia with red~ced spore Illlmbc:rs. Other genera like B/akt.!leu. produce ~porangia wilh very few spores
(Fig. 3A 8),


(3) Specialized merospor:mgia. These are unusual small mitosporangia .... hich of!en
contain a ro.... of spores, as in SYlluphalis (Fig. 8.2 A) and Piplocepl1(1lis (Fig. g.2 8 ). AI
maturity the sporangial wall breaks down and the SpOTCS are se t free. MUltiple
merosporangi:l are usually fonned on a Spo!ei~! hcad eel!. which may break off and cany
the spores aWli) with it. Merospomngia may be: (A) dry and their spores wind-d ispersed,
or (B) slimy and sticky.
(4) The logical end-point of this reductive process is a single-spored mitosporangium.
which is in fOlct found in man y genera. These arc often vinually indistinguishable from
the conidia of dikaryomyeotan anamorphs under the light microscope. but they h<lve an
outer sporangia! wall and a complete inner spore wall which often also fills and occludes
(blocks off) the stalk (Fig. 8.2 C). so release is often by mellolyti.; rupture of the stalk.
Oitaryomycolan conidia (the mitospores liberated by moulds). probably the most nllmerOtiS and import~nt fungal propagules of all. dont have separate inner and outer walls, and
retnin cytoplasm ic con tinuity with their p.1rent ce ll unti l release. wbic h usually occurs by
schil.oly tic separation of the components of the basal double septum (Fig. 8.20). ( A) The

A; Syncep~ JIi~

B PiprQ~,pn.lIs






co~spot9d .~..,myeola~
spo'a~ I <>!.

Ftg.3.2 t.lerospoo-angia, spoiangioles nrod conidia.

D. DI~"" ~mY<:Olan


ooe-spom:! sporangia or Cwmillghamtlfa are dry and wind.dispersed . (8) The umbellate
sporocl adia of Kick.ul/(I produce their sporangioles in a drop of slime. (C) The sporangiophores of some dung-inhabiting genera are very tall. and elaborately branched or
coiled, as in Spirodact)"lon (Fig. 3.4 F). I think these stroccures play an important part in
spore dispernll. becoming tangled in the haiTof thesedenlar)' rodents on whose dung tbey
grow, and being ingested during grooming acti vities,
In the Entoffiophthorales, one-spored mitosporangia are actively sbot away by three
different mecbanisms: (A) In EnfOmophrMra muscat(Fig. 3.6 E), the apex of the sporangiophore ruptures to expel the sporangium. Cytoplasm from the sporangiophore goes with the
propagule, and may help it to stick to the substrate when il lands. (8) Species of BasidioOOlus
have aline of weakness around the sporangiophore just below the apex,At maturity, the wall
spli lS there, and the spore flies away with part of the sporangiophore attached. As in a twostage rocket, the sporangiophore fragment falls away during flight. (e) In some species of
EmomcphlMra, and in ConidWbolus, the mitosporangium is projected by the release o f
pressure built up between the sporangium and a tiny. intrusi~"ll columella.

Ascospores - Shot or Not

[n Ihe taxonomic section of this book it is made dear that Ascomycetes and Basidi omycetes. though they may look very d ifferent. appear 10 have arisen from a common
ancestral group. Many of the superficial differences between their teleomorphic fl"1Jclifications can be traced back to the different kinds of meiosporangia they produce: asci and
basid ia. It is worth comparing the mechanisms of these vital cells lind the ways in which
they have probably affected the evolution of their respective teleomorphs,
Firsl. tbc ascus (Fig. 4.3). which seems originally 10 have evolved as a tubular spore
gun: an elongated cell within which. once tbe spores have matured, turgor pressure builds
up untillhe tip of the cell bursts and the ascospores fly out. You will remember the two
ba~ic lines of asci. First, the unitunicate ascus with either: (a) an operculum or lid, opening
around a built-in line of weakness at the moment of discharge; or (b) an elastic apical ring
which either strelches enough to let tbe spores pop out through an apical pore. or turns
inside ou t as the spores leave, Second. the bitunicale ascus, in which the inner wall
expands upward after the thin outer wall splits, then shoots the spores out of an apical
Different ways of ach ieving lhe same end. In each case, the basic function of the
ascus is more or less the same. And moSI asci still CQfIform to this norm, At least those that
have some acress to the outside world do. Some are borne on apothecial ascomala in
e~posed layers (hymc nia), They c;m 'shoot at will.' whenever they are mature. Anyone
who spe nds much lime looking for fungi will e~perience the phenomenon of 'puffing' in
apothecial ascomat3. This happens when atmospheric humidity changes suddenly and
thousands of mature asci expel their aSC05pores simultaneously, producing a smoke- like
cfoud of ascospore!. Tbe theory of puffing is that Ibe many simultaneous jets of ascos pore s generate a general movement of the air above the hymenium, which carries the
spores muc h further than if the asci fired individually. Cookeina Ju/cipes (Ascomycetes,
Pezilales). a colourful tropical cup-fungus, produces 215.000 asci per cm'. which liberale
1.720.000 ascospores. Cook~i_ asci are straight. but their lids develop on the side toward the light. so the spores shoot in the right direction.
The asci in some apothecia have evolved li ght-sensitive mechanisms in th eir tips.
so that they can aim their spores tOward the light (e.g. Ascobolus). Other asci develop
inside ascomata that open to the outside world only by a narrow pore (an ostiole). These
asci are more protected during development, but they can't aU fire at once; they have to
take turns, Each ascus, as it ripens, must stretch righl up the neck of the ascoma to the


ostiole before it can shoot its spores. Some ostiolate (perilhecial or pseudodlecial) ascomata
have light-sensitive necks, making sure mat their asci shoot toward the light. This is
especially imponallt to fungi growing on the dung of herbivore s, (e.g. Sordaria and
Pod05pora) which must gCt their spores away from the dung and onto the plants Iheir host
animal will eat.
The site of a projec tile has a considerable influence on its range. In Ihe dunginhabiting Saccobclus the e ight ripe ascospores are glued together, and are expelled as a
single projectile. Since Saccobolus is one o f the commonest fungi found on dung. there
must be some advantage to this strategy. Podosporajimico/a, whose ascospores are large
anyway (averaging 54 x 37 !-1m), shoots all eight as a unit, and so achieves the phenomenal range (for an ascus) of 50 cm. Most asci, however, expel their spores separately. either
in a single burst or al shan intervals. Cord)"ctpS mililans (Fig. 4.18 D-F) has " ery long,
narrow asci. with a very fine pore in their thickened tip. The ascospores are 400-500 !-1m
long, 2 !-1m thick, and arranged in a parallel bundle. A ripe ascus suddenly protrudes from
the ostiole, the first ascospore flashes out after a second or two. followed at oue-second
intervals by the others. After the eighth spore has been shot, the tip of the ascus di sappelll'S.
and is soon replaced by that of another ripe one. No one knows how this precise sequence
is executed.
And then there are asci that don't shoot the ir spores. We believe that the shooting
mechanism has been losl only in situations where it has become useless or inadapti ve.
This happens if the fungus adopts a cryptic habitat: if it fruits under bark or underground.
for example. The known te leomorphs of the co mmon mould s, Penicillium (e.g.
Tularomyces) and Aspergillus (e.g. Euroliz.m, Fig. 4.21 A) produce closed (cleistotheClal)
ascom3ta, and their asci are spherical and have no shooting mechunism. Truffles fruit
underground, so their ascomata areclosed, and their asci are spherical (Fig. 4.10 G). Thei r
spores are dispersed by mammalian vectors, which can find aoddi g up the buried a.scomata
only because thesc emit uniquely attracli ve aromas. For many years, the French hunted
truffl es with the aid of female pigs, because these had such good noses for truffle s and
were so enthusias tic. We did not know until recently that the pigs were literally 'turned
on' by a chemicallhey normaUy encounter only when it emanates from rutting boatS. In
some suange way, truffles ha"e evolved a sporedispersal mechanism thai involves a
mammalian pheromone.
It is easy to understand why asci Ihat develop in closed aseomala don't shoot their
spores. Bu t quite a few ascomycetes wilh ostiolale ascomata have adop ted the same habit.
10 the celluloly tic genus. Chnt/omium (Fig. 4.1 3 B). the walls o f the asci break down as
the spores mature, liberating Ihem into the cavity o f the ascoma in a mucilaginous matrix..
As the mucilage imbibes water and expands, it oozes OUI through the ostiole. and forms a
long tendril or a gooey mass. Chactomium species typically ha ve a mass of coiled or
branched hairs growing from the upper part of the ascoma: these h;J.irs act as a natural
holder for the spore drop. It seems likely that these spores are set up for arthropod or rain
di spersal. rather than the original airborne route. The genus Ophioswmu (Fig. 4.21 B)
follows a very similar paUern. but here the ascoma usually has a long, tubular nec k. When
the mucilage expands, it can escape only by moving up the neck. carrying the as~'OSpores
with it and fonning a spore drop at the top, which sitson a fringe of specialized supponing
hyphae. These fungi often fruit in the tuonels of bark beetles, which pick up the ucos pores (or the conid ia of the anarnorph, another st:!lked spore drop) as they cmwl along
the tunne ls, then fly off to other trees. This is the devastating sccn!t of Dutch elm disease.
Again. human vectors brought the fungus to Nonh America, but flying beetle WCtors
have spread it ~cry effectively within lhis continent. Firsl found in Oh io in 1930, it
reached Tennessee by 19-'6. California by 1975. In Canada it was first detecH:d in Quebec

ttI1 Ul'1>E.CCB



in 1946. In fifteen >'car:; it had killed more than 600,000 trees in an area of 25.000 squ~re
miles. It has $inrespread to the maritime provinces, to Ontario. and as far west as t.laniloba.
though the discontinuous distribution of the elm in Canada suggests that the fungus
reached Manitoba by human agency, or from the south.
The ascomata o f Ihe powdery mildew fUngi (Erysiphales - Fig. 4.19) are closed.
and might easily be described as cleistothee ial. But their IIsci are elongate, often grow in
a radially oriented clusler, and can shoot their spores (molecular techniques have recently
shown Ihem to be related 10 the disromycetes). $Q we must assume, despite the absence of
an 05ti ole, Ihal the ascomata open at some point. How thi s happens in the genus
Phyllacrinia is a strange story Wilh some interesting twists. The ascomata of this fungus
have twO unusual features: a ring of radiating, tapered. needlelil:e appendages; and II ruft
ofsCCTetory hairs on top of the a~ma, that produce a blob of mucilage (Fig. 8.3 A). When
the ascorna is mature, the appendages all bend downward lind lever it upward, breaking its
hyphal conneclion~ ,,'ilb the leaf (F ig. 8.3 B). It is now frtc to be dispersed by wind or
waler. When the ascoma lands on a new substl1lte, the blob of mucilage will hold it there,
in the upsidedown position, so that th~ business end of each ascu s now points futilely at
the substrate (Fig. 8.3 C). Fortunately. there is a line ofweaknes.~ around theequatorofthc


Fig. 8.3 Adl-entll"e5 of Pllyllactinia ([rysphales) (see text\.


3s<:oma. Thi~ now splits open. and the lower half of the ascoma swing~ o .. er through 180
degrees (Fig - S.3 D). Lo and behold. the asci now point outward. and the spores can fjn~l1y
be shot away imo lIle air.
The dramatic spread o f some fungi causins powdery mildews has been well-do<;:u mented. si nce they affect economically imponant crops_ Fig. 8.4 sh ows the woy in which
the powdery mildew of grape. caus-:d by neCa/or. spread in Europe after its
introduction to England (from America or Japan) in 1845. By 1851 -1852 its airbo~
conidia had carried it throughout the wine-producing countries of the Meditcrnmean.

Basidiospores - a gentle rain (but not from Heaven)

The distances to which ascospores are projC1:ted ranges from less than a millimetre
to 50 cm. Basidiospores arc much more unifonn in si~e and ballistic mechanism. and are
projected for much smaller distances : 0.005 -0. 1 em. Let us explore the reasons for thaI.
Eve ryone is familiar with the ap pear:lOce o f a mushroom. but is probably much less aware
of how it works _As a basid ioma develops. its primordium is at first negatively geotropic.
as the stipe grows upward; then as the cap (pileus) spreads out sideways . it is diagcOiropic;
finally. lIle gills 8row downward. and are positively geotropic.
O nce the structu re is mature, we can see some of its potential an d some of its
limitations. The gills represent a huge area o f hymeniu m. capable of producing millions
of basidiospores. But gills are usu all y .. ery c1os-:ly packed. If a basidiospore: was shot
further than the distance between adjacent gills. it w0l.11d simply hit the next gill, and
probably lodge there. To take advan tage o f their enormous fenile area. agaric evolution
has fine-tuned their spore-shooting mechan ism. The spores must be launched dclicmely
from thcir basidia ~nd then ~llowcd to fr~e-fall straight down betwee n the g ill s until they
reach the o~n air below the cap. whe n natural turbulence will carry them away.
The Im~st ideas about the shooting mechanism of the basidium have already been
presented in chapter 5. and there is no need to de scri be them ex haustively here _ In shott.
a large droplet secreted at the b:lse of lIle asymmeuically-bomc spore just before dehiscence. merges suddenly wi th a film of water already present around th e body of lhe spore .
Thi s pro ..ides more than adequate impetu s for disju nction.


''8- 804 Spread of pmo.wy midew of grapesr. Europe 18<15_1852.



The:re are: perhaps 10,000 spe<:ie:sof agaric, and all, within fairly broad limits, share:
a similar design - they tend to look like: open umbrellas. This is bc:<.:ausc: they are in fact
biological,umbrellas, If the hymenia of most basidiomycetes get wet, they Stop shooting
spores, since th e droplet-film interaction is 'drowned: The: umbrella sbape is so effective
that it has evolve:d over and over again , Basidiomata that look rather like umbrellas (or in
some cases , half-umbrellas) are found among the Aphyllophoralc:s (in the Cantharellaceae,
stipitate Hydn3ce:ae and Polyporaceae), the Tremellales (Pseudohydnum, Phlogioti$),
and the Auriculariales, as wdl as the ubiquitous agarics and boletes,
The annual weeds are among the: most successfu l and most recently evolved oflhe
flowe:ring plants, They have an equivalent among the agarics: the genus Coprinw;, Members of this genus have many unique and sophisticated features that earn them a place of
honour in this chapter. Coprinu.s coma rus (the shaggy mane:: Fig, 8.S) is a large and
common agaric that froits on disturbed ground in late fall, the fIrst frosts triggering formation of bas idiom at a before it is too laIC. Almost everything about Ihis mushroom increases
its efficiency as a producer of spores. The sti pe, though tall, is hollow, on

Fig. 8.5 Agarica.1es: Coprinus comatus showng gi-spacng and ~


p - ... -


:;.. ,.' J ' ...




material. The cap does not spread out like those o f most other agarics, but is very deep and
aimOSI cylindrical. Most of the basidioma is made up of a tightly packed lllT3y of extremely thin g ills. These gills are SO close together that each has to produce a sprinkling
of large. specialized cells called eystidip to keep its neighbours from touching it. In
addition, the gills are not rigorously kept vertical, as they are in most agarics. There is no
way that spores coul d be fired from the surface of these gills and reach the world outside.
No way, that i~, except one:
In most agarics, any areaof a gill will have basidia at various stages of development.
But in Coprinus the process is highl y regimented . Only the basid ia at lhe bouom edge of
a gil! are penniued to mature. Their exposed position allows them to shoot their spores.
But what about all the other basidia higher up? In order to expose them. the tissue at the
lowe r edge of the gill undergoes scl f-digestion (a utolysis). The process resolves into a
beautifu lly orchestrated sequellce. A perfectly timed wave of spore matumt ion and sporeshooting. followed immediate ly by a wave of autolysis, sweeps up the gills. The cystidia
near the g ill-alge autolyze first, so that they will nOl be in the way of the spores. As sporeshoot ing proceeds, the enlire cylinder o f gills gradually melts away, as the top three
diagrnms in Fi g. 8.S show.
The basidia of agarics may differ in size and shape, and even in tlte number of ~pores
they produce, but they are re markably unifonn in the way they carry their spores. These
always develop at the ends of tapering outgrowths of the basidium. An d in functional
(which is to say, spore-discharging) agarics they always sit asy mmetrica ll y (Fig. S.2 B),
This asy mmetry se ems to be absolutely diag nostic of basidiospores that are ac tivc ly shot
away. If yo u find a basidium with spores symme trically mounted on their Sterigmata (Fig.
S.8 A- E), you can say defin itely thaI those spores will not be activcly propelled from their
perches. Why should that matter? Well, it is an indicator of many other things that have
happened to the fungus during the course of evolution. It marks a rnd ical change in thc
biology of the organism.
As we saw in chapter S. most families of agarics have produced what wecall sequesIrate offshoots which have lost their abili ty 10 shoot basidiospores. a loss that has gone
hand in hand with changes in the development and morphology of the mature basidioma.
In general, gills become crumpled. or even indistinguishable, as the hymenium-bearing
tissues assume a loculate or spongy aspect, and in many cases the edge of the pileus, or the
partial veil , encloses the sporebearing tissues eve n at maturity. Stipes may be los t, and
basidiomata may adopt a hypogeolls habi t.
We believe that th ese fonns represen t some of the mas! reccnt evolutionary developments in the fungi. Sequestrate forms seem to have arisen independently in no fewer
than fou n een families of agarics. probably as a response to exceptionally dry conditions
which would damage the exposed hymenia o f nonnal agarics. Spore dispersal must now
be delayed until the basidioma breaks up, Of may be carried out by insectS Of mammals, In
fnet. tile California red- backed volc Clelhri()l1omys califomicus Ih'es almost exc lusively
on basidiomycetous iru ffiC!l such as Rhl~opogol1, which is a sequestrate, hypogeous derivative of Suillus (Boletaceae), and the vole may be an imponant distributor of their
Some of the orders of Gasteromycetes h~\"e colourful common names - puffballs.
enn hstars. bird 's ncs! fu ng i. earthballs, stinkhoms - that suggest their specialized methods of ~pore dispersal. Puffballs ( Lycoperdalcs) producc a mas s of dry basidiosporcs (the
gleba ) inside a papery shell with a hole in the top. Raindrops cau$C this thin outer pcridium to dimple, forci ng a small puff of air mixed with spores out through the opening.
Wind blowing across the open ing call also suck out spores. Earthstars are just puffballs
with an outer. fleshy peridium that devetops several splits running radially outward from

the The se:gments thus fonned open by bending backward. and a~ they reflex
further and further. they lift th~ gleba above the sUlTOunding leaf litter. exposing it to the
rain and wind. My riostoma has several evenly spaced ostioies.
In the biT(rs~nest fungi (Nidulariales), the basidiospores of most gener.! fonn inside
several small se:edlike packts called peridiolcs or. more colloquially. eggs. These: sit in
a deeply funnel shaped splash-cup receptacle. Which focuses and reflects the kinetic
energy of falling raindrop~. Some of that energy is transferred to the peridi oles. which are
thrown for some distance.
[n the earthballs (Scl<,rodermatales), a group otherv.'ise e:memdy passive in its
spore dispersal. there is one ahertanl family. the Sphacrobolaceae, which has rather SUTprisingly evolved a new kind of active spore dispersal. The positively phototropic
basidioma of Sphauobolm stellmu.f is only 2mm in diameter, but can catapult its gleba
- I mm in diameter - up to 7 metres, The peridium in this fungus has se veral different
layers, AI malllOty. the top splits and reflexes to expose the spherical gleba. The lower p:ut
of the ~ridium s.cp.1rate5 into two nesting cups which lOuch each O\her only al the rims.
Glycogen in Ihe cells of the inner cup is converted to glucose. and turgor pressure builds
up until the inner cup abruptly turns inside out and flmgs the gleba into space.
Sphaerobc/Il,\ often occurs on old dung. and tile evolutionary rationale for its explosive
spore dispersal is clearly similar to those for the very different mechlnisms we e)(amined
earlier in Pi/oOO/uI, SaCCobo!UI and Ptxlolpom.
The stinkhoms (Phallak;;) are perhaps th~ mOSt bi zarre members of this strange
menagerie. Thc youn g fruit body is cal led an egg. In Pha/ilrs (Fig. 5.7). the soft sllell splits
in the morning. as a d~nse mass of specialiled ti!>Sue inside tlkes up water from the
mucilage that sUlTOunds the embryonic basidioma, and elongates quickly to produce a
tall. spongy stalk. At the lOp is a receptacle. cO\'ered with a sugary but eYil-smelling
greenbh sli me in which the ba.,idiMpores are embedded. Th~ smell attracts a procession
of tlying insects, plrticularly dipteran fl ies. which gorge e.~citedly on the sl ime, llnd also
carry spores away on their feet. By evening, the green slim ~ is gone. ili m ission accomplished. The most highly e\'oh"ed phalloids seem to be those which. like Aserol. have
ba>idiomata wilh long, brighl red. r:adiating r.!ys Ihat can only be intended 10 supplement
their olfactory messag~ with a visull on~. As a plssin g vector (prob~bly a tlying an hropod) Illig ht say: "It's II flower. ;";0. it' s rotting meat. No. it's facce s !" Slr~ nge fungi i nd~ed .
that in the name of di spersal combine the qualities of flowers and eXL'rement.

Airborne Spores and Health

Spores arc mi cros~opic. >c~lcd units, Iypically formed ancl r~knsed in cnomlOUS
numbe rs. ami usually pussively dispersed thro ugh Ihe air. so that they ar~ present almost
nerywhtre. The)' contain one or more nuclei. some cytoplasm. and a minut<, food rc~r\e_
Like tiny secls. they will genninate in damp conditions to produce hyphae which. iflhey
~re luck~ enough \0 find food and mobturc, can e~tend and multiply to ~C"Ome ~ myce
limn. accumu late energy sUlpluscs. and eventuall)' make more spore~.

problem with spor~s is the same as th~l with pol1~n. Both lock any motive
po"er or navigalion~1 equipment. To make sure thai al kast a fe'" spores land in places
where Ihey will find food (c<;pt.'Cially if they are picky). fungi must liberate Ihem in
a.tronomical numbers. Some fungi are making and releasing spores from early spring
until late fall. Somc will c\'en release them in winter whe nen:r the tempcralf.lre ri:;es above
frcezin g poi nt (OC) ,
"'>cologi sts have described nearly IOO,O(X) fungi. and there is lillie doubt that
hundreds Ofloousand, more remain to be ~i5CO\crcd. Let's see just how many spores a few


individual fungi conlribute to the 101al. One specimen of me common bracket fungus.
Ganodenna applrmatum (see chapter 5). can discharg~ spores a day.
every day [rum the beginning of May to the end of Septe mocr (4.500,000.000.000 spor.::s
over the season). One fructificatiOn of another wood-inhabiting ascomycete. D(I/din;a
concentrica, can liberate more man 100,000.000 spores a day for many d~ys. A ~ing!e
wheat grain infected with stinking smut (Trlleria carie. ) can contain 12.000.000 spores.
One 2.5 em diameter colony of the green mould. Penicillium . can produce 400,CXlO.OOO
spores. Of coune. cven these huge numbers become greatly attenuated when the Spore~
are dispersed in me vastness of Ihe atmosphere. but the tOta! spore load of the outside air
is al ......ays significant, and can o n occasion be a real lhreat to health.

Funga l a ll ergies
The p rime SUSpe1:ts in respiratory allergics provoked by airborne particles were
originally the pollen gmins of plants. and mgweed (Ambrosia ~pp.. Asteraceae ). became
the villain of the piece (e\'en though most people ha"e no idea what the plants look like).
causing what is widely and inaccurately known as 'hay fe,er.' But po:oplc tended to forget
that allerge nic pollen is ac tuall y only a summ er proble m. while many respiratory allergics
persist in fall and winter. So scientists had to look elsewhere for o ther less sca$()nal
causath'e agents. and found them in the fonn of fungal spores. Skin teSl~ proved that such
spores can indeed be aliergenic.About 20% of me population is alopie, and e:tsily sensi li1-Cd by normal spore concentration. (up to 10' spores/m'). These proplc may react by
developing 'hay fever' or asthma. and may become se ns itized to a number of common
allergens. The other 80% of the popul~tion do nOI deve lop allcrgie~ so easily. The)" would
require exposure 10 higher spore concentrations ( 10' - lit spores/mi) such as occur only
during such cvents as haymaking. harvesting or grain handling. These eoncelltralions
may then produce allergic a!veoliti s (hypersen.itivity pn eumoniti s) resulting in breathlessness. Such sensitivily is usually restricted to (I single all ergen. and the condition is
u~uall)' re lated to the person's occupation (famler, grain -handler.) Many common fungi
are IlOW known to be allergellic. and more allergens 3re being recogni:ted as time goes on.
So all fungal spon:s should be regardcd as potentially allergenic. Sufferers from alkrgies
induced by fungal Spores could gain some relief by moving to hot orcold desertS. or to the
mountnins. or by tak ing an ocean cruise.Very high local con centrntions of spores can be
enCOUIHcr~d during epid<:mics of fungal plant diseases such as wheat rust. and the spore
concentrations to which fann worke rs handling mouldy hay are eXpoM:d can eventually
cause a ~erious and sometimes fatal allergic diseaseeaUcd "Farmer's lung' (Rippon 1974).
Here, repea!~ expo~urc to high concenl,Jtions of ~pores from a number of different
a ll ~rgenic fungi (oft~n spccies of p/!l1i/."illi1lm ~nd Aspergillus) can lead to ~ensiti7.~lion.
and produce acute or ~hronic symptoms. The acule stage is u$u~llr found in haryest<:rs
and threshers. who are brieny exposed to o"emhclming spore loads. They experience
chills, fever and generally fccl un\\,ell. but thcy will rceo,'er. The chronic stage is found
~mong ,ilo and mill workers who have low-level but constant e~posure to the allergens .
This is much more serio us. because it causes dcgcncru tive changes in the res pi ratory tract
which lead to obstruction of the airway. Patients become breathless after exertion. cough
constantly. and fe~l weak. The chronic stage may be a progressive cause of emphysema_
and may eventually be fatal. This disease was firsl described in Canada (Cad ham 192..;)
and is commonest in temperate regions where high rainfall encourages moulding of hay.
A simib r complaint has been seen in some ofiice workers when hidden air-conditioning
systems have. supported massive gro" th of similor moulds. Bronchial asthma is also
frequently provoked by airborne fungal spores_ usually belonging to the mould gene ..!
A/Unlaria. Aspergillus, Drechslera ("He/mimhosporil.m') and Penicillium. These spores
reach their highest numbers in fall. with anoth~r lower peak in spring.


A cautionary tale: bleeding lung syndrome and Stachybotrys

In 1993, ten cases of bleeding lung syndrome in infants in Cleveland were tentatively linked by the Federal Cemrcs for Disease Control and Prevention to Srachybo/rys
chartarum, a microscopic black mould that grows on damp paper - especially the paper
covering wallboard, Recently, the Tottenville Branch Library on Staten Island, N,Y, which
had a damp basement, was closed after a staff member had trouble breathing, and
Srachybotrys was found, Because of recurring SIl1.chybotrys contamination, there is a real
possibility that the entire Gorge Hospital in Victoria, s.c. may be pulled down and
rebuilt, at a cost of well over $30 million, The CDC has recorded at least 100 similar
instances in which a health problem has been associated with the presence of Srachybo/rys,
though there is still no solid proof that the illness has been caused by the mould. There is,
as scientists well know, a considenlble distance between correlation and causation. Are
the administrative decisions reported above reasonable? Some scientists believe that
Srachybotrys has been made a scapegoat for a varicty of symptoms which it may not be
causing. Unfortunate ly. SwchybOlr)"s has a history. There is no doubt that it produces
some nasty mycotoxins (sec chapter 21), but these have caused problems only in animals
(usually horses), and even then only if those animals eat hay on which the fungus is
growing - in other words, the horses actually consume measurable amounts of the fungus. But the Stochybotrys in buildings usually grows inside wall cavities or crawl spaces.
Certainly. no humans arc eating the fungus. So how can it get inside them and cause
sickness? As far as I can see, only by the inhalation of spores. How likely is that? Not very.
SwclzybOlrys chartarum produces its spores in tiny, slimy droplets, so the spores stay
where they are, and are not released into thc air. The only way in which they can become
airborne is after the colony has stopped growing and has dried out. and if the spores are
somehow disturbed by physical means. Interestingly enough, this physical disturbance is
likely to happen only when active attempts are made to remove the fungus.
As of September 2000, I am inclined to believe tbat the S/achybolrys scare is a form
of hysteria based on little more than the cooccumnce of the fungus and the symptoms.
and that we should not do drastic or expensivc things to remove or avoid the mould until
we are absolutely sure it is guilty as chargcd. The best remediation is to prevent the
entrance of water, and treat existing mould colonies with bleach. which kills the fungus.
In severe cases, the wallboard should probably be replaccd (though if the new board
becomes damp, the mOi,lld will probably develop all ovcr again). It might be a good idea
to encapsulate the mould with some kind of sealant spray before removing the affect":d
areas. Proper masks and protective clothing should be worn by those doing the work, and
thc mould should not be allowed to come in contact with skin. Areas such as wall cavities
or ba,ements th~t are subject to continuous or sporadic dampness should probably be
treated with a persistent fungicidc such as Benomyl (Benlute), which has low toxicity to

Spore sampling and counting

Once we know that airborne fungal spores cause plant diseases, and that they can
abo calise allergies and even some lung infections (Aspergillosis. Histoplasmosis. Coco
cidioidomycosis), it is apparent that we need to quantify and idcntify them. In theory, this
could be very difficult. because: (I) there are almost 100,000 known species of fungi,
most of which make spores; (2) there is no comprehensive publication dealing with the
id~nti fication of fungal spores; (3) the spores of many fun gi, and especially those that are





unicellular, are not particularly distinctive; with the corollary that (4) many of them
cannot be easily identified in the absence of the structures which produced them_
Fortunately, the situation is not quite as bad as it looks. All 100,000 fungi do not
contribute equally to the continuous rain of spores _fn fact, the vast majority of spores found
in the air are produced by very few fungi. Originally anallergy sufferer himself, Grant Smith
retaliated by taking a large number of photomicrographs of spores trapped by a new spore
sampler which he had developed_ It is still impossible to identify every photomicrograph
with the kind of precision we would like, but the pictures presemed in Smith's 1990 book
'Sampling and Identifying Allergenic Pollens and Molds' arc more representative and more
accurately identified than any previously assembled for the purpose of identifying airborne
spores.The spores in the air can be counted and identified in two ways: by 'viable' tech niques which depend on the germination, growth and subsequent sporolation of spores
trapped or sedimented onto a nutritive agar medium, or by 'non-viable' techniques, which
trap the spores by impaction onto a transparent slide, and so allow them to be directly
observed under the microscope. Each technique has its advantages and disadvantages.
Viable (culturing) methods allow us to identify such comnion spores as those of Aspergillus
and Penicillium to species, while non-viable (observational) methods will pemtit only the
recognition of a general 'Aspergillus-Penicillium' component, since the spores of these two
genera are yery small and very similar. But, more im!Xlrtantly, viable methods will not detect
many kinds of spores at all - slime mould spores, lichen spores, spores of obligate plant
parasitic fungi such a~ powdery mildews, and of many basidiomycetes - agarics, polypores,
gasteTomycetcs, rust fungi, smut fungi - since these do not genninate on standard culture
m~dia. In addition, 'viable' techniques take no account of dead spores, which may make up
half of the sampk. Fortunately, the so-called 'non-viable' methods enable u~ to re<:ord and
identify all of these _If a general or introductory survey is called for, I would recorrunend the
'non-viable' approach, since it detects the widest range of taxa, while if a more detailed
breakdown of some of the corrunon fungi such as Aspergilll/s and Penicillium wa~ needed,
I would suggest that a 'viable' technique be added_ My students and I have usually used a
Sarnplair impaction trap in which a small fan draws air at a constant and calibrated rate
(e.g.15 Jitres/minute) through a narrow slit, just below which sits a standard microscope
slide, its upper sidc covered with a thin layer oftrunsparem silicone grease. When the air jet
entering through the slit impinges u!Xln and is deDected by the slide, the spores (and any
other particles) tend to strike the grease layer and stick to it After a IO-minute collection
period, the fan turns off and the slide is automatically moved horizontally.a few millimetres
10 expose a new area of grease for the next sampling period. Thus a single slide can collect
a series of sample.> at one location at chosen intervals, or at a succession of localities.
A meta-analysis of 200 rcpons from around the world showed that Cladosporium
(mostly Cladosporium herbarum) represented an average of 33% (highest value 65%) of
spore counts in air samples, basidiomycetes [agarics, polypores, gasteromycetes, rusts,
smuts], 22% (43%), ascospores 14% (highest coum 45%), Aitemuriu 4.5% (13%) and
AspergiiluslPenicil/j!lm 3.5% (1g%). Twenty-one other individual taxa or groups were
also present in significant numbers. The total number of taxa actually recorded is of
course much higher (Smith gives illustrations of over 200 taxa) _
The spores of mushrooms (B~sidiomycetes: Agaricale,) are numerous in early fall
when the fruiting of these fUrlgi climMes. Since many of them live in forest" the spore
cvncentrations !e{;orded there will be much higher than those taken in cities. Rust aecios!Xlres will be most numerous in spring, urediniospores will be recorded mostly during
summer, and tdiospores in fall. Superimposed on these seasonal variutions are daily
fluctu~tions, some of which arc due 10 the timing of spore release in certain fungi. Airborne Cladosporium spores are most numerous around midday, probably as a function of
th~ wind "elocity, which is usually highest then, while Sporobolomyces peaks during the


night. A European study showed Ihat at an altitude of 2,000 me tres there are only one
quarter as many airborne spores as at altitudes below 1.000 metres.
Sin~ mOSt fungi grow 00 pl~nt material. the highest eounlS are recorded from the
countryside. those in cities be ing appreciably lower. Where viability has been tested , it
ranged from 20% to 90%. with the average sample showing o\"er SO% \'iable spores.
Wind increases spore counts. Rain h:lS three distinct effel.:ts. The impact of the first
drops tends to release spores. Soon after rain begins, ascospore d ischarge increases. But if
the rain is hea\"y or prolonged, it remo\"es most spores from the air.

The air inside buildings tends to reflel.:t the cond ition of the outside air, thou gh , pore
counts arc usually lower indoors becau~ there is no wind effect. Howe\lCr, if rooms are
d:unp, or if there is soil orpl.lOt material present, these may represent new spore sources and
counts may increase and become more diverse. Bathrooms are damp. ami moulds are often
found sporulating around windows. Kitchens have refrigerators and garbage conl.tiners.
both of which m:ly bespore sources. Living rooms often contain house pl.lOts. and both soil
and plllJ1ls may be spore sources. Air conditionin g systems, whjeh involve condensation of
moiscure, may become major sources of fung~l spores or bacteria. Activities such as house
cleaning (especially vacuuming, e.>:ccpt in the case of acentral V3!;uum system exhausted 10
[he e;(terior) and food preparation are known 10 increase airborne spore counts. The effecls
of su~h ~hange5 on the development of allerg ic symptoms are being researched, and though
there are :IS yet few proven connections betwee n individual fungal ta"\a and the onset of
respiralory allergies, properly designed epidemiological studies will, in my o pinion. lead to
the confirmation of current suspici ons. and the unma'lking of many fungal culprits.

Identification of Airborne Spores

One can aC4uire a true imprcss ion of the almost infinite variety of spores only by
personally exploring them o\"er a period of yeaI"S_ Some idea of that diversity can. how
ever. be gained from the illustrations in books such as those by [)Qmsch et al. (1980), Ellis
( 1971. 1976). Ellis and EUis (198 5. 1988). Cannichnel et al. (1980). Nag Raj (1993),
Sea"er (l9-l2. 195 1), Den nis (1978), Si"anesan (1984) and a series of \"olumes by
Breit<!"nbach and Kranzlin ( 1984 Ct seq.). Most recenlly, Smith ( 1990). coHaoorali ng with
a num ber of mycologist s. compiled a book of COIOUf photomicrographs of pollen and
spores trapped by the Samplair quantitative impaction spore Imp which he had de\"ised_

Further reading about spore dispersal and allergies

Adams. K.F.. HA . Hytk & D.A. Williams (1968) Woodlands as asourceof alkr
gens. with special reference to oo.sidiospores. Acta ,\Uerg . 23: 265-281.
Arx, J.A. von ( 1979) Propasation in the yeasts and yeast-like fungi. (in) The
W hole Fungus. pp. 555-571. (Ed.) B. Kendrick. Nalional Museums of
Can~da . Ottawa. (Now available only from Mycologue Publications.
8727 Lochsidc Drive. Sidney, S .C .. V8l 1M3. Canadn)
Breitenbach.J. and F. Kt.mzIin (Eds.)( I984C! seq.) f ungi ofSwitze.rland . \bls I-'!
Verlag Mykolosia. l ucerne .
Bulle r. A.H.R. (1909. 1911. 1924. 1931) Reseurchcs on Fungi. Vois. 11v'
Longmans, Green & Co.. London.
BllJllett, 1.H. (1976) Fundamentals ofi\ Iyrology. 2m! &In. EdwaniAmold. London.
Canllichacl. l .W. , B. Kendrick, I.L. Conners & L.. Sigler (1980) Ge nera o r
Hyp homycdes . Univ. of A!bcn3 Press, Edmonton.
Dt:: nnis, R.W.G. (1978) Britls hAscomycetes . Cram.:r. Vadu :.::.


Domsch, K.B. & W. Gams ( 1972) Fungi In Agricultural Soils. (fransl. P.S
Hudson) Wiley, Ncw York.
Domsch, KH .. W. Gams & T.H. Anderson (1980) Compendi um of Soil Fungi
Yols I & 2. Academic Press, NY
Ebner, M.R., K. Haselwandter & A. Frank ( 1989) Seasonal fluctuations of
airborne fungal allergens. Resource 92: 170-176.
Ellis, M.B . ( 1971) Dematinceous Hyphomyntes. Commonwealth Mycological In stitute, Kew.
Ellis, M.B. (1976) More Denlllllnceoos Hyphomycetcs. Commonwealth ~I y_
cologieal Institute, Kew.
Ellis, !-.LB. & J.P. Ellis (1985) Mierofungi on Land PhuIL~. Croom Helm.
Ellis. M.B. & J.P. Ellis (1988) 1\'lM::rofungi on l\'1isceJlancous Suhst ratcs. Croom
Helm. London.
Gregory, P.H. (1973) i\'licroblology of the Atmosphere. 2n d Edn. Leonard
Hill. Aylesbury
Gregory, P.H. & T. Sreeramulu (1 95S) Air spora of an eS1U ~ry. Transactions of
the Brit ish Mycologica l Society 4 1: 145-156.
Hi rst, 1.M. (1953) Changes in atmospheric spore cnntent: diurnal periodicity
and the effec ts of weather, Transactions of the British i\'lycologicnl
Society 36: 375-393.
Ingold. c.T. (197 1) Fungal Spores: th eir Liberation :tnd l)islK'l'Sal. Clarendon
Press. Oxford.
Kendric k:, B, (1990) Fungal allergens. pp. 4 1-50(in) Sampling and Identifying All ergenic Poll ens and illolds (Ed.) E. Grant Smith. Blewstone
Press, San Antonio, T",.
Kendrick. B. and F. OiCosmo (1979) Anamorph-Tdeomorph tonnections in
Ascomycetes. (i n) The Whole fung us. vol. I. (Ed.) B. Kcndrick . Nut.
Mus. Canada. Ottawa. pp.283-41O.
Kendrick. S. and T.R. Nag Raj (1979) Morphologicallcrminology in Fun gi
Imperfecti. (in) The Whole Fungus. vol. J. (Ed.) B. Kendrick. Nat. Mus.
Canada. Onawa. pp,43-62.
Kendrick. B. and R. Watling (1979) Mitospores in basidiomycetes.(in) T he
Wh ole Fu ng us. yo1. 2. (Ed.) S. Kendrick. Nat. Mu~. Canada , Onawa.
pp.47 3-5 4 5.
Lacey. J. ( 1981) The aerobiology of cOllidial fungi. pp 373-416 (in) Ili olo.:;..v
of Con id ial Fungi Vol. I (l~ds.) G.T. Cole and B. Kendritk. Academ it
Prcss. NewYork.
Nag Raj. TR. (1993) Coc1omyectousAnamorphs withAppcndage-Hearing
Conidia. l\lyeologue Pub!.. Walerl oo.
Rippon, J.w. ( 1974) MediclIll\lycol o~. W, B. Saundcrs. Philadelphia.
Sea\cr. F.J. (1942) The Nort h American Cup Fungi (O]lercula tes). Sea\er.
New York. (Reprimed 1978. Lubrecht & Cramer. Monticello)
Seaver, F.J . (1951) The North American Cup f'ungi (Inoperculates). Se;lver.
New York. (Reprinted 1978. Lubrecht & Cmmer. Monticello).
Sivanesan, A. (l98.f) Th e Bitunicate Ascomycet es and their anamorphs.
Cramer, Vaduz,
Smith, E.G. (Ed.) (1990) Sampling and Ident ifyi ng All erge nic
MOlds. Blewston", PresslAliergenco. San Antonio.

Poll en~


,~ UI'i>E.6es

Fungal Physiology

Fungi, being eukaryotic organisms, ha\'e many physiological processes in common

with other eukaryotes. But just as they have unique selS of morphological and behavioural
features, so some aspeclS oflheir ~Uular chemlstry differ from those of olher organisms. If you
a1 re~dy know aU about basic cell chemistry. )'011 can skip the nc~t section Dnd go directly to
the resl of the chapter. But why IlOI read through it anyway. just to refresh your memory?

Cell components
Proteins are large. complex molecules. made up of various mixtures and configurations of20 different am ino a dds. held together by peptide bonds. Because of the essentially infi nite number of structural possibilities that the building of a protein molecul e
preserus, most organisms make many uni que proteins. Fungal proteins are unique. yet
function just like those of other organ isms. Some are enzymes and struct ural components, others are associated with nucleic acids to fonn nucl eop roteins, and a third group
are conjugated with carbohydrates to fonn glrcoprote ins, which arc fou nd in membrane s
and the cell wall, as wcll as being secreted as ex~lluler enzymes.
Nu cleic ac ids are o f two kinds, commonly known as DNA and RNA. DNA is the
ccntral reposilOry of genetic information. DNA incorporates the gene tic code, in whic h
sequences of three bases (codons) code for individual aminoacids, and thus spedfy the
order in which these will be join~d together 10 fonn the variou s prote ins. DNA replicates
itself. an.d al so transcribes encoded in.formation inlO RNA. Some R..t"\l"A is associated with
proleins in ribosomes. some occurs as messenger R.t~A. and some as transfer R..t~A .
Ribosomes move alon g messenge r RNA strands , reading the succession of3-b~sc codons.
~nd Wingin g together ami no acids brought in by transfer R..t"A. [n this way, protei ns are

DNA and RNA both have a sugarphosphate sp ine. w!th p uri nes and py rimidines
anaclled to the sugars. The sugar in DN A is Zdeoxyribose. that in RNA is ri bose. One or
the pyrimidines of DNA. th ymIne. is replaced by u racil in RNA. DNA molecules are
usually in pairs, helically inten wined: RNA is singlestranded. DNA is concentrated in
the nucle i of cuk:uyotic cells, though some is also associalCd " 'ith the mitochondria (thi s
is because these: organelles were originall y independent prokaryotes). One way of categorizi ng DNA is by its base r:llio (percent guanine -+ cytosine). In the Eumycotan fu ngi.


reponed values range from 38% to 63%. The DNA con tent of fungi bas been found to be
very low, 0.15-0.3%. Their RNA content is mucb bigher, 1- 10% dry mass. Oftbi5. the
greater part is accounted for by ribosomal R..!'l"A. witb a much smaller amount of transfer
RNA. and even less messe nger RNA .
Carbohydrates are sugars, suga r tllcohols, and polysaccharides (polymers of sugars), all with the empi rical fonnula (C H,O)n. Most fungal carbohydrates are polysaccharides, such as chitin. chltosan, mannan. glucan. s tarch. glycoge n and. in the Oomycetes,
something resembling cellulose. Chitin, a prilM.!ipal wall compooent in the DikaryomycoUl,
is a polymer of IJ- I,4 N-acelylg!uCQsamine. Cellulose is a polymer of ~ 1,4 glucose. The
main storage carbohydrate in true fung i is glycogen, but the disaccharide. trehalose , and
sugar alc ohols like mannitol. are also used.
Li p ids all have an aliphatic hydrocarbon chain as pan of their make-up. Their
structure may be complicated by substitution wi th hydroxyl and carboxyl groups, they
can be saturated or un sa llirated, they may have arom atic moi eties, and they can be combined with carbohydrates and amino-acids. AU are soluble in non-polar solvents. Thcy
include the futty ac ids (saturated and unsaturated), fals and oils (fauy acids combined
with glycerol), phosph olipids, and s phingolipids.
The mai n fatty acids found in fungi are palmitic (CI6:0), oleic (C IS:l) and linoleic (C lS:2 ). The numbers in brackets indicate the number of carbon atom.~ in the
molecule. and the number o f double ( unsarurated) bonds. Most fatty acids are combined
with glycerol to fonn oi ls and fats, widely used as storage compounds. Phospholipids and
sphingolipi ds are components of mcmbranes, wh ere they are often complexcd with proteins. Isoprenoid lipids are based on isoprene, a 5-carbon branched chain molecule.
Terpenes contain two isoprenes: sesquiterpenes. 3; diterpc:nes. 4; trilerpcnes, 6. Carotenoids are diterpenes. and sterol s are triterpenes. Although ergosterol is the main fungal
steroid, mMy other stcrols are also present.

Metabolism may be defined as the sum total of all chemical reactions that support
life. These may be divided into an abolic and catabolic functions. Anabolic metabolism
convens food substrmes into fungal biomass, c.alaholic meta bolism extracts energy from
various substrotes, producing a denosine triphosphate (ATP). red uced nicotinamide-adenine dinucleotide (NAD H) and NADPH, as well as intermediates used in various anabo lic proc esses.
All important reactions in biological systems are initiated and controlled by en
zymes. In the absence of enzymes ffiOSl reactions would go on 100 slowly (if they pro-ceeded at all) to sustain life. Enzymes increase r:l!es of reaction dramatically, by factors up
to 10' . An enzyme consists of a prote in. often with a coenzyme such as a vitamin. and an
activator such as Mg ions. Enzymes often work in sequence, each catalyzing a particular
stcp in a melabolic pathway. Many fungi can produce enzymes that are rarely found in
other organisms, e.g. ligninases and cellulases.
Glycolysis. Of the three pathways by which glucose can be convcned to PYnJ valc
before it is oxidized in the citric acid cycle. mOSt fungi usc two: the Embd en-i\-Jeye rhof
(EM) aud the hexose monophosphate (ID,I). The EM pathway yields ATP and pyru"ale.
The HM pathway yield s NA DPH. the main reducing agent in the biosynthesis of fatty
add s and sugar alcoh ols, and ribose, used to make RNA . DNA and other nucleotides.
Fungi respire aerobically, regenerating NAD by transfer of electrons from NA DH to an
external acceptor, oxygen. Fungal fermentation in' o\ve.'; the regeneration of NAD by
transfer of clecirons to pyru vate. which is produced while the subs trate is being metabolized. This kin d of fcrm~ntatio n can produce IIlcohol or lactic acid. Everyone knows


about the feme ntati on of pyruvate to alcohol and CO, by yeasts such as S<I,",'liaromyces
cerevi$iae. but ~pe<:ies of Aspergillus. Fusarium and M"corc:m do illoo. Oomycetes and
Zygomycetes c:my oUllactic acid fermentations.
Respiration involves three processes: the dtric add cycle. electron transport. and
oxidatin' phosp horyl ntio n. all associated with the mitochondria. as they are in all eukaryotic organisms. The citric acid cycle acceptS acetyl units. builds them into citrate.
then oxidizcs them to CO" reducing NAD as it docs so. The el~ctron transport mechanism
transfers electrons to oxygen to make water. and along the way involves cy tochromes in
the phosphorylation of ADP to make ATP. Respiration can b<e inhibited in twO ways: by
uncoupling phosphorylation from electron transport, or by blocking electron tTunsport.
Many fUngicides are uncouplcrs or blockers.
G. The 3\'erage protein contains twenty or so different amino acids, bUitwoofthcse
amino acids, lysine and tryptophan. are of particular interest to students of the fungi.
Eumyeotan fungi and ehytridiomyeetcs make lysine by a pathway that is different from
that used by all other organisms, except the euglenids (unicellular, wall-less, flagellated
algae). Eumycotan fungi, chytridiomycctc$ and cugl nid , synthcsize lysi ne via eight
steps. ~ of which in\"011'c5 a unique intenncdiale, ((.amino ad ipjc acid (AA.A.). All other
eokaryotic organisms that ClIn milke their own lysine (()()m}~tes. gr~n algae and vascular plants) do so by a pathway involving seven StCps, and a unique intermediate cal1 ~d
iamino pimelic add (DA? ). The two pathways have nothing in common: evcry Step and
evcry intennediate is different. (Animals are lysine auxotrophs--they can' t make it:n all,
an d must get it in their diet). Apart from anything elsc, the two mdically different synthetic p:lthways suggest that the eumycotan fungi, chytridiomycetes and el.lglcnids may
have evolved from a common arn;eslral group, a group different from that which gave rise
to the 00lllycetes, green algae and higher plant,. and different from that which produced
th e anim~ ls .
Onl}' one s)"mhctic pathw:)} is known for tryptopha n. but genetic analysis oft~
loci controlling the sequ~nce of enzymes has shown Ihat while in tWO mycclinl fungi
(Ntlll"()spom and Aspergilllu) fOllr genes arc in volved, the yeast SaccharvmyCl!.1 requires
five genes. T he sedimenta!:ion of thc various enzymes on sucrose grJdicnts shows four
p~lIerns of enzyme aggrcgation, which are taxonomically distrihuted as fol1ow<; : (t)
ch ytrid iornycctcs. ascomycctcs. hol ob3s idiomycet~ s: (2) yeasts: (3) zygomycetes.
tclio myeetes: (4 ) oomyeetes. Although "'c ean't draw firm phylogellC1ie conclusions from
such d~ta. we can sugg~~t that group~ with different enzyme aggregation p31tCmS are
unlikely tll be clusely related,
Po lysaccha ride srn thesis, I need hardly emphasize Ihe importance of the hyphal
wall to most fungi: it is simply the m~in ske[etal component of the mycelium, impart in g
mechanical strength to the hyphae and protecting the livin:; contents from deleterious
outside influences ju~t as the cellulo'iC wall of the average pl~nt cell doc~. The principal
cnmponents of most fung31 w311s Jrc polysaccharid~~, such 3$ chitin (in the eumycotan
fungi and chytridiomycetes) and a cellulose-like compound (in oomy,etcs). The sugar
mon omers from which these polysaccharides arc built (N-acet}'1 glucosamin~ and g[u,o~e. respecli"eiy) arc hnked with a nuele(llide, then enlymically added to the end of D
growing chain. The 51lOres uf mall)' fling] are embedded in slimy mucopolysaech~ridc~.
"'hkh may be important in dispersal.
Lin!e need be said about the metabolism of specitic elemcnts, except to mention
th~t fungi arc carbon and nitrogen "~tcrotroplls. SO must be ~upplied with both in soni<l
combined form. A further restrittion in thc case of carbon is that the carbon source must be
an energy-rich slIbstanC1! previously synthesized by another organism, Common carbon
source., arc ~ugar5 . hemkelllllose. cellulo~c and Jigni n: the last 1\\'0 are relnti vely feeaki-


trant polymers that few other organisms can metabolize. presumably because they lack
th e ne~essar)' enzymes. Nitrogen ~an often be assimila ted in the form of nitrate or ammonia. bIll amino acids. polypeptides and proteins can also be digested by mally fungi_
Aguin. some rather resistant structural proteins such as keratin can be alladed by certain
groups of fungi (see chapler 23).
Seeondll ry metabolism is a strange pltrase. Surely the one wont metabolism. descrlbc~ the total spectrum of chemical activities going on inside a IlVing organism? But
on close inspection. it becomes apparcnl that some organisms produce qUll mities of
cel1ain substances thai do not seem 10 be pan of thc ordinary. ongoing business of uiSIence (which is called 'primary metabolism'). These substances ~ now called 'secondary
metabolites: and may be defined as: natllral products that are not necessary for growth. are
often prodUL't'd only by specific groups of organisms. during on ly part of thei r life cydc.
and arc derived from a few precursors formed during primary melUbolism. Why then arc
we so conscious of these substances? Although they occur only spomdically, secondary
metabolites tend to accumulate. since organisms usually produce them steadily, but do
not degrad~ Ih~m. In addition. tlley arc of{~n biologically active. Penicillin. griseofuhi n.
cyclos porine. anal oxin, ergOI alkaloids, and psilocyhin: all ure secondary metabolite,
of fungi, and aU are famous for lh~ir effects on other organisms.
Al though secondary metaboliles are rare in animals, they are common in plants.
bacte ria and fungi . Many are fonned o nly after the m:jui~ments of cell growth have been
satisfied. When growth SlOpS, il uems that some biochemical palhways are not sh ut off.
and thi ngs like fally acids an d amino acids accumula te. wh ile the tric arboxylic acid cycle
keeps on cycling, The organism now uses these raw materials. and a few others, to nmou
facture new end.products. For example. fauy adds give ris<: to polyacetylenes. amino
ac ids 10 ergot al kaloids and penicillin. We now ha\'c a large catalogue of secondary
metabolites. all derived from a relatively ,mall number of precursors.
Secondary metaboli tes c~n be placed in live groups. according to the area of pri
mllry metabolism from which they are \!eri\"cd. ( I) Glucose-dcrived substances like polysac
chandes, pcptidopolysaccharides. and sugar alcohols. (2) Condensation products of ac
ctate derived from the lICetate-malonate JXlthway of fatty acid synthesis. e,g. polykcti des
and phenolics. (3) Condensation products of acetate derived from the me.'ulo nic acid
pathway. e.g. lerpenes. (4) Phenolics deriwd from the shikimic aei\! pathway of aromatic
amino acid synthesis. (5) Deri" ~tives of other amino acid syntheses.
Acetate is the row material from " hich polyacetylenes. pol~kelidcs. Steroids and
terpenes arc synthesized. Polya ectyl e n e.~ are straightchain compounds containing conjugated acetylenic sys tems. Thes~ compounds f1uoresce brightly in u v. and so are easily
detected. Of the 400 polyacctylenes known. about 80 are funga l. and found exclusively
in basidiomyce tes. Polyketides 3re produced by many ascomycetes and conidial
anamorphs by conde nsation of acctyl uni ts with ma lonyl units, with simUltaneous dccar
boxylation. Examples are the antifungal antibiotic, l:risl'(lfu h'ln (see chapter 23), and {h~
mycotoxins. odlrutoxin and ana toxin (see chnpler 21). Terp ent'> and stcroids Jfe
biosynthesized from isopcnt<:o;. 1 pyrophosphate. which i.~ itself an acetate derivati \~
Th~ trich othecc ne mycotoxin, are sesquiterpc noids. Gibbe rellic acid is another fungal
terpt:ne that has also bt-en found to be an important plant growth regulator. The mrc
oto.~ in zea ralc none is a steroid. Though it produces profoun\! sexual dysfunctions in
youn g pigs, it is now widel y lIs~d in the fonnof implMls to promOte growlh of bed cattk_
Amino udds 3~ the buildinS blocks of proteins. but Ihey are also the raw mmerials
for many fungal secondary Tmtabo!ilcs_ Four groups sland out: (I) c~'d ic oligopep lidi.'S .
which m3Y be death-dealing loxins like the amanitins (8 amino acids), or lifesa\ ing
immunosuppress:ln ts like cyd osporinc (II amino acids): (2) indole alkal oids suc h a, the


hallucinogen psilocybin and the dangerous ergot alkaloids; (3) the J3-lactam antibiotics,
penicillin and cephalosporin; (4) plant growth regulators such as auxin. cytokinin and
ethylene, which are formed by many fungi.
So far, I have taken the usual anthropocentric attitude in this brief survey of fungal
secondary metabolites, concerning myself only with those that are of some direct importance to humans. In the interests of the impanial intellectual approach, it might now be a
good idea to consider briefly the possible roles of these substances in the lives of the
organisms that produce them. VI'hat value can a highly poisonous and extremely carcinogenic substance like aflatoxin have for Aspergillus flavus? What good, if any, is penicillin to Penicillium chrysogenum, or zearalenone to Fusarium graminearum?
It seems highly probable that these substances are not just waste products. Aflatoxin
may well give A flavus an advantage when it is competing with animals for food. Small
mammals may learn to avoid mouldy nuts or seeds: and if they don 't, they may be poisoned. Either way, the fungus wins. Po:nicillin, with its powerflIl bacteriostatic activity,
may be presumed to give P. chrysogenum an edge over competing bacteria_Zearalenone,
a mycotoxin that acts like a steroid sex hormone in pigs, is now be lieved to play a role in
the development of the Gibberella zeae teleomorph of Fusarium gramineamm.
Regulatory mechanisms. On reflection, it must he obvious that all of the thousands
of reactions and cycles that make up the metabolic activity of an organism must be under
some kind of control. Genes are turned on amI offby environmental and inherent developmental factors, but many processes have to go on all the time. or at least be constantly
ready for action_ Obviousl y, there isn't an overseer in the nuclens, turning all these switches
on and off as needs are ~rceiyed and fulfilled . Most processes investigated have built-in
controls, often simple but elegant feed-back mechanisms, which affeet the enzymes that
drive most reactions. For example, a different enzyme catalyzes each step in the production of leucine. If the raw material for Ihis synthesis is in good supply. the pathway could
churn out far more leucine than is needed: so, in a breathtaking ly simple solution, the
synthesis of the first enzyme in the series is inhibited by increased concentrations of the
end-product. leucine. The pathway effectively turns itself off when it isn't needed.

Growth is often defined as irreversible increase in volume, but usually implies some
other kinds of change as well: changes in components, metabolism. sha~, function. A
mycelial fungus will extend in all direction$ as its hyphae grow at their tips. The hyphae
become longer, they often branch repeatedly, a lot of wall materinl is laid down, the
amount of protoplasm and the number of nuclei in the colony increase. If the fungus is
ll.lcky. it will find more food than it uses l.lp in the search. so it can both grow and accuml.llate reserves that will enable it to sporulate. Fungal growth is usually measure d as increase
in fresh weight (unreliable because of variations in wate r content), or in dry mass (whi ch
for obvious reasons can be measured only once for any particular colony), or by increase
in the diameter or radius of the colony (which can be measured re~atedly). In unicellular
yeasts, growth is measured by counting cells, or by measuring the increase in turbid ity of
the cul ture medium. If we were trying to produce conidial inoculum for use in a program
of biological control (see chapter 14). we might express the success or the organism in
terms of the numbers ofpropagules it formed in a certain time. at a certain tem~rature , or
on a particular substrate. A mushroom-grower would be interested only in the mass of
basidiomata produced.
Beginning from the spore, growth proceeds in stages, which can be catcgorized as
germination. assimilati,'c growth, and s porulatio n. Each stage may require conditions
very different from the others. I wi\! examine them in tum. Much of OUf information about



the early stages of growth has been obtained by plant pathologists, who are very interested in how pathogens get into their host plants, and in how they can be killed at their
most vulnerable point, which is often the ge nn tube.
Other groups of organisms produce spores, but none produce them with such singleminded dedication, in such prodigal abundance, or in such an ex:uberanl variety of foOlls ,
as the fungi (Fig. 3.2). The spore, almost as much as the hypha, is a fungal trademark.
Spores may be single ceUs, or may be divided up in various ways into tens or even
hundreds of compartments. Some live for a few hours; others for years. But all have two
characteristics in common: they ensure the survival of the fungus through time, or space ,
or both; and sooner or later they genninate.
A donnancy phase usually precedes germination. Spores are often fonned when
conditions are deteriorating for the fungus. Tempenltures may be falling, water drying up,
food running out. [f the spores germinated immediately, they would face the very problems they were produced to circumvent. Many spores have a built-in timer, an endogenous constraint that will not allow them to germinate until a certain time has elapsed.
l\fany require prolonged cold treatment. Spores of many coprophilous fungi won't geOllinate until they have been exposed to high temperatures or to a specific chemical treatment: things that mimic what happens to them inside the gut of an animal. The signals
they receive while passing through the gut prepare them to germinate in the dung as soon
as it has been deposited, and so to have first access to the abundant nutrients it contains.
Spores of some rust fungi won't germinate if they land too close to the parent mycelium or
to sibling spores - this is called self-inhibition. However, spores of less specialized fungi
often have no such built-in inhibitions, and wi!! genninate as soon as appropriate conditions arise. In these cases. any donnancy must be regarded as exogenous: imposed from
outside by lack of environmental encouragement.
Germination of powdery mildew conidia requires only oxygen. and the spores of
some other obligately parasitic fungi need only oxygen and water. Most saprobi c fungi
need other factors, ranging from inorganic salts to various organic carbon sources. [f a
spore is to produce an extension of itself in the fonn of a germ tube (the first hypha). it
must increase in volume. The only way to do this in the absenco of an external food
supply is to imbibe water or to produce it metabolically. Of course, the food reserves of the
spore permit some synthesis of cytoplasm and wall material. but this is a limited resource
and is soon exhausted. If the young hypha is to survive, it must tind food.
The walls of resting spores are often chemically different from those of hyphae. and
are rel atively impermeable; but when they are ready to germinate, en zymes render the
walls permeable. so that the spore can receive chemical stimuli from outsidc. When germi nation begins. enzyme action intensifies, softening the wall. often at a preformed thin area
called a genu pore or germ slit. A genn tube e mcrgcs, the constituents of its cytoplasm,
nucl ei and wall material supplied by a renascent metabolism.
Once genuination has happened, growth and differentiation are the next phases.
Growth involves elongation of the young hypha at its tip, often with concurrent migration
of cytoplasm and nuclei in the direction of growth. Growth implies increase in volumc
and increase in dry weight. These increases may be achieved by <lbsorption of soluble
nutrients already available in the environmcnt. Morc usually, exoenzymcs have to be
secreted from the hyphal tip: they degrade the substrate into smaller, water-soluble mol ccules which can be absorbed and metabolized. However, if a hypha simply grew in a
straight line. it could not effecti ve ly explore or exploit th~ substrate, and no appreciable
biomass could ever be accumulated. This is where differentiation comes in. Soon after a
genn tube appears. it branches. Then each of the two resulting hyphae branch; and so on,
and so on (see Fig. 3.\). Soon. hyphae are growing in all directions possible, minutely


exploring the substrate and fonning the typical fungal colony, which will be sph~rical if
the fungus can grow in three dimensions, as it does in a liquid medium; or circular if it is
growing mainly in two dim~nsions. as it docs when it spreads across the thin film of
nutrient agar in a petri dish.
Growth rate. Since more and more fungi are being used for industrial orbiotechnologi,al purposes, it is important thot fermentations be carried out under the beSt po~sible
conditions of temperature, pH. and nutrition. Fungal physiologists have laid the groundwork for such applications. If we want to find out the best temperature at which to grow
our fungus, we set up a series of experiments in which conditions are me same in all
replicates, except for the temperature. The IWO common measures of growth rate are: (I)
increase in radiu s of colony over time; and (2) increase in dry mass of colony over time,
The first has the advantage that sequential records can be obtained from each colony. The
second is a more absolute measuremen t, but can be perfonned on ly once for each colony.
If we at'<! growing the fungu s on a solid substr~te like cellulose, i( is difficult to ~epamte
the mycelium from the substrate at the end of the experiment, so we have to measure
growth in another way: (3) by determining protein contem. Such studies show thaI growth
can be divided into several phases: (A) the lag phase. when growth begins slowly. then
grodullly accelerates; (6) the c.~ponenlial phase. when growth continues at a high and
steady rate; (C) the d l'Cli ne phase, as growth slows down and finally SlOPS; (D) death.
often accompanied by various degrees of autolysis.
This i;; the kind of picture we get when we study fungi in what is sometime, called
blilch culture, The fungus is grown in a flask or a fermelller. with a limited ;lmoullt of food
and space. When growth slows down, it might be be<;;ause (he fungus is T\lnning out of
food. BUI the decline often comes long before the food is exhausted. This dCterior.lIion is
oflen called staling. and is attributed to the accumulation of waste produel~ thaI inhibit
. met:iOOlism. If a fungus is inoculated at 0111' end of a very long horizo ntal tube with a !xd
of nutrient medium along its length, it can r~l11ain in the cxponential growth phase for as
long as there is fresh mcdium to e.' plore. Needless to say, [his c,mnot happen often in
n~turc, so staling mUSt be accepted as the norm. It may even be the switch m:1I shifts some
fungi into the rcproducti\<e mode.
Different fungi may grow at widely differing rates during their exponential phase.
as mJY the ~ame fungus ~rown under different couditions. One m.:3sure of growth rmc is
th.: lime i[ takes a fungus to double its dry m3S.s. A mOTe easily determitted measure is the
sp.!ciftc growth rate. which is deri,'ed from measuremenlS of a colony's ma...s at one-hour
imer.a!>. A fungus which increases in mass by 20% in an hour is said to h~,'e a spet:ific
gro\\ Ih rate uf 0.2. Fungi have ;1 wide range of spedfic growth nues. ('11(1(lolllilllll vi r(SCfm'
h,b gi,'en u ~pecific growth rate ofO,4 on gluco;;e. und a v31ue ofO,6 has been recorded for
N~lIrosf'<'T(I CfllJSC (or rather. for il'i ChrY$()nW(I anamorph). These examples havc much
higher specific gro .... !h ratcs m.:ln most fungi. Yet some other fungi. including some common saprobic zygomycetes (e.g. Rhizopils oligosporus). and soille yea~ts . .1L<;o han: gruwth
r~l e!; high enough to !e~ d to their COll\merci~1 cxploit~tioll. or to th.:ir de nunciation ;tS
'weed,: CleJrly. if we could undcr.;tnnd and perhaps circumvent th<! mechnnism$ that
limit the growth rate of many potentially u~ful fungi. biotechnological ;tpplications of
the'le organ isms would multipl}.
Localiz~llon of growth, The wails of ussimilative hyphae are not impenneahlc:
they have purcs Sl III i lar in sile to those in higher plant cell w~l1s. Hyphal w311s reduce but
do not prevent the outward mo, ement of watcr in dry conditions (dc.sicc3tion). and the
inward movement of deleterious substances from the environment. TlK-y do pre' ent [he
pa)sagc of most enzymes (large. proteinaceous molecules). and the exocnzyme$ on '" hi~h
fungi d<!ptnd are in fact ,>ectctcd almost cntirely at or ncar the hyphaltip, This suggests


th(ll most hyphal wall material must be laid down just bthind the hyphaltip. And c;.:;pcriments indicate that thi s actually hnpptns. What kind of e;.:;periments? Early observations
showed that the di stances between septa, and between the origins of successivc hypha.l
branches. did not change with time. E;.:;posing growing hyphae to osmOlic shock produced abnonnali ties only at their tips. Auorescent antibodies have been used to distinguish between old and new wall m1terial, and the resulting pattern of fluorescence showed
that ncw material was introduced only at the hyphal tip. Triti~ted N-acetylglucosamine
was fed to growing hyphae and its incorporation pinpointed by autoradiography: lIgain.
incorporotion was liltgely restricted to the apical micrometrc. These ilte vcry significant
observations. We can now Se<! why a fungus needs so many h)'phal tips, and how evcry
fungal colony is essentially .imilar to the 'fairy ring: driven \0 ever-expanding radial
growth by its need for food, and by the e;.:;haustion or staling of the substrate left behind.
Since bran ching is so \"i\;llto the sliccess of the fungus in e;.:;ploring ils substrate.
thc mtchanisms that control branching are of great interest. The phenomenon of apical
dominance is well known in. for example. roniferous trees. II appears that a similar domi nance can be detected in Ih", hypha! tips of many fungi. Fungi growi ng in culture often
have a characteristic distance from the hyphal tip to the fi rst bmnch. Different metabolic
inhibitors affect this relationship in different wnys. r,.litomycin C inhibits branch formation but not hyphal elongation: sodium fluoride hns the opposite effect. (l-olitomycin is
known to inh.ibit DNA synthesis, NaFto inhibit metal-activated enzymes. but this knowledge hardly help s us to explain tbeir differential effects on hypha! growth). In most fungi,
th~ leader and the first nne or twO branche~ grow faster th,1O the others: if the faster
growing tips are cuI off, the subordinate ones are 'released: and grow faster. If inhibited
branches are se-,'ered at their base. they proceed to grow fasler. showing thattne inhibi tion
originated wi\hin the fungal thallus. The amount and kind of some nutrients. such as
sulphur and nitrog",n , available to the fungus also influence apical dominance. The com plexity of the growth regulation sys tem is indiCated by the mapping of no fewer than 90
genes tbat control some aspect of colony morphology in NeumsJHlI"ll.
Septa (cross-" ol1s) are a diagnostic featul"<: of tnc hyphae of most true fungL A
$epwm is not usually laid down as a thin membrane, but rathcr begins as a ring of material
around th~ in~ide of the hypha. The ring grows inward, eventually b-ecomi ng an almost
complete bulkhe<ld which physically reinforces tho intrinsically strong tubular configuration of the h)"ph<l. If we could watch a septum form. the process would resemble the
dosing of an iris diaphragm in a camera or a microscope condenser. In somc fungal
hyphae there is a clear relationship between septum formation and nuclear distribution:
for eX3mple, in dikaryotic hyphae there is a septum for every twO nuclei. But io many
fungi there i~ no such relntionship, nuclei pass through the septal pore betwecn compartments ""ilh reiJtivc ease. and the mechanism that decid ..... where septa will be laid down is
obscure. Of course. many fungi are not restricted to the formation of individual hyphae.
e\"1:n during th'" assimi lati ve phase. V:uious stimuli trigger the devclopment of mycelial
strands. rhizomorph s and sclcro tia. But the true capaci t), for di fferentbtion t h~t is innat~
in most fungi is expressed onl y in the reproductive philse.
!\ ledia. 1n nOlture, fungi grow onjust about any organic substr.lte. When we grow them
in pure culture in the !llboratory. we usually pro\ide them with a special nlllrit;"e mooiom.
This may be liquid (a broth) or solid (a gel). Most identifi cation is done on solid media. but
mo~t fennentations and mall)" physiological experimems are carried out in liquid med ia .
Liquid m~dia are based on wllter. and may contain n variety of nutrients. buffers, etc. The
fungus is usually grown ~ubmergt'd, and its oxygen requirements are mel by shaking (small
!lash), or stirring and aerating {large fermenters).ln solid media. thc water and other componems are held in a gel by ag:u. This complex polysaccharizk. d~rh"ed from a reU alga. mdls

at lOOOC but OOes not solidify until it lOIs 10 45C, and is not metabolized by most fungi.
As linle:lS 1-2% agar solidifies most medifLAgar media are usually used to fonn thin layers
c;overing the bottom of petri plates, or to fin the bottom third or so of test rubes (called
<i1anlS' beCause mey are placed at an angle while the agar is setting). Plates are used to grow
culrures for idcntificatiOll. Typically, a small inoculum will be placed in the middle of the
plate. then incubated. The colony which develops. growing partly abo\'e me surface of !he
medium . and partly below it. will often show diagnostic features (colour, Ie~rure, sporula
tion, etc.) Living cultures are oflen stored in slants, or may be Iyophilixed (freezedried and
sealed in a high vacuum) for longterm storage.
If the culture ;s to be axeni c (or as we say, uncontam inated), the medium. which is
attractive and accessible to many microorganisms. must first be sterilized. This has usuall y involved pressure-cooking the medium in an autoclave at a steam pressure of 15
pounds/square ioch (2 aunospheres) for 15 minutes . The tempernrure reaches 120C,
effectively killing all microorganisms. But it also tends to caramelize sugan. and to
destroy thennolabile substances like miamin (a vitamin) and some antibiotics. Autodaving is acceptable for routine work. bill for critical physiological srudies, it is better 10 filler
the medium through membrane filten lhat effe<:iively remove bacteria and fungal spores.

Nutritional Requirements
C arbon nutrition. One of the principal distinguishing features of mOSt fungi is lheir
inability to fi ~ inorganic carbon. The simplest co mpound most fungi can usc as a source
of energy is the monosacch aride glu cose. Unlike most olher carbon sources, this doesn ' t
need to be enzymicall y brohn dow n to anything simpler beforc it can be absorbed.
Vinually all fungi are ready to met~bolize glucose at a moment's notice: they alre ady
have all the necessary enzymes, which are thus dcscribed as const ituti ve. Fructose. mannose and galactose are also readily used, but there is often a delay before assimilation
begins. This is bec-ause the enzymes in\"Olved in processing these sugars aren't necessarily ready and waiting. The fungus takeS a liule while to recogni~e lhe nature of the
substr.ltc. and to s)"mhesizc the proper enzymes. This process is called ind uction . and
produces ada pt i.-e enzymes_ If a 101: of glucose is present. it may actually suppress the
production of the enzymes that deal with other substrates: the fungus takes the easy route.
A little glucosc. on lhe other hand. may fuel the inductioo process, and shon en the lag
phase on many substrates.
Although many experiments have been done to compare the ability of fungi to use
differem single carbon sources, these may nOt tell the whole story. In nature. fungi usually
havc to deal with mixtures, and their behaviour in this situation can 't always be forecast
from single-substrate tests. We've already seen that the presence of glucose can suppress the
utili7.atiOll of other substrates. Perhaps the most impon:mt example of the mill.ed substrate
situation in\"OI\"CS lignin. Although the ability to degrade lignin (0 carbon dioll.ide is Olle of
lhe things for which many basidiom~'cetes (the white rot fungi) are most nOl:orious, they
can't usc lignin as soli!carbon source, and will break it down onl y in the presence of another
accessible carboo source, such as cellulose. cellobiose or glucose. Fungi may deal wilh
lignin only to gain h.>uer access to the cellu lose, or in order to release available nitrogen.
Culture medi a must also contain 3 source o f nit rogen . No fungus (in fact. no eukaryote) can fix atmospheric nitrogen. Many fu ngi can usc: nitrale, lhough ammonium nitrogen is even more universally metaboliZed. Ure~. amino acids, and various polypeptidcs
and proteins are accessible to some, but not all, fungi. A good nitrogen source for many
fungi is hydrolysed case in, a mixture of amino-acids . Sulph u r requirements can almost
always be met by incorporating sulphate in the medium, though some chytridiomycetes
require sulphur.containing amino-acids such as methionine.



Vitamins are coen?ymes that are required in minute amounts. Although some fungi
can make many of Ih~ir own vitamins. many are deficient for thiamin (vitamin B1, involved in caiboxylation), biotin (B7, carboxylation), riboflavin (B2, dehydrogenation),
pyridoxine (B6, transamination), nicotinic acid (83, dehydrogenation), and others. Vitamin deficiency is sometimes absolut~. in which case the fungus can be described as
auxotrophic in this respect, and won't grow urness one or more vitamins are supplied. In
other cases it is only partial, so that additions of vitamins may merely increase growth,
rather than making it possible. Vitamin deficiency may be temporary: Myrolhed"", needs
biotin for spore gennination. but not for myceli al growth. While many fungi require
vitamins, others can synthesize them from precursors. Thiamin, for example, consists of a
pyrimidine ring and a thia'lOle ring, linked by methylene. Some fungi, if provided with
the two rings, can link them and complete the molecule; other fungi need only the pyrimidine ring; yet others need only the thia:.mle ring.
Fungi also need a range of elements, whic h can be divided into two groups accord ing to the amounts required for normal growth. The macronutrients include: potassium
(K ), which is used in carbohydrate metabolism, enzyme activity, and to maintain ionic
balance: phosphorus (P), an essential component of nucleic acids, and of energy transfer
mechanisms; magnesium ~Ig). an enzyme activator required in ATP metabolism; sulphur (S), a component of some amino acids, vitamins and other sulfhydryl compounds;
and calcium (Ca), an enzyme activatonhat is also often found in membranes. Micronutrients, sometimes called trace elements. include: iron (Fe), found in cytochromes, haem
apoenzymes, and pigmenL,; copper (eu) an enzyme activator also involved in pigments:
manganese (1\"10), zinc (Zn). and molybdenum ~Io), all enzyme activators. Fung! get
along without boron, chlorine. fluorine, iodine and si licon, though these elements are
apparently essential to many other organisms. Incorporating iron in a growth medium can
be a problem, since ferric iron is extremely insoluble at pH values above 4, and ferrous
iron is quickly oxidized to ferric by the free oxygen most fungi need. Fortunately. a
chclating agent such as EDTA (ethylenediamine tetraacetic acid), which acts as a metal
ion buffer, will increase the biological availability of iron.
Although culture media must contain some available water, some conidial fungi
and yeasts are the most xerotolerant organisms known, able to grow at water activities (a.)
as low as 0.70. lfwe cons ider that most animals grow only above a.0.99 , most green plants""
wilt irreversi bly at a. 0.97, and most bacteria will grow nn ly at a. 0.95 or higher, this must
be recognized as a truly remarkable talent, though for us it is an expensive nuisance, as
you will read in chapter 20. Fungi that grow at low external water activities have comparably low internal a. as wel l. Yeasts control theirinlemal osmotic pressure by interconverting
sugars and pol yhydric alcohols such as glycerol and mann itol . and it seems probable that
mycelial fungi may well do this too, though that has not yet been established. Most
enzymes noonally operate in an aqueous medium. and if a fungus is to function at low
intemJI iI some enzyme-compatible water substitute must be pre~ent. It has been found
that glycerol can play this role.
Using the infonnation given above, you should be able to concoct a culture medium on which muny fungi would grow ",ell. By combining many individual chemicals,
you could make specific provision for their basic metabolic ne~ds. The medium you
produced would be a 'defined' or even possibly a 'minimal' medium. But many fungi
would grow even better on very complex substrates: things such as extracts of malt, or of
potatoes. or of yeast. Th~ se rich mixtures, though 'undefi ned.' appear to be nutritionally
optimal. and it is much easier to use one of them than to painstakingly measure out
increasingly minute amounts of a long list of trace elements and expensive purified
growth fuctors . Unless you are doing critical physiological experiments, you wou ld prob-

,.I " .' .i'.

152 CHAPTER 1\'l~r:

~bly grow ~110St fungi on potato dcxtros~ agar (PD.l,), malt extract agar (M EA), or some
ot her undefined medium _Recipes of media Suihlble for a wide rangc of applications can
be found in Me/hods In Microbiology VoL 4 (Ed: Booth 1966) and The ""{ye%SY Guidebook (Ed: Stevens 1974). Al~, rememkr {hat your lxst efforts to cuhure many groups of
fungi are doomed to fru5tration. Th~ physiology of many obligately parasitic fungi is
intimately linked with that of their hosts. so no ordinary medium will suppon growth of
m~mbers of the Uredinales. Peronosporaceae. Erysiphales. Laboulbeniales, Glomales.
and oth~rs. The simplest system in "hich mOSt of these organisms can be studied is a
'dual" cullUrc: fungu s + host.
Transpo rt Fungi can absorb food only in the form of relatively small molecules
lile glucose. Water moves inlo hypha~ by IXlssivc diffusion. drh'en by osmOlic differentials. Although the cell wall is more or les.~ permeable in eith~ direction to the kind of
molo:ules the cell seeks 10 accumulat..,. it limilS the inflow of water by offering a physical
resistance (wall pressure) to expansion _The pla~maJcmma is semipcnneable, and controls
the movem ents of solules. The membrJIlc itse lf is large ly lipi~-~Ctu(IJJy a double l ~)'er
of phospholipid moleculcs-which tends to keep water-soluble compounds oul. Transpan can be p:lssh'e or active. In passin' u~nsport. the substrate movcs along a concelltra
tion gr~dienl or an electropotenlial gradient. Actil-e tronspon requires an inv~slment of
energy. usually ATP, by the organ ism. Desirable substances may be carried in. or unwanted material expelled. In a~tive uan;;pon. the Substance being moved is believed 10 be
pumped through special channels lin~d with proteins called pcrmeases, or 10 become
bound to a specific carrier protcin, "hich is responsible for uanspot1ing it across th e
membr:l!lc. Cllrriu prOl:eins also aid in passive 'facilitated diffusion:

Cllions such as: potassium. ammonium. m.lgnesium. calcium. manganese and iron
arc all accumu!:ued against high concemnltion gro.dienls. sho""ing that .lctivc. carriermediatcd transport mo:hanisms arc in'olvect. If a fungus is loaded with ,;()dium. then
supplied with potassium. sodium wilt be cxpelled as potassium is taken up, This kind or
bt'haviour is ca ll ed countenrilnsport. The dival ent c~ l ions. 1\Ig0. Ca~ nnd Mn " . will be
tak~n up only if phosphate is ~lso a\~ilable. and Fe-is chelatcd with siderochromcs
before being transported. The transport of ions such as phosphate and sulphate is also
carricr-mediated. Once phosphate i$, the cell. it is con\eIted 10 polyphosphate. und
internal concentrations of orthophosphate dOn't ~hange. The study of nitrate UplJk.e h~s
bt'~n hindered by the lack of a Te,1\ly se n_, iti v;: meu suri ng Icchn iq ue , so it isn' t cc nai n th~1
~~ITjer, arc invohed.
Glucose and other sugar.; mow across the piasmakmma of fungi by fncditated
diffusion. or by nctive tr.msport, or by 2 combin~tion of the 1.... 0. A sin;lc fungus may hu\e
S<!\"(~ral different meeh~nisms. Somc 01 the aC11- e mechanisms are constitutive (always
present and read, whik some are in~ucible. Amino acids are also lr.mspofled actively.
NfI.rtupora cnLISt! has been shown to havc al 1~3~\ live differ<: lu amino acid tran ,port
syskms: one carries only m~lhiomn~: anothcr. on ly aciJic amino ~citls: a thirJ. only
basic umino adds: the fourtll. aroma!j,' ;md 31iph~tic umino 3cid.~: the fifth. aromatic.
aliphatic and b:J~ic amino acids. AminO:lcid I mn~port syslemsdiffer from those for sugars
and ions in thal no countertransport h:!5 !xen detected.
Cetl ulosc lind L ignin Decompositio n_ Fungi produce an extraordinary spe<:lrum of
enzymes. and can Jegrade just about Jn~' organk sub;;trat~ _ Perh:lps the mo,t import~nt of
these ,Ub,tr:ltcs are \.C ellulose and lignin B inion s of \on nes of cellulose i, produced by the
high~ r plants every year. It fonlls tht gr~atcr part of their cell walls. and, being apparently
enable 10 re<:yc le it themselves, lhey dis:::ard it in \'ast quantities every year. Autumnshcd
!eaves. the entire bioTffi15s of annual plants. and el'er.tually the corpses of the much longerlived lr~es: all ar.., beq ue~lhed to Ih.., fungi. beCause no Olh~r organisms c~n initintly


unlock the e nerg y they contain. The key to this wealth is the complex of run gal celiuJases
(some bacteria produce, but generally operate under weuer. more alkaline conditions). Trichoderma viride is a well known cellulolytic fungus that is commonly isolated from some forest soils and from decaying plant mat~ri111. It produces three distinct
cell u lolytic en:r.ymes: ce ll u lase, which hydroly-.:es all kind s of cellulose; glucan
ce llobiohyd rolase, which degradi:S crystalline cellulose to cellobiose; and the glucanast.'S,
which hydrolYle amorphous cell ulose. T here arc two kind s of glueanase: the
en doglueanases, which produ ce cell ulose oligomers, and the exoglucanases. which attack those ohgomers. cJellv ing off one glucose unit at a time_Exoglucanascs ondce!iobia<;eS
digest cellobiose. releasing glucose. The enzymc:s of the cellulase complex are all glycoproteins. and are resistant to thermal deml\uration,
Plants also produce vast quantities o f lign in. This recalci trant polymer strengthcns
the waUs ormany plant tissues, especially those involved in secondary thickening. Their
deposition in wood tcnds to mask the cellu lose content of the cell wall~. Some fungi (the
whi te rot Basidiomycetes) are the onl y organism s we know that can unequ ivocally de grade ligni n: and even they cannot use it as their sole souree o f carbon. Ugninases are
oxidative rather than hydrolytic enzymes. Many whitc rot organisms produce an extracellular poly ph enol oxidase called laccase. which must playa cri tical role in lignin breakdown. since organisms that don't have it can't att;lck lig nin. Other as yet undiscovered
enzymes are also almost cenain to be involved.
P rotein digestion_ Although some proteins ore water-soluble, they cannot cross the
pl asmalemma into the fungal cell unl ess they are broken down into small ol igopept id~
fragmenlS contain ing no more t~n 3-5 amino <lCid molecule5. Hence the need for cxtNcellular proteases. Fungi like Saccharomycts ce,.~dsi(lt, "'mch produce only intracdlular
preteases, catInot assinu lnte proteins. At thc orher end of the scnle are orgnnism> likc Trichophyto/I and other dennntophytcs. which can att:lCk keratin, a tough strucrural protein_
There an: two main kinds o f protease: exohydrolases, which nibble individual amino acids
from the ends of peptide chains; and endohydrolascs, which will cknvc a chain into two
large fragme nts, dOl.lbling the number of c nds on whic h the exohydrolascs can operatc.

Environmental Effects
Pb ysical parame ters like t~mpcratl.lre, lig ht, and gravi ty have profound effce ts o n
many fungi, but generalizations are dangerous. Some psychrophihc fungi grow at temperatures below OC: some thcnnoph iles can function at temperatures aoo\'e 50'C. Some
fungi need light in orde r to fruit: othn:; seem indifferent to illumination. ~hny manofu ngi
are extrclllely sensitive to gravity: ru nny microfUllgi are totally oblivious to it
It is helpfu l to tnow thc cardinal tem pera tures of any fungus we want to work
with. These are its minimum. opti mum ~nd maximum temperatures for gro\\lh, Most
rcs~ an;h ers find it co nveni en t 10 grow a fung us at its optimum tem peratur~. but this
ignores the fluctuating and often t:xtrcmc temperatures the organ ism mUSt face in much of
KonhArnt:rica. I have already pointed oUi that falling temperatures in autumn may induc.:
fru iting in some fungi (such as Coprinus Co"w tljS), donnancy in others: that [<',Img stages
o f m~ny fungi (such as M mlilitlia) mUSt be chilled be fore they will erminate; and that
heat treatment produces the same effect in others. From srudy oftheir assimilative
fungi can generally be categori zcd as psy chrophilic, meso philic or thermophilic.
Psychroplliles have minimum growth temperatures bel ow ooe, maxima below 20C. an d
optima in the nmge 0"-1
Mesophiles (the great majority of fungi) have minima above
O"C. maxima below 5ifC, and optima between IS and 4O'C. Thell1l()philes h:wc minima
above 20C. maxima above 50' c' and opti ma between 35 and 5WC. Establ ishing true
optima may not be si mple, as Fig. 9.1 shows_If 11 complete growth curve is not ploued al



each of the chosen tempcra!ures, incorrect conclusions could be drawn. Compare the
answer you would get if you harvested the experiment detailed in Fig. 9.1 at day 7 with
that you would get at day 14. Also note that the qu ickest stan-up does !lOt necessarily
eventually p roduce the most dry mass.
Some of the most spectacular effects of light on fungi are doc umented in chapter 8
(dispersal) and chapter II (ecology). Pi/obo/us aims its explosive sporangial mechanism
at thc light; Podospora points the neck of its perithecial ascoma toward the light: th~
individual asci of Ascobo/us point toward the light Each of these mechanisms involves
pos itive phototropis m . Phototropism implies the ellistence o f a photoreceptor. fo,'ost
phQ{otropic fungi respond best to blue light, and this is strongly absorbed by [l-carotene.
which is usually prese nt in the photosensitive organs, but the true nature of the photoreceptor has not yet been established.
Circadian rhythms. Some fungi in culture d isplay dai ly rhythms of growth. pigment production, or sporulation. which seem to be responses to the altemation of light
and darkne ss. Although Pi/abo/us Splwil'fOsporUs (Mucorales) didn't need light in order
to produce sporangia, establishmem of a regular 12-hour Iightll2-hour dark regime inc reased the number of sporangia produced, and led to a peak of discharge six bours aftu
the lights were tumed on. Continuous light destroyed this synchrony, but in continuous
darkness the cyclical discharge continued for several days, though with gradu ally decreasing intensity. Raising or lowering the temperature did not change this 24-hour rhythm.
Many Q{her such circadian rhythms have been recorded, includ ing some clock' m ut~nts
of Neurospora, but the underlying mechanisms of these cycles are no! yet understood.

~ 100

Time (00)

Frg. 9. 1Effect of lime and tC!"r'lpefature on grQI.Vlh of Phycomyces i1 a defoed medOn (Robbins



Reproduction: the Formation of Propagules

The foregoing paragraph leads me to a consideration of reproductive physiology in
fungi. If hyphae are the secret of the remarkable success of fungi in expl oiting their
myriad sl,Ibstrates. spores are the secret ofrneir ubiquity. Spores are omniprese nt, ensuring
that whenever a new substrate becomes available, fungi will always be there to colonize
it. We can express the strategy of many fungi quite simply: in the assimilative mode,
fungi produce hyphae; as long as there is food to be had, the fungus conce ntrates on
accu mulating reserves of energy. some to be invested in produdng more hyphae. !>Orne to
be stored. When food runs out, orstaling factors build up. or reserves reach an appropriate
level, or specific environmental signals are received. the fungus switches into the reproducli,"e mode and produces spores.
Some fungi produce spores directly on the assimilative hyphac; others [am} spe
cialized but si mple. one- or few-celled spore bearing struc tures. In these cases. the onset
of reproduction can be very rapid. In hyphomycetes like Penicillium, while assimilative
hyphae at the margin of the colony are still advancing, th e older hyphae are producing
simple conidiophores and conidia. This situation can be recognh:ed at a glance: the
margin is white, while the restoflhe colony is covered by a TIlass of green conidia. ln other
fungi . such as the agarics, the spore-bearing structure is large and complex. It takes longer
for these fungi 10 prepare fOf the actual production of spores; though. once ag3in. thcy::rn:
eventually liberated in astronomical numbers.
Careful physiological work on the hyphomycete Aspergillus niger has established
that several stages lead up to sporulation. These C3n be recognized by their difTenng
nutritional requ irements. (\) Low levels of nitrogen. with adequate glucose and aeration.
pennitted the development of foot cells and the subsequent elongation of conidiophores.
Addition of ammonium ion would prevent this. (2) Addition of ammonium nitrogen and
a TCA cycle acid permitted development of the apical vesicle and the phialidic
conidiogenous cells. (3) Glucose and nitrate were required for the formation of conidia.
We can not assume that exactly the same process operates in other fungi .
I have already mentioned the period of endogenous dormancy that is apparently
built-in to spores. The hyphae arising from spores al!>O seem to have a minimum growth
period before they will spomlate. Hyphae which have not emerged fro m this phase will
not sporu late. even in conditio~ that normally induce fruiting. Toward the end of this
tefractory period. the fungus bomes less able to take up glucose and other nutrient s.
This suggests some kind of membrane cont rol as part of the induction process.
The range of temperature which permits sporulation is narrower than that over
which assimilative growth can occur. For example, mycelia of Penicillium species grow at
temperatures ranging from 2 to 43C: conidia are formed between 3 and 4O"C. Gnonwl!ia
mlgari! grows between S and 3O"C. but produces ascomata only between 10 and 25C.
Since fungi grow in so many different habituts, and have such varied ecological
requirements, it isn't surprising that we can't generalize on the link between light and
sporulation. Light may inhibit, it may stimulate, or it may have opposite effects at differ
ent poi nts in de velopment. It sti mulates the production of conidia in th e Aspergillus
anamorph of a EurotiWII species. while inhibiting development of ascomata of the
teleomorph. The effects of light have ~n investigated from t\l.'O angles: which wave
lengths are active (the action spe~trum). and how muc h light is needed (the dosage response). I noted earl ier that blue light and near UV stimul:ned phototropic responses in
Plrycomycts (Mucorales). and the same wavele ngths (420-4g5 and 350390 nm) induce
fonnation of perithecial aSl:omata in Gda.t;nosp01"(/. Some ascomycetes and conidial
fungi respond to UV. but not to vi$ible light.


Although many fungi fruit only after exposure to light. the actual amount of light
energy needed can be very small. Initiation of Coprinus /ugopus basidiomata is triggered
by only 8 jouks (J) per square metre (5 second, atO.l foot candle). To induce pseudothecial
ascomata of LeptosphlU:ru/ina requires even less light (0.64 J m,). Most fungal responses
need only 0.5-20 J m"; remarkably little, considering the magnitude of the induced effect.
The development of reproductive structures obviously necessitates changes in
morphology ami development. but the nature of the physiological and biochemical
changes involved is not immediately apparent. Detailed comparisons of the mycelia and
conidia of the Chrysonilia anamorph of Neu.rospora crassa show th at some substances
such as trehalose, glutamic acid, glutathione. carotenoids and phospholipid. which are
present at low levels in mycelium, are round at much higher le vels in conidia. Others, such
as arginine. omithine, and adenine nucleotides, are more plentiful in mycelium.

The Physiology of Sex

Reproduction in fungi frequently involves sex, though the ir sexual bhaviour is
sometimes obscure, and one mode of sexuality evolved by fungi is unique and extremely
pro longed. Diffusiblt: chemical substances that trigger sexual acti vity are found in many
organisms. A differentiation has usually been made between hormones, which act on the
organ ism that produces them, and pheromones. which act on other sexu ally compatible
organisms. This differentiation is harder to make in the fung i. Closely related tau may be
homOlhallic and heterothallic. respectively, so a shared sexually active substance could
be ref~rred to as a hormone in the first case. and as a pheromone in the second. In the fungi
it is simplt:r to call them all honnones.
Th e chytridiomycete Allomyees has a water-uiffw;ible sex hormone called sirenin.
This is released into the wuter by the female gametes. and the >malkr. more motik ma le
gametes swim toward them by detecting the concentration grad ie nt. In vi tro exp~riments
with AUomyces showed that response decreased at hormone eonecntrations abO\~ 1000M.
Prdumably at this conccmrarion the receptor sites on the male gametes were saturated,
and they could no longer find their way up the concentration gradient. Mal! gamete>
normally maintain thei r sensitivity by breaking down th e sirenin they intercept.
The oomycetc Achlya ambisexua/is produces se.\ hormones in a ping-pong sequence. to coordinate the developm;;:nt of the male and female sex organ>. A potefltially
fenmk myce lium secretes hormone A. whidl causes an~ nearby potentiJlly male myce limn to develop antheridial bwnches. The male strain th~n relea~es hormone B. which
triggers the development of oogonia on the female myce lium. The developing oogonia
then rc\eJse hormone C. which auracts the amhcridial initials. These initial s produce
homlOn~ D. which causes the oogonial ini tials to lllatur~ . The anthcridia mature when
th~y [ouch the ocgonia. but hormone E might also be hypothesi zed. Two of thGse hormones have been isolated and charactcrizcd. Hormone A is called antheri diol. and hormone B. oogoniol. Pu re Jntheridiol will also induce chemotropism Jnd maturation of
antheridia. so it mJY also represent hormones C and E.
The zygomycetes provide classic IJboratory de monstrations of fungal .lnuality.
W~ plant a '+' strain of Phycomyces or JII /cor on one side of an agar piJte. and the
corrc,ponding '-' strain on the other. When the two meet, gametangia are fonn:d. then
zygosporangia. Because these events seem to happen when the mycelia tOllch. W~ don ' t
necessarily think of diffusible hormones. Yet there is chemistry here, too. Sil< ty y~Jrs ago.
it was demonstrated that compatible strains of Mucor would fonn gametangia. e\'en when by a semipermeable membrane. Much later. it was found that both mycelia
produce a sel< homlOne cJlled trisporic acid when grown close tog cther. This ind u c~s th~
tormJtiofl of gametangia. Th;;: fina l rendezvous of the gametangia is gu ided by 'obtile.


mating-type spttifie subsurnces which. thoogh demonstrably present, ha"e not yet been

The conjugation of yeast cells is governed by diffusible hormones. and by agglutination factors that ~ bound to the cell wa1!s. ElIch mating type of Saccharomyu5 ceTuiJine
has it.'; own hormone . One consists of oligopeptides of 12 and 13 amino acids. The other
has a molecular weight of about 600.000, an d comains protein and polysaccMnde. Though
they are so different. these substa nces have similar effects on the appropriate matin g type:
they inhibit the initiation of DNA synthesi" effectively locking the ce ll imo interpha.><:.
Budding stops, and cells of opposite mating type become mutually adhesive. Since isolated prolOplast~ won't stick together unless they manage 10 regenerate walls. the agglutination factor must be wall-bound. Cells of oppositc mating type have distinct but compkmentary peptidopolysaccharide agglut ination fac tors. Conjugation follows agglutina_
tio n. Sometimes the zygo te multiplies to form a generation of diploid cells, so metim es it
develops into an ascus- like meiosporan giulll.
Amo ng the ascomycetes proper, sex homtones have been par1i~lly purified for Nell.
rospom (Sordariales), and there is evidence for the existence of comparable hormones in
A5cobolu5 ( Pezi zales) and Bombardia (So rdariales). T he well-known mycotoxin
zearalenone, prodoced by the hyphomycete FU5arium gramintarum. apparently stimu
lates the developme nt of pcrithecial ascomat3 of its tcleomorph. Gibbudl" ~e"e
Among the basidiomycetes, it has been shown that oppo.~ite mating types of Tremel/a
(Ph ragmoba sidiomyeetes) have indi vidual. constitutive sex hormones. One of them h~,
been panially characterized: Tremerogen. as it is call ed. is a l2-amino acid li popcplide
with an isoprenoid conjugated to the sulphur of the cysteine at Olle en d. When the yea,tlike basidiospores are exposed to Ihis, they SlOp bodding and produce a conjugation'tu~ .
The red yeast Rhodo(()m/" has simil:rr hormones. Om." of these. nJm~ rhodotorucinc.
inhibits budding and induces formation of conj ugation tubes in the opposite mating
type. The resultant tcleomorph i~ RhodospDridillln (Uslilaginale$).
The situatio n in many basidiomycetes is co mplicated by the fact that although the
fim prerequ isi te fo r sex ual reprod"ctiOl1 - the bringing tog~th er of compatible nucleihappens a t the momc nt of dikaryotization. the ultimate sexu31 fusion of nucle i may b~
long delay~d. aod happens only to distllnt descendants of the original nuclear pair. Al_
though sex hormones may facilitate the meeting of Olonokaryotic myceli~l. other factors.
nutntional and environmental. probably determine the timing ofnude-ar fusion and meioSIS.
Although "cry few fungi h3vt bt;~n investigated for the prescnce of SO:.\ honnones,
it seems li kely that the ir sec retion is the norm rather th on the e.\ ception. [f ascomycete and
b;ls idiomycctc sex hormones arc show n to have some uniformi ty of structtJre and action.
it would be fJsdn~ti1\S to apply the m to the vast number of dikarYOlll>'cOlan anam orphs
for which no teleomorph is known, to see if sex ual dcvdopm~nt eQuid ~ initi:l.!cd, ~nd
1ll3ny lungstanding mYSteries solved.

Antifungal Compounds
The chemical industry


thousonds of new compounds every ye ar. Many

possible uses. Two quest ions commonly asked :rre: Are
they antib iotic? Are they fungicidaP So. by CmpinC<l! testi ng. new fungici des are found .
Until recc ntly it wus only afte r a co mpound h~d ~~ n discovered to be ftmgicidal that its
mode of action was invcstigmcd. though enough is now known about fungicidal action that
new fungicides call ~ designed at the mok""cul3l' level, I.;ith appropriate prosthetic groups.
Here are some groups of fungicides and the ir sites of action. ( I) Cop per. me rrury. di th i(l-

arc routinel y scrcened for



C'a r bamatcs. phtha limldes and Quinones teoo to be non-specific enzyme poisons that bind
to functional groups that nonnally maintain the secondary structure of proteins. (2) The
anti-fungal polyene antibiotics. nystatin and amphotericin B, form complexes wi th sterols.
and thus disrupt membrane formation. Oomycetes and bacteria, which have no sterols in
their membranes. are unaffected. (3) The sterol-inhibitors, such as bitertanol. triadimefon ,
and triforine, prevent the biosynthesis of ergosterol, the major sterol in many fungi, and so
might logically be ellpected to interfere with membrane synthesis. though whether this
actually happcllS has not yet been established. (4) Polyoxins interfere with chitin synthesis
in vitro by competing with chitin synthetase for its monomer substmll!, but have a di$llppointingly limited range of activity in vivo. (5) Cycloheximide is 8 pyrimidine analogue,
and blocks protein synlhesis by binding to ribosomes. (6) Benzimidazoles (e.g. benomyl)
bind (() the tubulin that normally fonn s the mitotic spind le, and so disrupt. nuclear division.
Once again, oomyceteS are 001 8ellSitive to benomyl, though theiT division is inhibited in a
similar way by colchicine. (7) Carboxins interfere with the metabolism of mitochondria in
many dikaryomycotan fungi, causing succinate accumulation.
As we learn more about the physiology and biochemistry of fungi we should be able 10
design molecules that will interfere in aspects of metabolism that are sprcifie to fungi. leaving
non-target l."Kganisms unaffu:d We will also find new ru;es for many fungal metabolites.

Further Reading
Aronson, J. M . (1981) Cell waH chemistry, ullrastnJ~ture and metabolism, pp, 459-507 (in)
Biology of Co nidia l Fungi. Vol. 2. (Eds.) G ,T. Cole and S, Kendrick. Academic
Press, New York.
Bannic ki-G arcia. S. ( 1966) Cell wall chemistry, morphogenesis. and taxonomy of fungi.
Annual ReYlew of l\'1ierobiology 22: 87- 108.
Ikrry. D_H. ( 1975) The en\'ironmental control of the physiology of filamentOUS fungi. pp. 1632 (in) 'fh(: rilamentous Fungi. '.hl I (&Is.) J.E. Smith and DR Berry. Arnold. London.
Burnett, J.H. (1976) Fundamentals ofl\lycology. Arnold, London.
Carlile. M.1. (19 70) The photort:sponscs of fungi. pp. 309-344 (in) Photobiology of Microorganisms. (Ed, ) P. Halldal. Wiley. New York. V.w. (1958) Physiology of Fu ngI. Wiley, New York.
Griffin. D.H. (1981 ) Fungal Physiology_Wiley, New York .
Holl. R. (1981) Physiologyofconidi al fungi. pp. 417-457 (in) Biology of Conidial Fungi.
Vol. 2. (Eds.) G.T. Cole and B. Kendri(k . Academic Press, NcwYork .
H3",ker. L.E. (1957) Th e Physiology of Rep r oduction in Fungi. Cambridge University
Press, London.
Lowe, D ,A. and R.P. Elander (1983) Contribution o f mycology to the antibiotic industry.
l\Iycologia 75: 361-373.
Mueller. E. ( 1971) Imperfett-perfcct conne<:tions in ascomycetes. pp. 184-201 (in) Taxonomy of Fungi Imperfecti. (Ed. 8 . Kendrick). UniVl:rsity ofToronto Press, Toronto.
Robinson. P.M_ ( 1978) Practical Fungal Physiol ogy. Wiley. New York.
Smitll. J.E. and O. R. Berry (Eds.)(1975. 1976, 1978) The Filamentous FungI. Vots. 1-3.
Arnold, London.
Smith, J .E., D.R. Berry and 8. Kristiansen (Eds.) (1983) Tile Filamentous Fungi. Vol. 4.
Arnold. l ondon.
Turi3n. G. (1966) Morpllogcnesis in ascomycetes, pp. 339-385 (in) The Fun;:i. Vol. 2(Eck) G.c. Ainsworth and A.S. Sus~man. AC(l(icmie Press. New York_
T urian. G . ( 1969) Dirrerenciat ion Fongique_Masson. Paris.

~ U~PE.eC2

Fungal Genetics Mendelian and Molecular


Genetics is the discipline that seeks to understand the ways in wh.ich the information needed 10 reproduce an organism is slored within iI, and how that information may
change and be reassorted before it is passed on to th e next generation. In recent ycars .we
have also become oonccmed with how this informat ion can be c hanged in a directed way
by human int<,rvemion. This chapter anempts to show how fungi are useful lools in some
areas of both Mendelian and molet:ular genelics. If yOUT background in this area is sparse.
you will find some useful introductory infOf1ll.ltion in chapters 1 and 9. If you still have
trouble \\!th what follows, I recommend th at you consult an e lementary gem: tics tell!
before trying agai n ..
In the simplest ternlS, genetic infonnation (the genome) is maintained in the ,eU as
1000g.linear sequences ofnudeotide base p:lin whi, h make up DN A molecules. Theorderin
whi,h these bases ocrur constitutes the gencti, code. and this 'ode specifies the sequences
of amino acids required to build all the proteins necessary for the construction and operation of the living organism. DNA molecules can be very long. incorporming many thousands of base pairs, and are ,alled'hromosomes. The genome of prokaryotes is contained in
a single. usually ciro::ular chromosome found in the cytoplasm. The genome of eukary()(es is
contained in twoocmore(often many more)chromosomc:s.. whkhare contained in a nudeus,
a special command module separated from the c)'1oplasm by tWO membranes.
The cukary01ic plants and animals differ from ea,h other in many ways, but both 3re
basically diploid. This means that their nuclei contain two matched sets of ' hromosomes:
(usuall y one set orig inally derived from a male g3mete, one set from a female gam ete). So
each chromosome has a 'double: Most genes on ea,h chromosome have a counterp~rt ,
,alled an allele, on the 'double: This ~Ilele affects the same ,h3f3.,rers, thou gh nOt
nC(.:es.sarily in the same way. FOf e:.;ample. one allele of a particular gene makes pea pl~nts
tall, while Lhe orner allele makes them dwarf. If ~ tall plant is crossed with a dwarf pl~nt,
the re will be more tall offspring than dwarf offspring. Plants will be dwarf only if both
alleles are of lhe dwarfin g kind. This shows that one allele can mask another: we say that
the 'tall' allele is d ominan t. the 'dwarl' allele Th is makes genetic analysis
diffi,ull. and also makes il hard to bcud pure lines of many diploid organisms, because it
is almost impossible 10 eradicate recessive genes. since you ,an't tell whether they are


presem or not (though it is easy 10 pure-breed for reccss ivc colour gClles. su(;h as those
expressed In white ratS and mice.)
The vast m~jorily of fungi are h~ploid. which means th~t their nuclei contain only
a single set of ctLromosomes. This gi~-es thcm ccnain advantages over diploid o.-ganisrns
for genetic studies. since there are no competing aUeles. and c"ery gene is potcntially
capable ofbcing expressed in the phenotype (the physical manifestation Or incarnation of
the organism). This .,bsence of maski ng makes gcnetic analysis much easier. The advanI~ges of using fungi in genetic studies are as follows:
(I) The mycelia of almOst all fun gi are populated wilh haploid nuclei
(oomyeetes, be ing chrornislan rather than cumycOtan. are atypically diploid), and many
fungi form large numbers of uninucleate. haploid s]lQres_ Th~se can be used 10 study
natuut]y occurring or induced mutations.
(2) The hyphae of closely related eum}'cotun fungi can fuse with one another
(anastomose) locally during nOffilal assimilative growth, exchanging ntlclei and thereby
producing heterokaryons (m ycelia containing genetically different nudei). The heteroknr}otic eondition confers great flexibility on many conidial fungi, helping them to
cope with different substrat~s and conditi ons. Heterokaryons can be investigated tinder
corumned conditions by isolating spor~s or hyphal fragments. and arc used by geneticists
in the complementation t~st (see below). The production of heieroknryons may also be an
essential step toward a long -delayed sexual fusion. as when basidiomycetes init iate
dikar)'otization by an astomosis between sexually compati ble mycelia.
(3) Hypha l fusions also lend to exchange of cytoplasm, producing
hetcroplasmons. These make it possible to Study extr.lnuc\ear genetic phenom~na . and
fungi ~re panieularly vuluable for !he investigation of cytoplasmic inheritance.
(4) The phenomenon of crossi ng-ove r. a vital part of the process of genetic
recombination, can be most degantly studied in ascomycctes like Neurospora or Sardaria.
The>e fungi havc very sho!llife cycles, Qlld eom'eniellt]y arrange the eight nuclei ~sulting
from m.:iosis and the subsequ.:'nt mitosis ill a linear sequence within the ascus. One nucleus
goe~ into each uscospore, nnd the nSCQSpores are arranged in single filt within Ihe n:umwly
cylindrical ascus. The a~ospor.:s in th is 'ordered tetrad' can be individunlly cultured and
ICS1<'d in various ways. Using appropri:ue marker genes: (a) first-division segregation can be
distinguished from sccond-dhision segregation; (b) reciprocal and non-reciprocal chromosomal exchanges can be det.:'cled; (c) chromosomes can be mapped; (d) interferen~ can be
;lUdic<J. (All the terms JUSt m~ntioned are di sc ussed in more detail below).
(5) The phenomenon of somatic crossing-ovcr was fir;t seen in the fruit fly
Orosopliila, but it can be much more easil y studied in fungi. Somali<; nudcar ftL~ions
occur. with low but predictable frequcncy in fung~1 helcroknryon s. The resulti ng d iploid
nudei occasionally undergo mitotic cross(wer. Somt: ofllie somatic diploid nuclei which
h:we undagonc mitotic cross-over cnn revert to the hapl oid condition through irregular
forms of mitosis. These haploid nuclei ha"e thus undergone genetic recombinmion without benef,t of sex , The process is called p,trastxual ity. Thanks to their production of
large numbers of uninuclcat~ ;;pores expressing specific genetic markers (t.g_ CO!Qur. or
nutritional deficiencics), conidial fun gi such as Aspergillus nidI/fans are espedally well
suited for investigations of this ph<!nom~non.
(6) Fungi can be handled rather like bacteria - many pure cultures can be
SlOte\1 in a small spact, and th~ generation timc is shon - yet fUngi ore eukaryotic, SO
resullS arc much more applicable 10 Ihe oth.:'r major kingdoms, ani mal s and plants.
Fung~1 genetics is not without its difficulti.:s. Fungal nuelei are often very small,
and we cannot do the kind of analysis .of chromosomal arrangement at the mewphase
stag.: of nuclear division that is possible in mlmy plants and animals. The drawings in Fig.


10.1 (councsy Dr_J. Ais!) follow a fungal nucleus through a normal mitosis, which [ake.~
aboul li ve minutes. It is immediately apparent that fUl1!zal di\'ision is not like that in other
organisms. 1lw: spindle dc\'elops illside the nuclear en,elope. There is 110 metllphase
platoe. The chromosomes are )'uy snwll and not "ery clearly visualized. Their disjunction
is 110/ synchronous. Most of the division happens inside an intact nuclear en'elope.
which evcntually elongates. constricts and fin~Hy givcs rise to two daughter nuclei.
It is not possible [0 count chromosomes a. easily a. in many other organisms, and
we have to rely on features di:;.cussed below. such as spore colour and assimilative abili ties. to investigate genetic trailS. .
The small size of conidia. ascospores and basidiospores makes them difficult to
handle individually, and the necessity for sterile technique to avoid contamination doesn't
make thing s any easier. But with practice. all th ese handl ing difficulties can be overcome.
Fungi have been widely used to study recombinotion and gene action. but they have been
little exploited in studies of population genetics. This may be partly because it is I)ftcn
h:ml to decide ""hat a fungal ind i,'iduaJ is: it has such a diffuse 'body: and through








Fig. 10.1 Nl.JClear

.r_".,__' f .
UlV ........ 't'I ISIS',





anastomosis the mycelia of eumycotan fungi often become heterokaryotic, containing
nuclear material from several different genomes. Nevenheless, the potential for such
studies remains, and is beginning to be ex.ploited in studies of biological species com_
plexes such as th at represented by the binomial 'Annillaria mel/ea'.

Investigating Crossing-over in a Fungus

using Marker Genes
Crossing-over is a nonnal pan of thc major process called meiosis. As meiosis
begins, the diploid cell has two sets of chromosomes. Each chromosome has already
replicated itself, and so is composed of two parallel strands or chromatids. Each chromosome comes to lie parallel to the same (homologous) chromosome from the other set: in
Fig. 10.2 the two 'white' chromatids represent one homologous chromosome. and the two
'black' ones, the other. If wc assume thut the 'black' chromatids carry a gene for darkcoloured ascospores, and the 'white' chromatids carry a different allele of the same gene,
onc that will produce light-coloured ascospores, then Fig. 10.2 a shows what happens in
the absence of crossing-over, and Fig. 10.2 b shows what transpires when a crossover
In the simplest crossover. shown in Fig. 10.2 b, a hreak occurs at the same place in
one of the 'white' chromatids and one of the 'black ' chromatids. The ends rejoin, but in a
new arrangement: thc pan of the 'black' chromatid carrying the dark ascospore gene is
now joined to pan of a 'white' chromatid and vice versa. When the four chromatids
separate, they will represent new combinations of genes.
This happens in the real world with ascospore colour in the dung-inhabiting fungus
Sordaria, as you can see in Fig. 10.3, when adark-spored 'wild-type' strain is crossed with
a pale-spored mutant.
As you can also see in Fig. 10.4, more than one crossover can happen between two
homologous chromosomes. This strange but vitally important process of genetic recombination accounts for the unpredictable mixes of parental genes !hat occur in the offspring of
sex.ual eukaryotes. Crossing-over ensures that sexually reproducing organisms vary in many





i r/'"r ("V
( r ( 1 (1 (r iii i

r! Tr

) 00

00 )





Fig. 10.2 (a) no crossing-over - f..5t division segregation pattern; (b) ~rossing-over between ascospore
~OIOUr gene and ~entrOl1lre - s.econd civision segregation pattern (see text).




ways. and so remain physiologically flexible. Crossing--over is one of the main mechanisms
involved in providing the pool of variability on which natural selection a<:ts.
If we have appropriate marker genes, like the ascospore colour gene just mentioned.
we can use the incidence of crossing-over to find out roughly whcre these genes are in
relation to the cent romere (the point at which the chromatids are functionally joined. and
the last thing to separate at mitosis). How can we do this? We begin by assuming that a
chromosome is equally likely to break anywhere along its length. IT this is !rue, then the
further away from the centromere a marker gene is, the more likely it is 10 be in,"Olved in
a crossover. Also, if we have two linked marker genes, the funher apart they are on a
chromosome, the more likely they are to be separated by acrossover. This kind of information allow5 us to make chromosome maps showing the relative (though not the absolute)
locations of our marlcer genes.
Our map-making rests on the assumption that we can keep track of the products of
meiosis. In most organisms we simply cannot recover and analyze all the nuclei arising
from one meiosis. Bm amazingly enough. we can do it in some ascomycetes, because their
meiosis takes place in a long, narrow rube called an ascus. Figure 10.2 shows how the
products of the divisions lie in a straight line. SO that their exac t origin can be traced. The
example I gave above involving light and dar:\;: coloured asoospores is in fact a real one. In
Sordariafimicola. ascospore colour is detennined by a single gene. Wild-type ascospores
are dark. but there is a mlllant strain with pale spores. Since Sordariajimicoia is heterothallic (olllbreeding). the maling of a nonnal dar:\;:-spored Sirain with a mutant pale-spored
strain can be used to demonstrate some features of crossing-over. In this panicular mating.
if no crossover involving the ascospore colour gene has happened. there will be four dark
ascospores at one end of the ascus. four light oncs at the other end. as in Fig. 10.2 a. But if
the segment of chromosome bearing tb.!colour gene has been cros~d-o,cr. then each half
of the 3iiCUS wi11 contain a pair of light spores and a pair of dark Ones, as shown in Fig.
10.2 b. These pairs can appear in ~veral different ~quences, depending on which of the
chromatids undergo crossi ng.over. Crossovers c~n take place between any two of the
homologous chromatids. 50 there are four possibilities for single crossovers: 1-3. 1.4.23.
In fact, crossing-over can be e\'en more complex than I have just described, because
it can happen twice between a particular pair of chromatids; or one chromatid can ex
change ~gments with both of its hornologues. Some of these possibilities are shown in
Fig. 10.4. Of cou rse. we can't watch these events. but we can explain the ascospore
arrangements resulting from crosses between strains with two marker genes by diagrams

fig. 10.3 Pefithcdal squash of Sordaria

fimicola - a cross between the dark
spored wid type and a pale-spored
rrutaot. Note rrst and second civision
segregation of ascospore (0Cu facIO!:

< .



SllCh as those in Fig. 10.4_ Not all gencs epress thcmsdvcs so immediately and un
cqui\'ocaUy as thai determining ascospore colour, bm the proce>s of segregation werks
just the same for any gene. In order to analY7.e other kinds of markers which don't express
thermelves visibly in the ascospore, we have to physically pick OUi the IIscospores (this
calls for great dexterity and lots of practice), and grow th<:m individually in culture. The
sequence of the spores inside the ascus is recorded. lind helps in the interpretation of the
subsequent genetic analysis.
As we have already seen. ifn o crossing-over happens between a particular gene and
the centromere. the four a"'t!OSpores atone end of the ascus will all be of one genotype, and
the four 01 the other end will all be of the other genotype. This arrangement is called the
'first division segregation pattern' he>;ause the tWO versions of the gene separate at first
division mciosis (see Fig. 10.2 a), But if crossingover has happened bel"'ecn the gene
and the centromere. the two different versions of the ge ne are not separated until the
second division of meiosis. This arrangement is called a 'SCl;ond di"ision segregation

rcz- ,
,'-' ._.

, -.




- . -- I -~:J
_:yj!'- J


Fig. 10.4

C~s ol





- ...----






.l --")

C--, -L

I . 1

:c"""t ,,= .

- --....

-r, -

C -


variou>doI..t>IecmSSOI/ers betlveen two marker genes.






and there can be four such panems ...... hich occur with about equal frequenc~. Any
particu lar gene wi!! show a definite fr... quency of crossi ng-over, which nalu"lIly increases
as its distance from the centromere increases, The recombination frequency for any gene
will equal half of its freque ncy of crossing-over. Th is is be.::ause only two of the four
chromatids arc involvcd in any particular c rossover. If we obsel"\.'c a squashed pcrith
ecium, and find that of 20 asci. 8 show evidence o f crossing-over in the ascospore oolour
gene. we can say that the frequency of crossing-over for our marker gene is 40%, and the
recombination frequency is 20%. That figure is also a useful way of placing the marker
gene on a chromosome map. One map unit is arbitrarily defined as the disl.:lnce between
linked genes (genes on the same chromatid) that will give 1% rewmbination. The gene
mentioned above is 20 map units from the cent romere. If a second marker gene has a
reco mbination frequency of 30%, this mea[lS that it is 10 m:ip units further from the
centromere than the first marker, It CDuld be only 10 map units from that firSt marker. but
it cou ld also be 50 mllp unit~ away, on thc other side of the centromere_
With patience and de~ terity, a two-faClOf cross can be done with the ascomycete,
N tll rosp om crass(/. (Sordarialcs)_ using two linked marker g,mes (with all eles A and a. B
and b). lllree mai n ascospore pntterns will emerge.
( I) The parental ditypc , AB AS AB AB ab ab ab ab: if there is no crossing-oyer
between the two marker genes. the two tetrads of 3SCOSpores wilt reflecllhecharacteristics
of the respective parents.
(2) The tetraty~ pattern. e.g. AB AB Ab Ab aB aB ab ab: when a si ng le crossover
happen s so mewhere between the two marker ge nes. four kinds of ascospore res ult. two
paremal types and two recombinants.

as as

(3) The non-parental ditype, Ab Ab Ab Ab

aB a B: if tWQ crossovers ocCllr
between the marker genes. atlthe products wi!! be rcei procal recombinam s. arronged in two
tetrads, None of the products have the same combination of genes as ei ther of the parent >,

The rdative frequencies o f these three pntte rn s can be used to calculate the linkage
dist:mce between the Iwo marker genes, and to deduce their positions relati\'e to each
other and the centromere.
It c an also be used to discover which of the two markers is closer to the ccmro mere,
~nd whether the m:,rkers are on the sa me or opposite sidcs of the cen tromt:re. For e:o;amp!e.
we an;llyze the ascospore arrangements resulting from a two-factor cross. and find that
there are 56 p,an:ntal ditypc asci. 44 tetrntype asci, and 0 non-parental ditypc asci. What
can we deduce from these data? tr tho: marker genes were unlinked (i. e. nOt on the same
chromosome). the frequency of pare ntal ditypc and non-parental ditypc asci would be
expected to be the same. Since no non-parental ditype asd are recorded. we can ass ume
that the two m~rkers afC linked (i,e .. on the same chromosome). In order to be able to pla~e
the markers in tbeir correct relationship to eac h other and the CC[llfomere. \\1(.' need to
aoalYle the 44 t<::trJtype asci fun her. Wc note that there arc lhree arrangements:
(i) 24 are AS AB Ab Ab as ~ S nb ab
(i i) 19 arc AS AB ab abAB AS ab ab
(iii) I hAS AS
aB Ab Ab ab ab
The marker genc~ could theoretically be arranged in one of three ways with respect
to the centromere:


(f) Centromere -

Aa - Bb
(If) C~ntromcre - Bb-A>
(II/) Aa - Centromcre - Bb


Ascospore pattern en above is a result of first-division segregation of lheAa marker.
and seconddivision segregation of the Bb marker (the B and b alleles have been e)(
changed, the A and a alleles haven 't). The crossover that produced this arrangement mUSt
have happened between the Bb gene and the centromere. but not between the Aa gene and
the centromere. If the twO markers are on the same side of the centromere. Aa must be
close r to the centromere than is Bb (gene 3l1'angement f). But ascospore panem (0 could
also be explained by gene amtngement (flf). in which the marker genes are on opposite
sides of the centromere. So far. only gene arrangement (If) can be ruled out. However. if we
now look al ascospore paltem (ii). it is clear that both Aa and Bb segregated at second
division.lfweassume there was only a single crossover. th is means that it must have laken
place nearer to the centromere th:1.O either Aa or Bb, and between the centromere and both
markers. So both marker genes mUSt be on the same side of the centromere. and gene
arrangement (I/f) can be excluded.
So, by II process of elimination. we have shown that only one of the three possible
gene arrangemen ts. (i) Centromere - Aa - Bb, fits all the observed facts. Even the
'oddbaU ascospore pattern (iii) can be explained by a two-chromatid double crosso,er.
between Aa and the centromere. and between Aa and Bb (you can easily work this out on
p:lper; it is not one of the examples shown in Fig. 10.4. but can be visu alized if the
uppermost example is revamped with the crossove r nearest the centromere happening
betwee n Aa and the centromere, rather than between Aa and Bb).
We can now calculate the 'map distances' of the marker genes from each other and
from the centromere. Of the 100 asci examined. 25 (patterns (i) +( iii had a crossover
between Aa and Bb. while 20 (patterns (i i) + (iii had a crossover between the centromere
and Aa. Applying the appropriate formula (half the number of recombinants. di\'ided by
the tot31 asci observed. multiplied by 100), we find thll! the distance between Aa and Bb
is 12.5 map units, and the distance between the centromere andAa is 10 map units.
Imenerenee occurs when crossing-over at one point reduces the chance o[ another
crossover in nearby regions of the chromosome. This phenomenon is detected by studying crossovers of three or more linked genes. Since the centro mere itself acts as a marker.
we have essentially a three-gene system in telrod analysis, which is therefore a good way
of st udying interference.
The events di~cussed above involved truly reciprocal cro~~overs . in which exactly
equivalent segments of chromatids are exchanged. Bu t sometimes the exchange is not
ellaclly equal. This is called non-reciprocal rcc.:ombination. or gene con,'ersion. and if
very closely linked marker genes are studied. it is found that crossovers are actually more
often non-reciprocal than reciprocal. This phenomenon is explained by the breakdown or
exdsion of shoo lengths of DNA during recombination, and their replacement by re pl ication from another chromatid. OllCe again. fungi like NeltroJpor(1 have been very useful in
elucidating gcne conversio[l.
"'lutant genes can act a~ markers enabling us to i[lvestigate the genetics of fungi .
The kinds of mutant genes a' ":lilable affect such features as morphology. colour. mating
type. and nutritional requirements. In some morphological mutants, lhe growth ratc or
brJnching pattem of hyphne is altered. with various effects on colony morphology. Neu,
roS{XJffl Cnl.lSU has button and 'ropy' muta nts. Other morphological mutations affect
reproductive structures: Aspergillus nidu/(ms has stunted conidiophore. and 'bristle: in
which the conidiophore hus no conidi um -producing uppurutus at its apex. Colour mu
tantS u5uall y affect spore toloUT: Aspergillus Ilige, has 'white: . fawn' and 'olive mutants.
Biochemical mutants are perhaps the most useful marl:;:ers. Biochemical mutants
usua lly require some nutrient that is not needed by the wild type. Such mutants are called
au.-..;otrophs. A minimul medium is concocted for the wild type (for Neurospora cras.w


this contains only inorganic salts, including a nitrogen source. sucrose, biotin and agar).
S3mples of the fungus an: cxposed to a mutagenic agent such as uiuaviolet light. then
plated out on the minimal medium and also on a complete medium, which contains malt
e ~t"lct and yeast c}Otract in addition to the ingredients listed for the minimal medium. If a
strain is found that will grow on completc medium, but not on minimal medium. somc
biochemical deficiency is suspected. Now II lillie detective work is called for. This strain
must be systematically tested to sec what it needs, by anempting to grow it on minimal
medium with additions of mixed vitamins, or mi}O ed amino acids. or nucleic acids. If the
minimal medium pl us miJr.ed vitamins keep it alive, then it is grown on minimal medium
supplemented with individual vitamins. In this way the specific requirement of the auxotroph can be pinpointed.
Fermentation mutants arise spontaneously in yeasts. resulting in inability to fennent
a particular sugar. Resistance mutants also arise spontaneously in .wild populations. but
their frequency of occtIlTCnce increases if the organisms arc c}Oposed to antibiotics. antimctabolites or othcr deleterious influences: such mutams lire actively sought in the laboratory.
The fungus is grown in a concentration of the deleterious substance high ellO\lgh to inhibit
IIOJIIl3.i gto","th: resistant mutants are the only ones to survive. SuppresSOt" mutants o\'ercomc
or compensate for any deficiency induced by an earlier mutation, and cause an apparent
reversion to the wild-type. PhysiolOgical mutants apparently changc the biochc:nustry of
the fungus subtly. altering its reactions to some environmental influence. such as temperature or light. One mutant of the zygomycete. PhY('Qr/!}'CtS blGktsleeanus. ha~ normal morphology. but its spowngiophores no longer grow towan.! the light.
Another group of biochemical mutants are those which produce greater than nonnal
amounts of particular substances. Although this kind of mut:!.nt hasn't been subj~ted to
very mllch ge netic analysis. it is sometimes economically import~ m . llle commcrdu!ly
e.lploited suains of Penicillium chrysogenum that produce such large "mounts of penicillin are mutants of this kind.

One Sex, Two Sexes, Many Sexes

reproduction will introduce more genetic var13tion to a population if the
genomes which meet. and are then reassorted during meiosis, come from different individu ab. That statement may sound strange and even superfluous to you, since you belong
to a species in wh ich such behaviO\lf is not only muuml, bul obligatory. BUl in many
cases, an indiv idual fungal mycelium can and does keep ilS sexual ity to itself - its
hyphae can produce sex organs of both kinds, which go through the processes of se}Oual
fusion and produce a viable zygote. Thi~ condition is described as bomothallism. Homothallic ta}Oa arc vcry usefu l if we simply want 10 demonstrate sexual behaviour in fungi.
~ince we dont have to worry about providing a suitablc mate. The :!.dvantage of this
systcm in Nature is probably two-fold: 10 pennit sc~ual reproduction when no appropriate
compatible mycelium can be found (the lonely spore hypothesis). and to perpetuate
particularly successful genotypes. which wou ld tend to be reassorted. and therefore diluted. by outbreeding.
M:my fungi. however. have evolved some ronn of reproductive diITercmiation of
individual mycelia: we call this phenomenon hcterOlhaliism. ~nd it enforces outbreed
ing. One approach is sexual dimorphism: the production of tWO kinds of sexualstructurc
which look and a~t differently, and are ofte n developed on different mycelia. In some
fungi. both kinds of SC}O organ can be formed by II single mycelium. but only gametes
originating from di fferent mycclia can fuse. This implics genetic control of sc}Oual reproduction through the development of mating types th3t incorporate incompatihility genes.
These make sc}o impossible bo!tween $trains of the same m:lIing type . In many fungi.

mycelia may be morph.ologically indistinguishable, yet invisible incompatibility factors
can prevent their mating. Incompatibility can prcvent anastomosis. or prevent karyogamy. In fungi like the ascomyce tes. wherc fusion of assimilati\'e hyphae does not initiate
the sexual process, vegetative incompatibility is not a barrier to sexual reproduction. and
is often determined. by entirely separate genes, so that a sin gle speci~s may be divided up
into a number of vegetati ve compatibility groups (VCGs). Such ascomycetous taxa as
Crypiwneclria parasitica (Diaporthales). NeJ<T()spora CT{Jna (Sorelariaies). and Fusarillnl
mOllilif()~(anamorphic Hypocreales). contain manyVCGs. In the basidiomycetes, where
fusion of ordinary, und ifferentiated assimilative hyphae is a prerequisite to the estahlishment of the dikaryophase, and dikaryotilmion a prerequ isite of karyoga my, vegetative
incompatibiJiry can effectively pre"ent sexual reproduction.
Basically, heterothallism implies that a haploid nu<:leus can complete the life cycle
only if it mates with another haploid nucleus carrying a different mating-type factor.
Heterotha ll ism is the fungal eq ui valent of the separate sexes found in many philltS and
animals. As we shall sec, the fungi. despite their restricted genome and relatively eonsistent organization. have evolved many and complex variatioM on this sexual theme.
The simplest kind of genetic system that can ensure olllbreeding consists of twO
"'iITerent alleles, which weean label 'A' and 'a: at the same locus. Pairs of mycelia carrying
the same allele will be incompatible (A ..... ith A. Of a wilh a), while pairs of mycelia with
different alleles (A and a) will be compat ible. This system effecti\'cly divides a population into two catcgories. and has the same eIT.eet as d ivision into two sexes . This two-allele
system is found in all groups of fungi other than the most highl y evolved basidiomycetes.
Examples or.: the zygomycetes Rhizopus and Phycom)"ces . species of the ascomycete
genera Nl'ltros(HJro, /umbo/us and SclerQlilliu. and species of the tdiomycete gellCra
Puccillia anq VS Ii/ago.

Bipol a r a nd Tetra pol ar Mating Systems

In Aphyllophorales. Agaricales and gasteromycetous basidiomycetes. compatibility i~ dekrmincd by one or two gen~. but each of these may hal'e many different alleks .
Only two or four a!lelcs are prese nt in any give n di karyon . at a single loc us or at two loci.
If all compatibility alleles occur interchangeably at one locus. the m~ting system of the
fungus is ealled bipolar; if they are found at two loci. the mating system is called
l et rapoiar .lfthe alleles occur ot a single locus. the offspring of a single basid ioma will be
of twO "'ifferent mahng types. If the alldes ~rc at two loci. olTspring of a singlc bas id ioma
,'-"ill be of four mating types. Although the products of meiosis in the basidiomycetes are
not an ordered tctrad. as they arc in the cylindrical asci of some ascomycetes, it is still
possible to c\llturc the foor basidiospares arising from an individual meiosis. Jnd use
them in compatibili ty trial s.
III bipolar fungi {most smuts. some sastCfOmyCetes. eOI'd/JUS comalus).the single
locus m which all compatibility alklf$ OCc ur can ~ called A. NOVo' "ecan label the allelc.~
in a gi"en dikaryon A I A2 (they must hoi; different. or th~ dikafyon .... ouldnt form in the
lir.t plnce). Otherdik ar)'on~ will probably haye di fferem alldes . which we can call'\3 A4.
A5 A6. ctc. Rlndom matings in populati Olls with such div~= mating-type alleles can be
almost 100<;0, successful. Remcmt><:r that random matings in populations of two-allele
organisms would be only 50% successful. Now we can ~ee why a multiple-allde system
mly be more desirable than a two-allele syste m.
In tetrapolar fungi (most Aphyllophorales. AJ;ruicales and gasttromycetes). we can
l~bel the two loci A and B. For a dikar)"on to be fertile, the aneles at each of the loci must be
different - .... e tan label them AI B I A2 B2. The haploid (monokaryotic) mycelia d",rivcd
from this dikaryon will be of four ki nds: A I B I , A 2 B2. A I B2, and A2 B 1. You can easi ly

F UN GAL GEl'.'ETI CS 16',1

wOfk out th:lt only 25% of random m:lIings among Illese siblings will be successfuL Of
course, malings of non-sibling monOkary0ll5 will again work much better: if we match up
Ille four genotypes jusl liSied with monolwyons deri\'ed from a dikaryon that is A3 B3 A4
84, success should be complete. But what if the al kle at ooe of the loci is the same as in our
original strain. so that iL> all~les can be listed as A I B3 A4 B4? What should be the peoccntage success of matings ber.>.ttn this and the products of this and the original Strain (A I BI
A2 B2)? Work itQut on paper. Your answer(y,'hich should be 50%) represents the number(lf
fertile dikaryons that will rc~ulL But if you did this experi ment. you would probably find
that you finished up with many more dikaryons than youexpeeted_Dlis is becau~ dikaryons
can form between partially incompatible monokaryons, though such dikaryons will nOt be
able to produce fruit bodies. In the e~an1ple I just gave, there could be as many as 87.5%
dikaryons (37.5<;(, of them sterile). and only 12.5% total inCQrnP'ltibility.

It has been found thai the genes at the 1111'0 loci often control different pans of the
dikaryOlizatiOll process. In the basidiomywes Coprinus /og~ and Schiz.op/lyllum commime, clamp connections de,-elop only if the dikaryoo is heterozygous (has different andes)
fOf the A locus. For e;.:ample. AI B I A2 B I would h.we hyphae with d amps, A l BI A I 6 2
""Ould nOi. Nuclear migmtion is controlled by the B locus, and would fail in A I BI A2 B I.
Of 230 species of Aphyllophorales. Agaricales and gasteromycetes examined. 1015% were homoth allic. about 35% were bipolar hel~rothal!ic . and about 55% tetrapolar
heterothallic.1t has been esti mated thut Schi!ophyllllm communI! probably has about 340
+ 120 different A Jlleles. and 64 + 12 different B alleles. Estimates in some other basidi
omycetes are of the ord~ r of 100 different al leles for eJch locus. thollgh the bird 's-nest
fun gi. Cye/hllI .Ilriallls and Crllcibu/um vulgare. nre be lieved 10 have on ly about 10
alleles for each locus _
Second3ry homolhalli~m can occur in heterothullic fungi. If an ascus conta ins only
four spores, as in Nellrospora lelrasperma. instead. of eight. there can be a compatible pair
of nuclei in each spore. Similarly, if a basidium bears only two spores. as in AgariClIs
bnuUlucellS, each of these may also contain two compatible nucle i. Homothallism is
possible. ewn in species with fourspored basidia. If an extra mitosis happens in the
basidia, two compati ble nucld may find their way into some of the basid iospores.
Homothallis m can also be introduced in what would otherwise be a heterothallic
fungus by mating-type switching . In addition to the fu nctional mating type aUele at the
uct ive loc us, SaccharumyC(s cuev[.riee has 's ilent' copic, of mJting-type :lUcks at two
o lher loci. A site_specific endonuclease cuts the double stranded DNA at th e active locu S.
The resull ing gap is the n r~ pajred by sp licing in DNA from one of the loc i at which the
silent copies resi de. This often means that onc all dc is replaced by the other. .~ the
mating-type of the organism is sw itched. Similar swi tchi ng occurs in another yeas t.
SchiW$Occharomyces pombe. and in the filamentous ascomycetcs. SclerOlinialrifoliomm.
Chromocrea spiJ1l1fosa. and Gfomueffa cin.~lIfa/a. though the mechanism is still obscure
in those fungi. The switching in ChromOCftfl and Sderorinia happens in only one direction. If the mechanisms in,-ol\"ed are like that found in Saccharomyces, it is likely that
only one of the mating-trpc alleles is present in a silent form. We do nOI yet know ho .....
much fungal homotha ll i:im can be accounted for by mating -type switching. In some
fungi. se lf-sterile spores with a single nllelCUS, and self-fertile spores with two nuclei. are
both de ve loped in the same fruit body. This kind of mating behavi our is cuBed
Recognizing the e~istence or compatibility genes is one thing. understanding how
they work is another_ The best-documented compatibility system is (hat of the yeast.
Sacch(lromyces c"ft,'isiaf _l"kr~ ttlc re is a single locus with two alleles. Each m~ting type
sec reteS a constilUtivc polypeptide pheromone wh ich causes cdls or the opposite mating


type to becomc arrested in the G 1 stage of the cell cycle. Such arrested cells agg luti nate
and undergo plasmogamy and karyogamy. If thc resultant diploid cells are 5taTVed. they
will undergo meiosis and produce haploid meiospores. Each stage of this process is
apparently under the control of mating-type genes. These gen es are regulated by DNA
binding proteins encoded by the mating-type aBcles. One of the alleles contains a unique
.sequence of747 base pairs. and enCQdes two regulatory polypeptides. Th;:: other allele has
a unique .sequence of 642 base pairs. and encodes tv.o polypeptides, of which only one is be reg i.llatory. The mati ng-type genes of other fun gi are Ci.lrrently being isolated
and characterized. and we should soon know how representati"e S. cuevisiatl really is. It
will be a tremendous challenge to explain how the hundreds of separate alleles we know
to ex ist in some in dividual basidiomyccte taxa differ and are regulated.

Interster ilit y
Compatible mating-types are not always enough to ensure successful sex. Sometimes. mnting fai ls despite apparent co mpatibili ty. There is therefore another genetic
system, which we can call an intersterility system. that can override the usual incom(Xltibiliry system. Unfortunately. weOOn't know nearly as much about the basis orthis sy$lem
as we do about incompatibility. The ki nds of barri crs invol ved are eithcr llrezygotic.
preventing ferti lization, or postzygQlic. res ulting in hybrids of reduced fertility or meiot ic offspring less fit than the parents.
Pretygotic barriers exist bet ...'ce n closely related populations of many well-known
basidiomycetes, including Amlillaria, Callybht. Capri/lwi. w ccari(l. Pnxillus. Pieuroflls.
Gtmoof!Tma and Hettrobusidion. Since intersterility is usually complete, particularly in
sympatric populations. the intersterile groups are equivalent to biological specic.~. In
some of these fungi, DNA reassoci3tionor DNA restriction fragment patte rns have shown
th~t the intersteri le groups 3re Jlso genomically divergent. Sometimes two enti rely intersterile sympatric popu lations are partly interfcrtile with a third population from anotller
arca. We do not yet know whether this thin! population could aCt as bridge between the
other two soli tudes. In Usrilago c),nodol1li$, intersterile popul Jtions and partly interfcrtile 'bridging' strains coexist within what appears to be a single complex species.
Posl7.ygotic barriers are present when malingoccurs, but mOSt of the resul!ing spores
are not viable. In closely related hetewthallic Ne tlrospora species. the reproductive barricrs appear to be mostly postzygotic. Intraspo..'Cific cross~s yield viable ascospores. but
interspecific crosses produce largely non-\iable ascospores.

Ascomycetes and basidiomycetes can be easily di stinguished when they reproduce
sexually. In this phase (the teleomorph) they form characteristic frttiting bodics (ascomata
and basid iomata) bearing unique me iosporang ia (asci and basidia) fro m wh ich, as we
h31'e seen, the products of a single meiotic event can ~ isolated and anJlp.ed. Many of
these fungi repmduce asexually as welL producing what are called anamorphs. which
form mitospores called conidia, and often occur wen separated in time and space from the
telcomorph. In fuct. we know thousands of anamorphs which have nOl yet been persuadcd
to metamorphose into a telcomorph. :"Iany of these go on. generation after gcneration. in
the 3sexual condition. and it now appears highly probable that many of them have entirely lost the ability to produce a telcomorph. thus becoming anamorphic holomo rphs .
We know th3t one of thc most vital functions performed by the tc leomorph is
genetic recombination. This rea.~s.onment of the gene pool during meiosis broadens the
ability of the population to cope wi(jt the stresses imposed by changing environments.
Conidial fungi, which are often highly opportunistic. and grow on a wide range of sub-


stratcs, might seem to be especially in need of the nexibility conferred by genetic recombination. One of their responses 10 this perceived need for genetic diversification is to
become heterokaryotic: 10 acquire more than one kind of nuc leus as a result of one or
more anastomoses. But we now know thaI they have also evolved II special mechanism for
generating some genetic recombination without sex. We call this process parasexuality.
The parasexual cycle has four stases. (I) Fusion (anastomosis) of adjacen t somatic hyphae. and eJ\change of nude i. em.blishing a heterokaryon. (2) Fusion of di fferent nucle i
in the vegetative hyphae, to form somatic diploids. (3) Somatic recombination (mitotic
erossing-over). (4) Don-meiotic redl.lction of the altered nuclei via aneuploidy (loss of
in<.l ividl.lal chromosomes) to the haploid condition.
This seql.lCnce of events is rare, happening in fewer than one conidium in a million,
but the number of conidia produ~d by most conidial anamorphs is astronomical, so parascJ\uality is a practical means for producins genetic variation. We don ' t yet know how
widespread !his phenomenon is among Ihe conidial fungi, but it has been detected in
species of Atpergillllj, Acremonillm, Fusarium and Verridllium, an d is probably common.
It is worthwhile to compare seJ\uality and parasexuality. (I) Sexual reproduction is
a highly organized, often precisel}' timed process, which is genetically programmed.
Parasexuality involves a rare sequence of uncommon eyentS which seems to operate by
chance, rather than by design. (2) In sexual reproduction. nuclear fusion is often mediated
by genetic factors. expressed as 'mating types: happens in highly specific suucrures. and
often involves many pairs of compatible nuclei. [n the paraSCJ\ual cycle, nuclear fusion i~
an isolated even t, not med iated b)' mating-type factors, nOt found in specialized strutrures, and involving only individual nuc lei. (3) During meiosis, crossing-o\'er probably
takes place in every homologous pair of chromosomes, and multiple crossovers are common. During somatic recombi nation. crossing-over commonly involves only one or a few
chromosomes. and never happens a..s often as during meiosis. (4) In meiosis. segregation
happens in a highly organized way during two specialized nuclear divisions. Somatic
ha ploidization probably occurs as a result of successive chromosome losses from an
aneuploid nucleus (2n- l) over several miloticdivisions until lhe stable haploid is reached.
The factors that initiate sexual reproduction vary enormously from one fungus to
the next, presumably because of their di vctsc ecological adaptations. so it is very diffi<:ult
to make generalizations. thousJ1 special media ha'<e been concocted 10 persuade such
importam genetic toob as Nellrospom to undergo sexual reproduction on demand. Th e
parasexual cycle can be e ncou raged in various ways. Camphor vapour settcts for somatic
diploids in some fungi. In species with uninucleate con idia. the best approach is to
produce a heterokaryon belween IWO aUJ\otrophic mutant, (each of which has a different
biochemical deficiency). then grow ils conidia on minimal mediu m. Neither oflhe original auxOlrophs will be able to grow. but diploid con idia will grow. since thechromosomes
from one parent compensate for th~ deficiency in the other sel. and vice versa (this is
called co mpleme ntation, and the diploid is described as being prototrophic). This lechnique has been used in Verticillium tllbo-tllTum. Aspergillus niger. and Aspergillus
nidufuns. and yields about ODe diploid conidium in 10'- 10' conidia. The subsequent
frequency of mitotic recombination ean be increased by X-rays. UN. mitomycin and
nitrous acid. Finally, to complete the cycle. low concentrations of p-fluorophenylaianine
or benlale (Benomyl) stimulate haploidiZlllion.
We can sec the potential advantages of the parasnual cycle \0 an ascJ\ual fungus.
bul is it of any use to the geneticist? As il happens. it can be used to detennine linkage
groups, the order of genes, and the position of the centromere. The genetic recombination
achie"ed is on a much smaller seak than in meiosis: on ly one Or two chromosomes are
involved. and the possibility of multiple crossovers is so low lnat il can be ignored. This




172 CHAIYfER TE..~

means that linkage analysis is mueh easier. The original diploids arc heterozygous for the
various marker genes. Those in which crossi ng_over sub,equenily occurs will become
homozygous for any marter genes that are distal to the point of crossover. The relative
frequencies with which such markcrs become homozygous ~ an indkation of their relative distance.~ from the centromere.

Extranuclear Inheritan ce
Some genetic phenomena can't be explained by reference 10 nuclear or chromosomal events. The logical corollary of lhis is thlltthe determinants may be tnlnsmined in
cytoplasm rather than in nudei. In some helerothallic fungi, the volume of cytoplasm Ihat
ae<:omp;mies one of the nuclei during a sexual fusion may be muth greater than that
associated with th e other nucleus. Al ternatively, iF one side of the fusion involves a
microconidium or a spermatium. this must inevitably bring much less cytoplasm to the
union than does the receiving panner. This sometimes results in tnc offspring resembling
the parent that contributed more cytoplasm, and implies the existeoce of cytoplasmit
gen es. It has been shown that in Aspergillus glaucIIs, attributes such as spore germination,
growth rate, pigmentation, and dens ity of perithecia ore under cytoplasmic control. A
well-known example of cytoplasmic control is the 'poky' mutam of Neurospora Crtlssu.
This grows more slowly than the wild-type, and cannot be speeded up by dietary supplements. If 'poky' is crossed with the wild-type, the 'poky' CQlldition is transmitted only
when the 'poky' str:lin forms the perithecium initial. which means thai it is essentially the
matcma l parent.
Another well-known example of extranuclear inheritance is the <petite' strain of
Sacc1raromyasurtvisiae. which ari~ with a frequency of abotH I etll in 50ll SuchccUs
give rise to smaller than normal colonies. which can respire only anaerobically, even
when oxygen is prescnt. This deficiency is due to Ihe absen<;e of impor!ant respiratory
enzymes such as cytochro me oxidase and sucdllie dehydrogenase. The mitochondria are
defective. Whole colonies can be com'cned to 'peli te' cells by growing them on medium
containing 3 ppm atriflavine. Di ploid "petite' cells don', R:produee sexually, but diploid
hybrid s derived from 'pctite' and normal haploid cells respire aerobically and can form
a.scus-Iike mciosporangia. If the meiospores are cultured. all are nonnal, and 'pctite' cells
ari ~ among their offspring only in the ominory 1:500 rolio. Normol yeast cells co ntain
cytoplasmic genes (in mitochondria) tontrolling the synthesis of respiratory cnzymes_
'Pctitc~' arise by mutations in the mitochondrial DN A. When a cell containing this tytoplasmic mut:lnt fuses with a nomlal haploid cell, the cxtranuclear genes from the normal
~ell rende r the resulting diploid normal again, and nornla! mitochondria find their way
into any r~su l tant haploid cells, which will all therefore be nonua!.

Genetics and Plant Path ology

Plant breede rs try to produ~e not only higher-yiclding varietie~ of crop and garden
plants. but also new disease-resistant strain s_ Th is is done by finding natural defence
me~hanisms that are pr~sent in wild relatives of the economically important host plant.
Painstakingly, the plant breeders introduce the resistante genes to the crop plants. AI
though such new cultivars may be immune to a particular fungal discase for a few years,
e\'entu~l1y a new race of the fungal pathogen appc~rs whiCh can overcome the resistance
of the plant. An alysis of this endlessly repetitive cycle of resistance and susceptibility It'd
to the theory of the gene-for-gene relationship between host 31ld pathogen. Th is suggests
that the evolutiollary paths of host and pathogen have been so closely linked for SO long
tllat for every gene in the host thai is capable of mutating to gi"c re.~istallCC. there is a
corresponding gene in the pat hogen whi~h c~n mutate to overcome that resistance.


C/odosporil.m (FllhiaJjllllUIII. a hyphom)cete. causes 1eaf mould of tomato. Three
gene~ that confer resistaocc to this fungus ilre known, and tomato varieties exist which

carry none, one, tv.'O, or all three of these genes. With the ai d of these hoSt varietie~. eight
races o f CladQsporillmjulVlun cao be discriminated. TIl.! most efficient way to differentiate these races is with three tomato varieties which ha\c. re,pectively, resistance genes I,
2 and 3, as can be seen from Table 10.1. 1 you examine me ei ght columns which give the
responses of the three tomato varieties to the different fungal races, you will see thnt each
column diffcrs from all the others. This means tha t ilny of the eight races Ciln b<l identified
by tes ti ng it against only three tomato variet ies.

Thble 10. 1

interactioos of races of Cladosporillmju/"um with three lom:uo varieties

Tomato with
resistance gene

Clado.!porium roces





That is ho w prevalence and spread of miln y important plant paulOgenic fungi is

monitored. It is al so the mechanism by which the existence of new physiologic race-1 of
pathogens is discovered. The more genes for resistance we re-eognize. the more pathogenic races ca n be distinguished. Almost 200 races of the flal rust fungus, M (/ompsoro
lini, have been identified by thei r r~:K'tions with 18 ho~t varieties. Puceinia graminis
subsp. lriliei, which causes wheat ruSt. has wt:J1 over200racc'i, and the number is growing
steadily in response to the efforts of the plant breeders.
The genetics of resistance have also bc.:n ex plored in Venluria inaequolis, the
('ppJe scab fu ngus, whic h is a bitunicatc ascomycete. It was found that the genes controlling vinlk nce exist in viru lent and avirulent alleles, which segregate regularly in the
osc us. Se ven of these genes were disco vered, and s.cven arple vurieties were found th at
would enab k their presence to be recogn ized. For example. the avi ru lent ullele of ge ne I
didn't affect Macintosh upplcs (which might simply mean th ~t M adnto~h carried a (':OITe '
sponding gene for resistance 10 that allele). Yellow Transparent apple was resistant not
only to aviro lent I. but also 10 the aviruknl andes of gcne~ 3 and 4. Each of the se~ .:n
apple varieties had a different resimnce gene or genes. which could be identified by
exposing the host to \W'iOU5 races of \~ inaequalis.
The natu ral testing ground for resistance of potatoes to the late blight fung-us,
Phylophrhora ill/el(a/ls (Oomycota) is centrol Mexico, where both sexes of the fungus are
present, and new physiologic races can arise more readily Ihan elsewhere. Worki ng;n this
environment. potato breeden have found it more useful toaim for 'fie ld resistance,' which
is mediated by man y genes with smull individual effects. rather th on con~entr3ting on a
few major re,istanee genes wi th all -or-none effects. The war goes on.

Rec ombinant DNA and Gene Cloning in Fungi

Since fungi have not been among the most impo rtant contributOf'S, 10 our knowledge
of DNA and how it worts, I will not burden you with the usual spiel on D;":A. its runctions


and its replication: you can get that from any first year Biology te.>:t book. In 3ddition, for 3n
overview of recombinant DNA technology, you should refer to a recent text on gene cloning. However, although fungal DNA is essenti31ly the same as that of animals and plants. it
is prescnt in relatively much smaller quantities: the fungal genome is only about six to ten
times larger than that of the bacterium. Escherichia <:o/i, having about 2.64.3 X 10' kilobases
(kb). Repetitive DNA makes np less than 20% of the nuclear genome. Most fungal DNA is
found itl nonnal eukaryotic chromosomes. bu t there is also a circular mitochondrial chromosome of about 30-200 kb, mitochondrial plasmids. and often some small, supernumerary
chromosomes in the nucleus, which do not appear to be essential for survival.
The techniques of molecular biology have not only given us a great deal of detailed
information about the genetic material, and even the actual sequence of base pairs which
make up parts of the genomic DNA, but also permit the movement of genetic material
from one organism to another, and the e.>:pression of certain genes from one organism in
another. [will set the scene by outlining the processes involved in moving gcnes from one
organism to another.
Recombinant DNA technology usually involves the following steps: (1) Ce lls of a
host (often the bacterium Escherichia coli) are brokcn, and their DNA e.>:tracted. (2) This
DNA includes plasmids, small closed rings of extrachromosomal DNA, which may be
used as vectors for the introduction o f foreign DNA. The vectors are separated from the
other DNA by ultracentrifugation. (3) Special enzymes called restriction endonucleases
cleave the plasmid vectors, and !cave them as linear sequences of DNA with 'sticky' ends
(unpaired bases). (4) DNA from the donor organism (the source of the desired gene) is
i;;olated and then treated with the same restriction endonuclcases, producing add itional
linear sequences with sticky ends that match those of the cleaved plasmids. (5) Vector
DNA and donor DNA are mixed: sticky ends rejoin, by complementary base pniring, in
various configurations - vector ends re -join. vector joins donor, donor joins donor. In a
few cases the desired joinings happen, producing a closed loop, which is pan vector DNA,
part donor DNA. (6) The sugar-phosphate backbone of the DNA is then properly repaired
by an enzyme callcd a DNA ligase, (7) The modified vectors are mixed with . m/; made
penneable by treatment with a calcium salt. This allows some of the bacteria to pick up
modified vectors. and so be transformcd. (8) The transfonned cells that bear the desired
donor genc can now be isolated, with the help of selectable marker genes pre"iously
incorporated in the vector. and can sub~e quelllly be propagated on a large scak
Why arc yeast> and filamentous fungi now being used in gene cloning. if bacteria are
such suitable hosts~ Fungi are valuable because: (I) l\"iany of the donor genes we want to
clone are eukaryotic. Bacteria aren't ideal hosts for this job. because their mechanisms of
gene transcription and tmnslation arc so different from those in eukaryotes. In fact. even if
su itably modified plasmids are successfully introduced to Escherichia coli, rebtively few
eukaryotic genes will be e.'Pressed by this prokaryote. TIllS is obviously not a probkm in
the fungi. which are all eukaryotes. The yeast Sacdwromyn:s ",:rn'isiae bypasses ,ome of
the roadblocks encountered when E. col; was the prillcipal host available. S. cere . . isiae can.
for example. gl}'Cosylate proteins, fold them, or can)" oUI other pust-tr,\!1siational modificotions which must be made if someeukaryotic proteins are to become functional. (2) S"cchalV"'yces cerevisiae and such filamentous fungi as Aspergillus nidulans are genetically wel!explored. and useful mutations are available in many of their biochemical pathways. (3)
Yeasts can be grown and handled in very much the same way as the bacterium, Escherichi"
coli: simplicity itself compared to the tis,ue culturing of animal ceUs.
Two techniques are commonly used to transform yeast cell,; one requires the removal of the cell walls, the other uses e mire cells. The first technique is carried out as
follows: ( I) The ycast cells are treated with (3-mercaptoethanol, a reducing agent, which

!~ liFP E-CCilil \

7'\; !'ilBL! QTl':i!:1'\



~ ' U NtiA L ti ~NJ~.: nt.: s


facilitates subsequent digestion of the cell wail. (2) The wall is digested by mixtures of
glucanases derived from snails or bacteria. (3) The resulting p rotoplasts (oflen called
spheroplasts) are washed and suspended in a stabilizing solution (0.6 M KCl or 0.8 M
sorbitol) to which is added the foreign DNA (vector incorporating the desired sequences).
(4 ) Uptake of the plasmid DNA during protoplast fusion is promoted by adding polyethylene glycol. (5) The tmnsfonned protoplasts are then allowed to regenerate a wall, and
are grown on a selecth'e medium (one containing a specific antibiotic, o r with a panicular
food substrate. depending on which marke r genes were used) which will allow only
appropriately transfonned cells to grow (because only they carry the appropriate marker
gene, which came with the vector and confers resistance to that antibiotic or the ability tu
metabolize that particular substrate).
The alkali s.aJ.t method permitS transfonn:uion of intact cells. Cells are incubated in
lithium acetate to make them competent. i.e. receptive to exogenous DNA. 1bc: DNA is
then incOl'pOrated in the presence of polyetheylene glycol 4000. Although transfonnation is less efficient than with protoplasts, the procedure is simple and quick. cells can be
stored for weeks without loss of co mpetence. and the problem of diploid fonnatioll during
protoplast fu sion is avoided.
The first demonstration that yeast could be transfonned with ell.oge nous DNA was
made in 1978, using a recombinant bacterial plasmid carrying the Saccharomyces Cl!"I'isiae
gene for an enzyme needed in the synthesis of leucine (LEU 2). This ge ne had earlier been
recognized in E. coli because it complemented a mutation in the bac terium that had
caused the loss of (he same enzyme. Several other yeast genes have now been clotlcd in .
wll by complementation of other bacterial mutants. These are useful marke rs which ca n
be inrorpornted in the ell.oge nous DNA along with the desired gent: their uptake an d
subsequent expression in yeast cells allows recognition and selection of yeast cells .... hich
have been appropri ately transformed: that is, which now carry the desired donor gene.
Most strains of Saccharomyces Cl!Tevisiae contain up to a hundred '211m pla s mid~'
per cell. Ench plasmid has about 6.300 base pairs. Hybrid plas mids made up of the entire
l!1m sequence. plus the LEU 2 yeast gene, plus a bacterial vector sequence, efficiently
transfonn )east celli that lac k the LEU 2 gene (As a consequence of the bacterial vector
sequence DNA having been repl icated in a baCteriuru. the 211m plasmid also works in .
coli, so it can serve as a 'shuule vector'). The complementatioll of the LEU 2 gene means
that those cells which have been properly transfonned can be selec tively isolated un
leucine-free medium, and subseq uently multipli cd. It has also been demonstrated th nt the
hybrid plasm id replicates in transformed cells. However. it appears that smaller plasmid s
containing only a fragment of 211m DNA are more versatile, gi\i ng higher frequencies of
transformation. and more copies of the plasmid in each transformed edl (up to 300). All
stages of gene-cloning can be carried OUt in yeast. but it is usually more efficient to
amplify recombinant plasmids in E. coli. The most important aim of the cloning exercise
may be to obtain gene products. but cloning also lets us produce a lot of homogeneous
DNA, which can then be used in the sequencing of ge nes.

Expression of Exogenous Genes in Yeast

Yeast genes generally ha\'e the following components: ( I) upstream promofer elements which include constilUli\e or regulated promoters (positive Of negati ve); (2) 20-400
bp downstream. a TATA promoter e!emellt (so named because it incoIpoT:ltes the b~~e
sequence. thymine -adenille. thym ine-adenine); (3) 30-90 bp downstream, a transcription
initiating site which initiates production of mRNA; (4) protein-coding sequences; (5) tnl.Oscription term.ination signals (see Fig. 10.5). TT:lnscri ption of the insened DNA depends on
the presence of a promoter sequence th~t is recognized by Ihe host R.."iA polymerase.


Highly e1>pressed yeast genes such as alcohol dehydrogenase I (ADH 1) or g!yccraldehyde-3-phosphme dehydrogenase (GJPDH) usually have very high mRNA lcvels. so
rTlO5t methods of e1>pressing exogenous genC5 in yeast have concemrnted on the production of high mRNA levels. This invo lves using multip le copy plosmids to boost the
number of gene sequences per cell. and fUSing coding sequences to efficient yeast promoters to iner~ase IrnnsCTiption.
Yeast genes may contain both constitutivc ilIId regulated promOters. which serve 10
initiatc transcription. Where both are preSent, the constitutive sequences are active a! all
times during cell growth. and may produce a base level of gcne expression which can be
modified by other upStream sequences. Regulate<! promoters nCi:d to be activated before
they will initiate transcripti on. but will in some cases produce much higher le\'els of gene
cxpression. Researchers initially tended to use constitutive promoters with high mRNA
levels. especially th ose from the genes men tioned above (ADHI and G3PDH). bUI found
that while these gave high yields of homologous proteins. they produced much lower
amountS of heterologous (donor) proteins. If lurge amountS of the desired protein are
deleterious to the host cell. it is bener to use regulated promoters. which are not derepressed until rcqUiRd. Good examples afl: those involved in galactose metabolism. such
as GALl. GAL? and GAllO. which arc repressed by glucose ilIId derepressed by the
addition of galactose to the medium_ If cultures arc grown with glucose or glycerol ~s
carbon source, these promoters wi ll re main repressed until allIlQst all the glucose has been
metabolised. If glucose is absent. and galactose is added to the medium, these promoters
can be induced about I.OOOfold, Gal a~tose induction is controlled by the GAUl and
GAL80 proteins. The GAL4 protein is a positive promoter that binds 10 specific DNA
sequences upStream of the codi ng seq uences of ge nes re~ u1nted by galactose. The GA L80
protein is a negative regulator which binds to the GAlA protein, preventing tl from
acth-ating transc ription. If galactose is add~d . it binds 10 the GAL80 prOtei n, ~lOppi n g
this from interfering with the GAL4 protein. which can then go about ils business of
promoting IrJnscriplion. Recently. hybrid promoters have been deve loped, combining
strong constitutive promoters with upstream wquences of regulated genes. One of these
has been used in the controlled expression of human interferon
Brewer's yeaSt must be provided wilh sugars if it is 10 produce akohoL If yeast
could be tmnsformed 50 th:l\ it possess....--d an amylase (a starch-degrJding enzyme). production of ethanol would be si mpler and cheaper. Variou s amy lase genes from bacteria.
)easts and fil amentous fungi have now been cloned and in Saccharomyces
urerisilil': commercial explOit at ion of these should soon be possible_
The cellulose and hemicellulose in wood represent almost limidess potential subS1r.!l~S for the fermentation industry. Complete degradatio n of cellulose to glucose requ ires
the activities of thrce successive enzymes: endoglucanase. exocellobiohydrolase and pglUcosidase, Trichodemm retJei secret<!S 3111hree cellulolytic enlymes. but normal cultures
of the t\lngus ;trcn' \ uwd to produce thes.<: enzymescommcrcially because al l tht enzymes
are inhibited by til<!ir end-products. The Str:llegy has been 10 isolate mutant. highly cellulolytic strains of Tridl0demm reesei. then isolate the genes for the three elUymes and place
them in \'ector$ with control stquenc<:s appropriate for their e~prcssion in a suitabk host. In
1987 the T. rHsei gen~ for en doglucanase was cloned. char3Cteril.ed and exprcsseU in S.
ctrel"is;n!'. Endoglucan~se and e:<;oglucafl3se from the b~cterium Cel/u/omO/uJ$ Jimi have
been clon~d. expressed and secreted in yeast in a regula ted rnann~r by 3Uaching their
coding sequerH;Cs to the melibiase promoter and signal r.equences from &u:charom)"us
carbbergellsis. Although yields are still too low for commercial e1>ploit~tion. theR is opti
mism thJt higher-yielding Strains will be developo::d. and that cellulolytic brewer's yeast
will be able to clarify beer and pro"ide cheaper fuel alCOhol.



It appears that redpient )'ca,1 strains can take up and maintain e.\ogenous DNA
even v.'ithout the mediation of vectors. The brewing industry has achieved this in two
ways. Beer normally contains dextrins that not degraded by brewing yeasts. These
dexlrinS give a beer greater body and a higher caloric content. The light beers which arc
so popular today (for reasonS that escape me) have had Ihcse de.~trins removed by an
exogeoous enzyme. ;glucoarnylase. This enzyme is produced naturally by some nonbrewing yeasts (for example, $U(;choromyusdiosroricus). Brev.'ers Raw therefore tried 10
get the ability to make this enzyme into their brewing strains. SO that these could produce
a light beer without assistll.nce. One approach has been to incubate the prOlOplasts of the
brewing yeast with partially purified high molecular weight DNA from the donor yeas!. A
second approach RaS been to fu se entire protoplasts of the two yeasts. Unfortunately for
this second method. the S. ditJsllllicus brought with it not only the glucoomylase. but abo
4-vinyl guaiacol, which ruined thc flaw)tn of the beer. Classical hybridiution techniques
,,"'ere then used to segregate the glucoamylase genc from the 4-vinyl guaiacol gene.
The flavour of Brazilian wines is oflen spoiled by an exccss of I-malic acid. Fusion
of the wine yeast prolOplasts with those of Schi:osacc/wromyces (Jombe, which mctabolizes I-malic acid, produccd a hybrid lRaI successfully reduced I-malic acid levels in the
wine. ProI:oplast fusion has some potential. becausc some characters impot1anl in baking.
brewing and distilling arc polygenic (controlled by many d ifferem genes). or are not well
understood genetically. Such charactcrs aren't suitable for enhancement by genc cloning
ortransfonnation.ln addition. protoplast fusion combi ncs whole genomes. and il is known
that increases in ploidy may increase productivity. Intergeneric fusions are often unstable. but if on..., 'petite' parent (wh ich has non-functional mitocho ndria) is used. more
stable hybrids are produced. probably i>eeause the hybrid contains functional mitochondria from only one parent.

Expressio n o f Eukar yo ti c Gen es in Filamento us Fun gi

Although for several years yeasts were the hosts favour...,d by gene -c1oners sceking
to cxpres.s heterologous cuk ~ryotic genes. they cunnot secrete enzymes in lhe quantities
produced by bacteria. BUI mycelial conidial fungi such as Axpergil/IIS lIiger can seel"l:te
enzymes more efficientl y than either yeasl.'i or bacteria. and are therefore becoming the
hosts of choice for expression and sC<.Tetion of ma ny enzymes. antibiotics and even
mam malian phannaceutical protcins. Transfonmuion in filamentous fungi was first repo rt~d for N(!I<fflSpOm cr(lssa in 1979. and tm nsformation systems have now been developed for many other filamentous fungi.
Genes in filamentous fUllgi are composed of a promoter. :1 trJnslation initiation
region. DNA encoding a secretory signal peptide (where ncces~ry). DN A encoding for
tile gene product. and D~A sequenccs fOl" tennin!lIing IT:J.nscription and for pol),adcnybtion
(Fig. 10.5).
When a gene is to ~ moved to a new hust. it is first u~~emb1ed in a vector plasmid
whkh ,on replicate in E. coli. A selectable marker may also ~ incorporat~d in thc plusmid. As mentioned earlier. markers may be sel<:cluble because they cOl11pensate for some
auxotrophic deficiency in the host. or (prcfcr:l.bly. since in many ..:uses we are nOi dealing
with auxotrophic hosts) because they confer upon the host resistance to an antibiotic. or
lh~ ability to metabolize a panicular food substrate. The hyphae of the ho,;t fungus arc
enlymic:..lly stripped of their walls. and the transformation of the resultant protopl;!sts
proce~ds mu~ h as it does in ye~sts . Following trJnsfonnarion. the protoplasl5 com':l.lesce
on a regenerative medium which le ts {hem reeonStitute their hyphal walls. In fungal
transform:l.lions. the VC1:tnr DNA usually becomes integrated into the !\ost !,!enome. Bovine chymosin. a mammalian protease uscd in cheesemaking. ha$ been successfully


expressed and secreted in Aspergillus nid[.lrms. The cDNA sequence encoding the
chymosin was auached to transcriptional. trunslational and secretory control elements of
the glucoomylase gelle from AJ~'8ilIus niger. All four unitS were incorporated into a
suitable Ve<:tor, wh ich was used 10 transform Aspergillus nidulans. Acti>~ human interferon a2 und a bacterial endogluc:rnase have also been cloned in A. nid"lalis. this time
using promoters from the A. niger glucoamylase gene and the A. nidulallJ alcohol dehydrogenase gene. HulTUlll tissue plasminogen activator (tPA. a prOlease used to dissolve
blood clots) has been expressed and secreled in A. nidulans. One of the vcctors con
structed for this pu rpose is illustrated in Fig. 10.6.

Molecular Taxonomy and Population Genetics

Fungal idcntification is often difficult, even with good. mature specimens of the
usual reproductive structures in hand. If all we have are sterile mycelia, or fungus-inhabited substrates, identification has been vinually impossible. But now. with the advent of
a variety of molecular techniques, the impossible JUSt takes a little longer.
We can detect the activity of specific enzymes. We can use probes to identify
particular base sequences in the DNA- We can do immull(Klssays, using antibodies raised
in a mammal against unique t:omponenlS of the organism. Or we can use sodium
dodecybulphate polyacrylamide gel electrophoresi s (more succinctly known as SOSPAGE). This technique separates the proteins in any mixture by their molecular weight.
An electrical field is used to draw the protein molecules through a porous get Smaller
molecules move more quickly and so trave l further in a given time. Eventually. Ihe
concentrations of the various protein mol ecules are made visible by staining with dyes or
silver-based reagenlS. and the resulting spatial and imensity pattern of bands compared,
often by computer. with those derived from known organisms. Rderen ces describin g
these techniques ure givc n at the end of the chapter.
11 has become possi ble to compare parts of the DNA or RNA sequences in the
genome of different organisms with a vie .... to esl:lblishing their degrees of biological
relatedness. RhizoPQgoli is a fal se trume, D hypogeous. mycorrh izal basidiomycete with a
closed basidioma. a convoluted hymen ium. and non-shooting basidia. For anatomical
reasons_ this fUngus has been toought to be related (although nobody knew how closely)
to 'norma!' epigeous members of the Boletaceae, which produce basidiomola with a stipe,
a cap. hymenium-!ined tubes. and spore-shooting basidia. In recent molecular studies of
these fungi. a number of fragmenlS of Suilllls mitochOlidrial DNA (mIONA) were cloned
and hybridized with mtDNA from other members of the Boletaceae. This showed that IS



DNA encocllng deslrtd gene procluet

control region

DNA encodIng
signal peptlcla
lor secretion
Fig. 10.5 Components of a fungal gene.

and transer!ptlon
termina-tloll 11g:nals


different regions of the mitochondrial genome of Rh;z.opogol1 subcaeruitscens are vi(tu~
ally identical to those of founeen species of the 'normal' bolele genus, Suillus. This is
surprising because nOi only does the order of these 15 regions differ among species of
Suillus, but RhiwpogQn and Suilllls ha\'e traditionally been placed in different families
or even differenl orders. Their molecular similaricy, at least as far as this has been explored,
is in striking contrast \0 their morphological divergence.
Using the Polymerase Chain Reaction (PCR) technique, researchers can now TOUtinely replicate very small samples of DNA thousands of times. and ultimate ly produce
enough DNA to permit analysis of itS bast pairs. Base sequences from the mitochondrial
large subunit of the ri bosomal RNA gene show that RhiZOp<Jgon and Suil/IIS are very
closely related, and that both genera have diverged sharply from other boletes tested. In
defence of classical (a)(onomy. I must point out that many mycologists have long believed that Rhizopogon is a secondarily reduced or sequestrate (non-spore-shooting)
derivative of the genus SlIillus. It is encouraging that this relationship has now bec:n
d.nunatically affirmed. This work also demonstrates eithcrthm major morphological changes
may not be reflected by corresponding changes in t1K: genome. or thai we have nO{ been
looking in the right places to find the genetic reflection of those differences. [t also
emphasizes lhal our concepts of fungal relationships must be based on as many kinds of
information as possible (not jusl morpholo;ical, and not just mol~ular).

Armillaria m~iI~a. the only truly diploid basidiomycete. produces assimilati~e

mycelial clones up to 400 metres in diameter, and up 10 several hundred years old, infect ing many trees. and several different clones may be present. When homokaryons ana,to-

Xba I

IpiA lerminalor

tpiA promOIer

Psi I


Xba I [PuvlIJ

BamH I

Fig. 10.6 A plasrrid vector, pM 159, constructed for

actMltor gene i""I li spergillU$ nidulans.

Xba I [PuvllJ


the lunan tissue pLlSrmogen

mose. nuclei migrate but mitochondria do not. so the resulting mycelium is uniform in its
nuclear component. but has at least twO seclOrs with different mitochond.rial genotype,.
Therefore. an examination of mitochondrial DNA polymorph isms can now help us disCO"cr the history of those clones.
The uses of molecular technique~ in mycol og y are multiplying. and I must begin by
warning my readers that it is almost impossible for any publication to keep pace with the
lntest developments in thi s field. However. the attempt must be made!
DNA sequencin g. usually after amplification by PCR (the polymerase chain reaction). is now being used to idemify important fi.mSi . such as commercially grown specie,
or serious plam pathogens. or to find the appropriate talonomic niche for fungi whose
ta.wnomic position is problematic. A small r",gio n oftbe genome of several individuals in
one species is compnred to the DNA .~eq uence of the eql.livaJent region in other taxa_
Currently the region being sequenced and compared most commonly is the rRNA (ribosomal RN A) operon. This operon consists of three genes under the control of a single
promoter. The genes are: (1) the small subunit gene (SSU). (2) the 5.85 gene. and (3) Ihe
lars~ subunit gene(lSU). Fortu nalely. in most fungi these genes are alT'.mged in Ihat order.
and so CJn be located and compared. The fiTht gene transcribed is the SSU. After this comes
an irllergenie Spacer Region (IGS) which contains an intem3ltranscribed spacer region
(ITS I). the 5.8S gene . and a sc<:ond transc ribed spacer region (ITS region 2). At the Olher
end of me IGS is the LSU.
The rRNA operon is pan of a mUlti -gene family consist ing of repeated array~ of
operons. Different genes arid reg ions in the rRNA operon have differem degn.""Cs o f $Cquem:e conservation (the likelihood that changes will enter the sequence of base pairs
01 er time). Th: vnt)'ing pres,ure for sequence conservation is due to the differing degre es
of importance of the different sequences: areas th at are less imponant in the function of
the genes tend to vary more than areas that arc crucial. This is beeause Jny ch ~nges in
th ,"c crucial areas might wreck the gene's ability to make its product. The rather mySleri au. Internal Transcribed Spacer regions (ITS). since they do nO{ themselves code for a
g~ll~ produc t. are fnr more variable than the genes. The ITS regions have pwved most
suitabk for comparisons between rdated species. T he 5.8S gene is small. highly consef\~d and w o f liule value for phylogenetic comparison. The SSU is also conserved. b ut
~in,c it is larger than the 5.85 gene. more variation has crept in. and it has hccn used for
cumpmsons among genera and higher la:ta. 1bc LS U is the Icast conSCf\\!d of the threee
gene> and hJo; allowed comparisons within nnd bctWtCll 5pecie~_
0:-<.-'1. s~quencing after PCR amplificJlion has been used to idemify speck'~ of
Am:i!/"ri(l (an d m,my other fun gi). But these technique s are 110t rest ricted to identification of known species. Th~y c,m also be used to conm:ct or compare previously unidentifiabk mycelial (nen-sporulating ) cultures with fungi that have been identified using thdr
sporulating st rucltlrcs (whether sex ual ltelc mnolllhic 1or ns.:::t ual {annmorphic1). The ON A
protlk, of non -fruiting eultures havc been comp;=d with the profiles from D;.YA iwlnl<!d
from (ruit hodi<,s of Amlil/a n". nnll with thi, evidence in hand. new species of Armillaria
ha\c b.!~ f1 described. This raises some problems. such as how the ne w t3J\n could be
idcntif;~d without reso!1tO e~pcnsi'-e and time-c(>n'>uming molecular techniques. but the
da: (of a handheld sequencer sure ly e;mnot lie more thnn a decade in the futllre!
At present. 1!ouC\er. sequencing e"ery fungJI isolate to identify it is far too tim\!"'on.l~ming and e.~pensive. Thcr~ fore. a quicker and simpler technique based on the po!ym~r.I"~ ch3in ~;'\(.tjon (PCR) and the specificit)' of restriction enzymes (ReStriction Fragmem Length Polymorphisms Of RFLPs) has ~ Il d<,vi scd. This is the "PCRfRFLP" tech
nique. It invol\"es the ampliiicatioo of a specific gene or region of the senorne by PCR. The
amphfi~d fragmentofOi'OA is then cut" ith oneer more restriction enzyll1CS. and the resu lt-




ing restriction fragments are separ.ued using gcl electrophoresis (the smaller fMl8ments!hoost with fewer base pa;1l; - tr.Ilelling further along the gel) which produces specific
banding Pltterns called profiles. These banding panems look rather like !he barcodes used
by chel::k-<IUt scanners to identify products in mllly stores. TIle b:md profiles generated in
this \\'ay are chosen so that one (or at lcastjust a few) types of profiles are spedfic to one
species of fungus. In this Wly fungal species can be ''fingerprinted'' and compared
The specificity of the PCR reaction also ofrell; possibilities fOf identification. DNAbased primers can be identified Which have a sequence that is unique - found only in a
panicular species _Thus when PCR amplification using these primers works. we can say
that the fungal isolate be ing examined belongs to a given species or group of fun gi. Such
techniques also lend themselves to fluorescent quantification. Commercial techniques
using fluorescent quantification have not yet been developed for fungi but are already
being used for a number of bacterial pathogens of humans.
In the years ahead we can look forward to molecular help with some of ou r more
difficult taxonOmlC problems. al!hough I do not foresee a day when our taxonomic concepts arc based entirely ou DNA seqoencing. II is importam to stress that a fungus is much
more than the sum of its base pairs! Despite this stricllire of mine. papers are now being
published in which diffcrent names are gil'en to fungi that are morphologically indistinguishabk - the taxonomic decision is based almost entirely on DNA sequences. It will
~ intcrcsting to see if such names stand thc test of lime.
How would you like to be told that twO groups of organ ism~ that can be distinguished on ly by their DNA are being described as different species? Looking at DNA
sequence data derived from species we know to be distinct, we are gelling an idea. at least
in some groups . of how diff~rent fungi must be before thcy can be considered as distinct
\u.,a. It might be suggested that if twO gTOUps have occupied the same kind of niche, this
may have caused them to relain morphological similarities. but they may also hal'e been
genetically isolated from each other for so long that the base sequence of their DNA has
changed. However. we ha,'C to remember that at thc end of the day the whole pu~ of
taxonomy is to help us to identify organisms. and if it becomes too difficult to do this
using morphology, can we justify using the more expcnsh'c techniques? Th~ answer may
Ix! thaI we need 'functional classification' and phylogenetic classification. Currently the
Botlnical Code of Nomenclature does not allow the description of specics without n::fer~
cnce to their morphology. I Jnd many other mycologists think that molccular data is
important and exciting , but should be correlated with morphologiCal comparisol1~ and
with comprehensive po pu lation and mnting type ~lUdies _ This is the ideal we should
strive for.

Genome Projects
...l ost people are aware that a large number of laboratories are ~"()lI~lbornling in the
!>Cquencing of the tlllin:: human geoome. This is 3 hugc projcct and is nOt eXpo:1:led to be
completed for some time. But the entire geoo/l"lC5 of some othcr org3nism) have 3lready
been sequen~d: these include many viruses. some bacteria andonc fungus. SIIct;hllrQm)"Ce)'
ctrr-.isille (ba.l;:ers and brewer' s yeast). The genome of SacdwromYCt:$ ha.<; been founelto
contain nbollt l2 milliDn base pairs w\th about 6,000 recognizable g~nes. divld~d among
16 chromosomes. The SaccharomY"fS genome is the first fungal genome to ha\'~ been
completely seqLlenced. bu t other genome proj~cts are under construction for such mainSlays of genetics as NnnQ;pOI"ll era.lsn and As,nrgillll;' nidlilims. All of these projects will
make it easier 10 place any sequcnced fragment. and thus to know where specific genes are.
Dnd ""h;!llheir funclioflS are. The future of fungal genelics looks c:<.citing.



Hypovirulence or reduced virulence associated with the presence of dsRt'\'A has
become a well recognized phenomenon in some fungal pathogens. The first of these
mycoviruses to be well characterized was the so-called "hypovirus," so named because it
causes hypovirulence (reduced pa thogenicity) in the chestnut blight fungus,
CT)'phollcclTia parasilica. This virus apparen tly has no coat protein, and can' t exist
outside the fungal celL It is transmitted from one strain of the fungus to the next during
anastomosis (the fusion of somatic hyphae). Fungal mycelia are capable of anastomosis
only when they belong to the same vcgetative compatibility group (VeG). Diverse fungal
populations with many d ifferent VeGs will tend to inhibit the spread of the virus. So,
while mycoviruses are potentially [Xllent biocontrol agents for fungal pathogens. they are
likely to be more effective in pathogen populations wi th low genetic diversity. A growing
number of mycoviruses have been found in fungi. Some, like the Crypholleclriaparasilica
hypovirus , are associated with symptoms such as reduced virulence of the pathogen
(similar viruses have been found in other ascomycetes such as Ophiostoma ulmi and
Diaporthe ambigua). Other myc oviruses are cryptic. The best known of the more cr)'ptic
mycoviruses are found in the well studied yeast. Saccharomyces cerevisiae. These viruses
are a%ociated with the killer yeast phenomenon , where one of the viral genomes codc~
only for a protein toxin. The other genomes code only for a coat protein and an RNAdependent RNA [Xllymerase. Neither of these last two genomes have any apparent negative effect on their host. Most mycoviruses do not appear to be closely related. and a
number are based on DNA sequences rather similar to those of some plant viruses.

Further Reading
Beggs, J.D. (1981) Gene cloning in yeast. pp. 175203 (in) Genetic Enginee ri ng 2. (cd.)
R. Williamson. Ac~demic Press, New York.
Bennett. J .W. an d L.L. Lasure (Eds. ) (1985) Gene Manipulations in Fungi. Academi c
Press. Orlando.
Bennen. L\V. and L.L. L~sure (1991) M ore Gen e Man ipulations in Fungi. Academi c
Press. New York.
Berka. R.M. and C C Barnett (\989) The development of gene expression systems for
ti lamentOlls fllngi _ Biotechnology Advances 7: 127- 154.
Blum. H . H. Beier ~[1{1 H J . Gross (1987) Improved silver staini ng of plant protcins, RNA
and DNA in polyacrylamide gels. Electro pho resis 8: 93-99.
Brasier. C!-.l. (1987) The dynamics offungal speciation (in) E ~'olu tionary Biology ofl he
Fungi. (Eds) A.D.t.1. Rayner. CM. B r~sier and D. Moore. Cambridge University
Press. Cambridge.
Bruns. T.D .. T.J. White and J. W. Taylor (1991) Fung~1 molecu lar systematics. Ann. Rey.
Ecol. Sys l. 22: 525-564.
Bruns. T.D .. R. Fogel, TJ. White and 1.0. Palmer (1989) Accelerated evolution of a falsetrumc from a mushroom ancestor. Na ture 339: 140- 142.
Bruns. T.D. and 1.0. Palmer (! 989) Evolution of mushroom mitochondrial DNA: Suilh,s
and rdated genera. Journal of Molecu la r E ~'ol utio n 28: 349362.
Burnett. 1.H. (1975) j\lycogenetics. Wiley, London.
Burnie. J.P.. R.C Matthews, I. Clark and L.LR. Milne (1989) Immunoblot tingerprinting
of Aspergilfus/umigaws. Journal of Immunological !-.let ho ds 118: 179-186.


~ 'B''- 1 i.)
r-. -:!": ...
~ vf"'A


Glass N.L and G. Donaldson (1995) Development of primer scts designcd for usc with
PCR to amplify conserved genes from filamentous ascomycetes. App!. En,iron.
l\Iicrobio!. 61: 1323-1330.
Harrington, T.e. and O.i\I. Rizzo. (1999). Defining species in the fungi. pp 4)-71 (in)
Structure and Dynamics of Fungal Populations. (ed. ) J.J. Worrall. K1uwer Academic Press.
Harrington, T.e. and B.D.Wingfield (1995) A PCR-based identification method for species of Annillaria. i\Iycologia 87: 280-288.
Herskowitz, L (1988) Life cycle of the budding yeast Saccharomyces cerevisiae. l\Iicro.
biological Re,iews 52: 536-553.
Hibbeu, D. S., Y. Fukumasa-Nakai, A. Tsuoeda and M.1. Donoghue (1995) Phylogenetic
diycrsity in shiitake inferred from nuclear ribosomal DNA sequences. i\1ycologia
87: 6 Ig638.
Jackman, P.1.H. (1985) Characterisation of microorganisms by electrophoretic protein
patterns (in) New Methods for the Detection and Characterisation of j\licro-organisms. (ed.) C.S. Guueridge. Wiley, U X
Jahnkc, K-D .. G. Bahnweg and 1.1. Worrall (1987) Species delimitation in the Armillaria
meUea complex by analysis of nuclear and mitochondrial DNAs. Transactions of
the British Mycological Society. 88: 572575.
Martin, c.E. and S. Scheinbach (1989) Expression of proteins encoded by foreign genes
in SaccharumY"C:1 a revisiac. Biotechnology Advances 7: 155-185.
O'Donnell K. and E. Cigelnik (l 997) Two divergent intragenomic rONA ITS2 types
within a monophyletic lineage of the fungus Fusarium are nononhologous. Molec.
Phylogenelics Eyol: 103- 116.
O'Donnell K, E. Cigeloik and H. Nirenberg (1998) " 'l olecular systematics and
phylogeography of the Gibherellaf"jik"roi species complex. i\lycologia 90: 465493.
Old, RW. and S.B. Primrosc (1985) Principles of Gene i\Ianipulatioll; an Introduction to
Genetic Engineering. 3rd Edn. Blackwell Scientific, Oxford.
P~rkins, D.D. (1987) Matingtype switching in filamentous ascomycetes. Genetics 115:
Scheinbach, S. (1983) Protoplast fusion as a means Df producing new industrial yeast
strains. Biotechnology Ad"ances 1: 289-300.
Strathcrn. J.N., E.W. Jones, and J.R. Bwach (Eds.) (1981) The Molecular Biology of the
Y~ast Saccharomyces, Life Cycle and Inheritance. Cold Spring Harbor Monogr~ph Seri",s. VoL 1 lA. Cold Spring Harbor, New York.
St rathcrn. J.N., E.w. Jones. aod J.R. Broach (Eds.) (1982) The Molecular Biology of the
Yeast Saccharomyces, t'\'letabolism and Gene Expression. Cold Sp ri ng Harbor
Monograph Serics. Vol. I lB. Co ld Spring Harbor. Ncw York.
Taylor. J.W. (1986) Fungal evolutionary biology and the mitochondrial DNA. Expcrimental i\lycolngy 10: 259-269.
Van Bront, J. (1986) Fungi: the perfect hom? Biotechnology 4: 1057-1062.
Vo lk. T.1., H.H. Burdsall and M.T. Banik (1996) Anllil/llrillllabsllona. a new species from
western Nonh America. i\"Iycologia 88: 484-91.
Willhuhn, R.C. B.D. Wingfield. MJ.Wingficld, IV!. Wolfa~rdl and T.C. Harrington ( 1998)
Monophyly of the conifer [inhabiting] species in the CerlllOcystis coerulescells
complex using DNA sequcncc d~ta. i\Iycologia 90: 96- 101.

Fungal Ecology


Ecology is the study of organisms as lh~y relate to each other and their enviJo[\
ment. II must be 3pparenl lhat el'en in the taxonomic chapters I &a\'c a lot of ecological
infonnation. Think of the effects that fungi ha\"e had on people: the potato famine, the
downy mildew of ttlc French grope \ines. the blue mould of Canadian tobacco. the way

chestnut blight removed an important species from Ihe forests of eastern North America,
and the more recent loss of the beautiful American elm trees to Dutch elm disease. Fungi
may aller tbe


of our gardens. as their depredations persuade some people 10 give

up gro,.:illg roses (\xcause of the pr<,\aknce of black spot diseilSe. powdery mildew and
ruSt) or phlox (bcc:\Use of its slIs"plibility to powdery mildew), The early drop inflicted
on tlorse chestnut trees by Gllignardia blight (at l~ast In ea5t~rt1 North America) may
persuade us tu pl~nl other shade trees. But in this ch apter I wnnt to eXpl()re some other
areus of fungal ecology: some Oflh~ w~ys in which fungi int1uen~e the course of events in
a ' ariet)" of n:lIur:ll. as opposed 10 man-madc. habitats. I will e~plore their roles in four
natural habitats I and my undergraduate or graduate studems haw personally e~amined
in some detail. and then give a few more gen< ral com ment s.

The Succession of Coprophilous Fungi

The fir.;t habi tat is dung. We may tum up our no~es. but to some OIher organisms.
dung is u considerabk resource. I'hich is oon;;tan tly being produced in brge quantities
by billions of animals allover the world . You may think thut because it has PJs.~ed through
an anima!", digestive tract. every bit of nutritionJl value wit! havc been extwctcd from it.
Not true! Th~re may nOI be a lot of high qualit) protein left. but Ih~re is a great deal of
microbial biomass. as wcll as man~ food components. for example. cellulose. that neither
the animal nor itS gut microbiota managed to digest. There are alw excretory products
which, Ihough they ar~ of no further v~l u e to the anim~l, are high in nitrogen: herbivore
dung m~y cont ain 4% nitrogen _ more. in fact. than the plant mmenal originally eaten
by Ihe animal. So. al frc:quent intcnals throughout its life. e\er)' mammal cvacuates from
its suI a mass of fir.;t class fungal substratc. simply asking to be exploited.
Arc there. then. fungi which >pe<"iaJize in e~ploiting dung? And if there arc. 11Q\'.' do they
gain :IC<:ess to this substr:lte whcn it lxcomcs avail ~ble? 'The answcr.> m~y surprise you. About

175 gcneraofascomyceles are largely or aclusivdy found on dung. The extremely advanced
anctsuccessfuJ agaric genus Cuprinus hlS many specico; Ih:ltoccurexclushely on dung. Tht.--re
are also many ~peci:ilizcd dunginm.biting lygom~eetes. among which Piluboills and 50mc



of the el.:lbor'J!e anamorphs in the order KickxeLlaies are perhaps the rn()Sl spectacular. So there
is a numerous and speci:tlized mycow. of dung-inhabiting (coprophilous) fungi.
But how do they compete successfu lly for this su bstrate? The ans wer here may be a
little unexpec ted. but it is nevertheless perfectly logical. ThC5e fu ngi contrive to be first
10 exploillhe dung by the simple expedient of being in it when it is deposited. And whal
is the only wa)' 10 achieve that? To be eaten by the llnimal.
Co prophi lous fu ngi manage this trick in scveral ingenious wa)s. These processes
must take into account some immutable logic. I) Tbc fungi are growing in the dung and
will thercfore have to fruit on it. 2) Animals do not. in general, eat their ow n d ung (thollgh
rabbits do, rai sing interes ting questions about the coprophilous fungi associated with
them). 3) Therefore, the spores must bc somehow distanced from the dung in such a way as
to increase thei r likelihood o f being eaten by herbivorous mammals.
You have already read in earlier chapters abou t how ~everal fungi of he rbivore dung
achieve this trick: How the zygomyeete, Pi/oboll'S, aims and shoots its sporan gi a up to 2
metres toward the light. How the ascus tip s of the apothecial ascomycete A;cubohl.l
protrude from the hymenium and bend toward the light bc:for~ shooting their spores. How
the necks of the peritheeial ascomata of PodQspora and Somaria bend toward the light
bcfore tneir asc::ospores are e "'pelled. Each of these imkpendently e\'oJved phototropic
mechanisms is obviously designed 10 d irect the s pores away from any (){her adjacent
dung. and to increase the efficiency with which spore s are deposited on nearby vegetation
that has a good chance of being eaten by the animal.
Many other dung-inhabiting fungi arc: less specialiad than those I have just nlentioned. or h:we ~p<-"'Cialilatjons so subtle that we h~ve not ~d detected them. t\e vertheJcss.
the fact remains that with patient and repeated examination. we elln find a large numbcrof
fungi representing most of the major fungal grou~ on the du ng of many h~rbivOf(\us
mammals. Repeated observations will ,how that the variou. fungi tend 10 sporulate in a
reason~bly defi nite sequence.
First the Zygomycetes wi l! appear: Piloboills; the dichotomQ usly branched S[X1rungiophores of PiplOct'phalis which anac ks olher zygom)'cetcs; the tal! sporangiophores
of 5)"lIapha/i.f with thei r swollen apices and linear merosporangia: the gruceful multiple
re<:urved sporangia o f Cireinella minor: Rhopalomyces ,,It-g(l1iS. which parasitizes nematod~ eggs: Oll1ninglwm ella with i\~ apical vesicle and uni>por~d sporang ia.
Then the Ascomycetes: apothecial fun gi lik ~ A)"("oboiIfS, SaccoboiuJ. Thewtilells;
and the peritbec ial Podospom and Somaria. accom panied by a varie ty of conidial
anamorphs (Hyphomyce tes) such as the bl~stic-sy mpodinl Bmifimbria; the nem~tode
trapping Arr"robotr)":; with its clustered did) mosporous (two-cello:<l) conidia and its various ways of snaring nematode s. induding three-dimensional nets; the synnematal. slimyspored (arthropod- dispersed) GrapliiwlI: the synnematal. dry-spored Cepliaiatridmm:
~nd Tric/mms. another synnematal hypbomycete witb twisted. hair-lik e se t~e ari sing a ll
ovn the fertile bead.

And finally the BasidiomyceteS, main ly small (but profuse) species of the agaric
genus Coprinlls with liny caps, black spores, ~nd autolysing gills.
It has he<:n suggested that Ihis is a true ecological succession. albeit a miniature and
condensed one. Initially it was poStu lated thllthe seqllcnce wa~ a nutritional on e. Zygomycd es "111 generally a,similate only fairly access ibk carbon sources. such as sugars.
Their fast growth was assumed \0 give them an advan tage in findin!! the~e. and the ir early
dis.appearanCe was thought 10 be due to the e",h:tu5tion afthis substrate. The ascomycetes
and C1)nidinl anamarphs mat appeared nex t were assumed to bc able to as.<>imilatc m~


comple)( caroon sources such as hemicellulose and cellulose; while the basidiomycetes.
appearing last and persisting longest, were able to exploit both cellulose and lignin.
But when this hypothesis was scrutinized more carefully and tested by experiment
and Ilmher observation, it did not hold up. The growth rates of the various fungi were
found to be relatively similar, and the various carbon sources were not exhausted as
quickly il$ had been assumed, So a second hypothesi s was advanced. This one was based
on the time it took for each kind offungus 10 accumu late enough food reserves to pennit
it to fruit. It was argued that the simple sporangiophores of the zygomycetes cou ld be
developed after only a short period, whil e the more elaborate fruit bodies of tho: ascomycetes would require a longer build-up, and the even larger basidiomata of the coprini
wou ld need the longest preparation of aiL TI)is is a more reasonahle hypothesis, because
if wo: grow some of the dUllg fungi on laboratory media, we find that it takes Mucor
hielno/is 2-3 days to sporulme, while Sordaria fimicola needs 9-10 days, and Coprinus
Ireptemerus 7-13 days,
Some of the KickAeliales, zygomycetes often found on the dung of sedentary mJmmals (those with a defined home base, a small territory, and habitually used paths), produce eXlrt:mely complex and convoluted anamorphs_ Spimdactylon, possibly the most
complex of all. produces tall, branched sporangiophores that bear liny coil s w ithin whieh
develop innumerable one-spored sporangia (Fig, 3.4 F), The whole structure must be
dcsigned to catch on the hairs orthe rat or mouse as it passes by. This is made possible by
the habit;; 0[" the animal which. although it doesn't eat its own dung_ at least deposits it
somewhere along one of the trails it follows every day in its journeys to and from its den
or burrow. The final step, the ingestion of the spores, is presumably taken when the animal
grooms itself. JS mammals (other than human children) habitually do, Some coprophiloU!;
hyphomycetes (e.g., Graphillm) produce slimy droplets of conidia at the top of tJIl conidiophol\'$ or synnemaml conidiomala, Thcse spores are presumably dispersed by arthropods
which may Ihemsel ves specialize in seeking out dung, and may thus act as spec ifi c, and
very efficknt, "ectors for the slimy -spored fungi.
So we can assume that an assortment of spores of coprophilous fungi will be present
in dung wh~n it b deposited, and th at these will all have been triggered to germinnte by
some as!X'ct of passage through the mammalian gut. Whik Pi/obo/us is producing its
miniaturc artillcry c)(travaganza, the other fungi are growing and assimilating steadily
within the dung, preparing for their own appearance at the surface. The new hypothesis
had oeg\ecl~d only one imporwnt fa<:lor: antagonbm, After a few weeks , almost the only
fungi still sporu lati ng on the dung will be species of Coprillus, Th~se CJn go on producing J sequence of ephe meral basidiomata for months_ We now know that the various
compon~m5 of the substrate are far from e)(hausled after the initial flushes of growth and
sporulation_ What has l\'aU)' happened is that Coprinus ha> seized contro l by supprc ssing
most of the other fungi. Hyphae of Coprimls are actually extremely antagonistic to those
of many oth~r coprophilou$ fungi. If a Coprinus hypha touches Olle belonging to
Ascoliolll'i, the Aswboilis hypha collupses within minutes, We don 'I understand exactly
how this trick is done, but it is e~treme l y effective. and turns out to be a fJirly common
strntagem among the fung i, whose main competi tors for many subslrntes are other fungi_
Another intercsting and important gamhit used by Coprinu.1 involves repeated
3nastomoses_ Spores are more or less evcnly dispersed throughout the dung when it is
d~posited (Fig, 11.1 A), ~nd they all germinate more or less simuitJneously, producing
, mall mycelia wilhin the dung (Fig, 11.1 R C). When compatible mycelia meet, they will
~ nastomose. and soon the entire dung deposit is permeated by what is now essen tinll y a
sin gle mycel ium (Fig, 11 . 1 D), which can then pool its re,ources and produce more and
larger basidiomata , Cooperation pays off for Coprillus.




And don.'t forget the Interesting subplot.> that run concurrently with the mmn story
Several of the zYg<lmycc!cs that usually appear (e,g., Piptocephalis) are actually parasitic
on other zygomycetes, One common zygomyccte. Rhopalomyces eiegmls, parasitizes

nematode eggs. Nematode-trapping fungi such as ArrhrobOirys often sporulate, and devdop their characteristic rings and nets (see chapter 15). Keratinolytic hyphomycctcs
such as Microsporwn may appear on hair thm the animal has acridcmally eaten during

Occasionally, an undescribed species of fungus may be seen. For many years the
third year mycology class at Waterloo followed the dung succession as a laboratory
exercise . These undergraduates saw the zygomycete Stylopage allOmaia 011 horse dUllg
several years before it was formally described ill 1983. They also found an undescribed
species of Podospora (Ascomycetes). which is perhaps the 102nd species of this genus.
They also found the rare zygomycete, Helicocepha/um, which I had never seen before.
(Who says your students can't teach you anything?)
Horsedung is easy to obtain in most areas, comes in discrete units, andcan be handled
and observed without creating much personal distress . As many as 40 species of fungi
representing most major groups of eumycotan fungi arc commonly recorded from a single
collection of horse dung. Most of them can be identified fairly easily 10 genus with the help
of the specialized taxonomic literature that is now readily available (and by looking at the
pictures on the CD-ROM version), tbough , admit that some of tbe zygomycetes are not
easily recognized as such by beginners. Many of th~ fungi can be isolated in pure culture
without too much difficulty, and with a linle imagination. interesting experiments can be
devised to investigate various aspects of their behaviour. Perhaps now you can understand
why I and many other teaching mycologists ask OUf classes to put their culturally determined attitudes on hold, adopl an objective scientific approach. and study the Sf.lccession or
fungi on horse dung. then think about the biological mechanisms and manoeuvring that lie

Fig. 11 .1 Behaviour of Coprinus in dung. A:spores present when dung is deposited; B; spores
germinate synchronously; C: mycelia anastomose; 0: c:omposite mycel"lUITI c:an exploit the entir<:
substrate and produce large basiO!OfTlata.


behind the visible manifestations. Its a truly\oking mycological experience.
Now for another. smaller terrestrial system. the pine needle.

The Pine Needle Microsere

Wben I began my own PhD studies back. in 1955. I was presented with a problem
which. briefly staled. was as follows: "When we isolate fungi fro m the soil. the majority
of cultures will be of lightcoloured fungi. while a majority of the hyphae seen in the soil
arc darkly pigmented. Figure oue what's going on."
I tried int1umerable times 10 grow the dark hyphae. picking them out with

a mi

cromanipulator and giving them a variety o f delicious media. But they refused to grow. so
I eventually decided Ihat most of them must be dead. and that they had perha ps grown at
some other time and in some other place. I looked in the organic horizon above the
mineral soil. and found there a thrivit1g community of lillerdecomposing fungi. which I
proceeded to investigate (I did not realize it at tnc time. but this is fairly typical of PhD
projects, which 1IfC often changed in mid-course by unfol"C5eet1 events).
The pille needles making up the litter unde("\\-'ent a gradual transition from L- Fl -FlH layers oflhe organic horizon of the soil. I then decided to examine as many needlcs from
each layer and sub-layer as I CQuld process each month (the number turned out to be 300).
Living needles from lhe tree rcpresemed stage Olle it1 fungal colonization. Recemly dead
ncedlesconstilUted the L layer(pale brown). below which lay the upper FI (needles much
darker. but still tough ), then the lower Fl (needles blackish and softer). and finally the F2
(neeules greyish and fragmenting). By the time liner material entcred the H layer. it was no
longer w:ognizable as individual needles. Needle were treated in \'arious ways . (I) Some

........ ....".1....

c.... , ,;



....... ...


. ..... .




'.... ,..


,, ,


,...... ,....."".


.......' ..,."....

" "fl., ;.. ........ K'I


Fig 11 .2 Gener<olized scheme of the foxogal successionn Pinus sy/vesfrls ~ shoo.vng the
1O""(.lOf:t1 and ;pollial relatiOnsl"Vps oi the f~i mainly coocerned in the breakdown process

Provisional biomass estimates and arulUalliner production for
Meathop Wood soil (after Satchell 1970)


Dry matter biomass (kgiha.)























Other arthropods


TOIal biomass


Annuallittcr production


were washed repeatedly to remove loose surface spores and plated out in segments to
isol:ue fungi on and in the needles. (2) Some were surface steri1i7.l'<i before plating out. to
select fO intemll coloni1.ers. (J) Some were Walt-embedded and sectioned. (4) Some were
obser..ed directly over a period of incubation in damp chambers.
One of the first dramatic changes is the development of numerous ascomata of
Lophodennilllll pil1(/$/ri. which apparently often ~olonizes the interior of living needles
without producing ovcrt symptoms - in fact . it may be in~olved in deterring herbivores
from eati ng the living needles. The death and fall of the needle stimul ates this fungus to
fruit. The large number of lenticular black ascomata of Lophodermi/ll/l that can occur in a
single needle indicutes that it is a dominant colonizer. Other fungi fruit in Other needlesindividual needles may thus travel along several dccompositionll paths. though the
average time it takes a needle to become humified is about nine years. One pathway
begins with WpllQdumium. anothcr with p),cnidial conidiomat:l of l coelomycetous
anamorph. Fusic{)CL-UIil (holomorph probably BOIT)"mphaeria). The interior of the needle
b<gins to brenk down under the auacks of the fungi.
Meanwhile, on the surface of the needle. networks of dnrk hyphae develop. But
whm fungi do they represent? Mycelium without sporulntlng suucturcs is not very helpful unless one has access 10 moiccui.u- techniques. Fortunately. several of Ihese fungi
fruited either in nature or in damp chambers. The rU"S1 of these w3S SIiItl(lCOIII)"Ce$ monosporu
(which I mistlkenly described in 1958 as a species of /leUcoma). A sel'Ond major surface


colonizer was Sympodiella neieo/a. which 1 described as the type species of a new genu s
(it still Slands). Again. the conidiophores form an almost pure stand. Its unique characteristics are th:)! while lIS conidiopMre extends sympodially. the conidia ate thallic-anhric
(for those of you who are fans of conidium development - otherwise look back to ch apler
4). Another fungus that produced pure stands of external conidiophores .... as Verticicladillm
trjfidllm (an anamorph connec ted to an apol"hccial fungUS. ~sma~ierl'lIa acico/a. which
I never saw).
Now I began to find needles divided up hetween neighbouring fungi. Sections of
partitioned needles showed a black:. melaniled barrier between species.
New participants enter the picture. Once the needles have been softened up by the
fungi . arthro pods can eat the needle materi al. Oribatid mit~s. miniatur~ armoured tanks.
eat fungi and needle. In the lower Fl . the intcrior of the needle has collapsed or been
eaten. and the upper surface is cooted with a deposit of fr.lSs. whicb contains many fragments of fungal hyphae and spores..
Fig 11.2 plots the overall picture, foUowing the needles through nine years of
mainly fungal decay. The width of each bar representS th~ relat ive importance of the
fungus at each stage. Darkerbands show fruiting periods. At far left the fungi are tho5e that
grow on or in living needles. As we move to the right, the fungi involved in later stages of
decay are traeed.
Read the numbers in Thbie 11.1 carefully - they will amaze you. and they show
JUSt how important fungi reaHy are in the forest ecosystem. NOi mculy importa n!, but
produ cing greater biomass than any group other than the plantS.
Other spec ial substrates have e voked specialiled fungi: kerati n is attac ked by some
of the Onygenales and their anamorphs; wood by many Aphyllophorales. Extreme physical conditions have se lected specialist fung i which, by e,'oh'ing th e ability to cope with
high or low temperatures. or low water activity. have c~selllially escaped from competition. and gained ac.:ess to untapped food supplies . Some fungi are the most osmotolennt
organ isms known (see chapter 20). The cycling of anumorph and tekomorph. which 1
ment ion many times in connection with pl ant disease fungi in chapters.f and 12. is often
largely a mailer o f their response to specific ecological conditions. wbich tum on and off
large segments of the genome. The fungal ecology of se wage. compost mushroom beds.
ag ricultural and foreSt soils. natura!!y deco mposi ng plu nl rem ai ns, some cheeses. bread.
wi ne und bee r, crops in the field and after harvest. the ai r. lhe space between )'our toc:s. and
the tissues of immu ne deficient or immune-suppressed people: all can be the subjects of
worthwhile, an d even important, studies of fungal ecology.
i\-Jany o f the food webs illustrated in ecology textbooks miss Out more than half of
the organisms involved in the transfer of energy and nutrients. They oft~n stress macroscopic organisms. wh ile omiuing microscopic organisms such as the saprobie and mycorrhizal fungi. This neglect is un fortunate. especi~ll y sin ce we now apprcc ia l~ that microorganisms. being at the b.ase of food webs, provide nutrients and mutua1i5t ic symbionlS for
almost all plants and animals. The basic links in terrestri al food webs lie in Ihe soil "hich
is. of course, where a huge number of fungi still live. E ~~r;: attempt to understand terrestrial trophic systems must Start and finish with soil organisms. And surely the fu ngi are
among the most import:1ll1 of those.

Amphibious Fungi in Streams

The third area o f fungal ecology I want to examine is a Stream flo ..... ing through a
.....oodland. somewhere in the temperate lone. We already kr.ov. that the tiny chytrids and
oomycetcs liye here. but we migh t not cxpect to find man:' of the t~'pically terrestrial




~ ,-,

. dikaryomycolan fungi. However, if you collect some stream foom and examine it under
the microscope. you will see that the bubbles"have uapped a rather unusual kind of multi~
armed spore (this is simply a physical phenomenon - a surface tCl15ion effect _ and theTe
is no other relationship between the bubbles and the spo.-es). In fact. the water contains
what we call tetraradiate spores of many Sile.~. Pass a litre of stream water through a filler,
then stain the filter in conon blue and examine it through the microscope. and you win
see morc of these often large and strikingly shaped tetraradiate fungal spores (Fig. 1\ .3).
Other spores will be unbranched, long, thin and arc-shaped, sinllate or sigmoid (s-shaped),
All are produced by conidial anamorphs tho! are specially adapted for living in Streams.
Where do these spores come from. and how do the fungi that produce them make a Jiving?
The first due came when limnologists (biologists specializing in freshwBt~r systems) began to examine the energy budg~tsof streams. Because some Streams now through
forests. th~y are heavily shaded during the growing season. This mc:ms that few green
plants (primary producers) can grow in them. It was found that more th:m half, and SOillCtimes nearly all. of the energy supponing organisms that live in streams comes from


.lulUmn-shed leaves of trees that grow over the Streams. This source of energy is de~cri~
as 'alloc hthonous' (which means ',,:oming from somewhere else').
When they flnt fall into the water, these: leaves are extremely unpalatable to Stream
invertebrates. but as they are colonized and 'conditioned' by microorganisms, they apparently be<:ome tastier. Ex perimentS in which batches of leaves were trellted with eithcr
anti fungal or antibacterial amihiotics sllowed that the fungi were ehiefly instrumental in
making leaves palatahle to animals such as Gammam_1 pselldolimnat lls. a numerous
amphipod crustacean living in the Stream (another amphipod lives on the beach below
my house in millions. eating decayin g tidal jctsam, mostly seaweeds and, no doubt. the
fungi growi ng on and in them). In a feeding experimcm. Gammarus chose to cat fu ngal
mycelium rather than unconditioned leaf discs. Later experiments with l eavc~ conditioned by indi vidual stream fungi showed that not only were some of the fungi that
produce tetraradiale or sigmoid conidia most active in conditioning leaves, but their
mycelia and sporu lating structures were also highly numtioos food for dctritivorous
stream anim.als such as Gammarus. An imponant ecological role had been established for
these fungi.
But many qucstions remai ned, Were those fungi with letraradiate sporcs related to
one anOther? Did they ha\'e telcomorphs'? (which would help to answer the firsl question).
Since stn:a!IlS alo.,,'llys tlowthe same way. and have a natur",1 tendency to carry small things
like spores downstream , where diclthe inoculum for the upper rcaches come from? What
were the advantages of the tetraradiate and sigmo id spore shapes? The informati on we
needed was gradually accumulated ove r several years of experimcnts. until eventu~l1y we
wen: in a position to givc some Urlswcrs .
.\Iany of the tetraradiate (fOlic-armed) spores, though similar in configufllfion at
maturity. developed in rathcr different wayS. I will describe just two of these. In some.
three armsrew upward and outward from the toporth<! rlJ';t-formcd am} (e.g. TtmKh(l~tllm
in Fig. 11.3). In others. one arm grew upward. the other!hrce or four outward and downward al the same time from a cenlm! cell (e.g. um()fln;aa in Fig. 11.3). Somc of these
conidia ...'ere thallic. some blastic. A few had clamp con~c{ions; most didn' t. This impression of di\'Crsity wasconfinned when some of thc telcomorphs were.disco~ered . Some
wen: unitunicate ascomycetes. both opereulate and inoperculate, producing apothecial
~nd ~rithecial ascom ata. Some wcre bitunicate asromycetes. Some were basidiomycet~s.
II became clear that the morphologically similar anamorphs were actually n mi"l:~d
bunch: fun gi of vcry different origins th aI had undergone comergcm evol lllion. mo lded
by selecti on prcssurc imo similar shapes. The teleomorphs also provided one nnswer to
the qu~stion of how these fungi got upstream: ascomata and hasidi omatll.. unlike the
anamorphs, were not submerged in streams. and they liberated airborne ascospores or
oosidi05pores. The group has been christened the amphibious fungi. beeause of it~ immet>Cd anamorph.i and emergenllekomorphs.
But "hy d id so many of these taxonom ically d iverse amphibious fungi evolve
conidia with similar shapes? It was found that as they w~re carried along by the WateT.
tetraradiate spores somclimes entered the layer of still Watef JUSt above the sulface of
subm<:rged !eo\'cs. and then made three-point landings on these leaves. We know thai a
tripod IS the most stable config uration. able to .tand firm o n irregular surfaces. The spore.
fomlcd microscopic tripods that gavc thcm a foothold <,In the dead leaves for long enough
to gcmlinatc from the ends oflhc lhr~ arms. and attach themselves to the substrate before
being swe pt away. The n:ason for the sigmoid shape has not yet been fully estab lished.
After coloniZing the leaves. the amphibious fungi sporulate again, and it was found
th:u they wOllld do this only in highly oxygenated conditions. and with the phySical
stimulus provided by nOVo'ing water.



If the ~pore numbers are charted over the entire ye ar. it will be seen that their
numbers peak in fall and spring. In !he first place. the massive new input of autumn-shed
leaves pru,-ides the necessary substrate. In the second C3SC. spring run-orr will also carry
plant d~bris into the stream. The entire process is diagrammatically summarized below,
showing mal the fungi are vital intermediaries of energy flow in streams, providing 3 link
between dead leaves 3nd troUi (Fig, 11.4).







I, '

I' I

Fig. II.": Enefgy flow n s(reams:lcaf -+iungus-+CammarU5-+trout.


Aero-Aquatic Fungi in Ponds

One good aqulllic habit:lt deserves anOlher. so after sorting out the role of fungi in
Streams. w switched our attention to woodland ponds. The pond in question lay in the
heart of the woods behind my house in Waterloo.
Again. primary production within the pond was limited by the forest canopy. Again.
there was a specializcd group of fungi living in the pond. though no one knew if these
fungi played an important role in the ecology of the pond. In miscase the fungal propagules
commonly found were hollow. and floated. Again. this end was achieved in several differ_
ent ways. of which I will desqibc only two: The pond gradually dries out in summer. and
the rolonized leaves come to lie just below the surface of me water. (I) A conid iophore
emerges from a dead leaf. emerges into the air. and branches like a tree. Eventually. the
ends of the fine branches all swell up and fuse with their neighbours to form an air-filled,
watertight structure. This is the propagule of Beverwykella (Fig. 11.5). (2) Another conidiophore grows up from a dead leaf, emerges through the water surface, and its tip begins to
grow in cireks, Coiling repeatedly on itself in wider and wider, then narrower and nar-


rower gyxcs, it eventually builds a barrel-shaped, air-filled, watertight struc ture, This is
the propagule of Helicoon (Fig. 11.6).
Another apparently rare pond fungus is th e tiny floati ng gasteromycete ,
Limnoperdon. It has been recorded only from our pond in Ontario and somewhere near
Seallle, Washington, though it surely occurs at many places between those widely sepa rated localities - people just haven't looked carefully. The fruit bodies are hollow, and
are lined with non-shooting basidia - the spores are symmetrically mounted and the
sterigma is not pointed (see discussion in chapter 5), Young basidia have a clamp connec tion at their base,
Because these fungi live and grow under water, but produce their spores only above
the surface, they are called the aero-nquatic fungi. It 's obvious that the structures of the
two kinds of conidia described above, thoogh functionally equivalent, are not closely

Fig. 11.6 Ocvelopmcrlt of the fioatlngpropagoJeof HeUman.

related. Again. convergent ~volution has bc~n Ilt work. the sekction pressure applied by
We finnUy disco\"~rt:d whm thi~ was. It wos the need to be frnt on the sc~n~ when
new substrate appears. \\I"h~n Il dead l~af falls into a pond. it docs not sink immediately. II
may actually fallon top of $Orne of [he floating propagules, or the propagules may be
drawn to the floating leaves by surface tension. In either case. these fungi will be the first
pond-adapted species to enter this new substrate. The leaves soon sink to the bouom of
the pond. carrying their new colonizers - hyphomycete or gasteromycele - with them.
These fungi also have the abiliry 10 grow at low oxygen levels. and to survive the virtually anaerobic conditions thnt prevail at the bottom of a pond for extended periods during
the winter. Sporulation wi]] happen again wheo the pond begins to dry out during thc
follo"'ing summer. and the water level subsides until the colonized leaves are once more
JUSt below the surface. We found til~lthese aero-nq uatic hyphom)'cctes play an ecolog ical role parallel to thai ofthc amphibious fungi in streams: conditioning the deoo 1ea\"(:~.
and making them palntablc to the detrilUs-ealing in"crtebrates such as snails; and venebrates such as frog s. whose tadpoles live in the pond and ~ke1etonize leaves after the fungi
have 'conditioned' them. e'entually metamorph()!;ing into tree frogs which represent the
apex of the pyramid of life in the pond.
$Om~ ~cologica!

Fig. 11.7 MeL:lllized bourodariesbetwet;n'territories' of diiicfent mycela in a bIod of rattng wood.



Other Habitats
The biosphere has myriads of othtr habitats. each unique in various ways. and each
making spedal dcm~nds of the organisms that live in it. The roots of plan IS creale special
conditions around themselves, and have establish<ed especially intimate relation~ with
hundreds of endotrophic and thousands of ectotrophic mycorrhizal fungi (which have
chapter 17 10 themselves). Other rather less specialized saprobic and parasitic fungi also
abound on and near rOOts. The su rface of living leaves is inhabited by a spedalized
mycota. while dead and decaying leaves are subMr.lteS for a succession of other species.
The soil, into which most leaf remains are incorpor.ued, is itself a mass of microhabitats,
and is the richest resc(VQiroffungal diversity. And of course the leaves of di fferent pl~nts.
and the various soil types, will have different subsets of the total mycota. Julict Frankland.
in her 1998 Presidential address to the British Mycological Society, gave a nice overview
of the problems and progress in our study of fungal succession, exemplifying them with
an aute<:ological study of the agaric, Jlyuna ga/opus.
!\Ol all fungi can be parcelled om neatly into successi~'e steps of a succe~~ion.
Often, fungi compete for access 10 ~ sub,trate. Sometimes a natutnl phenomenon will give
us an unexpected insight into this struggle. Wood is often colonized by many different
mycelia. The boundaries be't"een the 'territories' of different mycelia can often be clearly
seen as black lines or zones, and the wood is described as 'spalted: (Fig. 11.7) The black
materia l is melanin-like, oxidiled and polymerized phenolics deposit~d by wood-rotting
fungi. and although the biological fl,lnClion of the zones isn't entirely clear. melanins arc
the precursor> of the hl,lmic acids. which are longliled and important detennjn~ntS of soil

Macrofungal Ecology - Help wanted!

Most of thc situations I have described in thi s chapter arc small or localized. If we
consider the macroscopic fungi. and their roles in such extensi"e ecosystems as forests,
we find that the State of fungal ecology is rela!i"el} primitive, meaning that we simply
doo't know very much about how those fungi act and interact under natural conditions. If
you doubt this, you could explore the mycological literature for information on where to
find morels (in my opinion. the best of all edible fungi). You will be kd a merry dUnce,
from old apple orchards and dead elms to re<:ently burned forests. Until relatively recenlly, no one even seemed to know "hether morel s were mycorrhiZ-:ll or not (m y undermnding is that they an.: opportunistic saprobes, exploiting new substrates. then fading
aWity. Dilly to appear so mewhere else when new food sources pn:sent thcmselves).
As for the ubiquitous agarics, which are undoubtcdly th~ most widely collected and
sludied ofal! fungi, [have to report that things aren't mllch beuer. Only Europe holds out
a candle in the darkness. Since Europeans havc heen collecting ~nd recording macrofungi
for centuries. Ihey have lhe kind of database that allo" s the present generation of mycologists to draw compariSons with thc p~st. This is why several Europea n countries have
'Red Lists'- compilations of macrofungi which ~em to have und~rgone serious de
dines in recent years, or even to have disappeared altogether. It is impossible to producc
such Red Lists for anywhere in NorthAmerica because records do nOl go bad farenough
~nd are, in any case. still fragment~ry. Although we may suspect thaI certain species are
declining or dis~ppearing . we h~vc no weJldocumenteJ hi,lOrical reason for saying so.
You can find out more ~bout red lists by going to a good search engine such as 'google' or
'al1theweb' and enlCring 'red list endan,g.:'rcd fungi' .
We understand that about half of the known ag?-rics are - they have an
intimale, mutually beneficial rel~tionship with many of OUf forest trees. and ecological


research has recently begun to focus on the effects on such fungi of various forest practices, and especially the c1ear-cuning of old-growth fore.sts which Still (regrcuably) goes
on in many jurisdictions. and most blmantly in British Columbia where I live.
One of my own gradUate student, has recently established that many of the fungi
associated with old growth forests do not re-coloni ze clear-cut h~bitats for 40-50 years.
And his suspicion is that the recolo nization happens by means of airborne basidiospores
which origin~te in nearby old growth. What if there is no longer any nearby old growth to
provide this inoculum? But intcmati on~l logging companies carry on in blissful ignorance of any such concerns.
Just when we thin k we have established a few principles based on the occurrencc of
froiting bodies of the myco rrhizal fungi. it is demonstrated by mol~cular tcrhniques that
in many cases the fungi prod ucing the fungal sheaths around the TOOlS of the trees are not
those whose basidiomata are appearing above ground. AR: we bade to square one? No
one seems sure at present. But I mention this to demonstrate how linle we actuall y kn ow
about macrofungal ecology.
A fascinating study by Tofts and Orton (1998) points out that although they ha,'e
been collecting agarics regul~r!y in a panic ular woodland in Scotland for 21 years. and
have recorded 502 species in that time. each year they still find species they have never
seen before. Over twenty years of collecting, and they still cannot say that they have 11
proper handle on agaric biodiversity in that woodland. They suggest that at least 25 to 30
years of collec ting, and possibly more, will be necessary before that goul can be attained.
This is not inte nded to put you off, to deter you from gctting involved in fungal
ecology. Rather th~ reverse. It is clear that the need for researcb in thi s area is critical. We
need good ecological st udi es just as much as we need molecular research on fungi. Some
groulldwork has tJc,en done in Britain. where the macrofungal assemblages characteristic
of many habit:ttS have been broadly outlined. But this is still far from an understanding of
the full role played by tbos~ fungi in the habitats be ing considered. The need for se minal
research has never been greater,

What's an ATBI ?
Of course. you can't do fungal ecology unless you know what fungi are present.
There is almost certainly no habi tat in the world whose fungi have been fully enumerated.
A group of 22 mycologists gathered in Costa Rica in 1995 and came up with a strotegy for
isolating and identifying all of the fungi (an estimated 50.000) in a particular hahit:u (the
Guanacaste Conservation Area) - an All-Taxa Biodiver,it)" Inventory for fungi (Rossman
et al. [Eds.J 1998 - see reference below). This ambitious plan called for a staff of a
hundred , 51 million wonh of agar media and 1.8 million slants to isola te the e ndophytic
fungi alone. Unfortunatel y alllhis would have cost about US52S million. so it hasn't
been done. BUI the need remains. and the ge nernllack of kno wledge about fungi means
that they are not usually considered when conser"mion issues are raised , Perhaps you ca n
hclp to chunge all that. A less ambitious ATBI is now und!f way in Great Smoky Mountains National Park, blll it is a long-term ende ~vou r - visit the " 'eb site at
http://w"w.disco\.e rli rC.o rgj
And baving outlined th at cunemly unsatisfactory stale of affairs. we must tum the
page to another. completely different aspect of mycology whi ch came to promi nence in
the middle of the nineteenth ce ntury. an d has remained ffOot and ce ntre ever since .. ,


Further Reading on Fungal Ecology

Baedocher, F. and B, Kendrick (1974) Dynamics of the fungal popu lation on leaves in a
stream, Journal of Ecology 62: 761-791.
Baerlochcr, F. and B, Kendrick (1981) The role of aquatic hyphomycctl's in the trophic
structure of streams. pp. 743-760 (in) The Fu ngal Community: its Organb.ation
and Role in the Ecosystem. (Eds.) E.T. Wicklow and C.c. Carroll. Marcel Dekker,
New York
Bell, A. (1983) Dung Fungi; an illustrated guide to coprophilous fun gi in New Zealand
Victoria Un iversity Press. Wellington.
Cannon, P,E (1995) An ATBI - How to find one and what to do with it. Inoculum 46: 1-4
Frankland, J.C. (1998) Fungal succession - unravelling the unpredictable. i\Iycological
Resource 102: 1-15
Hudson. HJ. (1980) Fungal Saprophytism. 2nd Edn. Arnold, London.
Kendrick, B. (1958) Microfungi in pine liner. Nature 181 : 432.
Kendrick , B. (1958) He/ieoma mono.~pora sp. nov. from pine liner. Transactions of the
British l\"lycological Society. 41: 446-448. [later made the type species of
Slimacomyces Minter]
Kendrick. B. (1958) Sympodie/la, a new hyphomycete genus. Transactions of the British
Mycological Society. 4 1: 519-521.
Kendrick, B. (1959) The time factor in the decomposition of coniferous leaf litter. Ca~Ja
dian Journal of Botany 37: 907-912.
Kendrick, B. (\961) Hyphomyeetes of conifer leaf liner. Thysanophora gen. no\". Canadian Journal of Botany. 39: 817-832.
Kendric k, B. and A. Burges (1962) Biolo8ical aspects of the decay of Pinus sylveslris leaf
litter. No>'a Hedwigia 4: 313-342.
Michaelidcs, J. and B. Kendrick (1982) The bubble-trap propagules of BewmvykeUa.
HelicootJ and other aero-aquatic fungi. !\'lycolaxon 14: 247-260.
Price, P.W. (\988) An overview of organismal interactions i[l ecosystems in evolutionary
and ~cological timc. Agriculture, Ecosys tcms and Environment 2~: 369-377.
Richardson, M.J. and R. Watling (1974) Keys to fungi on dung. British Mycologlc<ll
Society, Cambridge_
Rossman , A.Y., R.E. Tulloss, T.E. O'Dell and R.O. Thorn, ed,. (1998). Protoco ls ror anAl!
Taxa Biodh'ersity Inventory in a Costa Rican Conser\'ation Area. Parkway Publishers, Boone, Nortb Carolina. U.S.A.
Seifert, K., B. Kertdriek and O. /.\i.wase (1983) A Key to Hyphomycetes on Dung. Univcrsity of Waterloo Biology Series, 27. Department of Biology. University of Waterloo,
Tofts, RJ. and P.O. Orton (1993) The species accumulation curve for agarics and boleti
from a Caledonian pinewood. Mycologist 12: 98- 102.
Webster. J_ (1970) CoprophilollS fungi . Tra nsactions of the British Mycological
Society 54: 161 - 180.
Webster, J. and E. Descals (1981) Morphology. distribution, and ecology of conidial fungi
in freshwater habitats. pp. 295-355 (in) Biology of Conidial Fungi. Vol. I (Eds.)
G.T. Cole and B. Kendrick. Academic Press, New York.


Fungal Plant Pathology

in Agriculture and Forestry


We nre utlerly dependent on plants. Directly or indirectly they supply all OUT food .

So it is an ex tremely serious maner if something prevents our domes ticated plaTHs from
Hvi ng up to the ir g~netic potential in terms of growth and yield. Outside influences that
do this nrc said to cause dise~se. and are deal! with by (I broad collection of disdplines
grouped und~r the heading of Plant Pothology. At many universitic~. whole academic
dCJXlrtmenlS are devoted to it; enlire government iabor:!tories do nOlhing clse. This is
bccaul.C OUTCrops, in fidd or forest arc threatened by thouo;ands of disca~s, Plant P3lhol.

concerns itself both wilh


or physiological diseases caused by faClors

such as mineral deficienc ies, climate or pollutants, and with infectious diseasoes caused by
a horde of different organisms: n~mat()(ks, bacteria. myCQplasmas, viruses _ and fungi.
This ch~pter, as you might expect. ""ill ~ concerned only with dise~ses causcd by fungi .
Although insects are our chief competitors for food. fungi are a good second. Crops
in Ohio ~re attackcd by ahout 50 bac terial diseases, I 00 \"ir~l diseases. and 1.000 fungal
di.s.:ases. AboUl 60% of all pl ant disease li terature concerns fung~1 diseases. You h~ve
already read about some of these in tile ta~onomic chapter, at the beginning of this book'
ruSt" smuts. bhghts. down y mildews, powduy mildews. ctc. I am not going to repeat
myself: you should refres h your memory of the org~ni~ms im'olved by lOOking back into
that section. You could nen glance throuSh it now, before)'011 go on with the rest of this
chapter. (That's thc- great thing about a book: it's a wry fie.\ ible te~C"hing machine.) But I
will mention somc additional diseasoes here. just to b["()2.d~n your perspect ive.
E\'cr since Jlt'opk ~ame i:umers, thc) lIave had problems with fungal diseases of
plants. These dis~ases we~(fl ,i.ited upon them by Ih~ gods. as the ancient Romans
thougllt. but were a natur:tl consequence of growing plants in extensil'c pure stands. or
monoculturcs. Whether the fungi grow. swim. fioat. ride or blow from one ho~t plant to
the ne)(t. they w ill find a new home much more readil y in a monoculture th~n in most
n3.tur~\ plant communities. This is bc<:au~e most plant disease fungi hJve a limited host
range. and the very diversity of the comm unity means that ind ividuals of a panicular host
spedes are ofle n well separated. so may escapc in fection em~nating from their relatives.
Although fungal diseases ha\ e beel\ for thousands of years, III~y w~re
not conn.xted with the organisms that caused them until the mid nineteentll century.
Fonunatcly.the scientific re,'oluTion was in fuU swing when the pomo famine by



Phytophrhoru infeslans (Oomycota, Peronospora1es) strock Europe (Fig. 12.1). and il wa,
nOl many years before the relationsh ip between fungus and disease lVas fimuy cstab,
lished. This knowledge has not prevented many subsequent disastrous episodes wh en
particular fungi have ravaged field or forest. A few examples may help to establish this:
the down}' milde w of grape, caused by Plasmopam vi/ieo/a (Oomycota, Peronosporaks).
that almost destroyed the French win e indl.lstry; the chestnut blight caused by
C ..yphoneetria (ndothia ) parasitica (Ascomycetes, Diaponhales). which has killed almost aU mature sweet chestnut trees in North America; the wheat rust epidemics of the
'dirty thinies,' caused by Pucdnil1 grl1minis (Tcliomycetes. Uredinalcs). which mad~ the
depression an alllhe more biUer experience for prairie farmers; the southern eorn blight
epidemic of 1970, caused by Drech;/erl1 maydis (Hyphomycete;;), which destroyed up to
70% of the crop in several com-growing States; the Dutch elm disease, caused by
OphioslOtrUl u/mi (Ascomycetes, Ophiostomatales), which continues to decimate our beautifu l nat ive American elm oyer much of the continent; blue mould of tobacco , caused by
Peronospora tabacina (Oomycola, Peronosporales), which destroyed $100 million worth



> 90%
Fig. 12.1 Progressive attack of Phytophthora infestans on potato plarlt$.


of Ontario tobacco in 1979; the ' bayoud' fungus, which is killing the date palms in the
oases of Morocco and Algeria and speeding up desertification; the whimsically named
but incurable ' bre we r 's droop ' of hops, caused by a VU licillium (Hyphomycetes). which
is now spreading through the hop-growing areas of Britain _
And there will be more surprises, more defeats. and many ongoing battles against
the anny of fungi that encroach on our chosen plants , Why ~ fungi such a threat? Wby
can't we breed totally resistant plants, or synthesizt ultimate fungicides? The answer lies
in the remarkab le genetic flexibility of the fungi, some aspects of which are discussed in
chapter 10, Why, to ask an eve n more basic question, do the fungi attack living plants in
the rm;t place? The answer may well be hiddell in the distant paSt, but it seems to me thai
once there is a di vision between autotrophic and heterotrophic Ofganism~, it will only be
a mailer of lime before some of the heterOtroph$ seize the advantage by attacki ng the
autotrophs before they die, rather than respeclfully waiting until afterward. This calls for
the devtlopmeut of new talents: ways of overcoming the natural defense mtthanisms of
the target organi sms, of penetrating their cell walls, of ensuri ng dispersal from one host to
the next. The fungi have responded nobly to this challenge,
I've already pointed OUI that for thousands of years we didn't know thaI fungi
caused plant diseases; but even now. pinning the blame on the pathogen isn't always easy.
Finding a fungus froiting on a diseased plant isn't eno ugh to allow us 10 blame that
fungus for the disease. Pre-existing disease, and the necrotic tissue that oflen ~ul LS, may
open the way for exploitation of that tissue by secondary colonizers, wh ich mayor may
nOt be parasites themselve s_ We can 't hope to d,:,al with a disease until we know c)(nctly
which organism i$ causing it. Fungi can be unequivocally labelled as p:)Jhogens only
afler a number of conditions, known as Koc h's pos tulates, have been satisfied: ( I) The
fun gus mUSt be consistc ntly associated with the disease. (2) The fungus must be isolated
in Pu[~, axenic cultu re (3 culture on a susceptibk host haS to suffice for obliga te biotrophs).
(3) Wh,:,n the fungus is re-inocu btoo onto healthy host plants, il must produce Ihe original disease. (4) The fungus must then be re-isolated from the diseased plan!. If you have
becn through all those steps, tllere wo n't be much doubt in your mind about the pathogenicily of the fungus in question. Actuall y, even Koch relaxed these postulates a liule
because they were so difficult to meet in their entirety,

Classification of Plant Diseases

There are many possible approoches to an understanding of plant disease and ilS
controL We need to know the prec ise identity of the organism causing the disease, But
before we can hope to cunlrol the disea,e, we n~ed to know much more than that. We h~ve
to establbh the nature of the relationship tk:twee n Ihe funglL'i and its hOSI, how and where
and when il gets inlO the plant; the kind of sym ptoms il causes, the parIS of the plant it
attach: and above all, its life history, whi ch may reveal a weak point at which it may be
attacked, This kind of inform~tion can be treated s Y5tcm~tically in several different ways,
ca<:"h of which can materially lIssist us in oor pl~nning,
Hos t-Pathogen Relationships. To kill un~'s host is not the ideal strategy, Just as the
parasite is setlJing in comfortably to enjoy the amen ities of its new home, the host collapses lind dies, It is almost a~iomatic tha t a hosl and a paras;t,:, that have been assoo:;ialed
for a lung time have c~ \'olvcd to produce a balanced relationship in which the host
doesn't expel the parasite, and the para~ite doesn't kill the host. There is a finely tuned
genetic equilibrium between pathogenicity and re sistance (or tolerance), When a pathogen is introduced to a new host (generally one rc1:ned to its usuul host, but lacking the
a~cumulatcd gene~ for resis tam;e), the results are likely to be Catastrophic, See if you can
pick out these fateful meetings in the ex am ples discussed below.


UF o;:-C!:\'!

~ Sr&U OTEC.~


The adoption of II. parasitic existence necessitated many specialized adaptations.

Some: fungi evolved new enzymes: cellu lases that could dissolve the substance o f plant
cell walls, and p ec:tinases 10 dissolve the cement thai holds plant ce ll s togelher. At one

extreme, some fungi evolved diffusible lollins that killed host cells at long range. and
circumvented the problems inherent in expl oiting living cells. At the othe r extreme, some
fungi be<:ame so intimate with their hosts that they ultimately beeame dependent upon
the living host c~'!oplasm for many things: not just food, but also 11 variety of vital
enzymes. or even whole biochemical pathways. Some fungi produced p lant growth regulatoi"S that either increased or de<:reased the ability o f host cells 10 grow and divide.

In this way, three different kinds of pathogcn cvolved (I) Some are racu fUl ti>'e
parasi tfS: mese versatilc organi.~ms can Ih'c cither saprobically or parasitical ly. Many of
mese are pathogens o f annual herbaceous crop plants. and must survive betwecn growing
seasons as members of Ihe normal soil mycola. This ability make s them particularly
difficult 10 control. and virtually impossible to er~dicate: Fusarillltl oxyspo rum var.
cubense. which causes Panama disease of bananas. can survive in the soil for at least forty
years in the absence of the host. (2) Other fungi are nenot r ophs: basicall y saprobic, but
producing toxins specific 10 su>ceptible host cells. The Monilia anamorphs of Monilinia
species, causing brown rot of peaches and ocher stone fruits. belong to mis category. (3)
The last group are caned obligate parasites or obligate bi otrop hs, ~ause they have
long since iostthcir independence. and cannot grow al all except on or in a suitable hosl.
In fact . me dependence is oflen so complel~ that onl y one host species. or a fcw cultivar.;
of that species, will support a particular race of such a pathogen. The rust fungi. for
example the genus Pllccinia . are good examples of this third category.
Life cycle st udies. Often we can' t decide on the best wa y to tackle a fungal disease
until we know a greal deal abou t the li fe c ycle of Ihe fungus. For example. many o f the
obligaldy biol.rophic rust fungi hale cvolved complex panerns of existence m:u require
IWO hosts (such ru~t fungi are called heteroecious). with an obligatory an nual migfiltion
from one to Ihe other. We may be able to control the fungus hy eradicating one o f the hosts
(~ssu ming that it is neitherof economic imponance. nor rare, of course) wherever il grow~
too cl ose to the other. Perhaps the best- known example of this practice is th e widespread
eradicat ion of barberry (Berberis spp.) in NOTlh America 10 break the life cycle of Ihe
wheat rust fungus, Pliccinia graminis (Teliomycctes, Uredinales), or at least reduce its
opportunities for genetic recombination, since dikar),otization happens on the barberry.
The Spilococo anamorph of \~ntllria inaeqllo/is (Ascom ycetes'. Bi tunicatae) is a
virulent para~ite which attacks me italICS and fruit of apple trees and causes the unsighlly
scab disease. BUI il can also li~e saprobically. because the ascomala of me te\eomorph
develop in the dead apple leaves over the winter, releasing ascospores (the primary inocu
lum) in spring. To control the anamorph requires repe3led spraying throughout the growing season and , as the chapter on fungicide s c learly shows, the fungus quickly del'elops
resistance to e~ch new fungiCide. Removal of dead leaves from the orchard floor, and
sprayi ng with disinfectants while the trees are dom1:tnl. are valuable w:tys of reducing the
amoum of ascospore inoculum released in spring.
PhylOphfhoro infts/Ofl$ (Oomyoota. Peronosporale.s) produces easily detachcd and
subsequently airborne mitospofilogia; but when mese land on a new POUliO plant, they
still release swimm in g spores. The5e are delicate, shon-livcd, and can functi on only when
free water is pre~e nt on the potato leaf. Thi s st:tgc might be described as the Achilles' heel
of the fungus, since minute quantities of fun gicide in the water will kill th e zoospores. BUI
once the fungus i~ inside me host plant, control becomes much more difficult (Fig. 12.1).
II is clear {hal we must ha,e detailed knowledge of the life cycles of pathogcnic fungi if
we want 10 develop optimal disease control str.lIegics.


Stage or host del-eiop mcnt affected. Diseases can strike a crop at any point in its
development. Some imponant diseases, such as loose smut of wheat (Us,i/ago rrirle!:
Tcl iomycetes, USlilaginales) are s~d-bome. Others . sueh as damping-off (Pythium spp.:
Oomycm3.. Perooosporales) devastate tender s~dlings. Yet others anack !he growing or
mature pbnt (the hyphomyeet<:, A/umaria solani, causes early blight of potato: the
oomycete, Ph)"lophlhoro infe!ilatlS.late blight). Finally. some diseaseseause serious losses
after harvest (the hyphomycetes, Monilia and BOlrylis, cause soft rO! of peaches and grey
mould of strawberries. respectively). And many rOO! disease OQIanisms simply :ilt in the
soil and wait for an appropriate !\ost to appear. Their propagules are so 10ngJjved that it
isn't critical which year the host returns.
Some infections, notably !hose caused by smut fu ngi. some rusl fungi, and some
members of the Clavicipltales. spread throughout the plant. and are described as syste mic. Others, such as vascular wilts and heart-rots. are fC$lriCted to a single tissue. Yet
others atlac\;: a single organ, as in fruit or seed di seases, or anther smut. Finally, individual
infec tions of some, like the wheat rust just mentioned, are extre me ly loca1iud. and may
form olliy a tiny leaf spot.
As a systemic infection spreads, or as the number of small, individual infections
incre:lSCs. the host will usually develop physi cal symptoms. such as reduction in growth.
necrotic or discolou red areas. hypertrophied tissues. etc. Each di~ease has its own trademark. producing a particular of symplOms. though some diseases (stICh as smuts) can
rem~in asymplOffiatic for long periods, and in others, such as the heartrots of trees, the
symptomS are cryptic. But soone r or later, the fungus will reproduce. makin g it mllch
easier to name thoe culprit. It will be soollCr in wheat ruSt. where the anamorphit urcdmia
produce spores that can infect only wheat, and pass through several eighHlay ge nerati ons
as an epidemic grows. It wm be late r in the case of smu ts or fUngi. But always
the spore.\ are produced in astronomical numbers. because th e odds are so heavily ag ains t
th eir individual survival.
(t is interesting to consider just how disea.o;es damage their hosts. Damping-off
(P)lhiwn spp.: Oomycot~. Peronosporales) causes breakdown of seedling tissue by enxymie~!ly dissohing tnc pectic middle lamella between cells. and al so produces toxins.
This fungus can obviously derive its food from dead cens. The vascular wilts caused by
.spedes of FII.W rilll>l and \/enie!lIium (Hyphomycetes). ond OphiosliJma (Ascomycetes)
dr.lstically rrouce the upward movement of water in the xylem. The vessels become
bl ocked with hyphae and spores. fu ngal polySaccharides. or tyloses (outgrowths developed by the plant into the lumen of the vessels in an o.ttemp! 10 stop the spread of th~
fungus). Th~ transpiration stream is reduced to 24% of normaL and wilting and demh
inevit:tbly fol low. The dumping-off and wilt fungi don't strike me as paniculo.rly wdl
adapt:d to their hosts.
Ru st fungi ,TeliomycelCS. Ur~ dino.les) are obligately biotrophic. so they don 1 kill
the cells of their h~ts; and the combined biomass of many tin)' rust infections is probably
not large enough to CJUSC a serious dr~in on the plant. So why are yield s oftcn so draslicaU} r~duccd by lhese fungi" Th e answcr becomes clear when they rupture the host
eplder.nis to release their urediniospores. The plants waterproof ski n is broken in so
mo.ny places that in a dry prairie summer it can no longer maintaio turgor pressure. and ils
physiology is disrupted. Some other highly adapted pathogens don ' , kill. or even seriousl) damage. the vegetalivc organs of the plant. BUI they do SUbvert the energy the plant
norma!!y accumulates forreproduclive purp05Cs. Smut fungi (Teliornycetes, Ustilagina1es)
enter the pi~nt "hen the seed germinates, or may already be prc,I-Cnt as mycdium in the
gwi n. The ergot fungus (Clmict'ps: Asco mycetes. Cluvicipitales) gains access through
the stigma of the no"'er. BUI both fungi e\'emuaUy home in on the developing OV"dry. and


ultimately replace il with thdrown reproductive Structures . U we grew com and rye as we
do lettuce. just for the leaves, these diseases wou ldn' t be so serious. And if carrot leaf
blight didn ' t reduce the efficiency of the harvesting machinery (the leaves are weakened.
and break off. leaving the carrot in the ground). it might nOI be taken nearly so seriously
by the growers, since it doesn't drastically reduce the actual carrot crop.
H ost organ s attacked. Discases can be described as root rots, vascular wilts. leaf
spotS. etc. When a disease is first noticed. the fungu s cau sing it will not usually be
producing diagnostic structures. Symptoms may well develop in parts of the plant Ihnl
aren't being direcily attacked: symptoms of root disease will oflen manifest themselvcs in
the shoot system. ConsequeDily. many plant di sease manuals concentrate on describing
and illustrating setS o f symptoms by which diseases can be diagnosed early. Although
positive iden tification of the fungus may not be possible until it eventually fruits. or is
isolated and identifie d in pure culture. treatment must begin as early as possible. to
prevent the build-up of an epidemic. It is easy to lalk about such d isease.') as Allemaria
blight and Cercospora blight of carrots. as if these were easily recognizable entities like
mushrooms or mice. but th e truth is that the early symptoms are often very ineonspicl.lou >.
that they change continuous ly as the condi tion develops. and thut it takeS a very prac tised eye to make an early diagnosis of most diseases. Plam diseases can be class ified
according to the symptoms Ihey elicit:
(I) Necr osis. i<'neralized cell death . is the most extreme reaction. It can affect the
base o f the shoot. as in damping-orr (caused by PYlhium species: Oomycota,
PCrOtlosporales)~ or the lea ves, as in late blight o f potato (Phylophlhora infi"suUls:
Oomycota. Peronosporules): or storage tir.~;ues, as in soft rot of peach<:s. Necros is go.:s by
many names: anthracnose . blight. canker. scab. leaf Spol. shot-hole.

(2) Permanent wilt ing. caused by blockage of the xylem by hyphae or as a reaction
to a fungal toxin . as in wilt oft01llato (caused by \'1micil/iwtl: Hypho mycctes). Panama
disease of banana (Fusarium oxysponjm f.sp. Cljbens~: Hyphomycetes). and Dutch elm
di sease (Ophio5tomu ulmi; Ascomycetes. Ophiostomat:lles).
(3) H ypert rophYOI""hype rphlsia . caused by growth hormones (auxins ) liber~ted by
the pathogen. as in white rust of crucifers (cau.ed by Albugo Cilndida: ()Qmycota.
Peronoo;poral es). ,om smut (Usli!(lgo maydis: T<,liomycetes. Ustilaginales). and peach
leuf ,uri (Taphrina dejornums: Ascomycetes. Taphrinales).
(.4) Lea f abscission . caused by hormones produeed or sti mulated by the pathogen.

as in powdery mildC"<of gooseberry (Sphal'rolheca: Ascomycetes. Erysiphales). and cofft'.: rost (Hemile;(l "asla/rix: Teliomyeetes. Uredin ales) .
(5) Et iolatiun. excessive extension growth. caused by a growth hOffilone (glbb<:re llie acid) produced by the pathog~n. as in 'foolish seedling ' dbease of rice (eaus~d by
GibbtrtllaJuji!':'IITOi: Ascomycetes. Hypocreales).
(6) Pre\'entiun orreproducli on , cau>cd in various ways: Choke of gnls>cs (Epichlo
I)"philw: Ascomycetes, Clavicipilales) prevents flowering: ergot of grasses (C/OI'icep.r
purp/lfea : Ascolll yc~te~ . Clavicipitales) replaces the grain with a fungal scl"rotium: and
anther smut (Uslil(l80 vio/acea: Teliomycete.5. Vstilaginales) replaces the pollen with
fungal spores.
Irrespective of how we classify and diagnose fungal pb.nt diseases. the prime objective of plant path nlogy i~ to thwart the game plan of the pa thogens. and many disc iplines
now contribute to thL, end. The meteorologis t provides data whiCh will allow the plant
pathologist to forecast outbreaks of eenain diseases, lind prescribe appropriate pre\"enti ~e
measures: this teChnique is panicularly valuabl.: in dealing with btl' blight of potato.
Some plan! pathologists have delved into micromcteorology and aerodynamics to prone

206 <..: HAPU:lt TWELVE "

the way conditions within the canopy of a forest or of II field crop affect spore dispersal
and germination. The chemis t sYflthesizes new and e"er 11lQfC: sophisticated fungicides.
1be plan t brewer produces o;ulti vars with built-in resistance to specific diseases.
The plant pathologist is dealing. not simply with an isolated interadion between II
fungus and II plant. but with the overriding effects of climate and microclima te on how
that interaction develops through time. MOSt imponderable of all is the fungus itself
which. with itS endless genetic flexibility. is never more than one j ump behind the plant
breeders and the fungicide formulators. Sometimes there are other complicating factors:
the mysteriou~ wanderings of animal vectors such as the bark bee tle that carries DUlch
elm disease from tree to tree; and since Dutch elm disease: was brought, albeit acciden
tally, by people: from Europe to North America. the control of an plant imports assumes
tremendous importance_ Although some diseases are almost Ubiquitous, many are still
relatively localized. and governmentS try, with mue<! success, to exclude exotic pathogens by quarontine regul ations, employing plant pathologists to inspect incoming shipments of plant products. Much of what we know about long-range dispersal of fungi (see
chapter 8) concerns the spread of crop diseases, which will make themselves fdt, and
hence be docume nted, wherever they appear. Jt must be clear by now that there is no
simple formula for dealing with plant diseases. Each is a special o;ase; and each outbreak
will differ from all others in various ways. Plan! pathologists wil! never put themselves
o ut of a job.

Establishment of Disease
_When pathogen meets plant, a number of factors detennine whether disease will
de'elop. The plant may be entirely w.;isLlnt. extremely susceptible. or somewhere between those extremes. Thc fungu s may be enre mely viml ent. almost avil1llent, or somewhere between the two. The stage of development of the host may be important: damping.
off attacks only young seedlings; ergot ascospores can infect only grasses in flower. The
weather may be critical: many downy mi ldews have an absolu te requirement for free
Pemaps the most crucial phase in the deve lopment of any disease is the initia l
pene tration of the host. A microscopic spore \One in a hundred? One in a million?), lands

F.g. 12_2 Penetration of host by flXlgUS. A: sca~ electronmicrograph; B: iransrrission
eIec~ 01 . ,icrograph.


on a leaf. If the spore is initiating the first in Fe(;tion of the growing season. il is called a
primary Inoculum. and causes II primary infe(;tion. Spores produced by primary infec:tions arc called secondary inocula. So an ascospore of VMlllria imltqUllliJ, liberated
from the overwintered. dead leaves, is a primary inoculum. while the conidia of the Spilocaea
anamorph, prodoccd on the new season's gr(w,th, are secondary inocula. In smuts, there is
only primary inoculum, since the fungus doesn't fonn any further spores until the end of
the season. In either case. tbe more primary inoculum there is. the more serious the disease
is likely to be.
But all this assumes that the spore successfully infects the host, and we mustn't take
that for granted. Many things can go wrong. Does the kaf belong to a susceptible host? Is
the temperature suitable for spore germination? Is free water available. or is the relative
humidity high enough? And will it sta), that way long enough for the spore to germin:lIe
ond penetrate the plant? If our spore is typical. it will die. before or after germination. But
one in a hundred, (}[ one in a million. go on to establish themselves. Some genn tubes. and
the zoospores of some downy mildews, find their way to a stomate. bUI other fungi make
a fron!al assault (Fig. 12.2 A.B). The genu rube establishes an ap pressorium. a small
swelling of the hypha. that adheres \'~ry tightly to the plant surface. This gives the fungus
the physical le verage it needs in order to go ahead with the actual penetration. Now a very
narrow hypha partly digests. partly forces its way through the cuticle and then the cell
wall. Some pathogens always enter a cell, others JUSt as regularly grow between host cells.
Once inside, the hypha broadens out, e"'tends, branches. and establishes on infeclion if the plan t is susceptible. Plant resistance may take a number of forms: the cuticle
and/or the epidermal cell wall may be thick and tough enough to resisl penetratio n. In
hype rsensitive plants. the penetrated cell dies almost at once. This is enough to discourage many parasites. Obligmcly biotrophic fungi. deprived of the kind of nutrientS living
cells provide. will certainly die (of course. i f the fungus is a necrotroph. the h)'persensili\'e
reaction won't faze it). The host may lay down a sheath of material around the invader. and
this encapsulmion sometimes Stllr\'~S the fungus ou\. Specially produced cork layers or
abKission layers (;an effec:tively isolate the pathogen at a later stage: in shOthole disease
of leaves. the infected part simply drops OUt. Many defences are biochemical. /llos.! pathogen~. although their spores obviously land on an enonuous number of different plants,
can infe<:t relativel y few of them (sometimes only one). All the others mUSt in !;Orne way
deter or resist the fungus: this is what we call non-host resistance. Some plants contain
substances like Ilhcnolics. which inhibit the development of many fungi . Others produce
~pccial antifungal compounds culled phytna lexins. also often phenolic. only when attacked. The ge netic aspects of disease resistance are discussed ill chapter 10.

Epidemics of different dise:l..'\CS develop in different Wll}S. The inc idence OfSmUiS is
predetermined by the level of infection or spore contamination of the seed when the crop
is planted. But the severity of most Other d iseases depends on their success. not only in
producing primary infection. but in multiplying their sc(;ondary inocu lu m during the
growing season. This success. of course, is a product of the inler-olction of many faetors:
virulence in the fungus. susceptibility in the host. fa"ourable weather. lack of action by
laissez-faire farmers. Contlitions for th~ development of major epidemics of many dise~ses do nOl h~ppen every year. but some crops are always threatened. For example. if
apple growers did nol spray 820 ti mes per season to control apple scab (the Spilocaea
po",i anamorph of Venturia i"a~l]llGlis). between. 70% and 100% of their crop would be
unsaleahle. If peanut growers didn't spray 8-10 times ~ season for foliar diseases. they
""ould looe 10-75% of their crop. Peaches need foliar and post-harvest treatments if 80%

~'-~ "'::I


~ V l.,.



of the crop is not to be 10SI. Strawberry growers stand 10 lo;e 70% of their crop if it is not
sprayed severaitimes. Gr.lins, on the other hand, can often be protected against their worst
diseases by a single seed treatment. which preve nts losscs of up to 35%.
Let"s see how some of those diseases develop. Apple scab begins the :season with
asco.o;poteS. primary inoculum shot into the air from 3scom3ta dc\'Cloped in last year's
dead leaves. But it immediately swi tche s into anamorph mode: each infection dcriv~d
from a single ascospore soon produces many conidia on the cumnt season's leaves. These
spread the infection to new leaves. and the new infections soon prod uce even more
conidia. The number of conidia increases in a geometric progression, an d unless this
cycle of infection and conidium production is interrupted. the outlook is bad_ You will
find a detailed diSl.:ussion of the difficulties invoh'ed in oontrolli ng apple scab in chapter
13. It is an interesting SlOry, wilh no end in sight.
Other crops are threatened by more than one se rious disease. Potatoes. for example,
suffer from an early blight caused by Allernaria (H yphom~-cetc.~), then from late blight
caused by Phyrop/uh()ra (Oomyeetts). No single fungicide wi!! effectively control both
fu ngi. Mancozeb is commonly used for the Allemaril'. and Ridomil for the PhJlophthora,
and aclose watch is kept on the weather to determine wilen it is necessary to spray for late
Experienced plant pathologist~ perfoml an invnluJble ~ervice when they go OIIt
into a (,eld and d iagnose a disease, but Ihey cannot keep Imck of every diSt!asc on every
crop. And if the development of epidemics. ond the resu lts of control measures. are to b<:
documented. we need so me objectivt ways or decid ing how much disease is preScnt, and
how serious it is. Sometimes these take tile form of dtscriptions. as in Ihe following
excef1'llS from a ke)' for asscssing powo blight: ' Up to 10 SpolS pe r plant'" I % of crop
diseascd: 'Eve ry plant affected an d about one- half of leaf Jrea destroyed by blight: field
looks green flecked with brown'" 50% of crop diseased'. In other cases, visual aids are
pTO\'ided , which allo w farmers to assess the severity of JUnek for Ihem~el ves. Figur~ 12. 1







I L rJ".

' ,







Fig. 12.3 Diagrams uS<!d to assess severity of disease. A: Septoria gluIDe blntch of wheat; B:
Erysiphe pcr.Ydery mildev. of cereals.


shows a chan for assessing damage caused to potato plants by late blight. Fig. 12.3 A
shows a chan used with S~p/Qri(/ glume blotch of wheat. and Fig. 12.3 B one u~ with
po ....-dery mildew of cereals.
Some diseases begin very inconspicuously. The ergot fungus, Clal'ictps purpurta.
can gain entry to its host only through the stigma of the open OO\lo'er. Th is indicates
considerable eo-evolution of plant and fungus. If the fungus did not shoot its ascospow;
during the relat ively brief time that the grass flowers are N'<:eptive, it would miss the boat.
The very precision of this timing may be turned against the fungus if we ~'an develop rJe
eult ivar~ th at flower earlier or later than normal. The disease remain s vinuall)' asymptomatic until the fruit begins to develop, when it soon becomes app~re nt that the resoun::es
allocated for that purpose have been misappropriated. At the other ex treme are diseases
which manifest themsclves as soon 115 infection occurs. The soft rot of peach becomes
visible as a spot of necrotic tissue within hours offungal penetration. This is eaused b) a
spedfic phytotoxin produced by the Monilia anamorph of Monilinia /nlclico/a.
Some fungal diseases kill plants - PII)"loplllhora inln/ans can IUrn a field oi
thriving potato plants into a mass of rotting vegetation (cL the sequence shown in Fig.
12.1); repealed defol iation by the coffee rust fungus, Htll1iil'ia ''ilstarrix (Teliomycetes.
Uredinales), can kill a coffee tree: CryphOlll'Clria p<1r(Isirica and OphiOSI()ma ulmi (both
Ascomycetes) have killed milli ons of chestnut and elm trees, respectively. But many
diseases do no more than significantly reduce the photosynthetic activity of the plan t. So
why urI' they taken so seriollsly? The answer li es in the economics of the situation. Does
the di se3se attack one of our crop plants? Does it significantly redu ce crop yie ld? If th~
ans wer to both questions is yes, lhe disease automatically entcr:; the province of the plant
pathologist. But evcn after a disease has ~en recogni zed as a problem. it is by no me ans

cenain thai anything will be done about it. Economic considerations ~ re a.sain paramount
in rT\3uers of disease rontrol. Some diseases arc ensy and cheap to controL Ie would be
possible to suppress many others " 'jth an appropriate regime of sani tation and prophy,
laxis, but the return in increased yield would not cover {he cost of the progrom. This is
particularly true of many forest diseases. At the Olher end of the scale. greenhouse crops
are often so valuable that e~penshe control programs (from soil fumigation to repe~ted
applications of fungicide) are routine,

Control of Plant Diseases

Control measures range from hot Wilte r treatment of seeds to ki ll hitch-hi killg ~Jl{lres
of Ustilaso tritid, to chilling of fruit to returd spoilage by M on.iIi<l. We try to control
fungal plant diseases in fOUT way S: by ~:l:clU5ion, by eradication. by protection. und by
lmmuni1.a ti on. I'll discuss these in turn.
(I) We can exclude pathogens from suseeptible hosts in a variety of ways. (a) By
keeping them out of (he country: tbis involves quarantine regul~tions and careful inspection of all incoming plant material and <:oil. The price of freedom from introduced diseases is cca<;eless ~igilance. The poIa\o blight fungus crossed the atlantic to Euro~
before an yone knew that fungi caused plant disea<;e. But eve n now. full)' aware as we au
of the threat. pathogens are Still elll1ied inad\'en~ ntl y from continent 10 continent as an
unfortunnte side-effect of international trade. OphioslQm<l IIlmi entered the U.S. from
Europe in 1930. on elm burl logs imported for veneer. Regulations to prel ent the impon
of elm products to Canada were introduced in 1928 and 1934. bu t the di sease was seen in
Quebee in 194.+, having probably been introduced on crates nmde of diseased elm wood.
The con tents of the crates not having an ything to do with elm trees. the crates themseh~s
probably escaped scrutiny. This shows how diflicult it is for b\!reaucracies to cope ~ ilh
microscopic fungi. Other ways of excluding p.:!thogcns includc: (b) growing suseeptible


plan lS in conditions that are inimical to the development of the fungus, and (c) in thc case
of some obligate parasites which cannOt sur/ive without the host, using disease-free seed
or stock.
(2) It i$ worth Ir)'ing to control some pathogens by e radicating them. (a) By rigorously destroying all diseased plants: mOSt of the magnificent old elms in Fredericton,
New Brunswick, and along the Niagara Parkway in southern Ontario have been preserved
by the consistent and immediate removal of any tree found to be infected by Dutch elm
disease. (b) By pruning out affected branchcs (this wouldn' t work for Dutch elm disease,
because the pathogen spread~ though the vascular system of the tree rather rapidly by
means of microconidia). (c) By applying fungicide~; systemic fungicides will kil! the
fungus both outside and inside th e host plant, so eradication is sometimes possible.
(3) In some cases, it is worth protec ting healthy plants from the predictable attac h
of pathogens by dusting or spraying them with protectant fungicides. Through much of
the grow ing season the leaves of French grape vines look blue because they are covered
with a residue of a copper-containing spray which is repeatedly applied 10 discourage the
ingress of the downy mildew fungus. P/asmQpal"(1 vilic{)/a.
(:I) The use of cultivars which an:: immune or resistant to specific pathogens is now
very common. but actual immu niza tion. the induction o f antibodies to particular disease
organisms by challenging the Ilost organism with a dead or attenuated pathogen, which i~
so importan t in dealing with many diseases o f animals an d people, is il!\Practical in
plants: they simply don ' t have the son of immune system found in animal s. Neverth eless.
the h) pers~nsiti\"e react ion. in which the host cell dies as soon as it is penetrated by a
pathogen. can deny some parasites, especially biotrophic ones. a foothold. This reaction.
and the production of specifically antifungal substances, called phyloa1e.~ins, by many
plants. may be regarded as analogous responses.
To give you some idca of what prac ticing plant pathologists arc expected to know,
1 ",ill lht Ihe fungal diseases to wh ich I\\"O crops are susceptible,

Onio ns are attacked by: ( I) purple blotch (Allemliria porri: Hyphomycetes): (2)
neck T()t and grey mould rot (BolTyti! allii. 8mr)"tis squallwsa and Bmrylis cil!er~a:
Hyphomyce tes); (3) leaf bli ght (Borryti! !quam(}Sa). (4) smudge or anthracnose
(Collero/ric/rwn circinans: Coelomycetes); (5) Fusarium bulb rot (Fu.wrium oxyspor"m
f.sp. ((PC~: Hyphomycetes ): (6) downy mildew (P~TOtl{)s{J()ra des/fllelor: OomycOla): (7)
pink rOOt (pY'l:t1ociUlela laTes/ris: Coclomycetc~); (8) white rot (Sclerotillm cepiv()I"lIm:
steril e ana morphs); (9) smut (Uroc),stis magiC(;: Tc liomycetes). Of course. a givel\ crop
will not develop all ofthcse discases at once. but the co ntrol strategies used by farmers are
sufliciently diverse to be wonh outlining.
Fou r main strategies are adopted: (lJ C rop sanitat ion. Since many p~thogens overwinte r and complete thei r life cycle on the dec~ying remains of Iheir host ptant. il make~
se nse to destroy crop debris by burning it or ploughing it under. (2) C rop ro ta tion.
AnOlh<'t "'ay of reducing the populations of pathogcnic organisms is to alternate ~usce p
lible "ith non-susceptible crops. The length of T()lalion depends on how 1000g the pathogen can survive without the host. Sometimes a tWI)- or three-year rotation will do, but
since Scltrorirtln, Colletotric/rum, Prn:nt)Chlleril. and Uroc)"stis can survive in the soil for
~ long lime, rotations of at least five years would be neceSS:lf)' to reduce their inoculum
potential to a reason~bk leve l. Such long rotations are often impract ical. (3 ) ""u ngidd~
trea tments. Seeds are treated with fungicides to prevent dampi ng-ofr and smut. because
the inocu lum for these diseases is seed-born.:. Leaf diseases are difficult to lreat once they
have appeared. and require repeated. and thereforc e~pensive, sprayings. So a protcctant
spray is often applied before any di sease symptoms appear. Preventive spraying may be
repealed if weather conditions or disease forecasts call for it. (4) Res istant c ulth'arlO are


under constant de"e!opment by plant breeders. When available. they arc the most effec_
tive and the cheapest way of avoiding losses.
r-,Iorc spKifically. in onion fields. purple blotch. neck rot and leaf blight are controlled during the growing season by fungicides, and thei r inocu lum potential reduced
after harvest by removing and Qestr()ying pJ:mt residucs. Neck rot is basically a storage
rot. and can be minimi.1;ed by harvcsting the onions in dry wcatllcr, air-dry ing them before
Slori ng. then keepi ng them at OC and a relative humidity CR.H.) below 70%. Smudge
occurs at harvest time and in storage, so drying onions properly, and keeping them at OC
and 70% R.H., is recommended. Fuwrillm bulb rot is difficuil loeliminate.since Fusarium
species commonly survive in the soil as chlamydospores. or grow saprobicaJly on crop
residues. A ~-yearrotation is required to keep this disease in check. and use of resist ant
cultivars isreconunendcd. To become established. tnedowny mildew fungus Perol1Qsporo
needs cool temperutu res and rain or dew on the leaves Gust like potato blight, and for thc
same reasons). A few hoors of dry. sunny wcather will slow Pero"ospora down considerably. The fanner can hdp by avoiding mildew-contaminated sets, practising a two-year
rotation. spraying regularly with fungicide, and destroying infected Crop debris. If pink
root becomes :1 problem. a long rotation will be necessary. White rot also necessitates a
long rotation. though soil treatment with fungicide may deal with small problem areas.
Control of smut is achieved by cQJ.ting the onion seed with a systemic fungicidc. practising rotation, an d using onion transplants if the wi l i!i already contaminated: established
plants will not to.! affected by the disease.
It is instT\lcti ve to co mpare the fungal diseases attacking onions with those found
on ca rrots. Carrots are prone to Alternaria blight (Alternaria daad: Hyphomycetcs);
Cen;:ospora blight (Cercospoffl caralal:: Hyphomycetes); rosty root (PYfhium spp.:
OomycoCl); violet root rot (/?hiZOCfonia CTOCOntm anamorph of HdkoMsidium purpWl!Um:
Basidiomycetcs 1: Rhi.1;octoniacrown rot (Rhiwcwni/! folalli anamorph of Thanatephoru.1
cllcumeris: Ba ~i diomycctes): Sclerotinia rot (sclerotial anamorph of Sclerofinia
.clerotiomm: A.;.comycetcs); and black rot (Slemphy/iw" radicinum: Hyphomycetcs). Are
any genera conunon to both li!itS? Only Alternaria: this gives you some hint of the
diversity of patl:::ogenic fungi. and the difficulties faced. by the plant ~thologist . Which
group of fungi is most prominent in both lists? Dikaryomycotan anamorphs. mainly those
we call Hyphom:. cetes. This is a generalizatio n that holds across the entire spectru m of
plant disease t'unp. Of course. the diseases vary in distribution and in their economic
impact. CefCo,pora blight is favoured by hot. humid wcather. and develops in high summer. while Alternaria blight and Sc1crotioia rot like it cooler. and develop later. RUSty root
is mosl ~\'ere in wet soils, Rhitoctonia crown rot in organic soils after repeated carrot
crops. Sclerotir.ia rot prooobly causes the greatest losses_
Since the r.lnge of control measures avail able to us is much more restri ct<:d tha n the
variety of fungi innJlved. I don'l need to elaborate on Ihis exceptIO say that the measurcs
used will reflect sUI:h fcatures of the fungus as its longevi ty in the soil, the part orthe plant
it attacks. and e.;conomics. In the case of th~ two Rhi:oclOnia diseases, no effective co ntrol
is possible at pre;..:nt, SO the only possible recoursc is to grow carrots in uninfccted. soil. II
is hoped that resiitant varie ties I'il1 C\'entually be developed.

Plant Disease Forecasting

Plant di sease forecasting is not. of course. designed simply to tell the fanner when to
expc<: t an out~~ ak of a particular disease; it is meant 10 give him a chance to apply
preventh e mC.u"res that will cffectively StOP the development of the epidemic. BUI how
does it work'? In :>orne a~as . potato growers can now telepho ne computerized sys tems.
supply specifk weath~r d31a. and receive advice on the necessity or otherwise for crop


spraying to pre ve nt late blight. Simpler programs call for the grower to usc a
hygrothennograph and a plastic rain gauge to keep track of the daily m:llI:imum, minimum
and mean temperature. and dai ly r.linfall on a standardized record sheeLA blightfavoorable
day is recoroed as a . +', and the first spray is dictated by ten successive '+' days. E"ery
seven days afte r Ihis, the need fOf spraying is reassessed, using hu midity, temperature and
rainfall data ,
A weather-timed spray program has been dcvized to keepAlll'maria and Cercospora
leaf blights of carrot from kiBing more than 15% of the leaf area. Jfthis level is exceeded.
har..esting machinery tends to leaT off the weakened leaves, leaving the carrot in the
ground. No fungicide is applied until the bligh t covers 1%2% of the le;U' area. Then
fungicidc is applied before thc ne.'l.t forecast rain, or before the next night with a forecast
minimum temperature of 16cC or high er. At lcast 7-10 days are allowed betwee n subsequen t sprays, which are applied in conditions similar to those for t~ first spraying. Sprays
are not needed before forecast rains when the night temperature will be below 9C, because the fungal spores infect the leaves only when these are both wann and WCI for an
e.'l.tended period.
Although wetness is vital for the suc~essful establish ment of most leaf di sease~. the
.'I.erotolerant powdery mildew fungi are less affected by moisture, and more by the aV3ilability of inoculum: levels of airborne conidia. A thi rd f~clor is the in~reas ing sus ~eptibil
ity of some crops as they age. Programs have now been worked out to detennine the
critieal date for a single application of fu ngicide to forestall powdery mildew of barlcy.
the date of the fi rst spray to cont ro l powdery mildt:w of rubber, and the timing of suc!':essive sprays against powdery mildew of apple.
The value of plant discase forccaSting is, as one migh t e.'l.pect, economic. In the
carrot blight situation. an average of 2-5 sprayings were sa ved by following the program.
The saving resulted from delaying the first spraying. and making subsequent spraying
cOluingent upon the existence of conditions favourabl e to infection. rather than ritually
spraying every so many da ys_ Each program muSI be designed or modified to take into
aCCQunt conditions prevailing in the area where it will be applied _

Forest Pathology
The Americun sweet chestnut, Castane(. dentata. once grew from M;line to Alaoom.1.11 was a fine tree that thrived even in poor seiland on Steep hillsides. Some spedmen~ in the Grcm Smoky Moun tains were 4 melrcs in diam eter and 40 metrcs high.
Chestnut wood was eJucnsh'ely used for fencing and roofing. 10 make furniture and to
build barns. During the burgeoning industrial revolution of the nineteenth century it was
u!>l'd for lining mine shafts and in minc roof suppons, 3., railroad ties. as IclcgrJph poles.
and as fuel. Chestnut trees shared pride of place with elms as street and shade trees.
Appalachiun fanners fau ened th eir hogs on chestnuts. which were also roasted and used in
meat stuffings. The chestnut was the most economically imponant tree in the eastcrn
hardwood forests.
Near the end of the ninetcenth century. chestnut seedlings imported from the Orient
to New York brought with thcm the fungus Cryplwllt'crri(l (Elldotilia) p(lmsirica (Ascomyce t<!~. Dothioro!es). Th is introduction found a defenselcss host in tile American chestnut. The first diseased u-ees were noticed in 19().l in the New York Zoo, and from then on.
the epidemic mounted and sprcad re morsele ssl y. The early issues of Mycologia. thc Jou r
nal of the ~lycological Society of America. contain repeated rather pl.:lintive references to
th e ad\'ancing plague. Despite their agonizing concern. myCtllogists ami foresters could
only watch hdple ssly as millions of chcstnut trees died. and the face of the forests in
eastern North America changed. By the 1940s or 1950s practically all the mature Ameri-



Table 12.. 1 Some Important Fungal Diseases of Plants


Allemaria so/ani

Annillaria mell"(J (Agaric ales)

&1')'riS cinerea (Hyphomycctes)
Brtmia lacllieac


CeratOL),slis jimhriata

Cercospvrella hcrpO/richoideJ

Clul'iaps purpuna

Col/etOlriehulI! /indell!urhimwII!

Dip/ocurpon rosae

E')'siphe graminis + Oidium




potato. tomuto

early blight


forest treeS


StrawberTY etc.

grey mould

Captan. BellOmyl


downy mildew


sweet potato

black rot

wheat. b'lI'ley





clean seed



clean seed

black spot


powlkry mildew


rocHot. butt-rot

shorten rotation

rye, OI:her




Hererobasidion wmosum
(Aphy1lophoraJ cs)



can chcstnU1trees had died. rhough living roots are still sending up sprouts that reach a
fairsizc before being killed by the fungus. and some large tIe<:S siill survive. because they
are apparently infected by a hypovirulent strain of the parhogen (apparently the result of
irs becoming infccted by a virus). All that is hislory now, a nd it's too l;llc 10 do much aoout
it, ex cept to slowly reintroduce scions of surviv in:,: trecs to areas in which the species us".d
to grow.
What of current concerns in foreslry? The lumber industry is a m3instay of the
economy in many areas ofNonhArnerica. but until rece nt years forests were 'mine(!' with
liuk tooughtto repl:lccment. since the resource wa~ ao;sumed to be \'inually infinite. or:lt
least entirety self-renewing. In Canada. a combination of depiction of first-growth forests
by clcarcl,!{ting. heavy 11\.'(: monality duc 10 inseclS nod diseases (which togcrhercau>c an
annual loss of almost 130 milliun cubic metres of wood), and ~xtensive forest fires.
~ombined to produce a po lential wood shor\(lgl:I. Even if on ly 20 million cub ic metres
cou ld be saved. this would provide 39.000 jobs. $800 million in wages and salaries. and
forest products wonh 52.9 billion. All this makes fungal discases important. because they
are one of the m3in faclors contributing to the tosses.

Tree diseases are often distirw::t1y unspectacular in appc:araoce. and their effects are
insidi ous rather than dramati<::. Trunk decays and root rots progress steadily. year in. year
out. Oll<::e established in a tree , they cannot be eradicated. In Canada alone, the various
rots cause a combined loss estimated at 30 million cubic metres of wood each year.
Root-rot caused by Phellimu (Porill) wtirii (Basidiomycetes, Aphyllophoraies) is
widespread in West Coast forests. and ise~pecian y destrUCtive in Douglas f1r(Puudmsugll
Intnzil'sil). Despite e:uensivcsrudies, we still have nocost-cffective way of preventing or
eliminating this problem. Nevertheless, it appears that losses could be reduced by earlier
cutting of infec ted stands, selective culling to favour the establishment of less susceptible
tree species. and the use of red alder in rotation to reduce the amount of Phellinus inoculum in the soil. Other silviculrural practices that would be helpful include: stump remo\al. fumigation. prescribed burning, fertilization. interplanting. sanitation, biologkal
eontrol. and host tolerance Of resistaoce.
Heart-rot caused by Foml's pinl (Basidiomycetes. Aphyllophorales) is also a severe
problem in western forests. Trees with signs of internal decay should be cut because
Fomes pini , unlike many other rot fungi. doesn't cause further decay after harvest. Root
rot caused by Hererobasidion annOS/l1IJ (Basidiomyce tes. Aphyllophorales). an aggressive parasite that infects cut stumps. spreads from root system to root system, and kills
many different con ifers. was the subject of nearly 600 publications betwee n 1960 and
1970. ReCQmmended management procedures include; wide spacing in new plantations;
preventing stump infection by applyi ng inoculu m of Peniophora gigallfea (Basidi
omycetes, Aphyllophorales) (biological control by a saprobic competitor): decreasing
the number of th innings per rotation; removing as muc h of the stump and taproot as
possible during logging; regcnerating by seeding instead of planting; and usi ng resistant
species. At present. the single best way to reduce losses caused by decay fungi appears to
be to shorten the rotation time: in the southern U.S., heart-rot losses in pi nes have been
reduced from 30% to below I % simply by decreasing the age at which trees are harvested.
A survey of forest putholog ists across Canada showed that rOOt-rot causcd by
Armillaria mtlltll (Holobasidiomycetes, Agaricales) Wil!; the only disease placed in the
ten most important diseases for all sill. forest regions. and was among the top three for all
ell.cept the Qucbec region. Whi te pine blistcr rust. ca used by Crenar/iu", ribicota
(Tc1iomycctes, Uredinales). was among the top ten diseases in all regions of Canada but
one. This disease produces spre~ding cankers on branches or main trunk that may evcntunlly gird le and kill th e trce. mc:mw hile producing the accial stage of the fungus . Thi ~
fungus. like many others causing rust diseases. has two h[l!;ts. so eradication o f the alternale host. Ribes spp., has be<:n widely practised. Cronllrlium cQmll1,drae, ca use of the
similar Com~ndr;;r. rust on lodgepole pine and other t~o- and three-needled pines. is not
susceptible to this form of control. be<:ause its alternate host is acommon and inconspicuous herbaceous plant.
In the so uthern Un itcd Slates another ~tem rust called fusi form rust. causcd by
Crona rti"", filsiforme. b responsible for losses of about :530 million a year. T his disease is
on the increase as a result of: (I) the use of infected nursery stock; (2) widespread monocuhure of susceptible tree spo.."cies; and (3) an increase in the altcrnate host. red oak. following improved lire prevention. The only practical contrOl measures are the use of fungi
cides in nurseries. and the breeding of resistant tree cultivars.
Gremmeniella ubietina (Agcomy,etes. Leotialcs) cau,es a serious canker of conifers . <especially pincs. in northea stern North America. The fungus has two raccs. The
Am.:rican race is vcry widespread in Ontario north of latitude 45. and kills many young
trees in their flISt decade. Once more than two metres taU, they seem able to survive the


depredations of this race. But since 1975 the European race has ~n round kill ing mature
pines in New York SUlle, and at a few locations in Quebec. New Bronswid,. and Nev.
foundland. All infected material disco,ere<! has been destroyed. and the situation is being
closely monitored.

Integrated Pest Management

Integrated pest management (rPi\!) is now a concept to be reckoned with. Although
the idea hasnt yet been full y incorporated into agricultural and forestry practice. it is the
nell.tlogical step for plant pathology. This approach considers all the pestS and pathogens
which attack a pan icular crop. and devclops an overall plan to control them . The crop is
considered as an ecosystem. and all factors influencing that system are taken into ac~
count. InsteZld of simply applying chemical sprays at regular intervals, all possible control measures are considered. Sanitation. crop rotation, cultivation practices . sow ing date ,
plant spacing, use of resistant eultivars, di sease forecasting, and biological control. as
well as chemic al con trol. Sprays may be fewer but more complex . with components aimed
at widely differing organisms. such as fungi and insects. Obvioudy, integrated pest management calls for a lot o f preLiminlIJ analysis. and detailed but flex ible planning; processes that arc facilil~ted by computers. We can C};pe<:1 to see ~ 101 more !PM in future.
bec~use il5 sophistiCZltiOn ....ill result in less ell.pensive pest CQutrol. and will reduce ou r
usc of. and dependence on, chemical pe sticides.

Further Reading
Agrios , G.N . (1978) l' lanl
Carefoot, G.L. and

P~tholo g)" .

2nd &In. Academic Press, NcwYork.

E.R. Sprott ( 1%7) Fami ne on the Wind . Rand /".'l cNaJly. New York.

Dickinson, e.H. ~nd 1.A. Lucas ( 1977) Plant Pa thology a nd Pl an! Pathogens. Blac kwell
Scientific Publishel"$, Oxford.

Oisease Compendium Se r ies ( 19171988)American Phytopathologica l Society. SI. PauL


Barley, Bee t. Citrus. Com. COlton. Elm. Grape. Ornamental foliage plants.
Pea, PeanlJt. Potmo, Rhodexkndron & Azale a, Rose, Sorghum, Soybe;m. Straw.
berry. Sweet polnto, Turfgrass. Whcat).
Horsfall. l.G. andA.E. Dimond (Eds.)( 1959I%O) Plant Pathology. Academic Press. New

James. C. ( 1971) A manual ofassessmenl keys for pla nt diseases. Canada Department of
Agriculture Publ ication No_ I-US. American Phytopathological Society, SI. Paul.
Johnston. A. and C. Booth (Eds.) (1983) Plant Pat hologists' Pocketbook. 2nd Edn. Commonwealth M ycolog icullnstilUt c, Kew,
Kenaga, C.S . E.B. Will iams ~nd R.J. Gree n ( 1971) Plant Disease S)'lllibus. Ball Publish~
els, lafaycuc.
Large. E.e. (1962) The Advallce orthe .,' ungi. Dover. New York
Roane . M .K.. GJ . Griffin and 1.R. Elkins (1986) C hestnut blight, other End othia dis
eases, and the gen us End olhia .APS Press, SI. PauL
Roberts, D _A. and C.W. Boothroyd (1972) Fu ndame ntals o f Pla nt Path ology. Freeman.
San Francisco.
Scopes, N . and Ledieu. 1\\. (Eds.) (l979) Pes t and Disease Control Ha ndbook.
Publishers, Croydon.


i!!'i: BIBI.!OT ECA




Fungi have ravaged OUf crops ever since we invented agriculture, As soon as \I.'C stan
to grow many of Ihe same kind of plant close together (a mon(l(: ulture), any other organism s
!hal make a living from mal plant "ill find life much casier. since IRe nCX I meal (called iI host)
is siuing right beside the P',"iOO5 one. Bul until about ISO years ago. we had no idea what
caused mOSI plant disea,es. and until we learn ed that pathogenic fungi were actuallycnrane00" spore.dispe~d living organisms. rather than 'humours' or 'cflluvia of the earth. or of
thunder. oror snakes: we couldn'l do anything about it. So, fOr examphl, the destruction of
the Irish pol;\\O crop by Pilyrophthora il1/l!$ta1l5 (OomycOIa) during the 18405 went compkt.:l)" unchecked. for all it5 terrible effects on me human population. lbe fitst practical
fungtcide: "a, n 'I devised until fony years [ater. by a univer;ilY prof<essor in Fr-Jl1Ce.
Even IOday, over a third of al! crop [o,ses are due to fungal diseas ~s, They cost
Anl~rican fanners alone more th an $)5 billion a year. Some pathoge nic fungi (e.g. P"ccinia
gWl/linis: Uredi naJ<::s) can lxst be conlfo[]ed by breeding resistant plant varieties. Hut all
comm~rcin! npple varie ties ar~ Stl5ccptib1e to applt: scab (cause d by the Spill)cnen pomi
conidial anamotph of the bilUnicJte a'IComycele. Venll4rin illneq"alis). The eondilion~
conduei\ e to infection are precisely known. and oceur up 10 20 lime ~ each growing season.
Unprotec ted orchards muy prod uce no s~leabk fru il al all, so fun gicide ffillsllx: applied 615 lillles each year. Over 5 1.5 billion are now spent, worldwide. on fungicides of all ki nds.
Thi ~ chapter is an exploration of our increasingly sophisticatcd effort~ to combat pathogenic fu ngi with chemicals_

The First Generation: Inorganic Fungicides

In the 1880s. the famous I'i neyard, of Bordcoux were being d~vo,tated by a re~o:nt
accidental introduction from America, P/05mIJfX'Tn \'ilico/ll (Oomy~). which cau5C'S downy
milclew of grope. Strolling through a lineyartl ~t SI. Julien in the :. kdoc. Profeswr MtlJardct was
surpri""d to see that the vi nes bordering the path looked much healthier th,Ul thO$<: further
:lW~y, When he asked the vigncron how these planlS h3d hccn !re:lted. he was told that il was
thc (U,1Om to ~pancr the vines n~ar the p:lth with ,orne: conspicuous, poisonous-looking
~ub~wncc such:ls verdigris, to del~ r pa.~~rs-by from e:l ting the gropes_ MilIard~t. who knew a
lOt about the fungus and its habits (much had been lenmed ~ince the lembl,;: poIato blight
Cptd<:mics), "ent away and COllC(Xt;:t! a ~ariet)o of "'itdlC.~ brew,>. op(imistic that he could
potwn the fungus when it was <ll ilS most vulncmb1e.jw;t after the winddi:'ipersed mitOSlXlrangio
had rekased their delicate zoospores OIl the wei surface of lilt: plant. He: finally sculc:d on 0

blend of copper sulphate and calcium hydroxide (quic ldime), This soon btcamc famous as
Borden ux mi.xtu ~ (in FJench. 'Bouillie Bordclaisc). OIher copper mlphaLe-based fungicides
followed: Burgundy mixture. in which the lime was replaced by sodium carbollUle. and Clle,hun[
miMure, in which it was Il::placed by ammonium carbonate. Although Bordeaux mixture i~:m
efficient. wide-spectrum fungicide. it has !lOW largely bten re-placcd by Comulations of coppo:r
oxide, copper hydroxide. and copper o:l;ychloride.
Bo,deaux mixture. and almost all olher fungicides developed before 1960, are called
p rotecla n l.s: Ihey are toxic to palhogenic fungi. but only if the)' intercepf the fungi outside
the host plant. If !he pL::m t's e ~terior is nOL thoroughly coated witb fungiCide. the fungu s
can slip through the defence. Once inside its host, many pathoge ns can' t be rca.;hed by the
chemical. and have on ly the pla nt's internal defenses to deal wilh. Inorganic fungiCides
al so lend to damage the plant itself(they are phytotoxic as well as fungit oxic), and they can
be washed offby rain. This necessitates repeated spraying during the growing season, and
ultimately leads 10 a build-up of tOllic s ubstances in the soil. Long-leon use of Bordeaull
mi llture on grape vin es has produced con cen trations of up 10 130 ppm C{l pper in the soil.
One early alternative to Bordeaux nUlltuer was su lphur, applied ase1ememal sulph ur
or as lime-sulphur. It is not tmie \0 animals. and is still occasionally used to oonlrol pow.
dery mildews, apple scab and peach leaf curl. but it may 'seorch' leave s, causing them to
drop. and can have a dwarfing effect on planK
M e r curous chl or id e was also found to be an excellent broad-spectrum fungicide
(heavy metals denature a wide range of enzy mes), but its residues can cause both acut e
and chroni c toxicity in animals. Its l D", to rats-the amount OIat will kill halfofthe animals
ellposed to it-is loS mg/kg. and longterm exposurc to even vcry low le"ds of merCury
eventuall y causes sevcre brain d am ~ge (Mi na mata disea>e).

The Second Generation: Organic Fungicides

The orga llo-mercurials were the first of a new generation of fungicides that waS
develope d in respon>e to this problem. T hey retained the pe!;istent fungitox icity of the
mercury, but in rompoonds th~t weer less poisonous to animals (thci r LD" (ra\) ranges
from 30 to 100 mg/kg). The general formula formanyorgano-mercurials i~ RHgX, when: R '"
aryl or ~Ikyl. and X == chloride. acetate. etc. For ellample. the prolCclant organo-mercurial.
uresa n. is 2-m ethuxyet hyl mereurie w35obviously unwise to spray orbroad
cast such to.,ic co mpounds. and fungicides containin~ mercury were mostly used as seed
dress in gs (though phenyl-mercu ric ac~I:\ I ~ wa.~ used in orchards for 20 years until it W3.~
officially proscribed in 1971)_ O rgano-mercurials successfully C{lntroHed many seed-borne
and soil-borne diseases such as rots . seedling blightS nnd dam pi ng-off. but they have now
been erplaeed by less tolt ic chemi cals (sec Thiram. Capt an. Carboxin).
O r ga nn-t;n fungicides were s imilar in principl~ tothe organo-mercurials. They were
often relatively phytotoxic, but one of them. Iri ph enyl-tin hydroxid e, (Du -Ier). was widely
used 10 conlrol potatO blight. It ~ LD.lO (rat) is 108 mg/kg, and it is belie"ed to act by
uncoupling oll idilti ve phosphoryla1ion. An Of'"'.,ano-copper. CQpper naphthena te (Cupr;no!),
cann ot be used as a plant spray or a seed treatment: it i.> a broad- sp~ctnJm biocide and is
used as a wood preserv'ltive .
The phenols. anothcr group of organic funllkid<,s. are like oopper nnphthcnat .. in
that they are disinfect a nts (general biocides) ralher than pruteclants. P\'ntachl oro phen ol
is widely used as a wood prcservati'e. and in the control of slime d~velopm~nt during
poper-making, Ihough environmental coocerns arc now inhibiting some of its applieatioo~
Another phenol. 4 ,6-di oit ro-o-c r esol (ONo e). is used as a disinfectant spray forofchMd
floors. It is aimed at the saprobic overwintering sl:.\ge.~ of such pathogenic fun gi as Vemu,ilj
inul'quaiis. whose tele-omorph develops in dead apple lea'cs. and provides the ascospore


inoculum that reinfecls the host in spring. DNOC is also used in 'dormant sprays' (sprays
which would damage living leaves, so are applied to kill fungi and other pests while fruit
treeS are still dormant). Phenols apparently work by uncoupling o:ddative phosphorylation. The LD", (rat) ofpentachlorophcnol is 210 mg/kg. and that ofDNOC is 25-40 mg/kg.
The 1930s saw Ihe introduction of the d ith lOC",u b amates . an importanl f1mjly of
organic. protectant fungicides with very low phytoto)(icity. There are d imethyl-di thlocarham ates. and ethy lc ne-bis-di lhioca r b a m ates. The dimethyl-dithiocarbamates include
Thi ram, F erbam . and Ztra m . Thiram is used as a seed treatment, to control damping-off
diseases. It has an LD", (rat) of 400-900 mg/kg .
Ferbam and Ziram are used to combat leaf pathogens. and have LOW! (rat) of 17,000
and 1.400 mgi\.g, re$pectively. The elhyrene-b is-dithioca r l)amates (E BOOi) ind~ Nabam ,
" I aneb , L\I anCOlcb and Zineh. The LD",s (rat) of these four fungicidcs are 400, 7.000. over
8,000, and 5.200 mg/kg. respectively. As you can see, the last three seem to be particularly
non-threatening to an imals. But the EBDC fungicides are not really safe: when they break
down . ethylene thiourea. acarcinogen. is formed. This happens wilen EBDC-cofllarninated
plant parts are cooked. Ethylene thiourea causes teratnlogical effects (malformed o ffspring) in rats at a dosage of only 10 mglkg. Despite this drawback. the dithiocarbama tes
are still the most important of the organic, proteclant fungicides. This is because when
copper compounds were replaced by dithiocarbamates. poInto yields rose dramatiCally; the
dithiocarbamates caused w much less damage to the plants. As you might e)(pett. special
precautions are now taken to avoid contamination of food with dithiocarbamate residues.
Wh31 do >'ou th ink th e most important of these precautions might be?
Another important groupof prOletlant. organic fungicides are the p htha limides. The
bc.<.t-knownoftbese is Capta n . though Capta rol (Dirola ta n) alld Fotpet (ph alta n)arc also
widc:ly used. Captan was registered in Canada in 1951 as a foliar treatmcnt and a seed
dressing. often in mixes with other fungicides. It h~s a very short hal f-life in soi! or water.
and has lillie toxicity to Inammn ls: its LD", (rat) is 9,000 mglkg. Like heavy metals, it acts 011
many si tes in the target fungi. so resi stance is unlikely to develop. Captan is widely used 011
fruit crops. especially apples, peaches and str.lwberries, 10 contrOl many pathogens. It has
been estimated that without this fungicidc, 25% of the fruit crop would be losl It is also
used to protect conifer seedli ngs against grey mould (80Ir)"li.5) and powdery mildew. About
13 million kg of Capt an are I.lsed c~ch year. It is the centre of some controversy, since it has
been uUeged to have some carcinogenic effects. and has been partially banned in Swedcn.
Rccrnt North American studics find the accusations unproven, point out that no fully
effective substitutes are available. and suggcst that fruit gro ..... ers goon using it. con<;ervalively. and with strict precautions.
Some quin on cs arc used as organic. protCC13nt fungicides. Okh lone (Phygon) is one
of the most effective treatments currently approved for usc against apple scab. Chlorani l
and Dich lora ne control downy mildews (Oomyoota); Chlaranil is so effective that 5775.000
in vested in it brought a return ofS 19.000,000 to the pea industry in 195 I.

The Third Generation: Systemic Fungicides

A new generation of fungicides was born with the appo:aranCe of the benzimida7.oks
in the 196(k. Benomy l (Ben la te) was the first systcmic oreradicant fungicide-the first to
get inSIde the plant and kit! the fungus where it had pre ... iously bei!n safe from attac k.
Benomy! is apopl astle- it acculllulmes mainly between, rather than in, living cells. and
travels upword in the trunspiration stream flowing through the dead xylem ~essels . Since it
is not retained in Ii"ing cells. it docs not move downward in the phloem. A benzimidazole
fungkide applied neat the ground may lravel up to the growing tips of:l. plant, but not
down into the rooiS. Benomyl is stab!e and non-tox ic-its LD", (rat) is 10.000 mglkg-'"'


it was effective against many a5C0mycetes and theircollidial anamotphs at extremely low
doses. Whereas with Malleb il look 5.4 kg a.i./ha (kilograms of active ingredielll perhccl'
are) tOOOlltrol apple scab, a mere O.3 kg a.i./haof Be nomyl did thejob. S euer still. because
S"nomyl is systemic a!ld stable, fewer sprays were needed. Evcn Benomyl's mode of action
was new- it absorbed to the spind le fibres of dividing ascomycetous nucle i. disrupting
micro tubu le assembly, and so abon ing the division process.
But even Benomyl was not a panacea. It became commercially available for usc on
apples in 1973, and was immediately widely adopted by apple fanners because it oontro!led
aU major fungal diseases of this crop. By 1975. some apple pathogens had begun to de
velop resistance to the new fu ngicide. Before very long, both VClI7uria inaequalis (the
cause of apple scab) and Penicillium cxpatIJum (which causes a storage rot) had become
ratherresistant to Benomy!. Howe ver. th iseradicant fungicide remains activc against many
other disease organisms. and is still widely used. especially in tombination wi th other
fungicides . Although Benomyl acts on a wjd~ range of fungi, basidiomyceteS arc relativel y
unaffected by it. and one possible future large-scale use of Be nomyl is as a treatmelll for
the roots of outplanted conifer seedlings: il shou ld g ive their basidio mycetous
ectomycorrhizal fungi (see chapte r 17) a bead ~tan by suppressing the competition.
Some of the new ambimobile systemic fungicides are also selective-they kill certain
groups of fungi and 001 othcrs. l1Iissbould enable os to treat certain diseases without totally
disrupting the soil myeota. or discouraging the vital mycorrl!izal fungi. Some of the newer
fungicides. for example fose lylAl (Alieue, :lluminum ethyl phosphite) and the acylalanine
Mctala,\:yl, (Ridomil, Subdue, Apron), act selectively on members of Phylum Oomycota:
g~nera such as Pilytopillhora, Pytilium, P{cwnopara. and Peronospora. whicb cause TOOl
TOIS. damping-off and downy mi ldews. MetalMY! has been shown to control many ofthesc
fungi. including PYlhillm and Phylophthoru on soybeans, Phytophlhora on strawberries.
and Plasm()p<JNl on gr:lpe. Af'i:erthe very destructivcepidc:mic of blue m()llld (Pl'ror.ospom
rabocina) whith rQl;ked the tobacro farmers of Ontario in 1979. MetaJaxyl was quickly regis
tered for soil application to control this disease, Atiette is registered in California and Haw3ii
to control simil~r pYlhiaeeoos fungi on avocado and various tropical fruilii. As a bonus. it has
hce n shown to stimulate the growth of c~rtain e ndomycorrhizal fungi.
Ano ther new family of systemic bUI non-se lec tive fungicides are the sterolinhibi
tors. These act by preventing the biosynthesis of ergosterol, the major sterol in many
fungi. Since ergosferol is a basic component of fungal membrones, any shortage will se
verely cunail fungal growth. Ellampics of this new group are Bhe rlano l (Baycor).
Triadimdon (Uar lelon). fenarimol (Rubiga n, nloe), Trifn rine (Funginox, Saprol).
Etacomnole (Vangard), Triarimol (Trimidal). Prochlor:tz (Sportak), and Fendap'.mil.
On apple, sterolinhibitors give good control of scab (Spil(Xaea anamorph of Ve/lluria
ilwequo l i~': Ascomycetes) , powdery mi ldew (Oidium aoamorph of Podosphaao
leucotrkha: Ascomycetes). and cedarapple rust (Gymnosporungil,m juniperi "irginianol':
Tdiomycetes). if applicd weekl y-----{hcy lad long-tenn re , idual activity. On stone fru its.
sterolinhibitors control brown rot (Mollilia anamorphs of MOllilinia spp.: Asoom}'cetcs).
leaf curl (Taphrina spp.: Ascomycetes). stlol-holc (CorJlleum sp.: Coelomycetes). and
cherry leafspot (COCCQfflyces hiemalir. Ascomycetes). In other words, they inhibit the
dcvclopment of a wide range of unitunicate and bitunicate astomyce!es. ascomycctous
anamorphs, and some oos idiomycctes as weI!. Earlier, I mentioned that the dithiocarbamate
protec tant, Maneb. used to control apple scab at 5,4 kglha, could be replaced by the
lx:n zimidillwle systemic, Benomyl. at 0.28 kg/ha. The sterulinhibitorsystemic. Fenarimo1.
will do thc same job at an cvcn lower douge: only 0.065 kglh a.
But as you probably suspect, sterolinhibitors aren't ~rfccl, either. On stone fruits
they don'! work ",el1 against peach scab (Cladosporium, carpep/li/um: Hyphomycetes) .


RhizopllS (Zygomycota) fruit rot, or Alltimaria (Hyphomycetes) fruit rol. And , orne resistance has already developed in certain pathogens, such as powdery mildews (Ascomycetes).

Resistance to Fungicides
As yol.! read through the earlier sections of this chapter. you probably noticed that
the phenomenon of target resistance to fungicides became Lroublesome on ly after the
introduction of the systemic fungicides. It transpired that the resistance was developing,
not because these fungicides were systemic, but because they acted on very specific sites
within the fungus. A broad-spectrum fungicidc li ke mercury poisons so many enzyme
systems- it is a multi-site fungicide-that only an absolutely inconceivable number of
simultaneous genetic alterations could confer resistance on a pathogen. But BCllomyl
operate s by interfering specifically with microtubule assembly in ascomycetes, and it has
become apparent that some target organisms, when repeatedly exposed to Beoomyl, rapidly evolve strains that are resistant to this and other benzimidazole fungicides. This story
has been repeated with each new f~mily of systemics_ Resistaflce has been reported to the
acylalanin es (Metalaxyl), to the carboxamides. and even to some oflhe sterol-i nhibitors.
Dodinc is a pro tectantleradicant (LO", (rat) == 1,000 mg/kg) us~d against apple scab.
Resistance was reported in 1969, after this fungicide had been used exclusively in some
orchards for 10 years. Resistance 10 Benomyl was noted in 1975, after that fun gicide had
been used cxclusively and repeatedly for only 2 years. Orchardists who used Benomyl +
Oodine began to experience resistance to the combination in 1978. We now reali ze that it is
often best to ring the changes: to use mixtures of unrelated fungicides, or to apply a
sequence of different fungicides, as part of an Integrated Pcst Manageme nt scheme. Had
this bt.~n done in itially witll Benomyl, we would probably be expe rienc ing fewer resistance
problems with this fungicide today.

Choice, Formulation and Application of Fungicides

The many d iffercnt d iseases to which single crops are subject often call for a variety
of fungicides. Mctalaxyl, a systemic acylalanine, is very effective against an oomycete like
PilylOplllhora illfestans, which causes late blight of potato, bu t not agaimt an ascomycetow; anamorph like Allernaria solalli. which causes early blight. So the farmer has to u,e
something hke Mancozeb. an ethylene-bis-dithiocarbamatc (E HDC), as welL to control the
Alternaria. Interestingly eoough, the Phylophlhora has also developed some resistance
to ~1e talaxyl, a nd a Meta laxyVMaocozeb mix works ~tter than either fungicide alone.
RidomiL acommcrc ial fcinnu lation of Mctalaxy l. is now sold wit h a48% Mancolcbcon!cn\.
and some othcr acylalani nes arc now sold only mixed with protectant, residual fung icides.
Rc~em stone-fruit fu ngic idc trials have involved mixing or altem~ting stero l-inhibi tors with
other fungicides such as Benomyl, Captafol, Captan, Chlorothaloni l (Bra\o), Oichlone.
Dichlor~n , Dadine and Thiophanate-meth yl.
Tommo powdery mildew (uveif""a lauriw) is well controlled by Propicollazol (Ti lt),
orTriadimefon (B~ykt o n). both sterolinhibitors. while Benomyl is ineffecti ve. Howc,'er.
because Propicollazol an d anot her sterol-inh ibitor. Etaconazole (Vangard). have unde,;irablc gmwth-regu!ator effects on plants of the fnmily Solanaceae, they ~ren't suitable for
use on potatoes and tomatoes.
Perhaps I can place th~ development of fungici\ks and our atti !ud~5 toward them in
perspective by giving a case history. Hops (Hurl"'/"'" /"pulus ), which ar~ ;m invulu~bl~
navour ing:n:dient in beer (they ndd the bitterness), suffer from a destructive downy mildew
caused by Pselldoperollospor(l humuli (Oomycota). At the beg inning of the t"entietll century thj~ was treated wilh Bordeaux mixture. More recently, Zineb, an EBDC was the fungicidc of choice. But this brcaks down to th~ carcinogemc ethylcne thioll rea, so th~ brewing

industry asked that it he abandoned. MClalaxyl is an excellcnt substiru tc, h lll signs of resistance havc appeared, so this ambimobilc sy~temic is now often mi;I:cd with a protectant such
a, copper oxychloride. Satisfactory control involves using (I) resistant hop cultivars, (2)
sanitation-removing infected matcrial, (3) timely application of fungicidcs.
Many systemic fungicides arc almost insoluble in water, and the plant cuticle heps
water-borne substances out as well as in. So if these fungicid~s are dispensed as wettable
powders (WP), after the spray droplet has dried, most of the fungicide wi!! still be outside
the plant. More fungicide gets in if it is supplied as an emulsifiable concentrate (EC), and if
surfactants (to lower the surface tension of the spray and make it spread O>.lt over the
surface of the plant) and humectants (to slow the drying of the droplets) are incorporated.
These measures allow lower dosages to be used. New sprayers are now being developed
which increase the efficiency of application by dispersing the fungicide in finer droplets
than ever before, and by placing an electrostatic charge on the droplets, so that they will be
drawn dire.::tly to the plant.
The most efficient use of fungicides is ohviou~ly as ~eed dressings. Com is grown
on over40 million h~ctares in the U.S., and over 90% ofth~ seed is treated with fungicide.
Wlthoutthi, treatment, it is estimated that yield would be reduced by 10-12% in most yean.
Seed treatment involves some contamination of the ,oil, but since the newer fungicides are
nOI very peNistent, and the amounts applied per hectare are minute, thi s is not a serious
problem. Seed and root dips are also sometimes employed.
Many crops need more than seed dressings if disease is to be adequately controll ~ d.
COllon receives seed tre~tment. in-furrow treatments, and some foliar sprays for 'cotton
rust. Without fungicides, it is estimated that 20% of the cotton crop would be lost. Peanut
leaf spot (Cercospor(l: Hyphomyce tes) is potentially devastating. No resistant cultivars
exist; crop rotation docsn't help in controlling leaf diseases; and the cond it ions17.."i1Iikclioo (leaves wet for4 -6 hours. or near 100% R.H. at temperatures alxl\'e 22"C) exist almost
e\'ery day in the S.E. United States. Fungicides have to be applied every two weeks. Los,es
due to leaf spot diseases are now 2.5- 15 %. Without fungicide, this figure would soarlO 2075%, and peanuts would not be worth growing.
No discussion of fungicides would be complete without some menlion of several
other techniq u~s for controlling or eradicating fungi. (I) Soil steri lization may invol ve
>t~am or dry heat treatment, or chemicals such a;; formalin, chloropicrin and methyl
bromide. Some of the same chemicals are also used to co ntrol arthropods an d fung i in
stored food. The Canadian Government has recently banned f,ve chemical fumigants,
induding ethylene dibromide, which has been identified as a carcinogcn, and mOSl other
a\'ailable fumig~nts are under inveSligation. (2) Ami -mould compounds are often added \0
paints. fabrics, paper, cosmetics. soaps. etc. Many modcm fungicides are good candidat.:s
for such uses, because they have low solubility in watn, an: non-toxic to mammal s. ~re
biodegradable, and arc not very persistent. (3) Mould inhibitors- weak acids such as
sorbic. benzoic. acetic. or propionic acid , or their esters, which are fungus inhib itors rath~r
th3n fungicides- arc added to some foods. Calcium propionate, for examplc, is added to
bread to extend Its shelf-life.

Further Reading
Canadian Journal of Plant Pathology-recent issues.
Johnston. A. and C Booth (Eds.) (1983) Plant Pathologist's Pocketbook 2nd Edo. Commonwealth Mycological Institute, Kcw.
l"o"larsh, R.W. (Ed.) (1977) Systemic Fungicides. 20d Edn. Longman, London.
PhJ1oputhology-rccelll issues.


Fungi as Agents of Biological Control


In recent years we have begun [0 understand the consequences of the widespread
alld !"(."peated IISC of chemical biocides [0 control the host of organisms. such as insects.
weeds and fungi. that threaten human interests. You probably know that while many pests
became resistant to persistent pesti cides like DDT (:I chlorinated hydrocarbon), predatory
bird~ such as the Peregrille falcon suffered population crashes as a result of the biological

accumul:uion of DDT residues. Since we, too. aTe at the tOP of many food webs, this and
O(~r ellamples could hardly be ignored. We soon phased out the more persistent pesticides. at least in North America. and imensified the search for replacements.
;-:ewer generatio ns of pesticides are less persistent, but are often very to)(ic to many
non-wgct organisms. including the natural enemies ofme peSts arKi. not too surprisingly.
humans, The elimination of natural enemies may allow outbreaks of secondary pests. and
rapid resurgence of the target species, once the pesticide loses its activity. To rnJke things
WOl"$ e. some peStS soo n de velop resistance to each ncw formulation. Ne vertheless. many
chem,cal peslidd~s give quick results and a high level of control, nnd no subs titutt~ aft
yet available for most of them. SO we will incvitably go on using Ihem for many purposes:
but it makes good sense to look for less dangcfOlls altern ~tives, Biological control--often
shoruned to biocontr ol-is one of these alternatives.
How does biocont roi work? We bcgil1 by looking for a l1atural pred:lIor. parasite. or
COmlXtitor of th~ organism to be controlled. then we try to shiftlhc ecological equilibrium in favour of this bioo:;ontrol agent so that it can drastically reduce the population of
the target organism. These are simple principles. bU I their practical application is often
;';alU ral enemies of pests and pattlOgens m;\y be few. rare. or inconspicuous. They
may be found only in restricted :treas, or at specific (imes of year. they may have compkx
life hlstones Inl'oll'ing two hosts. and they 01;1)" auack friend as wdl as foc. They may
even hale be",n I,,[t behind when the peSt 'migrated' to a new area or continent. II often
t~kc,; pat ient d~t!C lh'e work to bring them to light. then years to test their host nnge,
dcvelop techniques (0 mass-produce them, and learn the most effective ways und times to
introduce them to the hosl population_

It is encouraging to know that biocontrol h~s alrtudy had several spectac ular successeS-)OU may already be aware of the moth (CacroblaJlis: Lepidopte ra) which was
introduced toAuslralia to controithe pri pear (Opumlc.; Caclaccae) which was taking
o,'er n;t areas of grazing land; and the myxomatosis virus which was introduced to



control the population ell: plosioD of rabbits. I will tell you about a few Dlher famous
victories (which narurally in\'Oh'e fungi). and about some promising or potential applica.
tions of fungi in this area.
Most early attempts at biocontroi pined one arthropod against another, for exampl e, ladybugs (Coleoptera. CoccineHidae) against aphid s (Homoplera, Aphididae).
Bm the fungi are. potentially at least, better biOCQrurol agents than any anhropod, be
cause: (I ) Fungi hau: an eXlIemely high reproductive capacity. (2) Fungi ha ve a "ery
shon generation time. (3) Fu ngi are often highly specific in their action, attacking only
the host with which they have co-evolved. (4) Fungi often produce resting stages or
saprobic phases that can survive fOf a long time when no host organism is available, If you
will also compare these four features with the characteristics of chemical pesticklc~, you
will understand the advantages of using fungal biocontrol whenever possible.
So why haven' t the fungi eomered the market? The problem was panly one of
perception. panly one of proctice. Unde r natural CQnditions, the population of a fungal
parasi te may build up to very high levels. bUI not quic kly enoug h to control the target
organism during the period when it causes the most damage. There's not much advantage
in a fungus killing off most of OUf houseflies in September. when the nuisance has been
around all summer. and the frosts of October would have done the job anyway.
So fungi have 5Cveral potential shortcomings as biOCQntrol agents. (I ) They may
only d3m3ge. rather Ihan kill. their host. (2) They may only reduce, rather than climin3te.
the target population _ (3) They may do both of these things relath'ely slowly. These
outcomes are not entirely sntis f~ctory to humnn s. who are used to the quick action and
high killrate of chemical biocide;. But the nontoxic, target-specific. self-reproducing.
selfperpetuating characteristics of fungi are persuasive incentives for conSidering them
as aitemath'cs, so we are making efforts to overcome their deficiencies.
Sev~ral critical facl~ must be manipulated before we can coont on success. (I) It
must be established th at the biocontrol fungu s is not pathogenic to any economically
valuable orga nisms that might be ex posed to it (2) A large am ount of inoculum must be
avail:l.ble. (3) This mu:;! be properly di>tributed early enough to saturate the target popu
lation well before that reaches its peak. (4) Climati~ conditions must favour grow th.
sporu lation and dispersa l of the fungus_
Whe re can we make effective use of fungi in biocontrol? Pri ncipally in three areas:
(I) contro l of anhropod or other invertebrate pests. (2) control of weeds, and (3) con trol of
fungi causing plant di seases or biodeterioration. I'll exa mine the se area~ in tum, and give
some case histories_ Even where fungi alone cannot give effecti ve biocontrol, Ihey may
often be usefully combined with other agents, biological and/or chemical. in an integrated pest management progrnm. {Integrnted pest management, or (PM. is discussed in
Chapter 12).

(1) Control of Animal Pests by Ento mogenous Fungi

Ar1h ropods. and par1icul.lrly insect~, are our greatest competitors. They dam age or
destroy our crops before and after ha['.'esl, and transmit many fatal or debilitat ing diseases, In the Third World, insect control is often a maUeroflifeordeath. A numbcrof fungi
are lethal p;lrasites ofanhropods: in most cases the fungal spores an:: released in enonnous
numbers. and can infect the host at any stage of itS life cycle_ The spores gcrminate on the
host curicle, the gemltube penetrates the chitinous e.los keleton, and bnmching hyphae
riddle the \isccra. Sporebearing structures of the fungus eventuall y emerge from the
corpse. liberating fresh inoculum. We are only now learning how toell:ploit entomogenous
fungi in biocontrol.


Several of these fungi cause specUcular ep idemics in natural insect populations,
and arc now be ing grown in largescale art ifici al cuh .. re 10 produce inoculum wit h which
we hope 10 induce cpi~mics o n demand. I will mention examples from Ihree fungal
Phyla : these range from establi shed success stories to pro mis ing newcomers, wit h one
t ase o f tantalizing, but as yet unfu lfilled, potentia l. M osl of my examples are illustrated in
Fig. 14.1. Fuur hyphomycetcs have proved so successfu l th~ t spray concentrates eomain
ing their sPores are now sold under trade names as m}coinsectic id es--but don't look fOr
them yet at your local hardware store Of nursery.
(I) B eGlweria bllJsilll1(l (Hyphomycetes) has a fascinating history. In the early 1800s
the so-talled muscard ine disease was ravaging the silkworm industries of Europe . Si lk
wonm died. the ir corpses harde ned. and a whi te bloom appeared on them. The disease
spTad rapidly through silkwonn colonies, but no one knew w hat eaused it. though there
was some notio n thaI il was probably 'environmemal" in origin. Bassi, an Italian Stientist,
subjected the larvae to the mosl barbarous treatments: 'the poor t reatu res died by thou
sands and in a tholl sa nd ways' Eventually he di scovered that the disease was cau sed by an
'infectious prillciple' which he identified as the whi le powder on the mummified corpses.
Hc even re<.:ognized that il was a parasiti c fungus . So orig inaLed, in 1834, the germ theo ry
of di sease-.a mi lestone in t~ history of biology. Conidia of the fungus around whith the

Conidia!>of" .

Fig. 14.1 Genera of fll1gi used in biocontrol of ar thropods.


theory was cO[lceived are now nm<;s-produeed as a preparotiO tl called Bovcrin. and have
been used in Rus sia since 1965 to co ntrol the Colorado potato beetlc (Lep tinoUlrsa:
Coleoptera) This pest, if IdE unchecked, will completely strip potato plants of th eir
leaves. The Boverin, which contains 30 billion conidia/g. is sprayed onto th~ potato
field, t"i cc, at a rate of 1-1.5 kglha, with 15-21 days between applications. Boverin also
co ntrols codling moth (Carpocapsa: L",pidopt"'ra), whos", l~rvae cause enonnoo;s lo>ses
by to;nndling into young apples. In damp seasons. natur41ly occurring B. bas;i'lI1o helps
control chinch bngs (Rlissus leHcoplerl~l) in lawns.
(2) JHetarhizium allisopliue (H yphomy cetes) . availabl e as a comm", rc ia l
mycoinsecticide u.ntkr the namc ]l.Ietaquino, is widely used in Brazil to control Cercopidae
(Homoptcra) (the nymphs are known as spittlebugs and suck large qua[] titics of sap from
their host plan t; the adults ar~ callcd froghoppers) on sugarcane and in pastures. The same
hyphomycete has also been used with great snccess as part of an integrated pest management program in Ih~ South Pacifi c Is lands ofTongatapu and Western Samoa. The Rhinoceros beetle (Oryctes) arrived on thesc islands about 1930. h subsequently killed all newly
planted coconut palms by chewing up the young shoots, and similarly prevented most of
the existing palms from reproducing. The introduction of M elarhiziHm and all
entomopathogenic virus in 1968 soon controlled the beetle. Now, yonng trecs survive,
and old trees once again bear fruit. Mosquito larv ae of the genera Anopheles, Aedes, alld
Culex are also attacked by Mewrhizium. as are sprucc budwonn larvae.
(3) Hirwlella Ihompsollii (Hyphomycetes) causes spectacular epidemics each year
among populations of cilrus rust mite (Phyllocoplnlla: Acarina) in Florida- but ollly
after the fru it has been damaged. Mass -produced as a mycoacaricide und",r the trade
name i\Jycar, it is now sprayed early in the season 10 pre\'ent thc build-up of mite populations.
(4 ) l/enicillimn lecanii (HyphQmycetes) causes natural.epidcm ics in two groJJPS of

plant-sucking pests: aphids (Homoptera, Aphidoiden) which canse malformation and

transmit virus",s, a[]d scale insects (Homoptera, Coccoid<'n) in th.: trop ics and in greenhouse s. Its con idia arc now avai lable commcrcially under the trade names Ve r talec a[]d
Mycotal. Verta!cc contains a main which is highly pathogeni c to aphids, while Mycotul
lllcorporates another strain that i, lethal to g reenhouse whitefly.
(5 ) Nomuraea rileyi (Hyphomycetcs) doesn't yet havc a trade name, but IS nevertheless a[l eff: ctive mycoinsccticide, cJusing high mortal ity in caterpi llar pests (Lcpidoptaa.
NO<:tuid n~) on cabb~ge. clover ~nd soybea[l. It is b~ing intensively studicd for potcntial
large scak agricultur~l applicmion>.
(6) :'!y last example of a fungus being mass -produced for use in biocontro! of
insec t, is Elilomophthom (Zygomycota. Elltomopht hora!es). This may well be thc only
e[l(Omogenolis fungus that most p;:ople will ever see. It infects and kills houseflies, which
for som~ rea>oll u>u~lly crawl into;.m exposed location before dying. The cause of death
can be ascertained from the masses of sporangiophores emerging throu gh the insect's
cuticle. or fro m the halo of d ischarged sporangia aro u. nd the victim. Roland Th axter, who
made an inaedibly produc tive !ife's work of exp lori ng the fnngi growing 011 insects, was
drawn to this field when an epidemic of EmomophtllOra decimated the fly colony ma intained at Hnrvard for experim",ntal purposes.
Although ,pecies of Elllol1loplithora attnck Jphids. housefl ies, caterpillars. and
gra>shoppers, their us", in biocontrol has b<:en hindered by the sh ort lifespan of their
sporangia. and by the great depend;:;nce Qf the fu[]gus on such factors as rainfall, temperature, and ho st density. The spotted alfalfa aphid (Tllerioaphia) was first detected in Australia in \977. It had somehow contrived to arrive without th~ EnlOl1IOphrhora pathogcns
that often kill it in North America. EnfOmophlhora was introduced into Australian popu-


lations oflhe aphid in 1919, aod is apparently spreading. This themc, of a pest reaching a
new country and leaving its parosites or predators behind. is a recurring onc. and often
presenlS an opportunity for biO(:ontrol.
(1) Dutch elm disease is caused by an ascomycete. Ophiostoma ulmi. but is transmitted by bark beetles. In Brit:lin it has recently becn observed that a coclomycetous anamorph.
Phomopsis oblonga. oecurring natural ly in Iht': bark of Iht': elms. discourages or disrupts
the bret':ding of the local vectors. Scolyhls scolyfl/s and Scolyws m,dri.llrialilS (Coleoptera).
1111S may help control the spread of the dise3.'>C.
(8) CoeiomomYCI!S (ChytridiomycoUl) is an obligate parosi te of mosquito larvae,
and sometimes causes heavy monality in natural populations of such important diseasecarrying mosquitoes as Anopheln g(lmbiae, a notorious vector of malaria. Although
natural epidemics are fairly common occurrences, attempts to inf~t !:Irval mosquito
populations were un successful. The reason for this became clear in tik: mid 19105, when
it was discovered \hal Coelomomyces requires a eopepod or an osuacod as an obligate
alternate host if it is to complete its life cycle. This problem may weli prevent this fungus
(rom being e;o;ploited in the bioeomrol of mosquitoes. Yet sin,c these in s~ ts are probably
the most important pests in the world-there are seven million c~ of malaria eat:h year
in Africa. aoo half a million deaths. almost all of them children-strenuous effor1S arc
being made \0 overcome this impasse.
!fyou have sympathy to spare for insects, save it for larval scale insects (Ho moptera,
Coeooidea) and whiteflies (Homoptera, Aleyrodidae}--they are susceptible to the widest

Table 14,1 Some Fungal Pathogens of Arthropods


Trade name


Principal target

Otytridiomycota Mosquito larvae














\ 'ertalte




Colorado beetle. codling moth
DikaJyomycota Citnl'i rust mite
Spittlebug, mosquito 13f\<lC,
rhinoceros beetle, lepidoptemn
Lepidopteran 13J\<le
Whitefl}. scale insects



r-.. nge of etllomogenous fungi. They can be attacked by members oflhe Chytridiomycetes.
Zygomyceles. unitunicale and bitunicale Ascomycetes. Phragmobasidiomycetes, and
conidial fungi (Hyphoffi)'celes and Coelomycetes). Since scales and whiteflies are diffi_
cult 10 control by chemical means, I think we may evetllually use mycoinsecticides
routinely to keep them in check. Another potential application for biocontrol is in the
suppression of anhropods that infest stored food . where it is impossible. for obvious
reasons, to use regular pesticides. Table 14.1 lists some of the actual and potential uses of
fungi in biocontrol of arthropods.
Nematodes. rotifers. copepods, tardigrades. collembola. soi l amoebae and other
microscopic animals are also parasitized or preyed upon by fungi. I use the l.mer phrase
advisedly. be<:ause a number of microfungi (again from scveral major t.a)(onomic groups)
are actually predators of these animals: they ha"e evolved special trapping devices with
which they catch their prey. thereupon sending in hyphae to exploit the newly acquired
substrate. Other parasitic fungi have small spores ofunusua! shapes, which when eaten by
the unSl.1specting animal. catch in its gullet and colonize its viscera. But these stories, the
pictures that will help you to visualize this strange microcosm, and the possible roles of
such fungi in biocontrol. can be found in chapter IS.

(2) Control of Weeds by Plant Pathogenic Fungi

Now for a look at the second m:ljor area of fungal involvement in biocontrol. The
target organism ~ here are higher plants; pioneer species of remarkable vigour which
compete only too well with our domesticated plants. Weeds- they have e,'CIl spawned a
strange verb, 'to weed' (which actually means 'to de-weed'). and evcry gardener pays
tribute on his or her knees to their sucre,s. Until recently, farmers could control wet'<:!;
only with various forms of cultivation, but now they can call on broad-spectrum herbicidcs like Paraquat, and selective weedkillers such as 2,4D and 2A.S-T. These control
dicotyledonous weeds in monocotyledonous crops (fonunately, many of om staple food
plants arc grasses-whcat. com. rice, millet. sorghum. oats, barley, rye). And. of coursc,
they used to help us to keep marginaUy ahead of the dandelions which grow so well in our
lawns. Blit these weedkillers, aftcr being freely broadcast for years. were discovered to
have ingredients th:1t are toxic and terat ogen ic (caus ing developmental defects). And no
herbicide is available to control annual grasses in small grains. Even at their best. chemical herbicides bek Ihe finely tuned selectivity of many plant p:uhogenic fungi, which
often restrict their att acks to a single host species. For adiscussion of how fungi .mack and
damage or destroy plants. refer to chapter 12.
Of the more th an 300,000 plants, a mere 200 species cause almost all of our weed
problems. Two- thirds of the world's worst weeds are prcsent in North Amcrica. and crop
losses caused by weeds in th e U.S. are estimated to cost $14 billion a year. Man)" weeds are
plants which have b.::en accidentally introduced to a new area without their natural enemies. Of I! 7 common weeds in Canada. more than three-quane rs were introduced from
OIher contincnts. The classical biocon\fol strategy is 10 search in the .....eeds homeland for
fungal pathogc:-ns Ih.:lt help to keep it in check there. This section details several examples
of fungi (most of which are iIluslr:lted in Fig. 14.2) which are actual or potential biocontrol
agents fOT .....ceds. Rust fungi (Teliomycetes, Ueedinales) areoften extremely hw..t-spccifie.
and it is filling thot my first two e.umples of fungal herbicides should be members of this
(I) When European blackberry (Ru/ms sp.) began to encroach on ranges and pastures in Chile. introduction of a European ruSt fungus. Phragmidilltn vi(Jlacewn. successfully suppressc<l its spread. Unlike wheat ru~t. this species needs only one ho>t to com-


plele its life cycle-we say it is auloedous-so no other plants were threatened by its
(2) A Mediterranean plant, ChOrldrilla jlllll;ea ( 'rush skcletonweed'), was accidentaUy introduced 10 Auslralia in the early 19005, kaYing its natural enemies behind. It
spread rapidly. and infested hundreds of thousands of hecrares of whea\lands, competing
with the whe at for w3ter and nitrogen, and clogging harvesting equipment. By th~ 1940s
some farmers had gi\'en up growing ",heal. Those who persevered were later able to spr.t),
with 2,4.5,-T 10 control ii, though the cost of spraying vast areas, which in Australia give
low yields anyway. was almost prohibitive, In 1966 a search for potenti al biocontrol
agents was mounted in the Mediterranean region. By 1971 a rust fungus from hal}'.
P"cctll ia chQlldrilliml; was being released in Australia. The; introd uction was so success
ful that almost hal f a million hec tares no longe r need to be sprayed. This progrJ.Ill has
al ready saved Australia 112 times its COSt. in one of the most spectacular SIl!Xesses ever
ach ie ved with biocontrol. There is a footnole to thi s story: on its ho me territor), in the


>\ II~



ACf~""'n ium

Fig, 14.2 Genera of fungi usedi1biocontrolol weeds.

C,,/I.-e /rlol!u,,"



Meditenancan region, Puccinia chondrillina itself has a fungal hyperparasite (Eudarillca

t'aricis: Coelomyceles), and the mate rial being introduced to Australia had to be c~rcful1v
checked to make sure it was nO! contaminated by this hyperparasite, which might have
reduced its effecti veness.
In each of thc examples just given, the fungus is obligately biotrophic, so inoculum
cannot be mass-produced in artificial culture _ In these cases, small amounts of natural
inoculum have bo:en introduced to the area in which the host plant is growing, and further
spread of the pathogen has been by natural spore dispersal. In other examples of fungal
biocontrol of weedJ, of which I will mention five. it has been necessary to mass-produce
the fungal propagules and apply them as a mycohe rbicide spray. This mass ive 1Il0cuium
swamps any host resistance, and if conditions are right, initiates an cpidemic.
(3) Nonhemjoint vctch, Aeschynomene virginica . infests rice and soybeans in the
Unil~d States. It is severely attacked and often killed by the coelomyccte Colletotrichum
gloeol>porioid"s, but in many areas low levels of natural inoculum seem to prcclude
developme nt of an epidemic. According ly, plants were sprayed with a suspension con
taining 2-6 million conidialmL, and 95%-100% of the sprayed plants ,ubsequently su<:cumbed. This was the first practical mycoherbicide, which has now been patented and is
being produced under the trade name Collego_ The fungus overwinters on and in joint
\'~tch , eeds. but this natura l inocu lum must be augmented each year_
(4) Strangler \'in~, Morrenia odoraM , is a weed of Florida citrus groves lhat can
overgrow mature citrus trees. It is now controlled by a commercial mycoherbicide, Devine.
which contains an oomycelOus pathogen, Phytophrlwra palmivora. The fungus causes a
root and stem rOI. and can kjll mature vines in 3-4 weeks . One pint of the liqui d suspcnsion contains nearly a million chlamydosporesfmL, and treats an acre, wh~n diluted in 50
gallons of water. The fungus, once establi~hed in the soil. persists wdl from )'ear to year.
(5) A search has reccmly becn made for potential biocomrol ageflts of water hyaci mh (Eichhomia crassipes) , a beautiful but prolific aqumic plant wh ich has dogg~d
waterways, lakes and reservoirs in many parts of the tropics. In 1976 a pr~\'iously un known species of hyphomycetc, Cen:o.~pora rodma"ii, was found cau,ing a local epi
demic on Eichhornia in Flori da . This fungus has now becn patented as a mycoherbicide.
and is being produced commercially. follow ing extensive r~ ,earch to ensure that it is nO l
harmful to non-target plants or ~nim<l l s.
(6) Another hyphomycete. Acremoflillm zona/urn . which is also pathogenic to water
hyacinth. may y~t be used along with the Cercospora and other agcnts in an integrated
weed control progr~m. but there is still some concern about its host range . since it is
known to attack two valunble crop plants. figs (Fiols) and coffee (Coffea) . This demon "
strates the care that must be taken to cnsurc th at biocontrol agents are without unwanted
side-effects. But since the potential for fungal control of many weeds e:l.isls, it is stlrely a
matter of time before this i, developed. especially as thc more insidious effects of chemi cal herbicides come to light.
(7) A species of Col/elOiriciJllm (Coc lomycetes) is now used m some pUrtS ur China
to controllhe p~rasitic flowering plant CusCilta (,dodder' ). which cnn be a serious weed
on cert~in crops_
(8) Phomopsis cOfll'olvlIlllS i, being te,tcd in Canada as a potential biocontrol agent
for field bindweed, CO/lvo/nil", arvensis. Other e!>ample5 of actual or potcnt ial
mycoherbicidcs are listed in Table 14.2.


Ta ble 14.2 Ac1uai (A) a nd potential (P) appUcalioD5 or fungi in weed rontrol
Fungal Biocontrol Agenl

Weed Tatgel

(A) Puccinia ch()f1drillil1(1


Chondrilia ju/lua

(A) Phragmidii,m violnetllm


(rush skeletonweed)
R"bu$ sp. (blackberry)

(Al Coi/tlOtrichum xanthii


Xanthium spino$UIII

CA) C gloeosporioidu
(Coc:lomycetes) COUl'gO

Atschynomene virginiC/l

(Al Phytophlhora p"imil'orum

(OomycOfa) Devine

MOff1mia (X/orata
(strangler vine)

(P) Ascoch)"/a pleridium


Pleridium l'quilinJim

(p) Co/lew/richum mail'Orum


Sida spinosa
(pric!;J.y sida)

(P) ColielOirichum delllatium

Cassia /XCiden/ClIiJ
(coffee senna)

(Coe lomyceles)


C. demarillm

(bathUfSt burr)

(northern joint vet,h)

(bracken fern)

COrNo/vu/us afllfnsis


(field bindweed)

(P) C c()ffQt:/es

Abu/ilon rheophra.fli

C. gloeosporioides


Jusrimw decurrens

Crop infested &


wheat. Australia
pastull:s. Chile
r.rngeland., Australia

rice, soybean, U.S.A.

cilnJS, Florida

pastures. Britain

cotton. soybeans, U.S.A.



sorghum, U.SA
lima beans, U.sA
rice. U.S.A.


(winged waler primrose)

(P) AcremOlliljm sp.

Cassia $uratll:llsis



(A) AcmnQnimn diospyri


Dio$pyros virgillialUl

(P) Cerwspom Ilm/anae


umlWUI cornara

(Al Cercospora eUfX,:urii

Eupatorium adelloplwnull


(crofton weed)

(P) Alternaria c(Usillt

Cauia obtusifolio



(P) Alr..mario macra5pora


Anoda crisfara
(spurred anodal

COtton. U.SA

Anoda eris/ala

COlton, U.S.A


cotton, U.S.A

(p) Fu.<ariwlI lar..,irilllll

(Hyphomyce les)
(P) Fusarium /"Ieri/ium
( Hypoomycetes)
(P) Fusarium lat..rilium



eri~'/(j /(J'

Sida spimm,l
(pric kly sida)

pastures, Hawaii
r.Ulgeland. U.S.A.
rangeland. Hawaii
Au stralia
COlton. soybean. U.S.A.

cotton. soybean. U.S.A.


Tabl e 14.2 Actual (A) and potential (P) applications or fungi in weed control, cont.
Fungal Biocontrol Agent


Crop infested & Area

(P) Fusarilun solani


Cucuroi/a feutJ1l.l
(Texas gourd)

( A) Cerrosporo rodllwnii

Eiclwmio crossipes
(water hyacinth)

..".ater. tropi,s

Eichomin crassipes
(water hyacinth)

water. tropi,s

Eiclwmia crllSsipes
(water hyacinth)

water, tropics
waler. tropics


Eiclwmiu crossifles
(water hyacinth)

(p) !kferotinia sc/erolionllll


Cirsillnt arvenu
(Canada thistl c)

(P) Phomopsis cOIn'olm /us


CO/lI"O/vu/U$ nn'lmsis
(field bindweed)

(P) Acremonium co/w.1ll1n

(P) Cuwspo ra piaropi

(P) FlI50rillm Itlseum

many crops. Canada,

many crops, many

(3) Fungi in Bi o( ontrol of Other fungi

Thi s third area in which fung i have bioconlrol pote mbl m:ly initially seem 5tr.mge,
but I'm sure you will quickly appreciate the logic of $Ctting a fungus to con trol a fungus.
The main reas ons can be st:lte<.l very briefly: (A) Some fungi are par:lSitic on other fungir" e already mentioned one example in discussi ng the biocontrol of ChQlldrilla in AuStra
li a, (B) Fungi ofte n com pete strenuously with one another for substfme. (C) Preinoculation
of a host plant with avirulent strains of some normally pathogenic fungi, or with close but
nonpathogenic relatives of those fungi. can protecl the plant from aU3ck by virulent
strains of the same fungi_ ' will discuss several examples of each approach,
( I) Spha erellopsis filum (Coelomyeetes), oftcll discussed in the literature unde r an
older name. Darillcafilllm, is parasitic on many rust fungi (Teliomycetes, Ured inales), It is
credite<.l wi th keeping 50 me rust disea:;ts down to low levels in nutural host populations,
and it has been proposed as a potential biooontrol agent against the heteroecious rusts,
Crr)l!(! rlium 51rooi/ilwm and CronQrlillmjusijofme (which eaus~ serious blister rust diseases of pines), while they are growing on their other hosts, oak uees, The fungus can
mo"c from the oak to the pine only ifteiiospores are produced, so it is signifi cant that in
some natural populations of Cron(1rtilllll strobi/inum o n oak, 93% of lhe rust sori were
found to be infe\:led with Sph./lael/opsis, and only 0,8% formed le li05pores. Rescareh1:rs
ha,e concluded that the parasite was more likely to conlfol C. strobilinum, which was
growing actively in the oaks all summer, than C'/u:;iforml!, whose few ... ecks of activity
on th1: host did nOI give the Spho.ereliopsis enough lime to colonize the ru~t an<.l control
it. The future of Sphatrel/opSiJ in rust control is 5till uncenain,
(2) Tubt-rrulillQ maximll (HyphomycelCs) is anOther parasite of rust fungi that is
actil-e against CronGrtiWII ribicolll (Tcliomycete5, Uredinnles), the cause of white pi ne
blister ruSt. but. although ils biocontrol potential haS been hinted at by various forest
pathologists. il has not yet been exploited.


Table 14.3
Some n~tual and potential applications of fungi in the control of fungal plant dIseases
Target fungus

Rhizoc/(mia so/ani

Disease & ho>t(s)

Biocontrol fungus

damping-off. roo!
rot. stem C':lnker:
many ~rops

Trichodemm viridt

root disease: trees

Trichodemw viridt (Hyphomycetes)

silverleaf: plum

Trichodem41 viride (Hyphomycetcs)

H(/erobasidwn willosum
(Aphyll ophorales)

root disCa5C: ITe<:S

Trichodenna viride (Hyphomycetcs)

HelerobasiJion anllOSUIIl

root disea.>e: I..--e<:S

Peniophora giglllllea
(AphyJ lophor.ll cs)

Annillnria trU!IIM


Slere"", pllrplmmm

Pylhium spp. (Oom)'Cl'ta;)

Sclt!,mium rolfsii


stem blight:



Venicilfjum fimgicn/a
fl/sarill/!l m.!eum
Phyroplillrom cinllamomi

Vatidllium alboa/rlml
(Hyphomycctes )

dry bubbk:

TOOt rot: Ir~S &

herbs (48 fwli!ic~)

wilt: COllon

Venicillium dalrli<le
(Hyphomyce tes)

wilt: eggplJJ1[

Venicifllllm tUllrliot

wilt: mim

Aill'mnri(l :in"I'(I(

kaf spot: b;>ans

Cln"iceps pUrpUTeli

ergo!: gr'->,;cs

Sphaavrileca fi(liginl'(I

TrichlXkmw h(lJII(1/wn
Tric/rft!mm Irar.,iamun
Tr.chlJ(lemw sp. (HyP/1Ol1\yCClcs)

seedling blight: com

Chatlomium glahoslIIn
(1: nitunkalal!)
Le:/Copaxil/u,! sp. (Ag:mcnJes)
\ "or-irillium al/H)olUrum
(H: pholTIy~'Ctcs)
Ta!<lfoltl)'ce.r jla<'us (Eurotiales)
\i-nicilfillln nigrescel1s

poy,dcry mildew:


Ai:un.aria lenuiJ.r;'n(l
F!I.lUT;Um!wn (Hyphorn}cetes.)
Cicinnobo/u! aSaI;; (Cot!omycctes)


Tahle 14..3 (con1.)

Some actual and potential application.s of rung:! In the control of fu ngal plant disea'ieS
Target fomgus

Disease & host(s)

BiOo::ontrol fungus

CrQlII:mium ribicola

blister rust: pines

7id>erculirw maxima

Cronartium slrobilinllnl

blister rust: pines

Sphoerrllopsisjilum (Coelomyccte$)

Pllccinia spp. (Uredinalc;)

rust: many crop:;

Sphnuellopsis ji/WI! (Coclomycetcs)

Sderorinia sciemlio rum


watery rot: m:my

Coniorhyrium minitallS


Gaellmllnnomyces grominis

take-all: wheat

Phiolophom mdicicola

Crinipellis pemiciola
( Agarieales)

witcheS: broom:

CltuiJJbolf)lIIl! lIma::Ollcnse

BOII"pi s cinerea



grey moul d of

Gliodadilllll rosewlI

(3) Cicilln(Jbo/lIS uSa/ii (Coo!iomyccles) pard~itizes powder) mildews (Ascomycelt"S,

Erysiphales), and is now bei ng used as a spray to control Sphatrolheca on greenhouse

(4) CfadobolrYllm ama.:o nense (Hy phom ycetes) g ivcs control of Crinipdli~
pemiciosa (Hulobasidiomycetes. Agarkales), wh ich causes a seriou, dise~se of cocoa.
called witches' broo m.
Competition be twee n fungi is the area ill whi ch biocont rol of fungal pathugen s has
achieved its gfl:ate~t succes~s. Species of Trichoderma (Hyphomycctes), green moulds
common in some forest soils, arc powerfu l antagonists 10 many palhogens.
(5) Trichoderma \iride both parasitizes lhe hyphac of many othcr fungi and produce,~ an antibiotic. This double-barreled appro3ch allows il to deal effectively with soil
pathogens such as Rltiz()Ctol!ia solani (a sterile basid iomycetous anarnorph that causes a
variety of diseases on many hosts). and Armillaria mel/eo (Holobasidiom >'cetes, Agaricales),
wh ich kills ma ny species of trees.
(6) h iehoi!emm han;ianum, ma,s-produced in \: u) ture and applied to soil. controls
Sclerolium rolfjij (another sterile fu ngus which causes diseases of many hosts) 011 tomatoes and peanuts. A ph:umacemieal company is developing T.ltar:iantmt as 11 commercial
biocontr{)1 for SclerotiulII rolfsii_ Thi~ could be indirectly frustrated by the fact that peanUl~ arc very susceptible to anatk by Ctrcospqra (Hyphomyceles) ..... hith causes a serious leaf-spot disc3<;e. Repealed fungicidal sprays ne<:ded to comrol the Cef{;o.<[JQ'" also
reduce Ihe population of Trichode mw and lend to an increase in stem blight caused by
Sclerotium rol/sii.
(7) Ncyertl1eltss, in France, Trichodemw spray concenlrate is competi tive in pri ce
wi th the we ll-known S)"$lcmic fun gicide. Bcnomyl. and is u~d to control Verticillitlm
fimgico/a (Hyphomycetes). a o;erious p;ilhogcn of the cultivated mushroom, Agaricus
bnlllnesctns (~'garicales).


(8) Some basidiomycetous pa thogens of trec~ often gain entrance to their host
through wounds. It has been found thatappii cation ofTridwderm<l s!X>ccs to fresh wounds,
such as those caused by pruning of plum trees. win pre ..ent subsequent infection by
Sfueum pllrpll/"eum (Ho!obasidiomycetcs. Aphyllophorales), which causes sil verleaf disease:.
(9) Freshly cut tl"et' stumps painted with a Trichodennll spore suspension will nOt be
invaded by Helerobasidion amwsllm (Aphyllophorale.s), a vcry serious root pathogen
Ihal ~preads from tree to tree through root contact.
(10) A comme rcial preparation of the saprobic Peniophoro giganlea
(Aphy llophoralcs) is available for treating newly cut pine stumps to prOlecl them from
invasion by Helerobasidion.

( I I) Spraying apple leaves with spore suspensions of Chaelomillm g/obosum (Ascomycetes, Sordari ales) reduces infection by the apple scab fUngus. the Spiloc(!ea
llnamorph of Venturia inaequalis.








:;~ iJF PE.CCe

Fig. 14.3 fungal pathoge!"\s controledby Trichodermit and Peniaphora.

j .. . , -,,t

'; <;::C'
,. , .


( 12) Prou,;tion from some soil -bome disea~s can be obtained by trcating secds
with biOC'()nlrol fungi. For cxample, spores of Cha~lOmium will protecl com
against seedling blighl caused by FUJariml1 ros~um (Hyphomyccles). Spores of Penicil
lium spp. (Hyphomycctcs) will confcr s imilar protection on peas.
(13) Eggplant is started in pots berore outplanting. Inoculation of the potting me_
dium with spores of TalaromyceJ j1a vus (Ascomycetes. Eurotiales) has been found to
reduce the incidence o f will caused by Verticillium dahliae ( Hyphomycelc by 67%_
76%, and 10 increase yi eld by 18%-54%.
Preinocu lation or, as il is sometimes called. cross-protection. is now receiving
serious altenlion from plant pathologists.
( 14) Applicatio n o f wea kl y pathogenic strains of Vuricillillm alboa/rum
(Hyphomycetes) protected cotton plan ts from more virulent strains of thc sam~ wiltdisease fungus. This protection appears to 6cc rue from a kind of immunization process.



, C






r.g. 14.4



~biocor(roIagentsand theJ" targeI p<lthogens(see text).


The ",eak palhogen. while doing little damage, stimulutes the host plant to produce
phytoa1e:tins---speclfically antifungal compounds-which are then ready to repel suhsequcnt attacks by more pathogenic strains. Sometimes different species. rather than different strains of the same species, an: used to induce cross-protection,
(15) For example, the weakly pathogenic Verlicillium nigresceflJ (Hyphomyceles)
induces resistance in mint plants to the more pathogenic. wilt-producing Verticillium
In 1980. Ontario growers har..ested 33,000 tonnes of peaches ,,",onh over 514 million, But another S7.000 tonnes had to be imponed. Ontario should be growing more
peaches, yet peach production is graduaUy declining. Why is this? [t is largely due to a
fungal dise a>c called peach canker, caused by the coelomycetou. Cylospcra anamorph of
ul.eosloma (Ascomyce tes). The CylOspora can't attack healthy trees: it can gain access
only through wounds, such as those regularly caused by pruning. Infectiolls begin and
spread during fall and spring dormancy. Each year the cankers spread. yield decli nes, and
e\'cntually the Iree dies. Because of the deep- sealed nature of the disease. only limited
chemical control has been possible. even with the newesl fungicides. FonllnUttly. thtrt is


"') \ '' ;




Fig. 14.5 ....\ore f~ bioconIrd agents and lhei" target patlq,ti IS (see teJd).


now some prospect of biological control of peach ~anker by species of Trichoderma and
Gliocladiu ffl (Hyphomycctcs). " hich are highly competitive saprobes. and also actively
parnsitize many fung i.
Grey mould of ~trawbeni es is caused by Balrylis cinenm (Hyphom)cetes). and has
usually been combatted with the fungidde Capt:m. In recent years. the advisability of
usi ng Captan ha s been quest io ned. Fortunately, it has been estab lished th at the
mycoparo.~ite Gliodadillm roUllln (Hyphomycctes) can also control Balryljs. We know
that the crucial ,tage in the de\'elapment of the problem is during the flowering of the
Strawberry, well before the fruit fonns. An ingenious delivery sySte m has been designed. in
which honey bces leavi ng the hi ve a re automatically dusted wilh about 50,000
Glioc/adil,m coni dia, which they deliver directly to the flowers.
The years wad should ~ many advances in biocontrol by fungi: certainly our
increasing knowledge oCtbe ad'~ effects of chemical bi ocides on tbe biosphere and on
ourselves can only ac celerate tile search for alternatives.

Further Reading
Anon. (1980) Proceedings of\\'orkshopon insect peS! manageme nt wilh microbial agcms.
Boyce Thompson I nstirut~ . Ithaca.
Baker, K.F. and RJ. Cook ( 197.l.) Biolo~i cal Con trol of Plant P..llbogens. Fm:man. San
Baker, R. . P. Hanch ey and S.D. Donarar (1978) Protectio n of carnation againsl Fusarium
stem rot by fungi . Phytopathology 68: !495-150 1.
Bastos, C.N . H.C. Evans a nd R.A. Sa mson (1 981) A new h}~rparasit ic fun gus.
Cladoboll)"W1l am07.0ntnSf . with pote ntial for control of fungal pathogens of cocoa. Transactions of the British Mycological Soci~ty 77: 273-278.
Burges. H.D. (Ed.) (1981) Microbia l Control of !'ests and I'lant Disuses 1970-1980_
Acudernic Press. New York.
Charudattan. R. and H.L. Walker (1982) Biological Control of Weed s with !'Iant Pa thogens. Wiley_t-.'w York.
Cu!len. D.. EM. Berbce and J.H. Andrews ( 1984) Ch(1elOm iwlI glabo.lllm antagoniles the
apple scab pathogen. Vetlm ria in(1eqlwlis. under field conditions. Ca nadian Jourmil of Uolany62: 181 -1-18 18.
Culkn. J . ~I., PF. Kable and ~\. Can (1973) Epidemic spread of a IIlst imponed for biolog ical control. !'ialure 244: 462464.
Ferron. P. ( 1978) Biological control of in sect pest, by entomogenous fungi. Ann ua l Re\iew of Ent omology 23: -109-442.
Frcem~n. T.E. (1981) Use of con idial fungi in biologic al control. pp_ 143- 165 (in) BiologyofConidill1 Fungi. \ '0). 2. (Eds.) G_T. Cole & B. KendriCk. Academic Press. Kew
Glltterid&e. RJ . and D_B. Slope (1978) [!ffec t of inoculating soils wjth Phinloplrora
mdicjcola var. graminicola on takcall disease of whem. Plant Pathology 27: 131135.
Harman. G.E., I. Chel and R. Baker (1980) Trichodt nna hnmwllm effec lS on seed :md
se~dling di sease induc ed in rudi~h and pea by Pylhiwn spp. or RM:OClon;a .!Clani_
PhytopathQlogy 70: 1167-1 112Hasan, S. (198 1) ,.l,. ncw strain of Ihe ruSt fungus Puccini" Ch(Hldrjlfilla fOf" biological
control of skeleton weed in Australia. Annals of Applied Biolo~' 99: 11912-1..


Kelleher, J.S. and M.A. Hulme (Eds.) ( 1984) Biological Control Progra mm es aga ins t
Insec ts a nd Weeds in Canada 1969-1980. Co mmonwealth Agricultural Bureaux,
Farnham Royal.
~, B. (1981) PestS contrOl pests: bur at what price? New Scientist 89(1236): J 50-152,
Marois, J.1 .. S.A. Johnston, M.T. Dunn and G.C. Papavizas (1982) Biological control o f
Verticillium wilt of egg plant in the field. Plant Disease 66: 1166-1168.
Roberts. D.W. and R.A. Humber ( 198 1) EnlomogenOlis fungi. pp. 20 1-236 (in) BiolOl:Y of
Conidial Fungi Vol. 2. (Eds.) G.T. Cole & B. Kendric k. Academic Press. New York.
TeBus!. D.O. and G.E. Templeton ( 1985 ) Mycoherbicides: progress in the biological
control of weeds. Plant Disease 69: 6-10.
TeBeesl, D.O. (Ed.) (1991) Microbia l Co ntrol of Weeds, Ch~pman and Hall. Ncw York.
Templeton, G.E.. D.O. TeBeest. and R.J. Smith, Jr. (1979) Biological control of weed s with
mycoherbic ides. An nua l Review o f Phytopa thol ogy 17: 301 -3 10.
Trutmann. P.. P.l. Keane and P.R. Merriman (1982) Biological control o f Scl"rolil1in
sderoliorum on aerial parts of plants by the hyperparasite COlliOlh)'rium minilll1l$.
Transaction s of the British ]\'Jyco logicn l Society 78: 521 -529.
Webber. J. (1981) A natural biological contrOl of Dutch elm disease. Na ture 292: 449-




Fungi Exploiting
Microscopic Animals


As a tiny soil nemauxle wriggles along, its head passes through a tiny hoop. Its
body follows, sliding smoothly through . JuSt as it is about to clear the hoop. th is suddenly
innnleS inward and grips the wenn tightly. Thra~h about as it will, the wonn cannot
escape. Soon its tail end triggers another ring- trap. It has been captured by a fungus, and
itisdoomed todic(Fig.IS,\).

.' "

I I ,

Fig. IS. 1 A nematode caught by"~ constrictngmg traps.



Fungi are usually thought of as being slow and insidious in their lifestyle, insinuating themselves stealthily. silenlJy penetrating and permeating the substrate with their
hyphae and their enzymes. 11 come, as something of a shock to encounter fungi tllat set
traps to catch animals, UT have spores that instanlllneousl y inject their contents into their
unsuspecting targct. Yet these fungL and others almost equally bizarre. el(ist in the microcosms of the soil. the compost pile and the rolling log.
Relali\'cly few fungi attack large animals, and those which do are often specialists
with a taste for keratin. or opponunists able to STOW at the body temperature ofoircls and
mammals, or to attack inju red !ish. BUI as we desccnd the scale of size. we eventually
reach 11 point where any physical confront11tion betwee n fungus and animal becomes a
much more evcn contest. The tiny animals that roam through the soil make eJlcellcnt
proteinaceous dietary supplements. so perhaps it is not surprising that the 150 or so fungi
that have adopted this 'carnivorous' lifestyle are drawn from four of the fi~'e major fungol
groups (Chytridiomycota. Oomycola, ZygomyC()la and Dikaryomycota). l1le mechanisms
they have evolved in order 10 exploit this resource are diverse and ingenioU!;. We will
consider eleven such mechanisms.

FIS- 15.2 A: Calenilria (OrytrK~ota)i1fect~ nematodes by malic zoospoi"es;6: Myzocy'ium

l~wtaJ releaSll) inl!ctilie moIie zoospores; C: Hilptoglossit {Oc.m)mtal reIca~inror.e
harpoon eels (sec Frg. 15.31;D: ,\-Ierid (~sl p!QdJc~ infective Slicky conch.


ANl j\ I A I~"


M echanisms for Infecting Nematodes

and other Sm all Animals
(I) Motil e spores: The chytridiomycetes and oomycetes have motile eens. and ;n
carnivorous spedes these have taken on the responsibility of finding the prey. The un i ~
flagellate spor~, of Cme,wria (Chytri diomycota) (Fi g. IS.2 A) swim to a nematode by
chemota xis. and encyst near its mouth or anus before penetrating the cuticle and attack
ing its internal organs. The biflagellate spores of some spcc iesof MY:Jx:ytium (Oomyeota)
(Fig. IS.2 B) do the same thing. encysting on the surface of a new host. then penetrating
its cuticle. The zoospores of other species of M y::ocyfium disperse actively for a sbon
while. but then conserve energy by cncysling 3nd developing a special adhesive bud.
which can stic k to a passing nCTIkltode. This makes these spedes a combination of categories I and 3 (see below).

(2) Inj ec tl'd spo res: The oomycctous genus Hap/oglossa (Fig. IS.2 C, 15 .3) is
unique among fungi. It produces spores which, though non motile, are sophisticated
'harpoon cells: A harpoon cell adheres to the substrate and sits with Ihe balTel pointing
upward at a low angle (Fig. IS.3). It has a high turgor pressure. and is triggered byeontaet
with prey: a built-in line of weakness ruplUres. and an internal tube with a harpoonlike
tip is rapidly evertcd with sufficient fon:e 10 penetrate the integument o f tbe prey and
injecl sufficient m~terial into the animal to fonn a tiny infection uni!. This is an ex tremely
highly evolved mech~nism: its con sider~blc mecha nical com pkxity can be clearly seen
in Fig. 15.3. TIU! only comparable m~ch allisms I can thi nk of arc: (a) that of the zoo:;pore
in Pla.modiopham, a colonial pmtoctistan. and (b) that of the nematocysts of the antmal
phylum. Cnidaria (corals, sea anemones and jellyfish): there i~. of course. no sugg<ostion
of homology here.
Afler Ihcsc fungi get inside the animal. they grow through ils internal organs. absorbing nourishment from them. This is not healthy for Ihe animal. which SOOIi expires. lis
corpse eventually hOIl~s scveral to ma ny mitosporangia. which liberate large numbers of
thgd late or injective propagu1es to be gin the cyc le again. Sexual reproduct ion can also
occ ur. und M yWC),lilllll. for exampl e. some times fills its hos ts with oogonia. each ulti
matdy containing a thickw alled. resting zygote (oospore).
(3) A d h e.~he s pores: Meriflacrulll is a common nematodeexploiting rygom)"ccte.
From a pa.ra.~itized nemalode arise taU sporangiophores with helically twisted apical
It"j!ions_ Sticky one-spored mitosporangia arc produced on lhese. and are forcibly shot
away- If they dont nUlke contat:1 wilh a nemalode. lhey will germinate and form a small.
adhesivecoated secondary spore at the top of a liUle These stick to nemntodes:

Fig. 15.3 Detais of lhe harpoon eel of Hdptog/osSil.


some cause infection, while others form secondary spores, and the hos t worm may thos
spread the infection \0 olher nematodes while il can still move about.
HyphQmyceteS are well-represented 11ll1Qng the nematode-e)(plo iling fungi. and
have evolved the widest range of techni ques for gaining access to the interiors of nematodes. Verticillillm and M~ ria (Fig. 15.2 D) use the sticky-spore Ie<:hnique already mentioned. Once pcllCl17l1ed by the germ rube arisi ng from these conidia, the worm is doomed.
After a few day s. its body is riddled wi th assimi lative hyph ae. The n the fungu ~ breakS OUI
of this capsule and produces charneteristie conidiophore!, bearing adhesive tonidia. The
conidia of Nematoct01lIlS Itiosporus (Fig. 15.4 A), after becoming detac hed, deve lop a
vertical extension thaI en(\s in a slic ky, infe<:live swelling. The assimi lative hyph~c inside
the hosl h3vc clam p connections, showing that thi s is a dikaryot ic b.asidiomycc tous
anamo.-ph. Several species of Nemaloc/{;mus h/we been show n to be anamorphs of species
of Hohenlmehd ia (Holobasidiomycetes: Agari caks) (see also method 8. below).
(4) Ingested spores: Some byphomyeelCS have evolved conidia that art designed
10 be eaten by their victims. The conidia of Hmposporirlm angui/lllla~ (Fig. 15.4 B) are
crescent -shaped, with a sharp poin t at one end. These conidia literally Slick in the craw
(acruaUy the oesophagus) of the wonn. and from this initia l bridgehead their hyphae soon
penneatt the host. Evenrually. new conidiophores arise from the defunct nematode. It has
rec ent ly bee n d iscove re d tha t Ih e te leo morp h of Harpospo rjllm angulI/lilac is
Alricordyceps lrarposporifera (Ascomyc etes, Cla\"icipitales), which allacks millipedes.
This is the only case I know of in which the 3nalllOfph exploits One group of animals. tile
telromo rph another. Olher specks of Harpospor;wn al so have 'edible' con idia. Those of


conidium wtln "prign! stLCl<y e"t1ensiOf1

Fig. 15.4 A Nem,ltoctonus /eiospc>rU5 (~tic ba~ an,unoq:h) S1icky ccri:la
penetrari1g the IvJSI nematode ardOO<.~assi"rilti...e hyphaewithd.m1JCCIIl"'II:'COOn; 6;
Hilrposparium anguillu/,lC{anall"KXph ci AtricordfCt'ps harpasporiff>rJ. Ascomycetes,
ClavicptJ!esJpror:l.01g ~ and CuveQ, poi1tcd ccriia t:hat are i;lgesll'd by the host ,,-orm


" ..;.


H. diceraeum (Fig. 15.5 J) have a striking resemblance to a high-hee led shoe or clog:
th~ o f H. rhynchospqnlffl (Fig. 15.5 K) look like cartoons of small birds minus lcgs. In
e3ch case there is a subtle asymmetry. and OI1e or more sharp poims. which undOUbtedly
combine to help the conidia lodge in the muscle of the worm's buccal cavity or oesophagus. The longer conidia o f H. htlicQidu (Fig. 1S.S L) don't picrce the gut wall me<:hani.
cally, but germinate in the intestine and infect the worm just as effectively from there.
Ha rpospori/,m spirosporwn has sinuatc , twisted conidia wh ich are vcry sh arp at
both ends. These conidia are eaten by rotifers, and lodge in the gullet or mast1l)l. to initiate
an infection. AI least twel ve species of the hyphomycete genus DihtltfOspora parasitize
rotifers after th ey ingest conidia. Altho ugh these conid ia are nOt pointed, they still lodge
in the mouth, gullet o r mast1l)l., and penetrate the body cavity of the animal in the usual


Fig. 15.5 COOdaoi nematode,explciti"lg f~; thelarge spores{AGIare of trap.fornW-G~ the

sma" spores (H.O) either stick to nematodes or ale eaten by them. AG: Arthrobo trys spp.; H-l:
Harposporium spp.-H: H. bysmatosporum; t. H. anguillu/ae; J: H. dicera eum; K: H.
rhyncho5porum; L: H. he/icoides; M: Meria conospo ra ; N,.Q: Nematoclonus spp.


Mechanisms for Trapping Nematodes

The remain ing fun gi that exploit nematodes do so by trapping or snaring them. The
traps are of six different kinds, but can initially be categorized as either adhesive or non
adhesive. Some fungi have evolved a very efficient nematode glue (or glues) to which the
cuticle of nematodes adheres instamly and strongly. Others lack this feature, and have
developed even more interesting alternatives:
(5) Adhesive assimilati\'c hyphae: in some zygomycetes, thc assimilative hyphae
are cover~d with adhes ive. C}stopage can be recognized by its thickw alled chlamy
dospores (it does nN produce mi tosporangia). Stylopage produces a few large >pores on
upright hyphae.
(6) Adhcsh'cside hranches (Fig. 15 .6 D): afew species of Dacrylella (Hyphomycctes)
have speciahzed adhesivecoated side branches on their otherwise non-sticky assimila
tive hyphae. lbese branches project from the substrate just far enough to ensure proper
contact with passing n~matodes. We presume that this simple furin of trap gave rise to the
more. elaborate and sophisticated types reported ~l ow. Dady/ell" fOpepodii manages to
capture copepods with adhesive branches (it also uses adhesive knobs- see method 7 ).



F~,; .

15.6 TrJPping devices of nematodeexploitillg fUllgi . AC: stic ky knobs - A: Arthrobotrys

candida; C: Ncmatodonus sp. (ana mwph of Hohenbuehe/ia: Basidiomy<::etes, Agarica les) D:
sticky branches of Daclylel/a cionopaga; E: non,collstricting rings of Arthrobotrys candid.l; F:
net of Dildy/ella gephyropaga: G: net of Arthrobotrys oligo5poril ;H: constricting rings of
Arlhrobutrys anchonia.


(7) Ad heshe knobs (Fig. 15.6 A-C. 15.7 A) are speciali7.ed. swollen cells. coa ted

with nematode gluc, and often situated at the e:nds of short side-branches. The y are found
in ne:arly twenty species o f Arlhrobol1)'S, Daery/ella and NellUll(x/()IU~ (all H>-p/"oomyccteS).
Sometimes the: knobs are finnly enough anachcd 10 prevent a nematode from le:avillg the
sce: ne, particularly if the animal has stuck to se veral of them at once:. Oftcn the nemat ode
tears a knob loose from ilS moorings and makes good its t!5capc:. B ... I the ens ... ing freedom
is short-lived. The knob remains fi nnly auachc:d to thc worms cuticle, and soon sends in
an infective hypha. Game ovcr.
Some species o f N enl(lloCIOnU$ which ale anamo rph s of the gille:d f ungi
Hohenb/.,ehe{io and Resupinoms (Holobasidiomycetes. Agaricales). produce unique adhesive knobs shaped li ke: hour-g la.sscs. enveloped in a drop of glue: (Fig. IS.6 C). These
knobs do nOI break off. but hold ne:matodes firmly while infection proceeds. The clamped
hyphae of N enlo/(xto"us also be:arconidia (Fig. 15.5 N). but these Me nO( infectious until
they have germinated and formed a sticky knob at the end of the genn lUbe.
(8) Adh es ive nets (Fig. 15.6 F,G) Me probably the commonest trappin g device. si nce
they have been recorded in nearly 40 species of fungi. They may original ly have evol ved
by anast omosis of adjace:nt adhesive: branche:s (only Eumycotan fungi can do this). and
so me of them are still simple hoops. Others are more comple x. ranging from two-dimensional ladd e r-like arra ngements. to the con torted threedi mensional labyrinths o f
Arthrohol1)S oligosporo. the commoneSt nematode-trapping hyphomycete. These networks can arise only as a result of rep<atcd anastOmoses. The advantage of the more
complex systems is not simply tileir greater extent. but also the fact that l ~rgcr nematodes
are likely 10 bc:L-omc stuck at more than one point. and;\K therefore: less likel y to escape:.
The: adhcsive works equally well on dry and wet nematodes (though not on other soil
an imaL,). The nematodes are not just blind. insens ate victims: they often ~coi l violently
when they tOuch an adhesive net-an ,,ersive reaction that sometimes saves them from
cenain death. When the: fungus is successful in establishing adhesion. an infecti~'e hypha
soon penetrate:s the body of the prey. and the wornl becomes comatose within an hour: so
quickly. in fact. Ihat the fungu s is suspected of producing a loxin. Afte r Ihe prey has hc:e n
riddled by absorptive hyph3e. the convened biomass is exponed~transl()(:aled to the
extcrnal hy phae. which lise Ihe energy. spider-like. to spin new ncts. and also to produce
the distinctivc conidiophor~ s of ArthrobOirys oligQsporo , with their sUL""Ccssive: cl usters
of ty,o-cellcd. co!ourle,s conidia.
(9) Non-constrict ing rin gs (Fig. 15.6 E. 15.7 A). which could also be: called det achable rings. ar~ produ ced by four spel.'ies of ArthrobOlr)s and D"ctyicllo (H)phomycetcs).
A sing!.: byp ha grows around in a perf~ct circ le. tinally anast omos ing with a new bud
waiting at the: tOP of the: stalk-to-be:. The three-celled ring is stouter than the stallc When
:I nematode craw ls through the ring. this fi ts snugly around its body. and easily breaks
~\way from the narrow s talk. The worm g~s on i l~ way we aring its newly a~ quired coll~r.
As you will have deduced. inf~ction and ass imilation soon follow. All species with non
con~tricting rings produce sticl")' knobs as lIell (Fig. 15.7 A). In terms of the spre:ad of the:
pathoge n. it is interesting to note that fungi producing sticky spores. or dctachable knobs
or loops. may be carried somt dist ance by the anim al before it hecome, incapacitated.
(10) Constricting rings (Fig. 15.1. 15.6 H. 15.7 B-D) are the mOSI SOphistlclllcd
nematode traps o f all. They are produced by twelve Hypbomycetes. especially specks of
A rrhrobQ/rp and O(lelyiella. At first sig ht. thcse tra ps seem very si milar to non-constricting nngs: thc ring is composed ofthrce cells. borne on a stal k. But here the stalk is shoner
and stronger: these traps:rrc designed to stay put. Their oue: nature is revealed only when
they are triggered. If ~1 nematode passes through the loop. and louches the inside of one or
more of the cells, all three: cells s imultan~ou s!y innatc inward. in about one-tenth of a


se<:ond, and the n~matode is held in a vise-like grip (Fig, 15.1. 15.7 D). The inflated ceUs
soon squeeze the wonn so lightly that it is virtually garrottcd. Rings can be triggered by
mechanical stimu131ion or by heal, when no nematode is presenl. and in this case the three
cells eltpand to three times their original volume: until they lauch one another and the
centre of the ring is completely occluded. Between the contaCI stimulus and the implosive response there is adelay ofa few seconds. If a worm is luc ky, it may retract during that
period of grace, leaving a trap sprung but empty.
How do these traps work? A variety of experimental and observationaltechniqlle$
have now provided liS with a reasonable hypothesis. The three celts o f each constricting
ring trap have a high turgor pressure, generated by a high internal osmotic pressure. The
cell membranes are freely permeable 10 water. and the cytoplasm would take up more. bul
is prevented from doing so by the presence of lhe outer cdl wall s, which are ellening an

stK:ky knobs

B: de>lelgping




Fig. 15.7 Arthr obotrys (Hyf>homtcetes). A: A. f:andida with detachable sticky knobs, and
detachable oon-constrictl'lg rilgs; BD: A. hrof:hopaga- B: ~ constricting ring uap; C:
geminated cori!it.m which has formed a constricting mg trap; D: cooidumywith a constricting mg
trap wl>ich has caught a nem<ltode.



equal and opposite wall pressure. The trap waits for its victim. in a Slate of hydrost:lIic
tension. A clue to [u lUre e,'ents is given by the presence of 1100'0 inconspicuous lines of
weakness running around the inner faces of the ring ce lls. And if we look inside lIIe cells,
ncar the lines of weakness. we find folded reserves of wall material and membrane.
When a nematode enters the ring. and touches the cells, it triggers a rapid sequcnee
of events. The outer walls rupture along the lines of weakness, removing the inhibiting
wall pressure. The ring cells now take up water vcry quic kly o\'er their entire 5urfacc. The
cc:!!s expand inward from lIIe line of weakness, deploying the reserve wall and membrane.
The three inwardly expanding cells grip the nematode. but do not crush il immediately,
because their increase in volume has red uced their osmotic pressure 10 about a third of its
former value. The osmotic pressure is quickly pumped up again. IUrgOl'preSSure increases,
and the worm is strangled. All that remains is for the fungus to send in assimilative hyphae
which will extract tile vital nitrogen supplement from the animal.
This is dearly an unusual kind of mce hani sm to find in a fungus. U we try to unravel
the evolutionary steps that led to it. we begin with the ability of eumyeOtan hyphae to
anastomose. Without that. no trap is possible. When hyphae anastomose repeatedly. they
can produce a nctwork: some nematode-trapping fungi have gone no funber than this. But
wonns can wriggle out of passi vc networks. and there was obviously a selC'Ctive advantage
for the fungus to doing something extra to delain the moving meal. As is usually the case,
the various intermediate Steps in the daborotion of the trap mechanism arc nowhere to be
see n. Like so many other missing links. they have inconvcniently vanished in the mists of
ti me. Bu t we can dmw some analogies with other fungal mechanisms that depend on a
build-up of turgor pressure followed by its mpid release: the ascus. the basidiUm. the har.
poon-cel! of Hap/oglossa. thc subsporangial vesicle of PilobolWi. These show how a basic
physical plK:nomenon like IUrgOl"pressurc. learned with an appropri ately placed line of wall
weakness.. can be used for purposes as dil'ersc as shool:ing spores and catching food.
Many o f these fungi exploit nematodes only a.~ a dietary nitrogen supplement, and
they may often grow in places where an adequate su pply of nematodes is not forthcoming.
Here, the dcvelopment o f traps would be (I pointlcs~ waste of e n~rgy. To avoid th is possi
bility, the fungi will not produce traps unless they detect certain chemical trademarks that
indicate the presence of nematodes. [ t has also bec n confirmcd that the communication
gees both ways. The fungi seerete a chemical attractant which lures nematodes to their
doom . This attr:tetant may be ammonia or carbon dioxide.
The conidia of some of the trap-forming fu ngi wi!! sometimes produce a trap a lmo.~t
immediately after genninating (Fig. 15.7 C). This sugges ts that nematodes are a \'e ry
impol1ant p~rt of the diet of these pal1ieular fungi. It is also significant that the conidia of
trap formers arc usua lly quite large. enablin g the m to carry e nou gh reserves to build a trap
(Fig. 15.5 AG). Spores of species that rely on adhe~ive . mobile or ingested propagules arc
usually much smal!~r (Fig. 15.5 HO).

Chemical Warfare
(I I) Toxins: mycelia of the widely-ealen and cultivated 'oyster mushroom: Ple!'rvIIIs
oS/Utl/us, and se\<erol other Pleura/us speeies. secrete a substance lh al rap idly inactivates
nematod~s. allowing the fungus to colonize their inert bodies. Since P/t!"v/us species are
often primary ~olonizers of dead wood. a substrate notoriously deficient in nitrogen. the
nematodes may be an important compon ent of the fungal diet. us they uppcared to be for
the other agaric s (HQhenbueIJe/ia and Reslipilllltus) mention~d earlier.
A f~w fungi parasitize nematode eggs. RhopalomJces elegallS . a striking zygomycete
commonl}' encountered on dung. is one of these. N ematod~ eggs appear to release some


kind of anrnCl:mt which causes hyphae of Rhopa/()myces 10 grow toward them. On arrival.
Ihe hyphae eslablish appressoria. then peneU'ate the egg and assimilate its cOlllents.
Rhopa/om)'ces hyphae also parasitize adult nematodes.

Exploitation of Other Animals and Protists

Nematodes, as >'ou will already have noticed, are not the only animals preyed upon by
fungi. Amocbae. ra ttfers, tardigrades. copepods and even callembola (springtails) are
al$O exploited. The largest animal known to be captured by a predaceous fungus is a small
springtail. Anhroix>ttys tnlomopaga (Hyphomycetes) produces a prostrate hyphal Jl<!twork
from which arise c\ust.!rs of two-eclled u-aps.lhc upper cell of each bearing a large droplet of
glue. In a confromation like that of Gulliver and the Lilliputians. the coUembolan. which is
up to 130 ~m long, sticks to several microscopic droplets al oncc. and canno-l escape their

fig. 15.8Arotifer caughll7tone of lhe'lethal~ of Zoophag us lOorrrtco ra).


combined efl'.-cl. Anomer hyphomyccte, a species of Harposporilml, has been found attack.
ing tnrdigrade~. Zoophagus (Oomyc01a) traps rotifers by means of 'lethallol1ipops' _tic ky
knobs which the animals unwisely try to eat (Fig. 15.8).
Six hyphomyretes trap amoebae. usually teslllccous rhizopods.1l1ese fungi are drn\\ n
from four genera: Dacfyfdla. Pedilospora. Trid"maria and Triposporina. The amoeba
GeococC'us vulgari.! nonnally fc.::ds on fungi by attaching itself to the wall of a spore or
hypha an d sucking om the cytoplasm. But when it encounters Dacryll!Ua passalopaga. the
tables arc rumed. The fungus responds to the attack of the amoeba by gagging it with a
bulbous outgrowth that effectively prevents escape. Assimilative hyphue subsequently
digest the amoeba. Most amoeba-trapping hyphomycetes rely on sticky knobs to c(ltch
meir prey. The rarity of amoeba-l11lpping hyphomycetes can probably be explairlCd by a
difference of scaic, A robust hyphomycete would need to exploit a large number of me tiny
amoebae in order to accumulmc erlQugh energy to fonn conidiophores and conidia.
Somc years ago. when we first became aware of the ubiquity of the nemJtodc
exploiting fungi. it was suggested that they might be ustful in controlling the populations of pJnnt-~ilic nematodes in the soil. A number of attempts were made to obm,n
biological con trol of eelwonns by boosting natural populations of the fungi. or by shift
ing ecological equilibria in their fa\'our. UnfOrlunatdy. although small scale experiments
often gave promising results. field trial s were generally less succes~ful. A combination of
gre~n mlnuring and additions of nematode.destroying fungi gave the best results. Nema
tode-ex ploiting fungi are naturally present in all agricllltural soils. If they are already
actively exploi ting nematode populations, the impact of adding more fung;l\ inocu lum
might wcll be less than expected.

Further Reading
Barron, G,L. (1977) T he "'emalode- DeSlroying .' ullgi. Canadian Biological Publica
tions. Guelph.
Barron. G. L. (1981 ) Predators and parasites of microscopic animJls. pp. 167100 (in)
Biology of Conidial F ungi. Vol. 2. (Eds. G.T. Cole and B. Kendrick). Academic
Press. New York..
BalTon. G.L. ( 1985) Fungal para.~ites ofbdclloid rotlfers: Dihl!laospom. Ca nadian J ournal of Botany 63: 21 1-222.
Barron. G.L. (1986) A ne w H",p();poriwll parasitic in bdelloid rotifcrs. Ca nadian Jo urnal of Bntany 64: 2379-2382.
Barron. G.L (1987) The gun cell of HIIP/(}glossil mirabifis , i'> lycologla 79: S77-8S3.
Barron. G.L. (1990) A new predJtory Hyphomycete capturing copepods. Canadia n Jo urn:ll of Botany 68: 691 696.
Duddington. C.L. (1962) Predacious fungi :lOd the control of eelworms. Vje\'.. pohll ~ in
Rio lOg)' I: 15( 200.
Gray. i".F. (1987) Ncmatophagous fungi with particular reference to their ecology. Biological R ~" i ew 62: 245304.
Nordbring-Henz. B. (1988) Ecology and recognition in the n~matode/nemutophagous
fungus syStem. Ad.-anns in Microbial E(olng}' 10: 81 - 114.
Samuels. G.J. ( 1983) Ascomycetes of New Zealand o.AldC(Jrdycep~ IUlrpGspo rijem gcn. et sp.
nov. and its Harposporium anamorph. Ne w Zealand Jou rl131 of Boumy 21: 17 1- 170.
Thorn, R.G. and G .L. Barron (1984) Carnivorous mushrooms. Scicnce 224: 7678.
Thorn. R.G. and G.L Barron (1986) Nenwr(Xr()1II1S and the tribe Resupinat:lc in Ont ~rio.
Can:lda. i't lycota.'\:On 25: 321<453.



Mutualistic Symbioses Between

Fungi and Animals


At flIst sight. such relationships sculld bizarre. e'>cn unlikely. Wh at service could
fungi render that would make it worthwhile for animals \0 modify their whole lifestyle 10
~ccommoda!e such uEens? And what could be in it for Ihe fungi, which uSUally compete
with animals for food?

The first and most important driving force is

th ~

inability of animals to digest

cell ulose and lignin. Some animals. like me detri tivores in streams and ponds. wai t until
amphibious and aero-aquatic hyphomycclcs have exploited the plant remains. trn:n seek
out und eat the hyphae and conidiophores of these fungi. Many other anima ls. including
the herbivorous mammals and some termites, have overcome this deficiency in a more
efficient and reliable way. by harbounn g large popu lations of cellulolytic mic roorganisms in their gul. Then they cun eat the ce llul ose and li!"nin directl>', leav ing their g llt
microbiota to digest the s.e substrates for them. But certain soc ial insects. the mou nd building ter mi tes of Africa and Asia, and the leaf-cu tt ing a n ts of Central and $outh
America. have evolved a rat her differem strategy. They cultivate specific cellulolytic
fungi in underground gardens_ And [usc the words 'cuhi,-:ue' and 'garden' deliberately.
The in5('CI.'i establish pure. axenic cullures or speeial coevolved fungi. keep them consta ntly supplied with food and moisture. and ..... eed Oll! any comamin~nls. The fungu s.
then . receives vcry special treatment. and there is no doubt I h~1 il benefits from the
arrangement. How many Olher fungi have guardia ns th~1 keep out the competition. and
bring endless supplies of food? But then the ant~ and lennites have their turn. As you have
no doubt guessed. they arc exclusively mycophagous. The fungi have transform ed the
.....ood brought by the tenoites. and the leaves suppl ied by the ants. into digestible and
nutritious fungal biomass_


Ant s, l.eucoagaricus and l.epiota

The garden ing ants of the New World milke up the Tribe Altin!. Although you have
prohably never heard of them before. people in South America are only too fumiliar with
the m. Searchin g for leaves to feed to their tnme fungus. these anlS will defoliate trees and
growing erop~. In the sixteenth century. the invading Spani.u-ds may have conq uered the
native peoples of South America. but the O:l\ive ants gO! the beiler of them-their failure
to grow cassava lind citrus fruiu; attributcd to Attine ants. whose nests. at the base of


the trees, were 'white as snow' (presumably with fungal mycelium). Leaf-cutting ants of
the genera Alia and A cromyrmu have long been regarded as serious pests. and they stil!
make fanning difficult in some primitive areas. The native peoples eat the large females,
but this, unfortunately, doesn't seem an adequate population control for the ants.
Nevenbeles.'i, in tropical rainforests. these insectS and their fungi have an important
ecological role to play. In these forests. the turnovc r of organic maner and mineral nutTiems at the soil surface is very rapid, and few orglLllisms. inc luding the trees, penetrate far
into the soil. Here. a large ne st of Aua, with hundreds of fungus gardcns, vastly increa ses
the organic matter conlem of the soil. and opens it up for subsequent colonization by
many othcr organi~ms, In some areas of Trinidad. small species of Anine anlS achieve
den sities of 0111: nest for every twO square metres, and are a dominam feature in soil
ecology and nutritional Status.
Although the Allini compri se hundreds of species in more than 50 genera, Alta
.lcxdtns is the most economically important specics. and therefore the most intensively
studied. A winged female, carrying inoculum of the allimponant fungus in a speci3.1
pocket at the back of her mouth, and with her spermathec a stoc ked with perhaps 300
million sperm, establi shes the colony. First she e.-<pels the fungal pellet from her mouth.
and finds some plant material for it. As soon as the fungus starts growing. the qu~n lays
eggs 011 it. Soon she is laying about 50 eggs a day, but eats most of them herself until the
worker population is established, which takes about three months. A second entrance to
the nest is added after anomer year, then entrances proliferate: there are about 75 by the
end of the second year, and about 1,000 by the end of the third year. From now on, new
females emerge each year to establi sh colonies elsewhere. In case you are wondering why
these animal> haven '( taken over South America. it is worth pointing oUl !hat an estimated
99. 7% o f all new nests are d('~troy('d in their first six momhs.
When a fouryearold nes t was excavated. il was found 10 contain 1,027 s ... bternl
nean cham~, of whic h 390 had fungus garde ns. Another Alia nest. more than s ix years
old, had 1,920 chambers, of which 2 .. 8 contained fungus gardens. and 1,219 were empty.
The gardens were usually 2(}..30 em in diameter. and weighed about 300 g. It was calculated that this colony had consumed n~arly 6,000 kg of vegetation. Fig. 16. 1 B shows a

Fig. 16. 1Sectional views of - A: terrnte lTlOU'ld; 8: atlne ant nest. f!X1g31 garden!; Of combs are

shown i1 white.


section of a representative nest. with many entrances alld many interconnected chambers:
note that mOSt of the larger chambers cO/l tain fungus gardens (shown in " hite).
Tn the early day~ of the colony. the queen and the first broods establish the first
fungus garden, c..>;:cavating a chamber, filling it with "egetation brought by workers, and
inoculating the substrate with the fungus. Leaf-cutting ants forage For leaves along wellmarked trails which often extend up into the crowns of trees. The alliS have no diFficulty
in scissoring out large pieces of leaf. petal or twig with their Formidable jaws, though they
may have a liule trouble manoeuvring on their way home. Back in the nest. they cut the
material into smaller pieces. lick it allover, Chew the edges. and often deposit an anal
droplet 0 11 it. Theil they wedge il into the garden. and put rufLSof myceli um on it. Gmlcns
have a sponge-likc construction, containin g mnny cavities. The ants walk all ove r the
garden. probing the fungus with thcir antennae, licking and sometimes cating hyphae,
and depositing anal droplcLS. as in Fig. 16.2 A. SomeAttines are nO{ lea f-cuners , but they
ncvenhelcss grow perfectly functional fun gal ganlens on such substrates as plant debris
and illscct excreta.

c _termlte

Fig. \ 6.2 Mycophagous nsects and the fl.ngo1lstructures they eat.


The gll'den, invariably contain only one species of fungus. This is surprising. because decaying org an ic substrates are usually competitively colonized by a wide range of
different fungi. If a garden is removed from the colony. it soon be<:omes overgrown by
extraneous fungi or bacteria. From this, we deduce that the ants must have some kind of
chemical inhibitors that prevent the growth of unwanted microorganisms. It seems lik ely
that these substances. and perh:lps others that promOte the growth of the proper fungu s.
are present in the ants saliva and anal fluid. with which they constantl y anoinl their lame
fungus. in rctum. it f1ourishcs. and develops clusters of inflated hypha\ tips (Fig. 16.1 B),
which the ants cat. 1 muSt emphasize that although the insects CUt up and chew up thc
leaves they bring to the nest. leaves are never taten. Tht antS are txclusively mycophagous.
The fungi cultivated by the Anine ants ne,er sum to fruit in or near the gardens. so
various altempts ha,e been made to isolate them in pure culrnre. and matu re basidiom~ta
have sometimes developed. These belonged to species of ulU;oagaricIIS or Lepiola
(Holobasidiomyeetcs. Agaricaks). S~ies of X)"luria (Ascomycetes. Spbaeriales) and
AuriculaTla (Phragmohasidiomycetes. Auriculariales) may also be involved.
It has been suggested that the cultivation of fungi by anlS evolved only once, about
50 miUionyears ago, when they domesticat~d an agaric belongin g to the family U:piotaceue.
Not long ago, it was discovered th3t the fungal g:udens ofthe Auines were contaminated by a parasitic hyphomycctous mould. EscolopsiJ . Now it has been found that the
ants themselves carry colonies of an actinom)cetou5 bacterium. Streptomyces, on sp.:lcific areas of the cuticle of their ex oskeleton, and th at this bacterium produces antibio tic
substances which help to control the ESCQmpsis. So it looks as if the symbiO!'is actually
involves three partne~.

Termites and Termitomyces

Across the South Aliantic ocean from the territor;. orthe leaf-cUlling ants begins the
re:tim o f the fungus-growing temlites. The subfamily ;\lacrotemlitinae is found in the Old
World, ils twelve genera being variou sly found in subsaharan Africa, Madagascar, the
Indian subcontinent, and mueh of southeas t Asia. including tile Indonesian arch ipe lago.
Unlike m,lIly other termites. thesc hal'e no ce llulolytic protozoans in their gUI, so,li ke the
Anine anlS. they h:ne established a muru:J.!istic symbiosis with fungi.
Each colony is founded by a wing<,d male and femak, whicb wall themse lves up in
an underground chamber. The queen lays eggs. and tbe resuiting workers bri ng food to the
sequeslered couple, take eggs away for incubation, and build the nest. Tbc fungus garden
or comb surrou nds the royal ch:lmber. Above their nests. many fungus-growing termites
con.,truct mound, (term itaria), which can be an imprtssive 6 mttres tall and 3 metres
lInoss at the base. The mounds are penetra ted by air shafts leading to the nest below,
panicularly to Ihe fungus garden. which may be a large. central structure, 50 em in diameler and weighing as much as 25 kg, or a series of smaller combs (as in hontycomb:
riddkd with holes) in individual chamber> (Fig. 16.1 Al
A large colony rna>' contain a million temlitc s, which Forugt for wood and OIher
pbnt debris. Unlike the Attine ants, the t~nnites cat this materiol on the spot. so their
fungus gardens are made entirely frQm faecal material. "The g-ardcns have a sponge-like or
deeply convoluted app.:larance. and at many points on thei r surface spherical sporodochi~1
con id iomata de,dop (Fig. 16.2 C) witb mon ilioid co nidiophores bearing dik aryotic
conidia (Fig. 16.2 D). "The workers eat these. and ni bble Ihe garden itself. redepositing the
resultant Faecal material on the comb. Thecellulases orlbe fungus remain acti'e in the gut
of the insect. The .\.O\diers, nymphs, king an d queen don t eat the fungus diTel;t1y, but live
on sa livaI) secre tions provided by the workers.


The taxonomy of the tennite fun gi is beller understood than that oflhe ant fungi. for
the simple reason thaI termite fungi fruit in nature (Fig. 16.3). When tennites of the genus
PstudncanlhOlumes desen a comb. Ihe fungus produces basidiomatal primOfdia on its
surface. When the rainy season suns, rainfall of more than 2 em/day stimulates the pri_
mordia 10 develop long stipes. which grow up 10 the soil surface and produce a large
pileus. These mushrooms are identifiable as Termiiomycu siriarus (Holobasidiomycetes,
Agaricales). Interestingly, the combs of fungus-growing termites are often inhabited by an
additional fungus. a species of X)'/aria, which may also produce stromata on the comb.
Although about 30 species of Tl'mli/omyces have been described. only two species of
XY/llria have been found associated with termites.
Macrotemlitinae are regarded as major pests of tropical agriculture, and they are
destructive 10 wooden buildings. They take scaret: organic matter underground. where its
nutrients may remain locked up for years. However, there are a few minor compensations.
Tennites are food for many other animals, and many Tl'Fmiromyces species are among the
most highly prized. and the largcst. edible tropical agarics: so moch so thai a1lempts ha\'c
been made to domesticate them.

Beetles and Ambrosia Fungi

Although social insects like ants and tennites are the most \~sible, the moSt dram at i~,
and probably the most h.ighly evolved examples of animal-fungus mutualism, they are not
the only su~h relationships. A similar bond exists between wood-boring beetles of the
families Scolytidae. Platypodidae and Lymexylidae, and the ambrosia fungi they carry in
special organs called myeangi:l as they travel from tree to tree, and on which their larvae
feed exclusively. 111e fungus is introduced to weakened or freshly logged trees when a
female beetle burrows into them 10 lay its eggs, By the time the larvae hatch, the fungus h:lS
colonized the surrounding wood and is spof1Jlatins all o\'er the walb of the beetle tunnels.
Since tncy ~anoot digest wood, the larvae eat the fungal biomass_ wh.ich is called ombrosia_

Fig. 16.3 Ternl'fOmyCf.'5 basidomata arising from a subterranean fungal<:omh

1'- 'n


- i



Before an adult female beetle leaves the tree tosee" fresh habitat, it will rock back and forth
to make sure that its [J\ycan~um is stocked with the fungus (Fig. 16.2 E,F). Many species of
beetle have specific ambrosia fungi, though their l:m'ac may feed on other fungi lhat art
also found sporulating in the tunnels. The full speelr\lm of such fungi takes in some yeastS
(Saccharomyretes: ~coideo, Dipodoscus, E"domyces, Elidolllycopsis, HOllsell/do. Sac_
choromyces), ascomycetous an amorph s (Acremoniurn . AmbrositlIu, Dip/odia.
SCOpIJ{uriopsis), and some basidiomycetes and their conidial anamorphs.

Scales and Septobasidiales

There are almost 200 species of the Phragmobasidiomycetc order Septsidiales. AU
grow on the ,urfaces of plants, and an: associated with scale insects (Homoptera, Coccoidea).
Some oCtile insects are parasitized by the fungus, but do not die.And although the infectiQn
renders them dwarfed and sterile. they continue to feed from the plant, supplying the enclos ing fungus with a reliable flow of nutrients. The tough mat of fungal hyphae ( 150- I.OOO).lm
thick) that develops around parasitized inSttts protects many other healthy scales from
predators and parasitoid hymenoplcta 'The mutualism is not penectly balanced. because
the insects are OCCasiOllally seen to survive without the fungus.

Midges and Macrophoma

Some gall-midges (Diptera, Cecidomyiidae) have mutualist ie relationships with
members of the eoelomycetouS anamorph, Macrophoma (Teleomorph "" BorryospiJaeria
[Ascomycetes, [)othidealesj) which inhabit ' ambrosia galls:The dipteran larvae mUSt cal
the fungal mycelium, and the fungus needs the adult midge as its vector. The female gallmidge carries the fungus away in a pairor specialized pouches caUed mycang ia. and lays
some conidia with her eggs.

Woodwasps and Wood-rotting Fungi

Woodwasps of the genus Sinx (Hymenop(era. Sirieidae) often invade dead or dying
trees, but may also be implicated in tile death ofbealthy ones. They drill through the bark
oFthe In:<: with a long ovipos itor. and lay eggs in the xylem. A pairofmycangia associated
with the ovipositor are full of thallic-anhric conidia of a basidiomycele, some of which
are dc[X'sited with the eggs. Female I:lro";le also have mycangia in which the fungus is
maintained in a donnant corniition, embedded in wax plate~, The role of the fun gus is not
fully under5tood. and different workers have suggested that: (I) the fungus regulates
mo isture content and provides a suitable microclimate for egg incubation; (2) the fungus
reduces the intensity of the Ute's response to attack; (3) the fungus is eaten by the larvae,
Whatever the relationship is based on, it is appart'ntly an obligatory one, since it has been
eJ(perimentally established Ihat fungus-fr~e females cannot reproduce sucressfully. The
fungi a,sociated with woodwasp5 have bee n identified as species of Statum and
AmyIOSle~"m (both Holobasidiomycetes, AphyllophoraJes).

Anobiid Beetles and Endosymbiotic Yeasts

Anobiid beetle~ (Coleoptera. Anobiidae) live in wood. These beecles have pouches
called mycetomes at the beginning of their midgut. These are full of yeas t-li ke fun gi of
the g~nus Symbimaphrinu. Adult beetles trans mit the symbionts to tbei r offspring by
smearing the eggs with fungal cells. The newly hatched hrva e~ts some of the eggshell,
and becomes inrectt'd: Thc fungus apparently supplies vitamins and essential amino
acids. Its role is mainly to recycle nitrogen in a rather nitrogen-de Cicient habitat. It has
been demonstrated (by disinfecting the eggs) that beetles without endosymbionts cannot
grow. ~,en when given their normal diet.



Boletinellus and Root Aphids

A few years ago. another apparently mUlualistie relati onship between fungi and
insects W:l!i diSCO"ercd in the mycology laboratory at Waterloo, this time between a bolele
and a root-aphid. Bolelintl/lls mtrlfiioidt.l (Holobasidiomycctes. Agaricale5) is commonly
associated wilh ash treeS (Fra.l inus), and was oncc thoughl {o be their
partner. We eumined many ash rOOIS closely, and found that the>' "ere exclusively
endom)'corrhizal. The Boletinelllls was subsequemly found to produce hollow black
sclerotia near the roots, and within these sclerotia lived individuals of a root aphid ,
Me/iarhi"ophagIlS fraxi'lifolii (Homoptera, Aphidae) , From within this safe haven. the
aphid.> pierced the roots and sucked sap at their leisure, We suggested th.:u in ()!;.change for
housi ng and pro!eeting the aphid, the fungus obtained nutrients, especially su gars, e:o::creted by the aphid in its hone)'dcw.

Red-backed Voles and False Truffles

/ last example is perhaps less clear-cut than those above, since there isn't a true
'livin g with' invo l ved. Nevertheless, the di~ { of the Califo rniu red-backed vole
(Clethrionomys cali/omicus) consists almost udusi ve ly of the hypogeous basidi omata
of eClomyrorrhi:.wl fungi such as th~ genus RhizopogOfl (Holobasidiomycctes, sequestrate Boletaeeae), Thi s establishes the dependence of the vole on the fungi, but although
the fungal spores can sU!>'ive IXlss.age through the vole gut, and arc therefore spread by the
animal, it is unlikely th<lt the fun gus depends eluireJy on this small mlmmal for dispersaL
Although thlt more or less Uh:U,lsts th ... known e:o::amples of animal -fungus mutual istic symbiosis, there are almost eerwinly others out there waiting to be r~cogni'led,
Perhaps y()tl will discover and describe one of them,

Further Reading
B:lIra. LR, (Ed,) (1979) Insect-fungus Symbiosis. AlhmheJd, Osmun. Montclair.
Batra, L.R. and S.W,T. Batra (1967) The fungus gardens of insects. Scil'ntilic America n

217: 112-120.
Bissett, J. and A. Borkent (1988) Ambrosia golls: the signilicnnce of fungal nutrition in
the e"olution or lhe Ceddomyiidae (Diptera) (in) Coe,'ol lliion or Fungi wit h Plants
and Anim:lls (Eds.) K A Pi rozynski & D.L . Hawks\vorth pp. 203-225.
Brundrctt, M.C. and B, Kendrick (1987) T he relationship between Ihe Ash Bolele
(Bolerinellus merulioide5) and an aphid parasitic on ash tree roots. Sy mbi os Is 3:
Buchner. P. ( 1965) End osym b iosis or Animals with Pl ant i\Iicroo rganisms, Wiley, New
Couch, J.N. ( 1938) Th\! Gellus Se ptolXlsid iu m. Uni versity of North Carolina Press, Chapc-I
Currie. C.R.. 1.A, Scott, R.C . Summcrbell and O. l'.lalloch(l999) Fuou~-growing ants usc
antibiOlic-producing b~Cleria to control garden parasites. Natu re 398: 701-7~.
Fishe r. PJ., D.J, Stradling and D.N. Pegler (I m) Leaf cutting ants, their fungus gardens
and the formation ofbasidiofIlma o f ullcoagoric"$ gOflgyloplwrJls. i\Jycologist g:
128- l3l
Pirozynsl::i. K.A. and D.L. Hawksworth (Eds.)( 1988) Coe"olution or Fungi with Phill is
and An imuls . Academic Press, New Yo rk.
Weber, N.A. (1972) Gard en ing An ts: the Au ines. Memoir 92 American Philosophical
Society, Philadelphia.



Mycorrhizas: Mutualistic
Plant-Fungus Symbioses

When green plants first colonized the land. more than four hundred million yenrs
ago, the invasion may hnve >ucceeded because they established an intimate alliance--a
mmualislic symbiosis-with fungi. Early lund plams could photosynthesize effecliv~jy,
but hadn't yet developed extens ive root systems and must have been" hard- pre~sed to
a_cquire :"aler and mineral nlltrients. The filamentOliS fungi, which had themsel ves only
recently emerged from the water, were petfec!ly adap!Cd for exploring the soil and fin ding
those vcry things , bllt desperately needed energy-rich carbon compounds of the kind
produced by the plant". Traces of sugars l ind ammo-adds leak out of plants. and Devonian fungi were undoubtcdly attracted by these. The relation,hip5 presumably develoJX:u
in more thun one direction: some fungi remained soprobi": others became destructive
parasites, causing wilts and root rots; y_! mhcrs_eYalCd inlO-lu'!).utually beneficial sym-hiusih Proof of this lies in the fact that fossils of some Devonian plants contain well~
preserved fungal structures just like those we c~n find in the roots of more than 90% of
ealthy modem plant specie!; _
About a century ago, several biologists noticed that some plant roots, thou gh ext~nsi\Cly invadcd by fungi , were not diseased. The name m~Torrhi7,a (fungus root) wa,
coined in 1835. We now know that, especially in poor soils, mycorrhi zal plants gruw
beuer than non-mycorrllizal plants. This is because the hypJ:!ae of tile fungal symbioots
permeate IMge volumes of soil and obtain sCarce e!cments----especiall y phosphorus. whIch
is often limiting for plant growth which they pass on to the plunt in excllange fOf
photosynthates ,
Interest in these symbioses Ilas escalated dramatically in l"\Xem years, bec:)use of
the ir putemial benefits to agriculture. forestry, and the rev.:g.:tation of ecosyst~ms damaged by human activities such as mining. Some plants c:)nnot become e stablished or grow
normally without an appropriate fungal partner (oft~n ca lkd the mycobiont). Even when
plams can survive without mycorrhizas. those with 'fungus roots' ne",d less fertihzer.
withstand heavy metal and acid rain pollution bener. and grow beucr on the infertile soils
of margin:)l lands, un mine spoils and oth.:r areas ' n~eding revegetation , and at high
elevations. They also s,-,r ~ i ve transplant shock better, are more resi,tam to soil-borne
diseases, withstand higher soil temperJlUreS , higher soil salinity, and wider extremes of





-, -,' I

~\ ~f

soil pH. Mycorrhizal fungi are almost ubiquitous, and over

all higher plant species are nonna!!), mycorrhita!, and can be called phytoblonts.
Two main kinds of mycorrhilBS are conStantly found in association wilb our agricultural and forest crops. By far the commoner of the twO is the cn~otrophic mycorrhba
in which specialized hyphae of the fungus enter the cells of the ~L-C~ex and sel up
finely br.mched. microscopic intracellular interfaces (Fig. 17. 1). (\llho~about 300.000
plant species are believed to have endOlrophic mycorrhizas. onfy-a6(iut 130 species of
fungi have so far been described from suc h relationships. These fungi will gTOw on ly in
association with plant roots (i.e. they ate obligate biolrophs), and only one of th em has
eyer been seen to reproduce sexually_They are placed in the division ZygomycQ{a.
The second kind of mycorrhi~a is the tttotrophic mycorrhi~a , so caned because
the fungus grows around the root and between its cortical cells, but never actually pen
e!tates!he cells (Fig. 11.1). This kind of myoorrhiu is found in only about 2,000 species
ofpJants, but these include some of the mOst important forest trees-e,g., Pi nateae (pine,
spruce, fir. etc.), Fagaceae (beech. oak, southern beech). and Myrtaceae (eucalypts). These
plants ha"e about H)(JO fungal partners. Although these fungi are usually found only in
association with tree roots, mOSt of them can be grown in pu re culture, and almost all
produce se,'(ual fructifications in their natural habitat. They are nearly all members of the
Phylum Dikaryomycota. mostly basidiomycet es, though a number are ascnm ycetes.





otd arbuscvle

point of entry -;~7"''''

In tramatrleall'ly~~a

Hartig net

lu ngal manil a

Fig. 17.1 Diagrams of end>- and ecro.mycorrhi.ul structures.

The mycorrhizal symbiosis, whethc:r ectotrophic or endotrOphic, must have three
basic functioning components: ( I ) fungal mycelium exploring large volumes of soil and
retrieving mineral nutrients: (2) a fungus-plant interface where the e ~changeof chemicals
can go on; and (3) plant tissues which produce and store carbohydrates. Strangely enough.
within each of the main groups of mycorrltizas, the root-associated fung al components
look rather alike. and we have to refer to otller components, (4) the reproductive Structures, before we can identify the fungus.

Development and Morphology

of Ectotrophic Myco rrhizas
Ectomycouhizas (Fig. 17.1, 17.~A-q normallydeve!op 1-3 months after the tree seed
germinates. forming on tile 'shan' or~'feede( roots, near the stufoce ofthc soil. Roots may be
colonized by hyphae which grow ttuOOgh the soi l from another mycorrhizal root, or by
airborne spores. When the laner genninate, they c:m subsist on root eltu(iates until they reach
the rool ..c~l.lonization occurs only in the un suberized onc behind the root tip.1be process of
colonization invo 'lies: (A) peneU'1l.tJon 0
ae between the cells of tile root cortex to fonn
a characteristic Hartig nct; (B) establishment of a mantle ofhypbae around the outside of the
root and (C) extension of hyphae from the mantle into the surrounding soil. The fungus
produces plant grov.rth hormones which cause the short roots of the pJantto grow fasler, to
bcrome thicker. and often 10 branch in chara<:lerislic ways (e.g. dichotomously).

8: UClion~1 vit,.

fig. 17.2 EClomycorrl"izas. A: ~tomOUS rnycorrJ-izai short roots d Pinus; B: 5eCOOoal view of
p;lrt of Hartig net, note th.1 cortical cel is cornplelely SlI"I'Olnded by hy~e; C: SU'face view of part
of H<trtig net, showilg c~ ilter\ocking hy~


The Hartig net may be restrieted 10 the outermost layer(s) of Ihe rOOI, or it may
spread slowly through the cortex until il reaches the endodermis. which effectively bars
any penetrntion of the stde. As the hyphae insinuate themsel ves belween the coni~81
I:<:lIs. these separnte at the middle lamella. and an almost complete single layer of fungal
hyphae eventually surrounds each cell. though plasmodesmata still connect many corti~al cells. Far from being dd<:lerious. the p~sence of me Hartig net actually seems to
prolong the life of the cortical cdls. and of lIle root as a whole. The fungal manlle surrounding the root varies from a relatively loose weft of hyphae to a thiCK. pseudopareuchymalou. layer which accounts for nearly halfllle biomass of the mycorrhi la. The formalion of root hairs by the plant is suppressed. since they have been rendered redundant by
mycelial strands andlor individual hyphae nldiating from the mmltle. Compared to nonmycorrhizal roots. ec tomycorrhizas are: (I) a different colour; (2) thicker; and (3) much
more often branched--pinnatt'ly and racemosely in Abiu, Fagus and Eucalyptus. and
dichotomously in Pinus. The trul y diagnostic stmcture, hoy,ever, is the Hart ig net. the
funl;tionai extracellular imerface belw~n the symbionlS (Fig. 17_2 B.C).
Individual eclOmycorrhizas re main active for up 10 three years. Roots and mantles
often e.... tend at me same [ate, but the roo! sometimes breaks through and grows beyond
the man!le. The root may then be colonized by orner opponunistic eClomyeorrhiza!
funSi. whic h may be better adapted than the original partner for lIle sp.!cific soil microhabitat being ~ncountcred. A lree may thus have a number of different fungal partners on
its roo t syS tem at the samc time. Many of the fungi responsible for ectotrophic mycorrhilaS can ~ i sol ~ted in axenic culture witllOlI! much difficulty. but mOSt will not fro it in
culture. grow slowly, and reljuire vitumin~ like thiamine. some amino acids. and other
normall)' root-derived substances, as we ll as simple carbohydrates. Most of them ar~
completely incapable of degrading cell ul ose or lignin, although these substances are the
principal diet of many othcr saprobic ba5idiomyc~tes. If wc add to this picture the infor,
mllion thlt, when not aS50ciatcd with a tree. the$<: fungi cannO{ compete With fungi of the
s.:lprobic soil mycOla and are ad~ersely affected by to:tins present in humus and leafliuer.
\Ie gain the impression that in nature these fungi are moreo! less obligate root symbionts.
Sug~rs are translocated from the root to the fungal mantle. whcre they are convened
into trehalose (a disaccharide). manni tol (a polyhydric alcohol). and glycogen-all typical fungal carbohydrates_The glycogen is insolublc, and therefore unlvli lable for pos~ibJe reubsorption by the plant. More surpri singly. although the mannitol and trehalose
rem~in in solution in the fungus. the plant is incapable cf reabsorbing them. T llU ~ the
fungli sh(:tth acts as a sink where reserves of carbohydrates derived from the plant arc
stor~d. This has some interesting con~equences. ( ~ ) As autumn approaches, many of the
fu ngi mobilizc tht' stored carbohydrates ilnd produce flushes of large mushrooms or hypo8eou~ fruit bodies near the tret'. (2) Carbohydrates can be translocated through mycdial
str.lnds from established trees 10 seedlings of the same species. Thi~ mUSI help in the
maintenance of pure stand~. (3) The lree can reclaim some of the stored energy if conditions berome appropriate for a new surge of growth.
How much does a Iree invt'st in its mycorrhi~al panners? rf we add up the various
or:;ans of the fungus---the conspicuous fruit bodies. the extensive thou gh inconspicuou~
mycelium rami fying through the soil. ~nd the rootlet mantles-we find that trecs often
inwst at least 10% of their total production of photosynthates in their m)cobionts. The
drain of photosynthat~s from the trce is clearly more than compensatcd for by th e increased eflickn(;), of mincral absorption. Ilnd by the fact that the funga l mantic can al ~o
store mineral nutrients, e.g .. chloride. ammonium. and especially phosphate. that aren' t
immediately nt'cded by the tree. These can subsequcntly be released to the plant during
periods of deficiency orof active growth. Since the mycorrhizal fO(){lcts arc perennial. the
mantle can repeatcdly act as a slornge organ when the root is not acting as a growing


organ. This, and the ability of the fungus to frui t massivel y during a relatiyely shon limewindow, indicate thai eClOmycorrh izal plants and fungi are both adapted to grow in
c1imnl es wherc seasonal changes arc often dramatic, causing wide fluctuations in growth
rate and in the supply of nutrients. T