Annual Reviews

www.annualreviews.org/aronline

Copyright
1975.All rightsreserved

ARABIDOPSIS AS A ~3086

GENETIC TOOL
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

G. P. R~dei
Department
of Agronomy,
Universityof Missouri,Columbia,Missouri65201
by CNRS-multi-site on 10/24/05. For personal use only.

SPECIAL FEATURES

Theintroductionof a neworganisminto the repertoire of genetic tools is justified

on the basis of its aptness for investigations of newproblems,for newapproaches
to old problems,or for testing the relevance of principles discoveredin phylo-
genetically distant groups. In this review manyimportant publications must
be omitted to provide for the non-Arabidopsis geneticist a general outline within
the limited available space. Recentreviewsare available (1, 2) with comprehen-
sive coverage.
Arabidopsisthaliana (L.) Heynh.is a floweringplant of the familyCruciferae.
Its experimentaluse had beensuggestedfirst by Strasburgerto yield information
on the continuity of chromosomes,a phenomenon not yet generally recognized
in 1907. Strasburger’s student, Laibach(3), foundthat in the interphase nucleus
the numberof heterochromatic bodies were identical with the numberof chro-
mosomesseen at metaphase, an uncommonphenomenonin the majority of
plants.
Additional advantages for genetic manipulations have been found: (a) the
diploid chromosome numberis five pairs (3, 4), and autotetraploids are cy-
tologically stable and genetically normal(5, 6); (b) all primary trisomics
morphologically distinguishable(4, 7); (c) the life cycle maybe completedwithin
one month or it may be extended to several, depending on photoperiodic
exposure (8, 9); (d) in the laboratory, outcrossing is maximallyin the -~
range (G. P. R6dei, unpublished), and in nature it does not exceed 2%(10,
11); (e) the seed output of a plant mayexceed 50,000; (f) for phenotypic
classification, 5-10 or moreplants maybe crowdedin 1 cmz area (12), making
it possible to study very large populations; (g) plants can be grownto maturity
on simple, well-definedmediain standardsize aseptic test tubes (13-15); liquid
culture is practical (16); and the callus growssatisfactorily in bothdiploid (17-20)
or haploid states and can be redifferentiated into plantlets (21); (h) a large

III
 Annual Reviews
www.annualreviews.org/aronline

number of ecological variants are available (I, 2); (i) it can be crossed
several species of different basic chromosome numbers (22-25). The major
advantage of Arabidopsis is that it can be subjected to manipulations common
to microorganisms, which are impractical in most other higher plants.

CYTOLOGY AND CYTOGENETICS

Thoughthe chromosomenumber is low (n = 5), cytological analysis is difficult

because the chromosomes are very small (4, 25). The nuclear volume is ap-
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

parently the smallest among the higher plants (26), and the DNAcontent
the diploid nuclei is estimated to be 4 x 10~ nucleotide pairs (26) or 0.8
(27), respectively. Thus, many diploid plant species have one or two orders
of magnitude more DNAthan Arabidopsis.
by CNRS-multi-site on 10/24/05. For personal use only.

Because of the characteristic phenotype of the trisomics and the large popula-
tions that can be classified, recombination between selected markers and the
centromere can be studied on a practical scale (7). Double reduction in triplex
tetraploids can also be detected genetically.
In mitosis the homologous chromosomes frequently display some degree of
loose association (4). Whenthe seeds, heterozygous for linked cell or tissue-
specific markers and carrying other flanking genes, are irradiated with X rays,
single and twin spots can be detected on the treated plants. In a few cases
the somatic sectors have given rise to seed-bearing shoots, and the actual ex-
change of markers as expected in somatic recombination has been verified (28,
29). This premeiotic recombination has not been observed to occur sponta-
neously. The frequent association of the exchange with reduced transmission
of the chromosomalstrands involved indicates that the mechanismis not crossing
over. Apparently, the sector formation is due to a reciprocal but unequal translo-
cation type of event, induced at the four-strand stage of mitosis. The cytologically
detected mitotic juxtapositioning of the homologues(4) provides a support for
the.genetic observations. Actually, only a few individuals have been subjected
to complete analysis, yet equally well-documented cases of mitotic marker
exchange are not available in other higher organisms (the body spots of Droso-
phila are not amenable to generative progeny tests).
A genetic method for localization of chromosomal defects or segregation
distorters was developed on the basis of the correlations amongreduced trans-
mission, segregation ratios, and recombination frequency proximal to the defect
(30, 31).
An unusual gametophyte factor without female transmission, yet with a higher
than 50%seed set, has been mappedto linkage group 2. The cytological observa-
tions revealed twin tetrads in the carrier’s ovules, and in cases of reverse orienta-
tion of the meiotic apparatus there was a preferential selection for the basal
megasporecontaining the normal allele (32, 33). In the Cruciferae, certain other
genera commonlydisplay multiple megaspore tetrads (34).
 Annual Reviews
www.annualreviews.org/aronline

ARABIDOPSIS AS A TOOL I 13

EVOLUTION AND SPECIATION

Arabidopsis and its relatives are widely spread on the earth, especially in the
northern hemisphere (1). The gene center is probably in western or northwestern
Europe. The most conspicuous variation is in the response of flowering to natural
day-length and temperature regimes (8, II, 35-40).
Induced mutants closely resembling natural ecotypes were observed (9, 41a, 42).
Under laboratory conditions some of the X-ray-induced mutants showed an
extremely high selective advantage in competition with the wild type (9).
Berger (24) attempted 194 different interspecific crosses with various related
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

genera, yet obtained viable offspring in only 6 combinations. H.vlandra suecica

(2n = 26) can be successfully hybridized with Arabidopsis (2n = 10), and Hylan-
dra and Cardaminopsis arenosa (2n -- 32) can also produce sterile hybrids (22,
23: G. P. R6dei, unpublished). The tetraploid C. arenosa does not set viable
by CNRS-multi-site on 10/24/05. For personal use only.

seed with diploid Arabidopsis (22,.24, 25; G. P. Redei, unpublished), yet hybrid
plants can be obtained if tetraploid Arabidopsis is Used as either the male or
female parent (G. P. R6dei, unpublished). Diploid Cardaminopsis petraea
(2n = 16) also yields sterile offspring with diploid A rabidopsis (25). Thebotanical
literature suggested (43) that Hvlandra is an amphiploid of C. arenosa and A.
thaliana. The experimentally produced amphiploid does not support this hy-
pothesis (25), though it forms semifertile offspring with Hvlandra (G. P. R~dei,
unpublished). Cytological observations indicate that the genera Hvlandra, Car-
daminopsis, and Arabidopsis share homologous chromosomal regions through
some commonancestor(s) (24). The various possible combinations among these
species may yield a continuous series of new chromosomaltypes of plants.

MUTATION

The short life cycle and small size makethe plants attractive for screening and
testing mutagenic agents (see reference 1 for review). Because of its extremely
small nuclear volume, Arabidopsis appears to be the most radiation-resistant
amongthe higher plants (26, 44).
Mailer (45, 46) has developed a procedure whereby the effectiveness
chemical or physical agents can be assessed immediately in the plants grown
from the seeds treated, obviating the. culture of an additional generation. In
the siliques (fruits) of the 1 plants, d ominant and r ecessive l ethals a s well
as chlorophyll-deficient mutants (arranged in a somewhat similar fashion as
the spores in an ascus) can be detected approximately two weeks after ferti-
lization. This methoddoes not reveal a distinction between the direct physio-
logical effects of the mutagens or the nature of the genetic effect, but it is a
fast and economical way to gat,her information on various agents.
An alternative rapid procedure for mutation detection is to score somatic
sectors in mutagen-treated heterozygotes (47-49). Although the majority
 Annual Reviews
www.annualreviews.org/aronline

114 R~OE~

known genes in Arabidopsis have cellular autonomy in expression (50), the

phenotypic classification of the sectors does not provide acceptable information
on the nature or mechanisms involved. One study revealed that by phenotypic
criteria over two thirds of the sectors may be misclassified (51). The locus
specificity of a genetic alteration can be determined in special cases by paper
or thinlayer chromatography (51) or by analysis of seed progeny of the sectors
(28, 52).
For the isolation of mutants, the best procedure is to apply the mutagen
to the diploid multieellular germ line of the seed or seedlings. The maximal
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

number of mutants can be obtained most economically if the size of the M1

generation is maximaland if the number of offspring in M2is kept at a minimum.
If 24 plants are classified in the progeny of a single heterozygote there is .999
P to recover at least one recessive mutant. If instead, 24 M z individuals derived
by CNRS-multi-site on 10/24/05. For personal use only.

from 10 M~plants are examined, the chance for recovery of one or more mutants
in a particular progeny is reduced to .500, yet according to the cumulative terms
of a binomial there are .623 or .945 chances to recover at least five or three
different mutants, respectively, in the combined populations. The desirable
progeny sizes can be calculated or read from statistical tables (53, 54). If the
size of individual Mz populations is small enough to minimize the repeated
recovery of any mutant produced by the same mutagenic event, the handling
of the families by pedigrees is obviated. The bulk progeny tested will give a
fair representation to the majority of the M1 plants because the Poisson distribu-
tion prevails in the seed withdrawal. Using a "fluctuation test," the independently
occurring mutations can be identified (53, 54). Mutation rate can be expressed,
then, on genomebasis (as used in microbial genetics) by simple determination
of the level of ploidy and the number of cells in the germ line. The number
of the genetically effective cells of the germ line can be deduced from the
segregation ratio in large progenies of individual plants. In Arabidopsis, in the
dry mature seed the germ line is represented by two diploid cells (54-56).
By the use of these procedures, the efficiency of mutant recovery may be
improved by an order of magnitude, and mutation rate can be expressed in
terms valid through phylogenetic boundaries (54, 55, 57).
Arabidopsis provides unique opportunities for the study of reverse mutation--a
phenomenon never demonstrated conclusively in higher plantsS-through the
availability of conditional lethal markers. Millions of multicellular diploid or
polyploid seeds can be easily produced from thiamine auxotrophs. Dominant
.revertants can be then selectively screened as sole survivors in the absence of
thiamine. In the presence of flanking markers, by the heterozygosity and segre-
gation ratio of the survivors, contaminations can be ruled out with absolute
safety. Unless the reversion takes place in the germ line at a single-cell stage,
the segregation ratio is not expected to be 3: 1, rather 3:5 or 3:37, depending
on whether the germ line was at the two- or ten-cell stage, respectively, at
the time of the back mutation (G. P. Rrdei, unpublished). The overwhelming
majority of reverted leaf color mutants gave evidence for the presence of sup-
pressor mutation (52).
 Annual Reviews
www.annualreviews.org/aronline

ARABIDOPSIS
AS A TOOL 115

AUXOTROPHY

Arabidopsis became better knownto geneticists after Langridge (58) discovered

a leaky, temperature-sensitive thiamine auxotroph having a defect in the phos-
phorylation of thiazole or in the condensation of thiazole and pyrimidine moie-
ties of the vitamin. Subsequently, obligate auxotrophs for the pyrimidine and
the thiazole half, as well as mutants blocked somewherein two steps of the
coupling reaction of these precursors, have been detected (15, 57, 59-62). Ap-
proximately 200 independently recovered thiamine auxotrophs are known at
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

four or more loci (G. P. R6dei, unpublished). The nutritional requirement ranges
from absolute to minimal. Practically all the thiamine mutants are indis-
tinguishable from the wild type on properly supplemented media.
Certain alleles at the pyrimidine locus display low or high temperature sensi-
by CNRS-multi-site on 10/24/05. For personal use only.

tivity (61) and allelic complementation (63). Circular complementation

were repgrted at other thiamine loci (64).
The enzymes involved in the thiamine pathway have not been studied directly.
The complementation data indicate, however, that they are at least dimeric
(63, 65) or multimeric (64).
The allelic complementation at the py locus served as a critical model for
the muchdebated overdominanceconcept of quantitative genetics and illustrated
the role of phenotypic stability in heterosis (66). The reality of superdominance
was indicated earlier by "monogenic heterosis" in an inferred (67) or tested
(68) isogenic background.
Mutants involved in the defective synthesis of thiazole or in the coupling
of this moiety to pyrimidine exhibited an increased requirement for thiamine
when the culture mediumcontained glucose or its disaccharide maltose. This
deleterious effect was in no apparent way connected with the disposal of ac-
cumulated pyruvate. Furthermore, mutants concerned with the synthesis of the
pyrimidine precursor of thiamine were immuneto this glucose effect. Most
likely, as in bacteria, this is a catabolite repression type of phenomenon(69).
In addition to the thiamine auxotrophs, mutants responding to coconut milk,
carbohydrates, choline (70), biotine, cytidine (41), cytosine, uracil, arginine,
cysteine, methionine, histidine, tryptophan, nicotinic acid, paraaminobenzoic
acid, ascorbic acid, and inositol (71) have been reported. Researchers in Du-
shanbe isolated two sublethal plastid mutants responding favorably to feeding
by DL-leucine (72-75). In these variegation mutants, leucine administration
restores the defective structures of the plastids and increases the activity of
photosynthetic carboxylase enzymes. Caution may be required to interpret the
data because the leucine auxotroph of barley responded equally well to sugar
and synthesized leucine without much hindrance (76). An arginine mutant
(77) of Arabidopsis turned out to be nonspccific and sugar-sensitive (78).
In my laboratory more nutritional mutants were isolated than the combined
number of auxotrophs reported in all higher plants, yet all those for which
a requirement could be identified turned out to be thiamine mutants. In a
number of cases favorable responses to antimetabolites were confirmed (79-83).
 Annual Reviews
www.annualreviews.org/aronline

116 Rl~DEI

An analysis of the literature reports on mutation frequency and spectra in

auxotrophy for nonphotoautotrophic organisms (bacteria and fungi), based
isolation under nonselective conditions, revealed that vitamin, amino acid, and
purine and pyrimidine mutants occur in these organisms over the entire spectrum
(57). In all lower and higher green plants the mutation spectr a for nutritional
requirements is very limited, however. In Arabidopsis, mutations concerned with
several steps of the thiamine pathway occur about as often as in microorganisms.
The same holds for the nicotinic acid pathway in Chlamydomonas eugametos
(G. S. Gowans, personal communication). Yet, in neither of these green plants
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

could true amino acid auxotrophs be isolated in spite of serious efforts. In C.

reinhardi, arginine mutants can be obtained, especially if the isolation media
are free from NH4-salts (R. Matagne and R. Loppes, personal communication).
Onthe basis of statistical inference, with the frequency of thiamine mutations
by CNRS-multi-site on 10/24/05. For personal use only.

as a baseline, approximately 4000 nonthiamine auxotrophs could be expected

in Arabidopsis," none were found in my laboratory. Several assumptions to explain
this failure lack experimental verification (57, 70).

ANTIMETABOLITE-RESPONSIVE MUTANTS

Mutants at four loci respond favorably to antimetabolites. This is surprising

because only at four loci were true auxotrophs found that required the exogenous
supply of metabolites (thiamine or precursors).

6-Azauracil
A large number of different alleles have been isolated in two laboratories at
a variegation locus, im. (81-83, 85, 86, 88). The recessive mutants are involved
in the control of the differentiation of the internal membranesof the plastids.
Within single cells all the plastids are arrested before the formation of thylakoids,
or all absolutely normal chloroplasts are formed as far as electron microscopy
can reveal. The cells displaying the two contrasting phenotypes are distributed
in a nonrandom pattern, simulating high somatic mutability. Progeny of the
different sectors reveals no difference, indicating that the absence or presence
of normal plastids is determined only by a defective regulatory mechanismof
gene function. Under high intensity continuous illumination in the plants that
are homozygous for certain alleles, practically all the cells lack functional chloro-
plasts. Under low light intensity and short daily cycles of illumination, the
mutants can be barely distinguished from the wild type. Homozygotesfor other
alleles may develop normal chloroplasts under all light regimes in the majority
of their cells. The mutants that produce a near albino phenotype can be induced
to produce a more normal appearance by heavy doses of X irradiation (84).
Similarly the analog, 6-azauracil (6AU), whenincorporated in the aseptic culture
media (at the 10-~ Mrange), may lead to a gradual restoration of plastid
differentiation in the late-developing tissues. After a few weeks culture on 6AU,
the mutants may produce two thirds as much leaf pigment as the wild type.
 Annual Reviews
www.annualreviews.org/aronline

~RABIDOPSIS
AS A TOOL 1 17

In the mutant plants grown on the analog, however, the internal structure of
the chloroplasts is strikingly different. Instead of the normally straight arrange-
ment of the lamellae, curly or almost ring-shaped thylakoids are found. The
membranedevelopment seems actually more intense in the mutants so treated
than in the wild type. The abnormal chloroplasts seem to function well in
photosynthesis as shown by the presence of numerous and large starch granules
(82, 87).
Several of the enzymes function normally even in the white tissues; however,
an acid ribonuclease (RNase, 2.7.7.17), orotidylic acid pyrophosphorylase
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

(O5PPase, 2.4.2.10), and orotidylic acid decarboxylase (O5PDase, 4.1.1.23)

overproduced in the cells when the mutation is expressed (82, 85, 88). Mutation
in a single gene may lead to a derepression of three enzymes simultaneously.
All three are involved in the de novo synthesis of pyrimidines or in the degrada-
by CNRS-multi-site on 10/24/05. For personal use only.

tion of RNA.The overproduction of the two pyrimidine enzymes leads to a

disturbed pyrimidine:purine ratio in RNA.In the plants grown on 6AUmedia
the level of RNase returns to near normal, O5PPase is reduced below normal
levels, while the amount of O5PDaseis increased even further. The incorporated
6AUis readily converted by the plant tissues to azauridylic acid, a potent
inhibitor of the activity of O5PDase.Thus, through the repression of O5PPase
and the inhibition of the activity of O5PDase,the flow of metabolites through
the de novo pyrimidine path is effectively reduced. This is indicated also by
the even higher than usual levels of O5PDase, an enzyme very sensitive to
negative feedback and to the reduction in the levels of the endproducts the
enzymeresponds to with derepression. The reduction in the level of the RNase
may be due to the reduction in the level of the abnormal base-composition
RNAthat it is supposed to dispose of. Furthermore, this RNasehas significantly
reduced affinity for 6AU-2:3phosphate (81). The determination of activity
the pyrimidine enzymes was supported also by product analysis starting from
14-C-orotic acid (88).
The anomaly at the im locus in Arabidopsis bears conspicuous similarities
with hereditary orotic aciduria in man (89, 90). Both cases are characterized
by cellular variegation (anisocytosis, poikilocytosis, leukopenia, and hypochromic
anemia in man) and a favorable response to 6AU. The regulatory mutations
in man involve a drastic reduction in the activity of one or both of these
pyrimidine enzymes, whereas in A rabidopsis an overproduction occurs; however,
in both organisms, a near normal flow of the metabolites is restored by the
same anal6g.

5-Bromodeo x yuridine
5-Bromodeoxyuridine (BrdU) or 5-bromodeoxycitidine (BrdC) are very
mutagens in Arabidopsis (90a), 5-1ododeoxyuridine (IdU) BrdU, and BrdC
-0
91) promote flower initiation in this plant at very low Concentrations (10
M range). A similar though somewhat lesser effect of 8-azaadenine has also
been observed (79).
 Annual Reviews
www.annualreviews.org/aronline

118 R~DEI

A series of mutants are available that have an altered flowering response

(9, 16). Mutants at the gi locus mayrequire for flower initiation a period several
times longer than that required for the wild type under continuous illumination,
while the difference is minimal under 8-9 hr of light per day. Mutants at the
co locus flower later than the wild type under continuous light, yet flower earlier
on short days. The ld mutants are flowering only somewhat later than the ld +,
in 24 hr light; however, under 8 hr daily illumination these plants cannot flower
at all. Mutants at all three loci are recessive, but eo becomes dominant under
short-day conditions. The Columbia wild type of Arabidopsis is a facultative
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

long-day plant. Whenhomozygous,the ld alleles display a critical requirement

for illumination beyond 9 hr per day.
In liquid culture media containing glucose or sucrose, all genotypes flower
earl), in continuous darkness. Onsolid media this plant does not grow appreciably
by CNRS-multi-site on 10/24/05. For personal use only.

in the dark. In total darkness (after a single 1 hr light period to induce germina-
tion) flower differentiation takes place earlier than under any light regime. This
fact shows that flowering itself is a constitutive process and is negatively con-
trolled under light. The flowering inhibitor seems to be produced only in light,
and all the mutants are concerned with the synthesis or function of an inhibitor(s)
or repressor(s) of the process.
BrdUis without effect in dark cultures, but it returns the phenotype of the
mutants to near wild type under continuous light, and even under short days
it induces fast flowering in all, except in the homozygotesfor the /d alleles.
The incorporation of the deoxynucleoside analogs into the nuclei (92) and DNA
has been shown (16).
Brown(93) has suggested that BrdUand homologues are preferentially incor-
porated into the actively dividing flank meristem cells of the vegetative apex
and thereby temporarily retard mitotic activity of these cells. This retardation
triggers mitotic activity in the central initiation zone. Subsequently, the analog
is removed from the whole apex, and flower differentiation is initiated. His-
tological studies in several species, including Arabidopsis, indicated that flower
development is accompanied by this pattern of apical activity (94).
Flower-inducing material, according to plant physiologists (95), is synthesized
primarily in the leaves rather than in the apex. BrdU is incorporated in all
tissues of the plant and replaces 7-10% of the thymidine residues in DNA.
This substitution is too high to be limited to single gene(s). BrdU-substituted
DNAhas been shown to bind very effectively nonhistone protein(s) of Arabi-
dopsis chromatin. This acid protein(s) seems to be involved in the initiation
of flowering (16). The suggestion was made [on the analogy of the lac system
in Escherichia coli (96)] that if this acid protein (repi’essor) is tightly bound
to DNA,the flowering inhibitor(s) cannot be transcribed. Alternatively one may
hypothesize [on the analogy of the mammalianinterpretation (97)] that inducer
protein(s) may dislodge the histones more easily from the BrdU-DNA.There
is no indication that in this system histone(s) are involved in the inhibition
of flower initiation in light. Actually the involvement of histone is unlikely
 Annual Reviews
www.annualreviews.org/aronline

ARABIDOP$IS AS A TOOL 1 19

on the basis of the dark experiments,since the synthesis of this protein is even
under different conditions of development.

MISCELLANEOUS STUDIES IN PHYSIOLOGICAL GENETICS

Onerecessive mutantwas found that could convert protochlorophyll to chloro-

phyll only whenextracts of the wild type have been provided (98). A lethal
mutantwithout chlorophyll b lacked the ability to polymerizesugar into starch
(99). Other mutants displayed altered chlorophyll a and b ratios (67). Viable
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

chlorophyll-b-free mutants were also found and located in linkage group 4

(100; G. P. R6dei, unpublished). The ultrastructure of the chloroplast of the
chlorophyll-b-free mutants is apparently normal(101), yet the photosynthetic
ability is reduced(102). Thedefect wasattributed to reductionof protochlophyl-
lide b and/or its holochrometo chlorophyllide b; at another locus a reduced
by CNRS-multi-site on 10/24/05. For personal use only.

binding of protein-pigment content was implicated (103).

Mutantswith increased total pigmentcontent, modifiedabsorption of pigment,
and variable function of the plastids were reported (104). Yellow-greenmutant
with carbonfixation conditionally superior to the wild type wasobserved(105).
The independenceof the level carbon fixation from the pigment content of
the mutants was noted (106).
Three maintypes of acid phosphataseisozymeshave been detected in natural
populations. Group1 is controlled by three codominantalleles of one locus.
Group2 is more anodic than group 1 and is also represented by the products
of three codominantalleles. Group3 is the most anodic and is determined
by two alleles only. The variations observedare attributed to differences in
charge rather than in size of the protein. Hybridbands have not been observed
(107, 108). A rapid screening techniquefor invertase-deficient mutantsis under
development(109).
Three different types of chlorate-resistant mutants have been isolated by
Feenstra’s laboratory (110, 111). A mutantat one locus is defective in chlorate
as well as in nitrate reductase and requires ammonium in the nutrient medium,
although it can take up both nitrate and chlorate; mutants at another locus
are defective in chlorate uptake and display normal or higher than wild-type
nitrate reductase activity. The mutantat the third locus lacks any detectable
chlorate or nitrate reductaseactivity and has excellent resistance to chlorate.
Arabidopsisand its close relatives are very sensitive to the breakdownproducts
of autoclavedfructose media.Fructoseis readily convertedinto small yet highly
toxic amountsof hydroxymethylfurfural, hydoxyacetylfuran, levulinic acid,
etc. Thesecompounds selectively repress the level of fructose-1,6-diphosphate,
and fructose-l-phosphate aldolase. Other enzymesof the glycolytic pathway
are practically unaffected, indicating that they are underindependentregulation
(112-114). This reaction of the plant to fructose bears somesimilarities
hereditary fructose intolerance in man.The humaninborn defect is characterized
by aldolase deficiency and adverse response to this hexose in the diet. Like
 Annual Reviews
www.annualreviews.org/aronline

120 R~DEI

the earlier mentioned variegation mutants that resemble hereditary orotic aci-
duria, this is another case where comparative studies may help to understand
the mechanisms when studied in such distant organisms.
Aminoacid-sensitive mutants have recently been identified. The genetic defect
seems to be associated with the regulation of the branched-chain amino acid
path (G. P. R6dei & G. Acedo, unpublished).

PLASTOME GENETICS

With X irradiation, maternally inherited plastid defects have been induced (115).
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

Halogenated deoxyribonucleosides (92) and acridine dyes were observed

induce odd types of non-Mendelian hereditary changes (116).
One nuclear gene mutant was found to induce only a specific type of plastome
alteration. The mutator itself exhibited Mendelian inheritance whereas the
by CNRS-multi-site on 10/24/05. For personal use only.

plastome alteration was transmitted only maternally, In the homoplastidic mu-

tant cells only osmiophilic globuli or small vesicles could be detected by electron
microscopy, while in cells containing a few normal chloroplasts even the defective
plastids could form some thylakoids (117).
Another chromosomal plastome mutator with two slightly different alleles
has been localized in linkage group 3. In contrast to the above-mentionedsystem,
the mutations affected not only the color but also the shape of the leaves, and
male and/or female fertility were also altered in a sectorial pattern. The fre-
quency of plastome mutation was very high and took place in both forward
and reverse direction. Within single cells, up to six different structural alterations
could be seen through the electron microscope. Not all the morphological
alterations of the plastids appeared defective. Onetype of mutant plastid could
be isolated in homoplastidic form in whole plants after the removal of the
mutator by repeated backcrossing with the wild type. This type of plastid
developed internal lamellae in normal or greater amounts; the thylakoids,
however, were irregular, undulated, or curly in shape and occasionally the
membranes showed some bulging. Photosynthetic activity must have been very
good, because in soil culture a copious amount of starch was seen in the mutant
chloroplasts. Other types of mutant plastids represented various defects in prac-
tically all steps of the differentiation of this organelle. Mitochondria or other
organelles wcrc apparently unaffected. ThE fact that homoplastidic mutant cells
could be obtained indicated that the genetic information carried by the 20-80
plastids is redundant. Because various types of plastids appeared within single
cells, lack of epistasis or dominance was inferred. One type of chloroplast
alteration involved sterility of the gametes and/or altered shape of the leaves,
indicating that these different phenes are determined by a single pleiotropic
mutation in the plastome, or perhaps a more plausible assumption is that they
are linked. Recombination could not be studied experimentally, however, be-
cause of technical difficulties (118, 119).
The numberof different types of plastome alterations could not be determined
accurately because intracellular environmental effects and mutationsoccurring
 Annual Reviews
www.annualreviews.org/aronline

ARABIDOPSIS
AS A TOOL 121

in different ontogenic stages could not be separated in the defective types. The
circumstantial evidence suggested that a large number of plastome sites can
respond to the mutator. The mutability of the chromosomal genes remained
unchanged in the presence of the mutator. The existence of nuclear mutator
genes, specific for the plastids, shows that the autonomyof the plastome is
limited, and most likely the control for the replication of the chloroplast genetic
material resides in the nucleus. On the other hand the plastome can control
characters (leaf shape, fertility, etc) that are commonlydetermined by nuclear
genes (118, 119).
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

A series of nuclear gene mutations was shown to determine sequential steps

of chloroplast differentiation independently from the plastome (120).

NOVEL MECHANISMS OF INFORMATION TRANSFER

by CNRS-multi-site on 10/24/05. For personal use only.

Transformation
In the last 15 years L~douxand his collaborators have studied the possibilities
of uptake and processing of macromolecules by the cells of higher organisms.
The main findings with Arabidot)sis as a recipient are only outlined here. Sur-
face-disinfected seeds were germinated for 4 days in tritium-labeled thymidine
(’~HT) or in aHT bacterial DNAof higher buoyant density than that of the
plant. Subsequently, at various stages of development, intact plants or different
organs were extracted and the density profile of the DNAwithin the plant
cell was analyzed in CsC1 gradients in the preparative ultracentrifuge. The
thymidine provided as such was taken up poorly by the plant and did not affect
the density ofArabidopsis DNA.The seeds treated with the foreign DNAhave
readily taken up the bacterial nucleic acid and incorporated it into plant genetic
apparatus. After incubation with E. coil (O: 1.710) or with Streptom),ces coelicolor
DNA(#: 1.730), the extracted plant DNAdisplayed, besides its normal density
peak (O: 1.698), newdensity fractions approaching that of the donors (p: 1.707
and 1.720, respectively). The intermediate density fractions were concentrated
in the cotyledons until flower development when a translocation to the flowers
was observed (121, 122).
When seeds were treated with Microccus lysodeikticus cold DNA(0:1.731)
and the growing plants were fed with :~HT, replication of that heavier than
the normal Arabidopsis DNAwas observed. The foreign DNAwas further traced
by density and labeling in subsequent three or more generations of the plants.
The label provided by 3HT alone was diluted out through the mitoses by the
time of new seed formation, in contrast, 10 50% of the 0.7 ng exogenous DNA
taken up by a seed was still present in the flowers and 1% was detected in
the following generation.
Alkali denaturation did not produce substantial.heterogeneity in the reex-
tracted plant-bacterial DNAcomplex, and only the expected density increase
that is characteristic for single-stranded molecules appeared. Sonication, in
contrast, yielded DNAwith a wide range of density, On the basis of these
experiments it was suggested that the foreign DNAis associated with the plant
 Annual Reviews
www.annualreviews.org/aronline

122 RI~DEI

genetic material end-to-end in covalently linked heteroduplexes (122) or

intercalated into the" chromosomesat nonspecific locations and functions like
episomes (123).
Whenmutants blocked at various steps of the thiamine pathway were treated
with DNAof a number of bacterial species, prototrophic plants were recovered
with the high 10 4 to 10 e frequencies. The thiazole mutant, however, could
not be corrected with DNAof a thiazole-negative E. coli but it was effective
for the pyrimidine mutant of the plant. Similarly, DNAof two bacteriophages
lacking the genetic information for thiamine synthesis failed to bring about
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

correction. The plants showing favorable response to the foreign DNAdeveloped

slowly as though their thiamine supply would have been insufficient. Actually
this is expected, because at the time of treatment, the seed contains thousands
of cells and it is most unlikely that a larger number of them could be corrected
by CNRS-multi-site on 10/24/05. For personal use only.

simultaneously. The most unexpected observation was made in the following

generation. The corrected plants appeared as homozygousprototrophs and failed
to yield auxotrophs by selfing. By the end of the treatment with the foreign
DNAthe germ line of the seeds must have had two or more diploid cells.
In case only one chromosome would have been corrected in the germ line of
any on~ individual, the expected mutant : wild-type ratio in the following gener-
ation corresponding to one-, two-, four-, or eight-cell germ lines would be 1:3,
5:3, 13:3, or 29:3, respectively. Recently, in the progeny of corrected plants,
fed with thiamine after DNAtreatment, wide segregation ratios have also been
observed (L. Ledoux, 1974, personal communication). For the failure of segrega-
tion of the corrected plants there is no rational genetic explanation. The correc-
tion appeared dominant in the crosses with the original auxotrophic line. In
later generations of the crosses with the wild type, only a few obligate auxotrophs
and a number of other leaky types were recovered (123).
It is desirable to release the results of experimentswith stocks carrying flanking
markers of the genes corrected. There is a need to transform stocks marked
on all chromosomalarms to makefeasible an analysis of the modeof association
of foreign DNA.More investigations are necessary on competence in eukaryotes.
All experiments have to be designed and conducted in such a way that the
results would be amenable to test by techniques of classical genetics.
The experiments as surveyed here are consistent. Biological studies are fully
appreciated, however, only by general reproducibility (124, 125).

Transgenosis
The term coined by Doy, Gresshoff & Rolfe (126) was defined as the "transfer
of genetic information from one cell to another, followed by phenotypic expres-
sion." This definition may include gametic union, though it was used in the
context of information transfer by specialized transducer phage from bacteria
to plants. The term "transduction" was avoided in the absence of knowledge
of the mechanism involved. From three main types of experiments actually
only one was performed with haploid Arabidopsis callus, while the others were
done with Lyco19ersicon. Tomatocells died on 2%percent galactose media except
 Annual Reviews
www.annualreviews.org/aronline

ARABIDOPSIS AS A TOOL 123

when 108 hpgal + particles were added. The gal- or lac + information was useless,
however. Similarly, the survival and growth of tomato callus on lactose media
was observed after the addition of q~8Oplac +. The production of a bacterial
enzyme within the plant cells was ascertained enzymologically and immunologi-
cally. Both tomato and Arabidopsis callus treated with phage ¢80supF+ contain-
ing the suppressor of an amber mutation proved deleterious, indicating that
the UAGcodon in the plants fulfills an essential, positive role. The mechanism
of transfer and the inheritance through the germ line have not been shown.
Technically. it may be feasible to use nucleic acid hybridization techniques to
see whether any DNAwas actually transferred in the process of transgenosis
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org

and whether isolated phage DNA would accomplish the same results as the
particles. Additional information is required before a comforting evaluation
concerning the meaning for geneticists can be made.
by CNRS-multi-site on 10/24/05. For personal use only.

ACKNOWLEDOMENT

This contribution from the Missouri Agricultural Experiment Station (Journal

Series No. 7218) was supported by NATOGrant No. 950.

Literature Cited
1. R6dei, G. P. 1970. Arabidopsis thaliana
(L.) Heynh. A review of the biology
and genetics. Bibliogr. Genet. 20(2):
1-151
2. R6dei, G. P. 1974. Arabidopsis thaliana.
Handbookof Genetics, ed. R. C. King,
2: Chap. 8, 1-51-80. NewYork: Plenufii
3. Laibach, F. 1907. Zur Frage nach der
Individualitat der Chromosomenim
Pflanzenreich. Beih. Bot. Cbl. 1 Abt.
22:5-24
4. Steinitz-Sears, L. M. 1963. Chromo-
some studies in Arabidopsis thaliana.
Genetics 48:483-90
5. Bouharmont, J. 1969. Evolution of
chromosome numbers in Arabidopsis
ol loids. Chromosomes Toda 2:
~9~01 ~Y
6. R~dei, G. P. 1964. Crossing experiences
with polyploids. Arabidopsis Inf Serv.
1:13
7. Lee-Chen,S., Steinitz-Sers, L. M. 1967.
Location of linkage groups in Arabi-
dopsis thaliana. Can. J. Genet. Cytol.
9:381-84
8. Laibach, F. 1951. i]ber sommer- und
winterannuelle Rassen von A rabidopsis
thaliana (L.) Heynh.-Ein Bcitrag zur
Atiologie der Blt~tenbildung. Beitr.
Biol. Pflanz. 28:173-210
9. R6dei, G. P. 1962. Supervital mutants
of Arabidopsis. Genetics 47:443-60
10. Shape. J. W., Lawrence, M. J. 1971.
The breeding system of Arabidopsis
thaliana. Heredity 27:299-302
11. Jones, M. E. 1971. The population
genetics ofArabidopsis thaliana. I. The
breeding system. Heredity 27:39-50
12. Myerscough,P. J., Marshall, J. K. 1973.
Population dynamics of Arabidopsis
thaliana (L.) Heynh.strain ’Estland’
different densities and nutrient levels.
New Phytol. 72:595 617
13. Laibach, F. 1943. Arabidopsis thaliana
(L.) Heynh. als Objekt ftir genetische
und entwicklungsphysiolog~sche Un-
tersuchungen. Bot. Arch. 44:439 55
14. Langridge, J. 1957. The aseptic culture
of Arabidopsis thaliana (L.) Heynh.
Aust. J. Biol. Sci. 10:243-52
15. R6dei, G. P. 1965. Genetic blocks in
the thiamine synthesis of the angio-
sperm Arabidopsis. Am. J. Bot.-52:
834-41
16. R6dei, G. P., Acedo, G., Gavazzi, G.
1974. Flower differentiation in Arabi-
dopsis. Stadler Genet. Symp. 6:135-68
17. Ziebur, N. K. 1965. Tissue culture.
Arabido, psis Inf. Serv. 2:34-35
18. Yokoyama,I(., Jones, W. H. 1965.
Tissue culture of Arabidopsis thaliana.
Plant. Physiol. 40:LXXVH (Abstr.)
19. Shen-Millcr, J., Sharp, W. R. 1966. An
improved mediumfor rapid initiation
of Arabidopsis tissue culture from seed.
Bull, Torrey Bot. Club 93:68-69
20. Anand, R. 1966. Preliminary studies on
callus culture of Arabidopsis thaliana.
Arabidopsis Inf Serv. 3:15
21. Gresshofl; P. M., Doy, C. M. 1972.
 Annual Reviews
www.annualreviews.org/aronline
124 RI~DEI
Haploid.4 rabidopsis thaliana callus and
plants from another culture..4ust. J.
Biol. Sci. 25:259-64
22. Laibach, F. 1958. i~lber den Artbastard
Arabidopsis suecica (Fr.) Norrl. ×
thaliana (L.) Heynh. und Cardami-
nopsis (C. A. Meyer) Hay. Planta
51:148 66
23. Kribben, F. J. 1965. Interspecific hy-
bridization with Arabidopsis..4rabi-
dopsis Research, ed. G. RObbelen,
26-30. GOttingen: Univ. GOttingen
24. Berger, B., 1968. Entwicklungsge-
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org
schichtliche und chromosomale Ursa-
chen der verschiedenen Kreuzungver-
tr~iglichkeit zwischen Arten des Ver-
wandtschaftskreises.4 rabidopsis. Beitr.
Biol. pflanz. 45:171-212
by CNRS-multi-site on 10/24/05. For personal use only.
25. MOsi~ek, J. 1967. The chromosome
morphology of Arabidopsis thaliana
(L.) Heynh. and some remarks on the
problem of Hylandra suecica (Fr.)
LOve. Folia Geobot. Phytotax. 2:
433-36
26. Sparrow, A. H., Price. H. J., Under-
brink, A. G. 1972. A survey of DNA
content per cell and per chromosome
of prokaryotic and eukaryotic orga-
nisms. Brookhaven Syrup. Biol. 23:
451-94
27. Bennett, M. D. 1972. Nuclear DNA
content and minimumgeneration time
in herbaceous plants. Pro¢. 1~. Soc.
London Set. B 181:109-35
28. Hirono, Y., ROdei, G. P. 1965. Induced
premeiotic exchange of linked markers
m the angiosperm Arabidopsis. Gene-
tics 51:519-26
29. Hirono, Y., ROdei, G. P. 1965. Concur-
rent products of premeiotic recombin-
ation. See Ref. 23, 85-90
30. Hirono, Y. 1964. A genetic method for
the localization of chromosome defects.
Genetics 50:255
31. Li, S. L. 1968. Genetics of thiamine
metabolism in Arabidopsis. PhDthesis.
Univ. Missouri, Columbia. 236 pp.
32. ROdei, G. P. 1965. Non-Mendelian
megagametogenesis in Arabidopsis.
Genetics 51: 857-72
33. ROdei, G. P. 1965. Genetic basis for
abnormal segregation. See Ref. 33,
91-99
34. Vandendries. R. 1909. Contribution ~
l’histoire du dOveloppementdes cruci-
f~res. Cellule 25:414-59
35. H~irer, L. 1951. l~ie Vererbung des
Bl0halters frt~her und sp~iter som-
mereinjahriger Rassen von Arabidopsis
thaliana (L.) Heynh.Beitr. Biol. Pflanz.
28:1-35
36. Napp-Zinn, K. 1962. ~Jber die gene-
tischen Grundlagen des Vernalisa-
tionsbed0rfnisses bei .4rabidopsis tha-
liana. I. Mitt. Die Zahl der beteiligten
Faktoren. Z. Vererbu,ngsl. 93:154-63
37. Napp-Zinn, K. 1963. ~ber den Einfluss
von Genen und Gibberelinen auf die
Blt~tenbildung von Arabidopsis tha-
liana. Ber. Dtsch. Bot. Ges. 76:77-89
38. Napp-Zinn, K. 1964. Ober genetische
und entwicklungsphysiologische
Grundlagen jahrszeitlicher Aspekte
von Pflanzengesellschaften. Beitri~ge
zur Phytologie, ed. K. Kreeb, 1-17.
Stuttgart: Ulmer
39. Ratcliff, D. 1961. Adaptation to habitat
in a group of annualplants. J. Ecol.
49:187-203
40. Grifling, B., Langridge, J. 1962. Phe-
notypic stability of growth in the self-
fertilized species, Arabidopsis thaliana.
Stat. Genet. Plant Breed Nat. Acad
ScL, Nat. Res. Counc. Publ. No. 982:
368-94
41. Lan~ridge, J., Grifting, B. 1959. A study
of h~gh temperature lesions in Arabi-
dop~is thaliana. .4ust. J. BioL Sei.
12:117-35
41a. Reinholz, E. 1947. AuslOsung von
ROntgen-mutationen bei Arabidopsis
thaliana (L.) Heynh. und ihre Bedeu-
tung ft~r die Pflanzenzt~chtung und
Evolutionstheorie. Field
T Inf. .4gem
Tech. Retd. 1006:1-70
42. McKelvie, A. D. 1963. Studies in the
induction of mutations in Arabidopsis
thaliana (L.) Heynh. Radiat. Bot.
3:105-23
43. LiSve, A. 1961. Hylandra-A new genus
of the cruciferae. Sven. Bot, Tidskr.
55:211-17
44. S.parrow, A. H., Schwemmer,S., Bot-
tmo, P. J. 1973. Influence of dose,
environmental conditions and nuclear
volume on survival times in several
~ amma-irradiated species. Int. J. Ra-
iat. Biol. 24:377-88
45. Mtiller, A., 1963. Embryonentest zum
Nachweis recessiver Letalfaktoren bei
Arabidotgsis thaliana, Biol. Zentralbl.
82:133-63
46. Miiller, A. J. 1965. On the chimerical
structure of M~plants. See Ref. 23,
152-53
47. Fujii, T. 1964. Radiation effects on
.4rabidopsis thaliana I. Comparative
efficiencies of 3,-rays, fission and 14
Me¥ neutrons in somatic mutation.
,lpn. J. Genet. 39:91-101
48. Gichner, T., Veleminsk~,,J., eds. 1965.
Induction of chlorophyll chimeras by
X-rays and ethyl methanesulfonate in
different heterozygous strains of Ara-
 Annual Reviews
www.annualreviews.org/aronline
bidopsis thaliana. Induction of Muta-
tions and the Mutation Process. 27-29.
Praha: Czech. Acad. Sci.
49. Hirono, Y., Smith, H. H., Lyman, J.
T., Thompson, K. H., Baum, J. W.
1970. Relative biological effectiveness
of heavy ions in producing mutations,
tumors, and growth inhibition in the
cruciferplant, Arabidopsis. Radiat. Res.
44:204-23
50. R6dei, G. P. 1967. Genetic estimate of
cellular autarky, E~perientia 23:584
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org
51. R6dei, G. P., Li, S. L. 1969. Effects
of X-rays and ethyl methanesulfonate
on the chlorophyllb locus in the soma
and on the thiamine loci in thegerm
line of Arabidopsis. Genetics 61:453-59
52. RObbelen, G. 1972. Untersuchungen
by CNRS-multi-site on 10/24/05. For personal use only.
zur genetischen Charakterisierung von
induzierten phanotypischen Rever-
sionen bei Arabidopsis Mutanten. Z.
Pflan:enziicht. 67:117-96
53. R6dei. G. P. 1974. Economyin muta-
tion experiments. Z. Pflanzenzi~cht.
73:87-96
54. R6dei, G. P. 1975. Induction of auxo-
trophic mutations in plants. Genetic
Manipulations in Higher Plants, ed. L.
Ledoux. 329-50. London: Plenum
55. Li, S. L., R6dei, G. P. 1969. Estimation
of mutation rates in autogamous dip-
loids. Radiat. Bot. 9:125-31
56. R~dei, G. P. 1974. Analysis of the dip-
loid germ line of plants by mutational
473-76techniques’Can. J. Genet.Cytol. 16:
57. Li, S. L., R6dei, G. P., Gowans,C. S.
1967. A phylogenetic comparison of
mutation spectra. Mol. Gen. Genet.
100:71-83
58. Langridge, J. 1955. Biochemical muta-
tions in the crucifer Arabidopsis tha-
liana (L.) Heynh. Nature London
176:260-6I
59. R~dei, G. P. 1960. Genetic control of
2,5-dimethyl-4-aminopyrimidine re-
quirement in Arabidopsis thaliana.
Genetics 45:1007
60. R6dei. O. P. 1962. Genetic block of
"vitamin thiazole" synthesis in Arabi-
dopsis. Genetics 47:979
61. Li. S. L., R6dei, G. P. 1969. Thiamine
mutants of thc crucifer Arabidopsis.
Biochem. Genet. 3:163 70
62. Feenstra, W. J. 1964. Isolation of nutri-
tional mutants in Arabidopsis thaliana.
Genetiea 35:259 69
63. Li. S. L.. R~dei, G. P. 1969. Allelic
complementation at the pyrimidine
(py) locus of the crucifer. Arabidopsis.
Genetics 62:281-88
64. Feenstra, W. J. 1967. Complementatie
ARABIDOPSISAS A TOOL 125
van thiamineless mutanten bij Arabi-
dopsis thaliana. Genen Phaenen 11:46
65. R6dei, G. P., Li, S. L. 1969. Physio-
logical resolution of the py locus of
Arabidopsis by means of allelic com-
plementation. Proc. XI Int. Bot. Congr.
Abstr. 178
66. Li. S. L.. R~dei. G. P. 1969. Direct
evidence for models of heterosis pro-
vided by mutants of Arabidopsis
blocked in the thiamine pathway.
Theor. Appl. Genet. 39:68-72
67. RObbelen, G. 1957. Untersuchungen an
strahleninduzierten Blattfarbmutanten
von Arabidopsis thaliana (L.) Heynh.
Z. lndukt. Abstamm. Vererbungsl.
88:189-252
68. R6deiG P 1962
.... Singlelocusheterosis
Z. Vererbungsl. 93:164-70
69. Li, S. L., R6dei, G. P. 1969. Genelocus
specificity of the glucose effect in the
thiamine pathway of the angiosperm
Arabidopsis. Plant Physiol. 44:225-29
70. Langridge, J. 1958. A hypothesis of
developmental selection exemplified by
lethal and semilethal mutants of Ara-
bidopsis. Aust. J. Biol. Sci. 11:58-68
71. Jacobs, M, 1965. lsolement de mutants
biochimiquechezArabidopsis thaliana.
M6thodeset r6sultats pr61iminaires.
Bull. Acad R. Belg. Set. 5. 51:735-47
72. Kasyananenko, A. G.. Nasyrov, Y. S..
Smolina, E. A. 1972. Leucine mutations
of Arabidopsis thaliana. Genetic
Aspects of Photosynthesis, ed. Y. S.
Nasyrov, 56-76. Dushanbe Tadzhikis-
tan, USSR: Donish. (in Russian)
(Chem. Abstr. 78:93057)
73. Babdzhanova. M. A.. Khaitova, L. T..
Kasyanenko, A. G. 1971. Action ofleu-
cine on the potential intensity of photo-
synthesis and on the activity of en-
zymes responsible for the fixation of
carbon dioxide in original and mutant
forms of Arabidopsis. Dokl. Akad.
Nauk Tad:h. SSR 14(5):50-52 (Chem.
Abstr. 76:560)
74. Labadakhanova, M. A., Khaitova, L.
T. 1972. Activity of carboxylation en-
zymes and potential intensity of pho-
tosynthesis m an auxotroph~c mutant
of Arabidopsis thaliana. See Ref. 72.
133 42 (Chem. Abstr. 78:80227)
75. Abdullaev. K. A., Usmanov, P. D.,
Nasyrov, Y. S. 1972. Heteroplastids in
cells of the mutant 40/3 of Arabidopsis
thaliana (L.) Heynh. Dokl. Akad. Nauk
Tadzh. SSR 15(8):48-50 (Biol. ~Abstr.
55:66544)
76. Land, J. B.. Norton. G. 1970. The
nature of the leucine ~requirement of
the barley mutant Xan-b . Genet. Res.
15:135-37
 Annual Reviews
www.annualreviews.org/aronline
126 R~DEI
77. Corcos, A. 1973. Isolation of an ar-
ginine mutant in Arabidopsis thaliana,
Genetics 74:June Suppl., s53
78. Corcos, A. 1974. Complications with
an "arginine mutant."/lrabidopsis Inf
Serv. 11:3
79. Hirono, Y., R6dei, G. P. 1966. Acceler-
ation of flowering of the long-day plant
Arabidopsis by 8-azaadenine. Planta
68:88 93
80. Hirono, Y., R6dei, G. P. 1966. Early
flowering in Arabidopsis induced by
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org
DNAbase analogs. Planta 71:107-12
81. R6dei, G. P. 1967. Suppression of a
genetic variegation 15~, 6-azapyrim-
idines. J. Hered 58:229-35
82. R6dei, G. P., Chung, S. C., Plurad, S.
B. 1974. Mutants, antimetabolites and
by CNRS-multi-site on 10/24/05. For personal use only.
differentiation. BrookhavenSyrup. Biol.
25:281-96
83. R6dei, G. P. 1965. Genetic control of
subcellular differentiation. See Ref. 23,
119-27
84. R6dei, G. P. 1967. X-ray induced
phenotypic reversions in Arabidopsis.
Radiat. Bot. 7:401-7
85. R~dei, G. P. 1967. Biochemical aspects
of a genetically determined variegation
in Arabidopsis. Genetics 56:431-43
86. RObbelen, G. 1968. Genbedingte Rot-
iichtempfindlichkeit der Chloroplas-
tendifferezierung bei Arabidopsiy.
P lanta8-O:237-5zl
87. Chung, S. C., R6dei, G. P., White, J.
A. 1974. Plastid differentiation on 6-
azauracil media. Experientia 30:92-94
88. Chung, S. C., R6dei, G. P. 1974. An
anomaly of the genetic regulation of
the de novo pyrimidine pathway in the
plant Arabidopsis. Biochem. Genet.
11:441-53
89. Pinsky, U, Krooth, R. S. 1967. Studies
on the control of pyrimidine biosyn-
thesis in humandiploid cell stratus,
I. Effect of 6-azauridine on cellular
~P7henotype.
:925-32 Proc. Nat. A~ad. Sci. USA
90. Smith, U H. Jr., Huguley, C. M. Jr.,
Bain, J. A. 1972. Hereditary orotic
aciduria. The Metabolic Basis of In-
herited Disease, ed. J. B. Stanbury, J.
B. Wyngaarden0 D. S. Fredrickson,
1003-29. NewYork: McGraw-Hill. 3rd
ed.
90a. Hirono, Y., Smith, H?~I. 1969. Muta-
tions induced in Arabidopsis by DNA
nucleoside analogs. Genetics 61 : 191-99
91. Brown,J. A. M. 1962. Effect of thymi-
dine analogues on reprodnctive mor-
phogenesis in Arabido~osisthaliana (L.)
Heynh. Nat_ure London 196:51-53
92. Brown, J. A. M., Smith, H. H. 1964.
Incorporation and effects of thymidine
analogues in gametophytic tissue of
Arabidopsis thbliana. Mutat.- Res. 1:
45-53
93. Brown, J. A. M. 1972. Distribution of
3 H-thymidinein Arabidopsis vegetative
meristems after 5-iododeoxyuridine
treatment. Am. J. Bot. 59:228-32
94. Besnard-Wibaut, C. 1966. Etude histo-
autoradiographique des modifications
du fonctionnement apical de l’Arabi-
dopsis thaliana (L.) Heynh. en photo-
periode d6favorable /~ la floraison.
C R. Acad ScL Paris 263D:1582-85
95. Chailakhyan, M. K. 1968. Internal fac-
tors of plant flowering. Ann. Rev. Plant
Physiol. 19:1-36
96. Lin, S. Y., Riggs, A. D. 1972. Lac
operator analogues: bromodeoxyuri-
dane substitution in the lac operator
affects the rate of dissociation of the
lac repressor. Proc. Nat. Acad. Sci.
USA 69:2574-76
97. Stein, G. S., Stein, J. S., Kleinsmith,
L. J. 1975. Chromosomalproteins and
gene regulation. Sci...A m. 232(2) :46-57
98. R6bbelen, G. 1956. Uber Protochloro-
phyllreduktion in einer Mutante yon
Arabidopsis thaliana (L.) Heynh. Planta
47:532--46
99. R6bbelen, G. 1957. Eine Blattfarbmu-
tante ohne Chlorophyll b von Arabi-
dopsis thaliana (U) Heynh. Naturwiss-
enschaften 44:288-89
100. Hirono~Y., R6dei, G. P. 1963. Multiple
allelic control of chlorophyll b level-in
A rabidopsis thaliana. Nature London
197:1324-25
101. Veleminsk~, J., R6bbelen, G. 1966.
Beziehungen zwischen Chloro-
phyllgehalt und Chloroplastenstruktur
m einer chlorina-Mutante von Arabi-
dotTsis thaliana. Planta 68:15-35
102. Kranz, A. R. 1968. Endogene und exo-
gene Beeinflussung der apparenten
Strahlungenergienutzung annueller
Pfl~nzen. A ngew. Bot. 51:271-78
103. Kranz, A. R. 1973. Monogenkontrol-
lierte Langzeit-Transformationen der
Chlorophylle in Bl~ittern yon Arabi-
dot~sis thaliana (L.) Heynh. Z. Pflan-
zenphysiol. 70:333 49
104. Kasyanenko, A. G., Timofeyev-
Resovsky, N. V. 1967. On some inter-
esting "chlorophyll" mutations in A ra-
bidopsis thaliana (L.) Heynh, Byull.
Mosk. Obsch. lspyt. Prir. Otd Biol.
72:100-105
105. Babava, T. N. 1971. Intensity of pho-
tosynthesis of Arabidopsis thaliana
mutants depending on the carbon diox-
ide concentration. Fotosin. Ispolz. Sol.
 Annual Reviews
www.annualreviews.org/aronline
Energ., ed. O. V. Zalenskii, 254-57.
Leningrad: Nauka (Chem. Abstr.
77:98882)
106. Svachulov~.. J. 1971. Carbon-~4Cdiox-
ide fixation, ribulose 2,5-diphosphate
carboxylase activity, and free sugar
content of two chlorophyll mutants of
Arabidopsis thaliana..Photos),nthetica
5:249-57
107. Jacobs, M., Schwind, F, 1973. Genetic
control ofisozymes of acid phosphatase
in Arabidopsisthaliana. Plant Sci. Lett.
1:95-104
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org
108. Jacobs, M., Schwind, F. 1975. Biochem-
ical ~genetics of Arabidopsis acid
phospnatases: polymorphism, tissue
expression and genetics of AP1, AP e,
and AP~loci. lsozymes, ed. C. L. Mar-
kert, 4:349-69. NewYork: Academic
by CNRS-multi-site on 10/24/05. For personal use only.
109. D’Souza, E. S., Maher, E. P. 1974. A
screening technique for mutants lack-
ing invertase activity. Arabidopsis lnf
Serv. 11:25
110. Oostindier-Braaksma, F. J., Feenstra.
W. J. 1973. Isolation and charac-
terization of chlorate-resistant mutants
of Arabidopsis thaliana. Murat. Res.
19:175-85 .
111. Oostindier, F. J., Fccnstra, W. J. 197~i.
Nitrate reduction in Arabidopsis tha-
liana. Arabidopsis lnf Serv. 11:8
112. R6dei, G. P. 1974. "Fructose effect’"
in higher plants. Ann. Bot. 38:287-97
113. R6dei, G. P. 1973. Effects of the degra-
dation products of fructose on the gly-
colytic pathway. Z. Pflanzenphvsiol.
70:97-106
114. R6dei, G, P. 1973. Effects of autoclaved
fructose media on metabolites in three
cruciferous plants. Z, Pflanzenph.t’siol.
70: 107-14
115. R6bbelen, G. 1962. Plastommutationen
nach ROntgcnbestrahlung yon Arab#
dopsis thaliana (L.) Heynh. Z. Verer-
bungsl, 93:25-34
116. Jacobs. M. 1969. Action of acridine
dyes on Arabidopsis thaliana plants
and their descendants. Bull. Soc. R.
Bot. Belg. 102:43-59
ARABIDOPS1SAS A TOOL 127
117. R6bbelen, G. 1966. Chloroplastendif-
ferenzierung nach geninduzierter Plas-
tommutation bei Arabidopsis thaliana
(k.) Heynh. Z. Pflanzenphysiol.
55:387-403
118. R6dei, G. P. 1973. Extra-chromosomal
mutability determined by a nuclear
gene locus in Arabidopsis. Murat. Res.
18:149-62
119. R~dei, G. P., Plurad, S. B. 1973. He-
reditary structural alterations of plas-
rids induced by a nuclear mutator gene
in A rabidopsis. Protoplasma77: 361 - 80
120. RObbelen, G. 1959. Untersuchungen
fiber die Entwicklung der submikro-
skopischen Chloroplastenstruktur von
Arabidotgsis thaliana. Z. Vererbungsl.
90:503 6
121. Ledoux,L., Huart. R., Jacobs, M. 1971.
Fate of exogenous DNAin Arabidot~sis
thaliana. Translocation and integration.
Eur. J. Biochem. 23:96-108
122. Ledoux,L., Huart, R., Jacobs. M. 1971.
Fate of exogenous DNAin Arabidopsis
thaliana, lk Evidence for replication
and preliminary results at the b~ological
level. Informative Moleculesin Biologi-
cal Systems, ed. L. Ledoux, 159-75.
Amsterdam: North-Holland
123. Ledoux, L., Huart. R., Jacobs, M. 1974.
DNA-mediated genetic correction of
thiamineless Arabidopsis thaliana. Na-
ture London 249:17-21
124. Holl, F. B., Gambor~,O. L., Ohyama,
K., Pelcher, L. 1974. Genetic trahsfor-
mation in plants. Tissue Culture and
Plant Science, ed. E. H. Street, 301-27.
London:Academic
125. Johnson, C. B., Grierson, D. 1974. The
uptake and expression of DNAby
plants. Curr, Adv. Plant Sci. 9:1-12
126. Doy, C. H., Gresshoff. P. M., Rolfe,
B. G. 1973. Biological and molecular
evidence for the transgenosis of ~enes
from bacteria to plant cells. Proc. Nat.
Acad Sci. USA 70:723~26
Annu. Rev. Genet. 1975.9:111-127. Downloaded from arjournals.annualreviews.org
by CNRS-multi-site on 10/24/05. For personal use only.