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When Earth started blooming: insights from the fossil record

Else Marie Friis1, Kaj Raunsgaard Pedersen2 and Peter R Crane3


Recent palaeobotanical studies have greatly increased the
quantity and quality of information available about the structure
and relationships of Cretaceous angiosperms. Discoveries of
extremely well preserved Cretaceous flowers have been
especially informative and, combined with results from
phylogenetic analyses of extant angiosperms (based mainly on
molecular sequence data), have greatly clarified important
aspects of early angiosperm diversification. Nevertheless,
many questions still persist. The phylogenetic origin of the
group itself remains as enigmatic as ever and, in some cases,
newly introduced techniques from molecular biology have
given confusing results. In particular, relationships between the
five groups of extant seed plants remain uncertain, and it has
sometimes proved difficult to reconcile estimates of the time of
divergence between extant lineages made using a molecular
clock with the fossil record. One result, however, is becoming
increasingly clear: a great deal of angiosperm diversity is
extinct. Some groups of angiosperms were evidently more
diverse in the past than they are today. In other cases, fossils
defy assignment to extant groups at the family level or below.
This raises the possibility that evolutionary conclusions based
solely upon extant taxa that are merely relics of groups that
were once much more diverse might be misled by the effects of
extinction. It also introduces the possibility that some early
enigmatic fossils might represent lineages that diverged from
the main line of angiosperm evolution below the most recent
common ancestor of all extant taxa. These, and other
questions, are among those that need to be addressed by
future palaeobotanical research.
Addresses
1
Department of Palaeobotany, Swedish Museum of Natural History,
Box 50007, SE-104 05 Stockholm, Sweden
2
Department of Geology, University of Aarhus, Universitetsparken,
DK-8000 Arhus C, Denmark
3
Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK
Corresponding author: Friis, Else Marie (else.marie.friis@nrm.se)

Current Opinion in Plant Biology 2005, 8:512


This review comes from a themed issue on
Growth and development
Edited by Liam Dolan and Michael Freeling

his widely cited letter to Joseph Hooker in 1879, remains


as one of the most persistent puzzles in modern evolutionary biology. Although much has been written on this
topic, a convincing understanding of how angiosperms
originated remains to be developed. One impediment to
progress is the apparent evolutionary distance that separates angiosperms from other living seed plants, and that
obscures morphological homologies. Another difficulty is
our poor knowledge of the enormous diversity of extinct
plants from the Mesozoic, some of which might be
relevant to our understanding of how specific angiosperm
features, such as the flower, carpel and stamen, might
have evolved from the reproductive structures of fossil
gymnosperms. However, although the enigma of angiosperm origin remains intractable, recent advances in
biology and palaeontology have contributed to a much
clearer picture of angiosperm diversification, including
some of the earliest known phases that occurred during
the Early Cretaceous.
Large-scale molecular analyses have resulted in increasingly well-supported models of angiosperm phylogeny,
including patterns of relationships among those extant
orders and families that appear to have differentiated
early in the evolution of the group [13]. Studies of plant
morphology have also provided new insights into the
distribution of critical reproductive characters among
these extant taxa [4,5]. At the same time, palaeobotanical
and palynological studies of Cretaceous angiosperms
[615,16,17] have generated a wealth of new data that
are pertinent to understanding the timing of major evolutionary events in angiosperm history. Most recently,
studies integrating results from molecular sequence data
with those from the fossil record have begun to offer new
insights into diversification rates and the age of different
angiosperm clades [18,19,20,21,22,23,24]. In this
review, we focus on the recent accumulation of palaeobotanical data on angiosperm floral structures from the
Cretaceous, and the implications of these discoveries for
our current understanding of angiosperm diversification
in time and space.

Available online 25th November 2004

First major radiation of angiosperms

1369-5266/$ see front matter


# 2005 Elsevier Ltd. All rights reserved.

The fossil record provides unequivocal evidence for the


presence of diverse angiosperm assemblages in the Early
Cretaceous, and indicates that many major lineages of
extant angiosperms were already differentiated by the
early Late Cretaceous. It has also become clear that there
was a distinctive and regular expansion in the diversity
and complexity of angiosperms over a relatively short
interval through the mid- to late-Early Cretaceous
(HauterivianBarremianAptianAlbian), and that this

DOI 10.1016/j.pbi.2004.11.006

Introduction
The sudden appearance of angiosperms in the Cretaceous, highlighted by Darwin as an abominable mystery in
www.sciencedirect.com

Current Opinion in Plant Biology 2005, 8:512

6 Growth and development

is paralleled by a marked increase in angiosperm abundance during the same period. This general pattern of
angiosperm diversification was first elaborated on the
basis of morphological evidence from pollen and leaves
[6,7], but a similar stratigraphic increase in diversity and
structural complexity is also seen among Cretaceous
flowers that have been discovered over the past 25 years.

and age estimates of the same divergence obtained using


different approaches can vary by tens of or even hundreds
of millions of years. In addition, because most analyses
use fossil taxa as calibration points, they face the same
challenges and uncertainties as traditional palaeobotanical studies regarding the reliability of these points
[23,55].

Following the first major discovery of fossil flowers from


the Late Cretaceous in Sweden [25], many new sites with
angiosperm flowers have also been discovered. In the past
few years, much new information about Cretaceous flowers has been accumulated from fossils from Europe
[12,2630,31,32,33], North America [3438], Asia
[15,39,40,41,42,43], South America [44,45], New
Zealand [46] and Antarctica [47], covering most of the
stratigraphic column from the mid-Early Cretaceous
(BarremianAptian) to the end of the Cretaceous (Maastrichtian). The fossil flowers are often preserved as charcoalifications, which were formed as a result of fire in
Cretaceous vegetation, and typically retain their original
three-dimensional shape. Many flowers also have pollen
grains in situ, thereby providing an invaluable link to the
dispersed pollen record. This link is of great importance
for phylogenetic biogeography and for understanding the
tempo and mode of angiosperm diversification.

An important motivation behind attempts to understand


the time of divergence of different angiosperm lineages is
to clarify the changing pattern of angiosperm diversity
through time. This will help us to better understand how
the extraordinarily high current levels of angiosperm
diversity have arisen. Early studies approached this issue
by quantifying the changing composition of the palaeobotanical record through time [56]. More recently, an
alternative approach has been to compare the estimated
time of origin of different angiosperm clades with their
present day diversity. This approach indicates that, typically, species-rich clades are relatively young and are
nested among the more derived lineages of monocots or
eudicots [18,57]. Clades that have extremely low levels of
species diversity are typically more ancient and diverged
close to the root of either angiosperms or of major angiosperm subgroups [18]. Magallo n and Sanderson [18] suggested that ancient species-poor clades are probably
relicts of groups that experienced early diversification
followed by extinction. Although these kinds of studies,
which integrate palaeobotanical data with insights from
molecular biology, offer considerable potential for future
research, there are also many difficulties that remain to be
overcome. This is illustrated below by two examples from
the fossil record.

Relationships of angiosperms
Resolving the relationships of angiosperms to other seed
plants is crucial to understanding the origin of the group.
In the mid-1990s, a consensus developed that Gnetales
were the closest living relatives to angiosperms, and that
the extinct Bennettitales and certain Mesozoic seed
ferns were also important for understanding the origin
of the group. More recently, however, attempts to resolve
relationships among extant seed plants using molecular
sequence data do not support a close relationship
between angiosperms and Gnetales, and instead have
suggested a range of alternative phylogenetic patterns
[48,49]. As a result, the relationships of angiosperms
remain uncertain and the prospects for understanding
the origin of characteristic angiosperm features, such as
the carpel and stamen, are as remote as ever.

Diversification rates and ages of angiosperm


lineages
In terms of understanding angiosperm diversification, an
interesting recent development attempts to use rates of
molecular divergence to estimate the timing of deep
splits between angiosperm lineages. This research
requires converting genetic distances into absolute ages
using different kinds of molecular clock assumptions
[19,20,22,23,24,5053]. Currently, much attention
continues to be directed towards developing and testing
methods that can help mitigate the difficulties posed by
the strikingly different rates of molecular evolution in
different angiosperm lineages [54]. Results are confusing
Current Opinion in Plant Biology 2005, 8:512

Chloranthaceae
Dispersed pollen assigned to the fossil genus Asteropollis
is among the first evidence of angiosperms to appear in
the Cretaceous and shows an almost worldwide distribution during the Early and mid-Cretaceous [58,59]. Close
morphological and ultrastructural resemblance between
the pollen of Asteropollis and that of extant Hedyosmum
(Chloranthaceae) has long been documented [60], and
this link has been confirmed by the discovery of pollen
grains of the Asteropollis type inside Cretaceous flowers
that possess all of the critical floral features of extant
Hedyosmum [58,61]. On the basis of molecular data, a midCainozoic age (45 million years ago) was suggested for the
initial divergence of extant Hedyosmum species [20].
However, Eklund et al. [59] showed that the Cretaceous
fossils fit equally well below, within or above the three
basal species of extant Hedyosmum (Figure 1). Taking into
account the proposed late divergence of the crown group
Hedyosmum, which include all extant and extinct species
that diverged after the origin of the most recent common
ancestor, they argued that a stem-group position for the
fossils is more likely, implying that not all defining
features (synapomorphies) of the genus were present in
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Floral evolution Friis, Pedersen and Crane 7

Figure 1

Age Mya

Crown group

Crown group

Fossil pollen and flowers with


distinctive Hedyosmum features

Paleogene

Origin of crown group


Origin of some defining
features of Hedyosmum
Origin of all defining
features of Hedyosmum

65

Lineage divergence
Stem representatives
Sister group lineage

Early Cretaceous

Mesozoic

Late Cretaceous

Cainozoic

Neogene

First unequivocal angiosperm pollen

Jurassic

144.2
(a)

(b)

Two alternative scenarios for the age of crown-group Hedyosmum (Chloranthaceae). (a) Plants with all the defining features of modern
Hedyosmum (crown-group Hedyosmum) are old and originated soon after the lineage divergence between Hedyosmum and its sister group.
According to this scenario, modern Hedyosmum developed soon after the first appearance of angiosperms in the fossil record and has retained
its defining features for more than 120 million years; this scenario is supported by the finding of fossil pollen (Asteropollis) and flowers
indistinguishable from those of modern Hedyosmum [58,59]. (b) Crown-group Hedyosmum is young and originated in the Cenozoic more than
100 million years after the lineage divergence between Hedyosmum and its sister group and almost as long after the appearance of plants with
distinctive Hedyosmum reproductive features. According to this scenario, some of the defining features of extant Hedyosmum originated some time
during the Late Cretaceous or Cenozoic. This scenario is suggested by molecular dating [20]; fossil data according to Eklund et al. [59] are equivocal.

the fossils. However, this indicates that Hedyosmum


experienced two major phases of diversification: first,
an Early Cretaceous radiation resulting in a worldwide
expansion followed by Late Cretaceous extinctions; and a
second, mid-Cainozoic radiation that generated the
extant diversity of the genus. There are no apparent
morphological innovations associated with the second
radiation and an alternative explanation is that the age
calculated for the crown group is erroneous. More
research is needed to establish which of these contrasting
hypotheses is more likely to be correct. A comparable
apparent conflict between molecular ages and the fossil
record has recently been demonstrated for the genus
Ephedra of the Gnetales [62].

Fagales
Dispersed triaperturate pollen grains with distinctive
protruding and elaborate apertures (Figure 2ad) are very
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conspicuous and diverse elements in Late Cretaceous


floras in Europe and eastern North America. They are
collectively referred to as the Normapolles complex.
Members of this complex diversified initially in the early
Late Cretaceous, expanded dramatically during the Late
Cretaceous and underwent significant extinction during
the latest Cretaceous and Palaeogene (see references in
[31]). Fossil flowers containing pollen grains of the
Normapolles type show that these plants represent a
complex of extinct lineages nested within Fagales
[28,31,63,64]. Endressianthus and Normanthus plants
recently (Figure 2eh) described from the Late Cretaceous of Portugal [28,31] are the most completely understood Normapolles flowers. They constitute extinct
lineages close to the root of the Betulaceae lineage
[31]. Other Normapolles lineages are more closely
related to Rhoipteleaceae, Myricaceae and Juglandaceae
[31]. Based on this emerging fossil record there is little
Current Opinion in Plant Biology 2005, 8:512

8 Growth and development

Figure 2

(a)

(b)

(g)

(c)

(h)

(e)

(f)
(d)

Cretaceous pollen and flowers assigned to the extinct Normapolles complex. (a) Dispersed pollen grain of Interporopollenites type (scale = 10 mm).
(b) Dispersed pollen of the Pseudopapillopollis type (scale = 10 mm). (cd) Schematic sections through an Interporopollenites-type pollen showing
complex aperture regions (taken with permission from [31]). Fragments of (e) pistillate (scale = 1 mm) and (f) staminate (scale = 0.3 mm) flowerbearing axes of Endressianthus, a new Normapolles genus described from the Late Cretaceous of Portugal [31]; pollen grains produced by
Endressianthus are similar to dispersed Interporopollenites. (g) Complete flower of Normanthus described from the Late Cretaceous of Portugal
[28] and (h) the same flower with part of perianth removed showing bisexual structure of flower (scale bar = 1 mm). The Normapolles genera
constitute a large complex of extinct lineages within Fagales. Endressianthus/Interporopollenites and Normanthus/Pseudopapillopollis are
closely related to Betulaceae.

doubt that Fagales were diverse during the Late Cretaceous, but that this was followed by considerable extinction before the radiations of diverse modern genera.

Pre-Cretaceous prelude and stem-group


angiosperms?
Although the fossil record unequivocally demonstrates a
first major radiation of angiosperms in the Early Cretaceous, the high diversity of these early angiosperms raises
questions about their possible pre-Cretaceous evolutionary precursors. Also, most analyses of divergence time for
angiosperms using molecular techniques have concluded
that their ages are considerably older than those inferred
directly from the fossil record [19]. However, there is no
definite evidence of pre-Cretaceous angiosperms. Reticulate pollen from the Triassic [65,66] are from intriguing
plant taxa that are potential angiosperm relatives, but
unfortunately there are no macrofossil remains that can
help to clarify the phylogenetic significance of these
Triassic forms.
Evidence from the history of other major clades of land
plants suggests that the characteristic features of angioCurrent Opinion in Plant Biology 2005, 8:512

sperms were probably acquired sequentially through time.


The recent transitional-combinational theory of angiosperm origin [67] suggests an evolution of angiosperms
from Jurassic seed ferns that occurred through three
fundamental transitions: the evolution of the carpel,
the emergence of double fertilisation and last the origin
of the flower in the Early Cretaceous. However, no
phylogenetic framework has been used to test this
sequence of character evolution and improved palaeobotanical data are needed to pursue these ideas more
rigorously.
One genus that has received particular attention in discussions of angiosperm origin is the Mesozoic seed fern
Caytonia [68,69]. The early assignment of Caytonia to
angiosperms [70] made it an obvious object for further
study. Palaeobotanically, however, Caytonia is among a
multitude of extinct plants, most of which have not yet
been studied in comparable detail. Some of the extraordinary diversity of extinct Mesozoic seed plants has
recently been exposed in a comprehensive atlas of Late
Triassic fructifications from the Molteno Formation of
South Africa [71]. Some of these fossils are assignable to
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Floral evolution Friis, Pedersen and Crane 9

previously known groups such as peltasperms, corystosperms and Bennettitales. However, the systematic position of many of these fossils is unknown and a more
detailed study of this, and other material, is imperative for
a better understanding of extinct seed plant diversity and
relationships.
The genus Archaefructus, with three species described
from the Yixian Formation of north eastern China
[15,72,73], has also been suggested as a possible angiosperm precursor or angiosperm stem group [15,67]. The
age of the fossils has been disputed, but there is now
strong support for a mid-Early Cretaceous age for the
oldest horizons that contain Archaefructus [74,75].
Archaefructus fossils are exceptional in that they include
specimens preserved as whole plants with roots, stems,
leaves, flowers and fruits [73]. Archaefructus is an herbaceous plant with a habit that suggests an aquatic life-style.
Carpels and stamens are borne either singly or in clusters
of two or three on short common stalks along an elongated
axis. Stamens are proximal whereas carpels are in a distal
position. There are no traces of bracts or perianth parts
and Sun et al. [15] interpreted the reproductive axis as a
primitively naked, multiparted and bisexual flower. This
interpretation is controversial and, alternatively, it has
been suggested that Archaefructus is a crown-group angiosperm that has advanced, rather than primitive, floral
features [16]. According to this interpretation Archaefructus was totally submerged and its reproductive axes were
inflorescences with many small, simple and unisexual
flowers that had lost perianth and bracts as an adaptation
to underwater flowering. Recent observations of Archaefructus eoflora show a small bisexual flower comprising
two carpels and one stamen between the staminate and
pistillate zone [73]. This supports the inflorescence
interpretation. However, although the Yixian fossils
beautifully show features of general morphology, the
preservation of details is typically obscured by pyrite
infiltrations [42,76]. More information is clearly needed
to provide a full understanding of the phylogenetic significance of Archaefructus.

The record of Cretaceous reproductive structures makes


it clear that there has been considerable extinction within
certain angiosperm lineages, and that the extant taxa
constitute only a small proportion of the total diversity
of the group. This raises questions about the extent to
which phylogenetic analyses based on extant taxa that
include these groups might have been distorted by
uneven sampling introduced as a result of differential
extinction.
In terms of the earliest phases of angiosperm diversification, the presence of diverse angiosperm species that are
difficult to link definitively with extant taxa raises the
possibility that some of these groups might have diverged
from the main line of angiosperm evolution at a level
below the common ancestor of all extant taxa. Investigation of these taxa, as well as studies of extinct groups of
gymnosperms from throughout the Mesozoic, will be
important to identify potential stem-group angiosperms.
Perhaps such investigation will also develop a clearer
understanding of the sequence in which the defining
characteristics of extant angiosperms were acquired.

Acknowledgements
We acknowledge Pollyanna von Knorring for line drawings of fossil
pollen and flowers and research grants from the Swedish Research
Council (to EM Friis) and from the Carlsberg Foundation
(to KR Pedersen).

References and recommended reading


Papers of particular interest, published within the annual period of
review, have been highlighted as:
 of special interest
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Conclusions and future perspectives


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appear to represent extinct lineages. According to analyses of molecular data from extant taxa, the few extant
groups that can be recognized definitively at the family
level or below are mainly taxa that belong to basal
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www.sciencedirect.com

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pertinent to our understanding of Cretaceous angiosperm diversification.
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23. Bremer K, Friis EM, Bremer B: Molecular phylogenetic dating of



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six fossils as calibration points. Importantly, this study shows that the use
of more reference fossils reduces variation in age estimates.

39. Frumin S, Friis EM: Magnoliid reproductive organs from the


Cenomanian-Turonian of north-western Kazakhstan:
Magnoliaceae and Illiciaceae. Pl Syst Evol 1999, 216:265-288.

24. Magallo n SA: Dating lineages: molecular and paleontological


 approaches to the temporal framework of clades. Int J Plant Sci
2004, 165:S7-S21.
This work provides an excellent overview with up to date references of
molecular and paleontological methods used in age estimates of clades.
25. Friis EM, Skarby A: Structurally preserved angiosperm flowers
from the Upper Cretaceous of southern Sweden. Nature 1981,
291:485-486.
Current Opinion in Plant Biology 2005, 8:512

40. Frumin S, Eklund H, Friis EM: Mauldinia hirsuta sp. nov., a new

member of the extinct genus Mauldinia (Lauraceae) from the
Late Cretaceous (Cenomanian-Turonian) of Kazakhstan.
Int J Plant Sci 2004, in press.
This work describes a new species of the extinct genus Mauldinia of the
family Lauraceae from the mid-Cretaceous of Kazakhstan. The Sarbay
flora is important as the oldest mesofossil flora from Asia and is crucial for
understanding early angiosperm radition.
41. Takahashi M, Crane PR, Manchester SR: Hironoia fusiformis
gen. et sp. nov.: a cornalean fruit from the Kamikitaba locality
(Upper Cretecous, Lower Coniacian) in northeastern Japan.
J Plant Res 2002, 115:463-473.
www.sciencedirect.com

Floral evolution Friis, Pedersen and Crane 11

42. Leng Q, Friis EM: Sinocarpus decussatus gen. et sp. nov, a new

angiosperm with syncarpous fruits from the Yixian Formation
of Northeast China. Pl Syst Evol 2003, 241:77-88.
The extinct genus Sinocarpus described in this work from the Early
Cretaceous of north western China is significant in being the earliest
fossil flower with a syncarpous gynoecium. Its distinct morphology
indicates affinity with eudicots and shows that angiosperms in the Jehol
Biota were diversified to some extent.

The authors provide a thorough analysis of morphological character


evolution in both fossil and extant Chloranthaceae. There are many useful
illustrations, mostly of reproductive features, and a comprehensive literature survey of fossil and living members of the group.

43. Maslova NP, Kodrul TM: New platanaceous inflorescence


Archaranthus gen. nov. from the Maastrichtian-Paleocene of
the Amur Region. Paleontological J 2003, 37:89-98.

61. Friis EM, Pedersen KR, Crane PR: Early angiosperm


diversification: the diversity of pollen associated with
angiosperm reproductive structures in Early Cretaceous
floras from Portugal. Ann Mo Bot Gard 1999, 86:259-296.

44. Mohr B, Friis EM: Early angiosperms from the Aptian Crato
Formation (Brazil), a preliminary report. Int J Plant Sci 2000,
161(6 Suppl.):S155-S167.
45. Mohr B, Eklund H: Araripia florifera, a magnoliid angiosperm

from the Lower Cretaceous Crato Formation (Brazil).
Rev Palaeobot Palynol 2003, 126:279-292.
This paper provides the first formal description of an early angiosperm
plant from the Crato Formation, Brazil. The material from this formation is
significant in comprising whole-plant preservation. Araripia is a magnoliid plant with leaves and flowers attached to the same branching
system.
46. Kennedy EM, Lovis JD, Daniel JL: Discovery of a Cretaceous
angiosperm reproductive structure from New Zealand.
New Zeal J Geol Geop 2003, 46:519-522.
47. Eklund H: First Cretaceous flowers from Antarctica. Rev
 Palaeobot Palynol 2003, 127:187-217.
Most of the fossil flowers discovered in Cretaceous strata are from the
Northern Hemisphere. This study is important in providing the first
evidence from Antarctica of flowers that have an organization and
structure comparable to contemporary flowers from other areas.
48. Bowe LG, Coat G, DePamphilis CW: Phylogeny of seed plants
based on all three genomic compartments: extant
gymnosperms are monophyletic and Gnetales closest
relatives are conifers. Proc Natl Acad Sci USA 2000,
97:4092-4097.
49. Chaw S-M, Parkinson CL, Cheng Y, Vincent TM, Palmer JD: Seed
plant phylogeny inferred from all three plant genomes:
monophyly of extant gymnosperms and origin of Gnetales and
conifers. Proc Natl Acad Sci USA 2000, 97:4086-4091.
50. Bremer K: Early Cretaceous lineages of monocot flowering
plants. Proc Natl Acad Sci USA 2000, 97:4707-4711.
51. Renner SS, Foreman DB, Murray D: Timing transacrtic
disjunctions in the Atherospermataceae (Laurales): evidence
from coding and noncoding chloroplast sequences.
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52. Wikstro m N, Savolainen V, Chase MW: Evolution of the
angiosperms. Calibrating the tree. Proc R Soc Lond B Biol Sci
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53. Chaw SM, Chang CC, Chen HL, Li WH: Dating the monocot
dicot divergence and the origin of core eudicots using whole
chloroplast genomes. J Mol Evol 2004, 58:424-441.
54. Sanderson MJ: Estimating absolute rates of molecular
evolution and divergence times: a penalized likelihood
approach. Mol Biol Evol 2002, 19:101-109.
55. Crane PR, Herendeen P, Friis EM: Fossils and plant phylogeny.
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56. Crane PR, Lidgard S: Angiosperm diversification and
palaeolatitudinal gradients in Cretaceous floristic diversity.
Science 1989, 246:675-678.
57. Magallo n S, Crane PR, Herendeen PS: Phylogenetic pattern,
diversity and diversification of eudicots. Ann Mo Bot Gard 1999,
86:297-372.
58. Friis EM, Crane PR, Pedersen KR: Fossil history of magnoliid
angiosperms. In Evolution and Diversification of Land Plants.
Edited by Iwatsuki K, Raven PH. New York: Springer Verlag;
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59. Eklund H, Doyle JA, Herendeen PS: Morphological phylogenetic

analysis of living and fossil Chloranthaceae. Int J Plant Sci
2003, 165:107-151.
www.sciencedirect.com

60. Walker JW, Walker AG: Ultrastructure of Lower Cretaceous


angiosperm pollen and the origin and early evolution of
flowering plants. Ann Mo Bot Gard 1984, 71:464-521.

62. Rydin C, Pedersen KR, Friis EM: On the evolutionary history



of Ephedra; Cretaceous fossils and extant molecules.
Proc Natl Acad Sci USA 2004, 101:16571-16576.
This study describes exceptionally well-preserved seeds with distinctive
characters of Ephedra from the Early Cretaceous of Portugal and discusses the finding based on a molecular phylogeny. The finding demonstrates that modern species of Ephedra have retained unique
reproductive features, including the peculiar naked male gametophyte,
for more than 110 million years. It also highlights the apparent conflict
between molecular dating of crown-group Ephedra and the fossil record.
63. Friis EM: Upper Cretaceous (Senonian) floral structures of
juglandalean affinity containing Normapolles pollen.
Rev Palaeobot Palynol 1983, 39:161-188.
64. Sims HJ, Herendeen PS, Lupia R, Christopher RA, Crane PR:
Fossil flowers with Normapolles pollen from the Late
Cretaceous of southeastern North America. Rev Palaeobot
Palynol 1999, 106:131-151.
65. Hochuli PA, Colin JP, Vigran JO: Triassic biostratigraphy of the
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Edited by Collinson JD. London: Norwegian Petroleum Society
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66. Cornet B: Late Triassic angiosperm-like pollen from the
Richmond Rift Basin of Virginia, U.S.A. Palaeontogr B 1989,
213:37-87.
67. Stuessy TF: A transitional-combinational theory for the origin
of angiosperms. Taxon 2004, 53:3-16.
68. Gaussen H: Les Gymnospermes, actuelles et fossiles.
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69. Doyle JA: Origin of the angiosperm flower: a phylogenetic
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70. Thomas HH: The Caytoniales, a new group of angiospermous
plants from the Jurassic rocks of Yorkshire. Philos Trans R Soc
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71. Anderson JM, Anderson HM: Heyday of the gymnosperms:
 systematics and biodiversity of the Late Triassic Molteno
fructifications Pretoria: National Botanical Institute; 2003:1-398.
This article is the result of more than 35 years field work and study of plant
fossils from the Molteno Formation. It describes one of the most extensive
collections of Mesozoic seed plant fructifications and describes an
unexpected and extraordinary diversity in reproductive structures of
extinct seed plants.
72. Sun G, Dilcher DL, Zheng S, Zhou Z: In search of the first flower:
a Jurassic angiosperm, Archaefructus, from northeast China.
Science 1998, 282:1692-1695.
73. Ji Q, Li H, Bowe LM, Liu Y, Taylor DW: Early Cretaceous

Archaefructus eoflora sp. nov., with bisexual flowers from
Beipiao, Western Liaoning, China. Acta Geologica Sinica 2004,
78:883-896.
The paper provides a description of a new Early Cretaceous species of
Archaefructus preserved as a whole plant with roots, stems, leaves,
flowers and fruits. Although anatomical and fine morphological details
are poorly preserved, this fossil shows excellent gross morphological
features and is significant in our understanding of the early angiosperm
habit.
74. Zhou Z, Barrett PM, Hilton J: An exceptionally preserved Lower
 Cretaceous ecosystem. Nature 2003, 421:807-814.
This review paper provides a critical overview of the Jehol Biota with
particular focus on the stratigraphy and palaeoenvironmental setting. The
fossil plants are also discussed briefly and the authors suggest a possible
pteridospermous nature of the Archaefructus plant.
Current Opinion in Plant Biology 2005, 8:512

12 Growth and development

75. Chang M-m, Chen P-j, Wang Y-q, Wang Y, Mioa D-s (Eds):

The Jehol Biota. Series. Shanghai: Shanghai Scientific and
Technical Publishers; 2003.
This book includes a collection of articles summarizing current knowledge
of the Jehol Biota, from insects to angiosperms. It includes high-quality
illustrations of the fossils as well as many excellent reconstructions. It also
provides a broad overview of geology and stratigraphy of this important

Current Opinion in Plant Biology 2005, 8:512

Mesozoic ecosystem. The book is written for non-specialists but is based


on strict scientific criteria.
76. Leng Q, Yang H: Pyrite framboids associated with the
Mesozoic Jehol Biota in northeastern China: implications for
microenvironment during early fossilization. Prog Nat Sci 2003,
13:206-212.

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