REVIEW
Chinese Science Bulletin 2003 Vol. 48 No. 24 2651ü2657
ABC model and floral
evolution
LI Guisheng, MENG Zheng, KONG Hongzhi,
CHEN Zhiduan & LU Anming
Laboratory of Systematic and Evolutionary Botany, Institute of Botany,
Chinese Academy of Sciences, Beijing 100093, China
Correspondence should be addressed to Meng Zheng (e-mail: zhmeng@
ns.ibcas.ac.cn) and Lu Anming (e-mail:[email protected])
Abstract The paper introduces the classical ABC model
of floral development and thereafter ABCD, ABCDE and
quartet models, and presents achievements in the studies on
floral evolution such as the improved understanding on the
relationship of reproductive organs between gnetophytes and
angiosperms, new results in perianth evolution and identified
homology of floral organs between dicots and monocots. The
evo-devo studies on plant taxa at different evolutionary levels
are useful to better understanding the homology of floral
organs, and to clarifying the mysteries of the origin and subsequent diversification of flowers.
Keywords: ABC model, origin and diversity of flowers, homology
of floral organs, evo-devo.
DOI: 10.1360/ 03wc0234
Before the establishment of classical ABC model of
floral development, comparative studies on the development of floral organs by using mutants between two
model plants Arabidopsis thaliana and Antirrhinum majus
indicate that they have surprising similarities in fourwhorl architecture of floral organs and their homeotic
mutants. After seeds germinate in wild Arabidopsis, firstly
rosette leaves develop from apical meristems. As vegetative meristems reach a certain stage or size, inflorescent
meristems initiate with the rearrangement of apical meristems, and then cauline leaves develop. Finally floral meristems come into being. Every floral meristem produces a
flower and the flower possesses four whorls of floral organs in a concentric arrangement, namely, the outermost
whorl of four sepals, the second whorl of four petals, the
third whorl of six stamens, and the innermost whorl of a
syncarpous ovary consisting of two carpels. Arabidopsis
has three classes of artificial homeotic mutants in terms of
four-whorled architecture of floral organs (Fig. 1).
Apetala1[1,2]/apetala2[3] mutants possess carpel, stamen,
stamen, carpel from the outermost to the innermost whorl
successively; apetala3/pistillata[4,5] mutants possess sepal,
sepal, carpel, carpel; agamous[6] mutants possess sepal,
petal, petal, sepal. They are termed A-, B- and C-class
mutants respectively. And three classes of genes act to
specify floral organs, namely sepals (A only), petals
(A+B), stamens (B+C), or carpels (C only). In Arabidopsis, A-function is conferred by APETALA1 (AP1) and
Chinese Science Bulletin Vol. 48 No. 24 December 2003
APETALA2 (AP2), B-function by APETALA3 (AP3) and
PISTILLATA (PI), and C-function by AGAMOUS (AG).
The so-called ABC model conceives two tenets: first, each
of the three classes of genes functions in two adjacent
whorls, namely A-class genes function in the first and
second whorls, B-class genes in the second and third
whorls, and C-class genes in the third and fourth whorls;
secondly, interaction between the three classes of genes
determines floral organs. For example, A- and B-class
genes are necessary to shape petals in wild plants, but sepals not petals develop at the second whorl in B-class mutants and stamens instead of petals develop at the same
whorl in A-class mutants because of the antagonism between A- and C-class genes[10].
The ABC model continues to be revised since it is
proposed. When FLORAL BINDING PROTEIN 11
(FBP11), termed D-class gene, is confirmed to determine
ovule, ABCD model is suggested[11]. Furthermore E-class
gene and ABCDE model (Fig. 2)[9] are proposed based on
the fact that SEPALLATA1 (SEP1), SEPALLATA2 (SEP2),
SEPALLATA3 (SEP3) are proven to be together with A-,
B-, C-class genes required for the specification of floral
organ identities in Arabidopsis. Recently Bs-class genes
are named because they are the paralogous cluster to
B-class genes, though they are expressed in carpel and
ovule rather than petal and stamen[13]. The differential
expression between the two clusters may be related to the
divergence between megasporopylls and microsporophylls,
namely the divergence of sexes during evolution[14].
With the coming of ABCDE model, the sufficient
and necessary genes conferring the identity of floral organs are clarified. Then the molecular mechanism of the
gene interactions becomes one of the greatest challenges
and finally some models are proposed. The “quartet
model” (Fig. 3)[15] suggests that products of A-, B-, C- and
E-class genes form quartets to determine floral organs.
Taking Arabidopsis for example, AP1-AP1-?-? quartet
induces the expression of target genes and finally the
formation of sepal at the first whorl. Similarly, AP1-AP3PI-SEP induces petal at the second whorl, AP3-PI-AGSEP stamen at the third whorl, and AG-AG-SEP-SEP carpel at the fourth whorl. Furthermore, quartets containing
the products of A-class genes inhibit the formation of
quartets containing the products of C-class genes, and vice
versa, displaying antagonistic action between A- and
C-class genes. Firstly these proteins form dimmers that
can specifically bind to CArG elements at regulatory regions of target genes, then two dimmers form a quartet via
C-terminus in proteins. Finally the quartet activates or
inhibits the expression of target genes, which produces
certain floral organs at certain whorls.
All the related genes indicated above except for AP2
share a highly conserved DNA sequence of about 180 bp
called MADS-box. MADS is an acronym for the four
founder genes MCM1 (from yeast), AGAMOUS (from
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Fig. 1. Classical ABC model, with reference to Coen and Meyerowitz[8]. Wild flowers in eudicots and their three homeotic mutants and
models corresponding to every kind of flowers are shown. (a) Wild type; (b) A mutant; (c) B mutant; (d) C mutant. Wild flowers have normal
four-whorled architecture namely, sepal-petal-stamen-carpel from the first whorl to the fourth whorl. A-class mutant has carpel-stamen-stamen-carpel because the antagonistic C-class genes function in whorls where A-class genes function when A-class genes are
mutated. Similarly, C-class mutant has sepal-petal-petal-sepal. Finally, B-class mutant has sepal-sepal-carpel-carpel.
Fig. 2. ABCDE model, with reference to Theissen[20]. Ovule is an independent floral organ to carpel. Besides A-, B-, and C-class genes, Dand E-genes are necessary for floral development. For example, B+C+E
are necessary and sufficient for stamen determination.
Arabidopsis), DEFICIENS (from Antirrhinum), and SRF
(from human). Following MADS-box are ~90 bp I-box
and ~210 bp K-box and variable C-terminus[21] sequentially. Therefore, precisely speaking, these MADS- box
genes should be called MIKC-type MADS-box
genes[22,23].
Until now, MADS-box genes have been found in at
least 39 species in 27 orders of angiosperms, and particularly the total number of MADS-box genes in rice and
Arabidopsis can be predicted from genomic map, for example, about 80 MADS-box genes exist in Arabidopsis[24]
and approximately 71 in rice. Furthermore, MADS-box
genes have also been discovered in gymnosperms[25,26],
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ferns[27] and mosses[23,28]. Particularly, although genes involved in ABC model of floral development are isolated
and cloned from ferns and seed plants, they are specifically expressed in reproductive organs of seed plants but
not in those of ferns[29]. So it is clear that MADS-box
genes function in the evolution of reproductive organs of
land plants. Therefore, to study the evolution of MADSbox genes and their functions in different land plant taxa,
especially flowering plants with unique floral morphology
on the basis of models of floral development established
in model plants might finally clarify the origin and evolution of angiosperm flowers.
In 1995 the ABC model was timely related to floral
evolution[30], which was introduced by Chinese scholars[31,32]. Here the major advances in research on the origin
and diversity of flowers and homology of floral organs
recently achieved via evo-devo (evolutionary-developmental) methodology are reviewed.
1
The origin of flowers
“Abominable mystery” is used to designate the sudden occurrence (appearance) of diverse angiosperms on
the earth in early Cretaceous (13090 million years ago)
by Darwin, then the origin of flowers unique to angiosperms could be called “mystery in mystery”. Historically,
there were two major hypotheses on the origin of flowers[20]. () Euanthium maintains that flowers originate
from bisexual strobilus in single branch as in CyChinese Science Bulletin Vol. 48 No. 24 December 2003
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Fig. 3. The “quartet model” of floral development in Arabidopsis, with reference to Theissen[20]. The model suggests that transcriptional factors have to firstly form quartets in order to bind to the regulatory regions at target genes, and then they activate or inhibit
the expression of these target genes, inducing a certain floral organ at a certain whorl. AP1, AP3, PI, AG, SEP are proteins of these genes.
“?” indicates unknown proteins.
cadoidea/Bennettialean/Caytoniales, and the most primitive flowers, like Magnolia flowers, possess perianths, and
furthermore their perianths, stamens and ovules are phyllomes. Similar theories are recently proposed, such as
Anthophyte (maintaining that Bennettitales/Pentoxylon/
Gnetales and angiosperms are closely related since they
all possess flower-like reproductive organs) and Neopseudanthium (maintaining that Gnetales is the direct ancestor of angiosperms, rather than only the sister to angiosperms)[33]. () Pseudanthium maintains that flowers
originate from unisexual reproductive organs in multiple
branch as in seed ferns, and the most primitive flowers,
like extinct Archaefructus flowers, are perianthless though
perianths evolve later, and their stamens and ovules are
axial organs[34].
Reasonably gnetophyte is an “outgroup” in terms of
research on floral origin, and its reproductive organs are
unisexual, namely female “flowers” consisting of nucellus,
inner and outer integument, or male “flowers” consisting
of sporangium and bracts[35,36]. From Gnetum gnemon 13
MADS-box genes are isolated and the phylogenetic
analysis on them is carried out. It is found that genes from
Gnetum always group together with those from conifer
while separate from those in angiosperms, indicating a
closer relationship of Gnetum to conifer than to angiosperms[26]. Meanwhile expression pattern analysis proves
the homology between the outer integument in Gnetum
and integuments[26] or even carpel[20] rather than petals in
angiosperms, because outer integument expresses C
homologue but not B homologue. Thus both results hint at
a unisexual ancestor of seed plants[37]. With regard to the
evolutionary mechanism from unisex to bisex there are
two explanations. The “mostly male” theory maintains
Chinese Science Bulletin Vol. 48 No. 24 December 2003
that the bisexual organ does not shape until an ovule as a
homeotic organ develops on a male organ[38]. Alternatively,
male cones reduce the expression of B-class genes (or
ectopic expression of Bs-class genes) at its upper part and
that part thus is shifted into female organs, which results
in bisexual organs finally. Or female cones reduce the expression of Bs-class genes (or ectopic expression of
B-class genes) at its lower part which finally is shifted
into male organs[14].
Furthermore, expression pattern analysis suggests
that throughout seed plants C-class genes may function to
distinguish vegetative and reproductive organs and thus
can turn vegetative into reproductive organs when these
genes extend their expression into the former to allow the
evolution of ever-complicating reproductive organs;
meanwhile B-class genes function to distinguish between
male and female organs, which represents a molecular
mechanism of sexual differentiation in the seed plants
during evolution. Additionally, the conserved function of
both genes confirms the single origin of reproductive organs of the seed plants about 300 million years ago.
The perianthless state in gymnosperms may be due
to the loss of A-class genes[29]. However, homologues of
AP1[25] and AP2[39] have been isolated from the taxa.
Primitive flowers may be perianthless with resemblance to
the flower of Sarcandra glabra[20,34]. This kind of flowers
requires just B- and C-class genes as gymnosperms reproductive organs do. Thus A-class genes and perianths
evolve later. Another conventional opinion maintains that
primitive flowers have perianths[40]. Perianths consist of
only petaloids expressing A- and B-class genes, while
sepals expressing only A-class genes are added later; or
perianths consist of only sepals expressing A-class genes,
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and petals form when B-class genes extend to the inner
whorl of sepals[20]. Thus it is urgent to characterize A-class
genes in basal angiosperms in order to clarify the origin of
perianths. Chloranthaceae includes Chloranthus, Sarcandra, and Ascarina which have no perianth and Hydeosmum which has a perianth[41], and belongs to primitive
angiosperms with Early Cretaceous fossil record[30]. In the
“Eight-Class System” of angiosperms, this family together
with another basal angiosperm Amborella and Laurales
belongs to Lauropsida[42]. Thus Chloranthaceae is important in resolving the origin of perianths within the range of
one angiosperm clade.
Fortunately studies on B-class genes are clarifying
the origin of petals. B-class genes in Ranunculidae cannot
stably and uniformly express during petal development,
which is different from its permanent expression in other
eudicots[43,44]. Though the result needs to be further supported[45], it stands for the conventional notion of distinct
origin of petals in Ranunculidae[44,46,47]. The result, furthermore, hints that other genes besides B-class genes are
necessary for petal determination in Ranunculidae[44]. Additionally, the duplication and divergence are relevant to
the diversity of petals in Ranunculidae, and this behavior
of B-class genes is synapomorphic to the taxa[49]. However,
the notion of the single origin of petals cannot be completely denied, because B-class genes may be unstably
expressed in Ranunculidae while their target genes for
petal development evolve an auto-regulation to shape petals even without B-class genes[44,48]. Therefore, it is also
possible that the ancestor of angiosperms possesses petaloid organs, and that eudicots, monocots, and paleoherbs
separately evolve distinctive protective sepals later[48].
While debates between euanthium and pseudanthium
stimulate the investigation on floral origin, evo-devo research comprehensively clarifies this issue. It is assumed,
though more evidence needs to be added, that flowers
evolve from unisex to bisex, and that male and female
organs originate once. As to the origin of perianths, the
ancestor of angiosperms may possess petaloid organs,
which express A- and B-class genes, or be perianthless.
2
Diversity of flowers
Being one theme of evolutionary biology, morphological diversity genetically is closely related to variation
in relevant regulatory genes[50], thus the diversity of flowers demands sufficient variation in genes involved in the
ABC model. Evolutionary analysis on CAULIFLOWER
(CAL) which is the paralogue of AP1, and B-class genes
obtained from wild populations of Arabidopsis using PCR
(polymerase chain reaction) indicates that these genes,
like other genes, possess enough variations of nucleotide
and amino acid within species[50].
Hawaii silversword ally (Heliantheae-Madiinae) is
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desirable to study adaptive radiation, since it possesses
abundant variation in growth style and reproductive organs. In 2001, A- and B-class genes, as well as a photosynthesis-related gene from this plant were cloned, and
their evolutionary rates were compared with those of
American tarweeds (Heliantheae-Madiinae)[51]. The result
shows that the ratio of nonsynonymous substitution to
synonymous substitution in A- and B-class genes significantly increases, but the rise of neutral mutation is not
common in Hawaii silvesword ally; additionally, the ratio
of nonsynonymous substitution to synonymous substitution in photosynthesis-related gene weakly rises. Therefore, variation in A- and B-class genes is related to rapid
morphological diversification during adaptive radiation,
and the adaptive radiation of these genes may result from
the directive selection conferred on reproductive organs.
As to how the variation of these genes results in
morphological diversity in floral organs, many studies
show that the function of these genes changes. Crucifer
Brassica oleracea has two copies of A-class gene AP1
namely, normal BoAP1-A and abnormal BoAP1-B. Because AP1 and its paralogue CAL together function in floral meristem (another function of AP1 is to determine petals), when BoAP1-B and CAL are mutated, the mutant
develops cauliflowers which have normal perianths due to
the normal BoAP1-A. In comparison, AP1 is a single gene
in Arabidopsis, when both CAL and AP1 are mutated, this
plant will develop cauliflower without normal perianth[52].
Additionally, Arabidopsis CAL can naturally produce
some alleles and then cause morphological diversity under
selection because these alleles have different functions[47,53].
“Sliding-boundary” of the expression of floral genes
can also cause floral diversity[10]. Flowers in Clarkia concinna have four sepals, four petals, four stamens and one
ovary. In 1992 its natural variant bicalyx was described as
with eight sepals, no petals, and normal stamens and one
ovary. Obviously, sepals take the place of petals. Crossing
test indicates that the phenotype of the variant is controlled by a single recessive gene and that the variant may
represent a natural population or species since it is highly
self-crossed and stable in fertility. Thus bicalyx represents
a natural morphological diversity caused by a single
gene[54], which may be due to the inward sliding of one Bclass gene expression[10].
Additionally, many eudicots such as Potentilla fruticosa, Sanguinaria canadensis, Actaea rubra, and Hibiscus
rosa-sinensis shrink the expression of C-class genes to
center so that the outer whorl of stamen turns into petal
and finally double-petal flowers develop[10]. Because of
the gradual shrinkage of the expression of B-class genes to
center, flowers in Magnoliaceae present all transitional
stages from an undifferentiated perianth consisting of
Chinese Science Bulletin Vol. 48 No. 24 December 2003
REVIEW
petaloid organs to well differentiated perianths consisting
of sepals and petals. The inward shrinkage of the expression of C-class genes results in unique characters in every
family of Zingiberales, for example, different petaloid
organs develop at the positions for 6 stamens in Musaceae,
Zingiberaceae and Cannaceae.
Although the “sliding boundary” model straightforwardly accounts for the transition among sepal, petal and
stamen, it fails to explain the cases in Ranunculaceae.
Ranunculaceae flowers have two whorls of petaloid organs that are identical within each whorl but different between whorls. It seems that there are two distinct petal
identity programs functioning in many genus of this family. Recently the duplication and divergence of B-class
genes have been discovered to be related to this morphological diversity of petals in Ranunculaceae[49]. Gene isolation and phylogenetic analysis reveal that in nine genus
of Ranunculidae three classes of AP3 orthologues exist
and species in which AP3-III can be detected mostly possess the second petaloid organs and vice versa. Thus
AP3-III may be related to the second petaloid organs
while AP3-I and AP3-II may be related to the first petaloid
organs.
Contrasting to most plants with four-whorled floral
organs, Lacandonia schismatica has carpel interior to
perianth and stamen at the center of flowers. This case
may be related to the activation at the center of B-class
genes[10].
It is necessary to point out that the ABC model of
floral development has neither purpose nor potential to
explain all floral diversities. Because the ABC model is
about the spatial expression of genes and homeosis of floral organs, it is difficult to clarify changes in floral organs
resulted from the intensity and time of gene expression[55,56], and changes in sex determination[20,57], number
and size[8,30], and symmetry of floral organs[8,58,59]. Therefore, the ABC model just opens the door in terms of the
research on floral diversity.
3
Homology of floral organs
Homology refers to the similarity caused by continual genetic information[60], namely possessing common
ancestor is the premise to discuss homology[61]. Two kinds
of homologous genes are orthologous genes produced via
speciation and paralogous genes produced via gene duplication, and only the former is significant to phylogenetic
reconstruction of genes[61] and identification of homologous organs.
The outer envelope in Gnetum was assumed homologous to the petal in angiosperms in 1986[62]; and the
outer envelope was considered apomorphic to Gnetum and
was not corresponsive to any part of flowers in angiosperms in 1999[36]. However, the outer envelope might be
Chinese Science Bulletin Vol. 48 No. 24 December 2003
homologous to integument and even carpel in angiosperms when it was discovered to express C-class genes
but not B-class genes[26] in the same year. Thus anthophyte
is falsified and other morphological homologies suggested
between taxa of seed plants face reevaluation[26,33].
The homology problem in flowers between monocots and other angiosperms is resolved by the expression
pattern of homologous genes. The mature male flower in
corn has one palea, one lemma, two lodicules and three
stamens, and one aborted pistil. The mature female flower
has one palea, one lemma, two lodicules, and one pistil
with silky stigma. Silky1 male mutant has palea and
lemma, but with the replacement of lodicules by structures
similar to palea and lemma, and with silky protrusion occupying the position of stamen. Silky1 female mutant has
three additional pistils. Because SILKY1 belongs to Bclass genes, lodicules are homologous to petals and palea/
lemma to sepal[63].
In monocots Alismatidae floral ontogeny research
shows that perianth and stamen originate from a common
primordium, though thereafter intercalary growth results
in the secondary fusion between them[32]. Later, this perianth/stamen combination is assumed representative of one
bract and one male flower. Therefore flowers in Alismatidae are thought to be originated from ancestral reproductive structure without differentiation between inflorescence and flower, which is also multi-branched with main
axis to differentiate “inflorescence” and lateral axes to be
compounded into “flower”[32]. Provided A- or B-class
genes are cloned from this kind of plant, it is possible to
test the hypothesized relationship between perianth and
stamen, and flower and inflorescence, furthermore to
propose on the origin of flowers in monocots.
In terms of homology of floral organs there are still
two typical cases[20]. Two whorls of perianths exist in
Liliaceae and each whorl consists of three petaloid organs,
however, the first whorl is homologous to petal because of
its expression of B-class genes; meanwhile perianths in
Rumex and many wind-pollinated plants is sepaloid,
however, the second whorl is homologue of sepal because
B-class genes do not express there. These studies make us
further understand the evolution and phylogenetic relationship between taxa relative to the morphological research.
4
Prospects
No other disciplines rely more heavily on morphologies of organs than evolutionary biology, and evolutionary
biologists are inspired when they know that morphologies
are developmentally controlled by only a few regulatory
genes that act as molecular switches. Morphology corresponds to gene; the evolution of morphology can be understood by studying the evolution of gene. So evo-devo
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appears. Currently, the ABC model of floral development
provides an operative work frame for this study. More and
more genes are characterized and plant taxa at different
evolutionary levels are included; not only coding seü
quences but also regulatory sequences are studied[64 69];
the level of such research can also be uplifted from the
level of gene to protein[70,71]. Additionally, the established
ü
frame of angiosperm phylogeny[72 74] and the timely proposed new angiosperm classification[42] provide the guide
to choose taxa and subject. Therefore, it is certain that the
research on floral diversity and origin will be prompted by
the studies on gene network of the ABC model of floral
development via genomic and genetic strategy throughout
whole angiosperms and especially on taxa of “missing
links”[75,76]. Clarification of the diversification mechanism
of flowering plants will supply the reason to protect and
use plants. Finally, while most materials are provided by
the studies using animals when evo-devo emerges, the
evolutionary research on floral development may enrich
the content of evo-devo and thus prompt its expansion
when its conceptual system is shaping now[77].
13.
14.
15.
16.
17.
18.
19.
20.
Acknowledgements We thank Profs. Hong Deyuan and Ge Song for
their support and suggestions on the project. This work was supported by
the National Natural Science Foundation of China (Grant Nos. 30130030
and 30121003).
21.
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(Received May 21, 2003; accepted October 10, 2003)
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