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Chinese Science Bulletin Vol. 48 No. 24 December 2003 2651

Chinese Science Bulletin 2003 Vol. 48 No. 24 26512657

ABC model and floralevolution

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, ChinaCorrespondence should be addressed to Meng Zheng (e-mail: [email protected]) 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 therelationship of reproductive organs between gnetophytes and

angiosperms, new results in perianth evolution and identifiedhomology of floral organs between dicots and monocots. The

evo-devo studies on plant taxa at different evolutionary levelsare useful to better understanding the homology of floral

organs, and to clarifying the mysteries of the origin and sub-sequent diversification of flowers.

Keywords: ABC model, origin and diversity of flowers, homologyof floral organs, evo-devo.

DOI: 10.1360/ 03wc0234

Before the establishment of classical ABC model offloral development, comparative studies on the develop-ment of floral organs by using mutants between twomodel plants Arabidopsis thalianaandAntirrhinum majusindicate that they have surprising similarities in four-whorl architecture of floral organs and their homeoticmutants. After seeds germinate in wildArabidopsis, firstlyrosette leaves develop from apical meristems. As vegeta-tive meristems reach a certain stage or size, inflorescentmeristems initiate with the rearrangement of apical meris-tems, and then cauline leaves develop. Finally floral mer-istems come into being. Every floral meristem produces aflower and the flower possesses four whorls of floral or-gans in a concentric arrangement, namely, the outermostwhorl of four sepals, the second whorl of four petals, thethird whorl of six stamens, and the innermost whorl of asyncarpous ovary consisting of two carpels. Arabidopsishas three classes of artificial homeotic mutants in terms offour-whorled architecture of floral organs (Fig. 1).Apetala1[1,2]/apetala2[3] mutants possess carpel, stamen,stamen, carpel from the outermost to the innermost whorlsuccessively; 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-classmutants 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 Arabidop-sis, A-function is conferred by APETALA1 (AP1) and

APETALA2 (AP2), B-function by APETALA3 (AP3) andPISTILLATA (PI), and C-function by AGAMOUS (AG).The so-called ABC model conceives two tenets: first, eachof the three classes of genes functions in two adjacentwhorls, namely A-class genes function in the first andsecond whorls, B-class genes in the second and thirdwhorls, and C-class genes in the third and fourth whorls;secondly, interaction between the three classes of genesdetermines floral organs. For example, A- and B-classgenes are necessary to shape petals in wild plants, but se-pals not petals develop at the second whorl in B-class mu-tants and stamens instead of petals develop at the samewhorl in A-class mutants because of the antagonism be-tween 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 determineovule, ABCD model is suggested[11]. Furthermore E-classgene and ABCDE model (Fig. 2)[9]are proposed based onthe fact that SEPALLATA1(SEP1), SEPALLATA2(SEP2),SEPALLATA3 (SEP3) are proven to be together with A-,B-, C-class genes required for the specification of floralorgan identities in Arabidopsis. Recently Bs-class genesare named because they are the paralogous cluster toB-class genes, though they are expressed in carpel andovule rather than petal and stamen[13]. The differentialexpression 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 sufficientand necessary genes conferring the identity of floral or-gans are clarified. Then the molecular mechanism of thegene interactions becomes one of the greatest challengesand finally some models are proposed. The quartetmodel (Fig. 3)[15]suggests that products of A-, B-, C- andE-class genes form quartets to determine floral organs.Taking Arabidopsis for example, AP1-AP1-?-? quartetinduces the expression of target genes and finally the for-mation of sepal at the first whorl. Similarly, AP1-AP3-PI-SEP induces petal at the second whorl, AP3-PI-AG-SEP stamen at the third whorl, and AG-AG-SEP-SEP car-pel at the fourth whorl. Furthermore, quartets containingthe products of A-class genes inhibit the formation ofquartets containing the products of C-class genes, and viceversa, displaying antagonistic action between A- andC-class genes. Firstly these proteins form dimmers thatcan specifically bind to CArG elements at regulatory re-gions of target genes, then two dimmers form a quartet viaC-terminus in proteins. Finally the quartet activates orinhibits the expression of target genes, which producescertain floral organs at certain whorls.

All the related genes indicated above except for AP2

share a highly conserved DNA sequence of about 180 bpcalled MADS-box. MADS is an acronym for the fourfounder genes MCM1 (from yeast), AGAMOUS (from

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2652 Chinese Science Bulletin Vol. 48 No. 24 December 2003

Fig. 1. Classical ABC model, with reference to Coen and Meyerowitz[8]. Wild flowers in eudicots and their three homeotic mutants andmodels corresponding to every kind of flowers are shown. (a) Wild type; (b) A mutant; (c) B mutant; (d) C mutant. Wild flowers have normalfour-whorled architecture namely, sepal-petal-stamen-carpel from the first whorl to the fourth whorl. A-class mutant has car-

pel-stamen-stamen-carpel because the antagonistic C-class genes function in whorls where A-class genes function when A-class genes aremutated. Similarly, C-class mutant has sepal-petal-petal-sepal. Finally, B-class mutant has s epal-sepal-carpel-carpel.

Fig. 2. ABCDE model, with reference to Theissen[20]. Ovule is an in-dependent floral organ to carpel. Besides A-, B-, and C-class genes, D-

and E-genes are necessary for floral development. For example, B+C+Eare necessary and sufficient for stamen determination.

Arabidopsis), DEFICIENS(from Antirrhinum), and SRF(from human). Following MADS-box are ~90 bp I-boxand ~210 bp K-box and variable C-terminus[21] sequen-tially. Therefore, precisely speaking, these MADS- boxgenes should be called MIKC-type MADS-boxgenes[22,23].

Until now, MADS-box genes have been found in atleast 39 species in 27 orders of angiosperms, and particu-larly the total number of MADS-box genes in rice andArabidopsiscan be predicted from genomic map, for ex-

ample, about 80 MADS-box genes exist in Arabidopsis[24]

and approximately 71 in rice. Furthermore, MADS-boxgenes have also been discovered in gymnosperms[25,26],

ferns[27]

and mosses[23,28]

. Particularly, although genes in-volved in ABC model of floral development are isolatedand cloned from ferns and seed plants, they are specifi-cally expressed in reproductive organs of seed plants butnot in those of ferns[29]. So it is clear that MADS-boxgenes function in the evolution of reproductive organs ofland plants. Therefore, to study the evolution of MADS-box genes and their functions in different land plant taxa,especially flowering plants with unique floral morphologyon the basis of models of floral development establishedin model plants might finally clarify the origin and evolu-tion of angiosperm flowers.

In 1995 the ABC model was timely related to floralevolution[30], which was introduced by Chinese schol-ars[31,32]. Here the major advances in research on the originand diversity of flowers and homology of floral organsrecently achieved via evo-devo (evolutionary-develop-mental) methodology are reviewed.

1 The origin of flowers

Abominable mystery is used to designate the sud-den occurrence (appearance) of diverse angiosperms on

the earth in early Cretaceous (13090 million years ago)by Darwin, then the origin of flowers unique to angio-sperms could be called mystery in mystery. Historically,

there were two major hypotheses on the origin of flow-ers[20]. ( ) Euanthium maintains that flowers originatefrom bisexual strobilus in single branch as in Cy-

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Fig. 3. The quartet model of floral development in Arabidopsis, with reference to Theissen[20]. The model suggests that tran-

scriptional 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 primi-

tive flowers, likeMagnoliaflowers, possess perianths, and

furthermore their perianths, stamens and ovules are phyl-

lomes. 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 Neop-seudanthium (maintaining that Gnetales is the direct an-

cestor of angiosperms, rather than only the sister to an-

giosperms)[33]. ( ) Pseudanthium maintains that flowers

originate from unisexual reproductive organs in multiple

branch as in seed ferns, and the most primitive flowers,

like extinctArchaefructusflowers, 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 consistingof sporangium and bracts[35,36]. From Gnetum gnemon13

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 angio-

sperms[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 theevolutionary mechanism from unisex to bisex there are

two explanations. The mostly male theory maintains

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 ex-

pression of Bs-class genes (or ectopic expression ofB-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 ofboth genes confirms the single origin of reproductive or-

gans 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 re-

productive 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, whilesepals 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 theorigin of perianths. Chloranthaceae includes Chloranthus,

Sarcandra, andAscarinawhich have no perianth andHy-

deosmumwhich has a perianth[41], and belongs to primi-

tive 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 impor- tant 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 sup-

ported[45], it stands for the conventional notion of distinct

origin of petals in Ranunculidae[44,46,47]. The result, fur-

thermore, hints that other genes besides B-class genes are

necessary for petal determination in Ranunculidae[44]. Ad-

ditionally, 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 com-

pletely denied, because B-class genes may be unstably

expressed in Ranunculidae while their target genes forpetal development evolve an auto-regulation to shape pet-

als even without B-class genes[44,48]. Therefore, it is also

possible that the ancestor of angiosperms possesses peta-

loid 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 re-

search 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, morpho-

logical diversity genetically is closely related to variation

in relevant regulatory genes[50], thus the diversity of flow-

ers 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 Arabidopsisusing PCR

(polymerase chain reaction) indicates that these genes,

like other genes, possess enough variations of nucleotideand amino acid within species[50].

Hawaii silversword ally (Heliantheae-Madiinae) is

desirable to study adaptive radiation, since it possesses

abundant variation in growth style and reproductive or-

gans. In 2001, A- and B-class genes, as well as a photo-synthesis-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 signifi-

cantly increases, but the rise of neutral mutation is not

common in Hawaii silvesword ally; additionally, the ratio

of nonsynonymous substitution to synonymous substitu-

tion in photosynthesis-related gene weakly rises. There-

fore, 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 fromthe 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. Be-

causeAP1and its paralogue CALtogether function in flo-

ral meristem (another function of AP1is to determine pet-

als), when BoAP1-B and CAL are mutated, the mutant

develops cauliflowers which have normal perianths due to

the normalBoAP1-A. In comparison, AP1is a single gene

inArabidopsis, when both CALandAP1are mutated, thisplant 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 func-

tions[47,53].

Sliding-boundary of the expression of floral genes

can also cause floral diversity[10]. Flowers in Clarkia con-

cinnahave four sepals, four petals, four stamens and one

ovary. In 1992 its natural variantbicalyxwas 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 con-trolled 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 bicalyxrepresents

a natural morphological diversity caused by a single

gene[54], which may be due to the inward sliding of one B-

class gene expression[10].

Additionally, many eudicots such as Potentilla fruti-

cosa, Sanguinaria canadensis, Actaea rubra , andHibiscus

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 tocenter, flowers in Magnoliaceae present all transitional

stages from an undifferentiated perianth consisting of

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petaloid organs to well differentiated perianths consisting

of sepals and petals. The inward shrinkage of the expres-

sion of C-class genes results in unique characters in everyfamily of Zingiberales, for example, different petaloid

organs develop at the positions for 6 stamens in Musaceae,

Zingiberaceae and Cannaceae.

Although the sliding boundary model straightfor-

wardly accounts for the transition among sepal, petal and

stamen, it fails to explain the cases in Ranunculaceae.

Ranunculaceae flowers have two whorls of petaloid or-

gans that are identical within each whorl but different be-

tween whorls. It seems that there are two distinct petal

identity programs functioning in many genus of this fam-

ily. Recently the duplication and divergence of B-class

genes have been discovered to be related to this morpho-logical diversity of petals in Ranunculaceae[49]. Gene iso-

lation and phylogenetic analysis reveal that in nine genus

of Ranunculidae three classes of AP3 orthologues exist

and species in whichAP3-IIIcan be detected mostly pos-

sess the second petaloid organs and vice versa. Thus

AP3-III may be related to the second petaloid organs

whileAP3-IandAP3-IImay 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-classgenes[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 flo-

ral organs, it is difficult to clarify changes in floral organs

resulted from the intensity and time of gene expres-

sion[55,56], and changes in sex determination[20,57], number

and size[8,30], and symmetry of floral organs[8,58,59]. There-

fore, 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 contin-

ual 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 dupli-

cation, and only the former is significant to phylogenetic

reconstruction of genes[61] and identification of homolo-

gous organs.

The outer envelope in Gnetum was assumed ho-

mologous to the petal in angiosperms in 1986[62]; and the

outer envelope was considered apomorphic to Gnetumandwas not corresponsive to any part of flowers in angio-

sperms in 1999[36]. However, the outer envelope might be

homologous to integument and even carpel in angio-

sperms when it was discovered to express C-class genes

but not B-class genes

[26]

in the same year. Thus anthophyteis falsified and other morphological homologies suggested

between taxa of seed plants face reevaluation[26,33].

The homology problem in flowers between mono-

cots 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 oc-

cupying the position of stamen. Silky1female mutant hasthree additional pistils. Because SILKY1 belongs to B-

class 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 peri-

anth/stamen combination is assumed representative of one

bract and one male flower. Therefore flowers in Alismati-

dae are thought to be originated from ancestral reproduc-

tive structure without differentiation between inflores-

cence and flower, which is also multi-branched with mainaxis 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 rela-

tionship between taxa relative to the morphological re-

search.

4 Prospects

No other disciplines rely more heavily on morpholo-

gies 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 corre-sponds to gene; the evolution of morphology can be un-

derstood 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 differentevolutionary levels are included; not only coding se-

quences but also regulatory sequences are studied[6469];

the level of such research can also be uplifted from the

level of gene to protein[70,71]. Additionally, the established

frame of angiosperm phylogeny[7274]and the timely pro-

posed 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 mechanismof 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].

Acknowledgements We thank Profs. Hong Deyuan and Ge Song for

their support and suggestions on the project. This work was supported bythe National Natural Science Foundation of China (Grant Nos. 30130030and 30121003).

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(Received May 21, 2003; accepted October 10, 2003)

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