REVIEW

Chinese Science Bulletin 2003 Vol. 48 No. 24 26512657

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:anmin@ns.ibcas.ac.cn)

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
2651

REVIEW

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] ,
2652

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 (130 90 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 Cy -

Chinese Science Bulletin Vol. 48 No. 24 December 2003

REVIEW

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,
2653

REVIEW
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 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 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
2654

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
2655

REVIEW
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 sequences 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 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].
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). identity functions require SEPALLATA MADS-box genes, Nature, 2000, 405: 200203. Becker, A., Kaufmann, K., Freialdenhoven, A. et al., A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes, Mol. Genet Genomics, 2002, 266: 942 950. Theissen, G., Becker, A., Winter, K. U. et al., How the land plants learned their floral ABCs: The role of MADS-box genes in the evolutionary origin of flowers, in Developmental Genetics and Plant Evolution (eds. Cronk, Q. C. B., Bateman, R. M., Hawkins, J. A.), London: Taylor & Francis, 2002, 173205. Theissen, G., Saedler, H., Floral quartets, Nature, 2001, 409: 469 471. Sommer, H., Beltrn, J. P., Huijser, P. et al., DEFICIENS , a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus : The protein shows homology to transcription factors, EMBO J., 1990, 9(3): 605613. Norman, C., Runswick, M., Pollock, R. et al., Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element, Cell, 1988, 55: 9891003. Herskowitz, I., A regulatory hierarchy for cell specialization in yeast, Nature, 1989, 342: 749757. Ma, H., Yanofsky, M. F., Meyerowitz, E. M., AGL1 -AGL6 , an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes, Genes Dev., 1991, 5(3): 484495. Theissen, G., Becker, A., Rosa, A. D. et al., A short history of MADS-box genes in plants, Plant Mol. Biol., 2000, 42: 115149. Purugganan, M. D., Rounsley, S. D., Schmidt, R. J. et al., Molecular evolution of flower development: Diversification of the plant MADS-box regulatory gene family, Genetics, 1995, 140: 345 356. Johansen, B., Pedersen, L. B., Skipper, M. et al., MADS-box gene evolution-structure and transcription patterns, Mol. Phyl. Evol., 2002, 23: 458480. Henschel, K., Kofuji, R., Hasebe, M. et al., Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens, Mol. Biol. Evol., 2002, 19(6): 801814. Jack, T., Plant development going MADS, Plant Mol. Biol., 2001, 46(5): 515520. Rutledge, R., Regan, S., Nicolas, O. et al., Characterization of an AGAMOUS homologue from the conifer black spruce (picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis, Plant J., 1998, 625634. Winter, K. U., Becker, A., Munster, T. et al., MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants, Proc. Natl. Acad. Sci. USA, 1999, 96(13): 7342 7347. Mnster, T., Pahnke, J., Rosa, A. D. et al., Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants, Proc. Natl. Acad. Sci. USA, 1997, 94(6): 24152420. Svensson, M. E., Johannesson, H., Engstrom, P., The LAMB1 gene from the clubmoss, Lycopodium annotinum, is a divergent MADSbox gene, expressed specifically in sporogenic structures, Gene, 2000, 253(1): 3143. Hasebe, M., Evolution of reproductive organs in land plants, J. Plant Res., 1999, 112: 463474. Crane, P. R., Friis, E. M., Pedersen, K. R., The origin and early diversification of angiosperms, Nature, 1995, 374(2): 2733. Wang, X., Evolution of MADS-box gene and development of reproductive organ of plants, in Advances in Plant Sciences (ed. Li, C.), Beijing: CHEP & Springer, 2001, 314. Sun, K., Chen, J., Chen, Z., Progress in studies on floral develop-

13.

14.

15. 16.

17.

18. 19.

20. 21.

References
1. Mandel, M. A., Gustafson-Brown, C., Savidge, B. et al., Molecular characterization of the Arabidopsis floral homeotic gene APETALA1, Nature, 1992, 360: 273277. 2. Irish, V. F., Sussex, I. M., Function of the APETALA-1 gene during Arabidopsis floral development, Plant Cell, 1990, 2: 741753. 3. Jofuku, K. D., Boer, B. G. W. D., Montagu, M. V. et al., Control of Arabidopsis flower and seed development by the homeotic gene APETALA2, Plant Cell, 1994, 6: 1211 1225. 4. Jack, T., Brockman, L. L., Meyerowitz, E. M., The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens, Cell, 1992, 68: 683697. 5. Krizek, B., Meyerowitz, E. M., The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function, Development, 1996, 122(1): 11 22. 6. Yanofsky, M. F., Ma, H., Bowman, J. L. et al., The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors, Nature, 1990, 346: 3539. 7. Schwarz-Sommer, Z., Huijser, P., Nacken, W. et al., Genetic control of flower development by homeotic genes in Antirrhinum majus, Science, 1990, 250: 931936. 8. Coen, E. S., Meyerowitz, E. M., The war of the whorls: Genetic interactions controlling flower development, Nature, 1991, 353: 31 37. 9. Theissen, G., Development of floral organ identity: Stories from the MADS house, Curr. Opin. Plant Biol., 2001, 4: 7585. 10. Bowman, J. L., Evolutionary conservation of angiosperm flower development at the molecular and genetic levels, J. Biosci., 1997, 22(4): 515527. 11. Colombo, L., Franken, J., Koetje, E. et al., The Petunia MADS box gene FBP11 determines ovule identity, Plant Cell, 1995, 7: 1859 1868. 12. Pelaz, S., Ditta, G. S., Baumann, E. et al., B and C floral organ 22.

23.

24. 25.

26.

27.

28.

29. 30. 31.

32.

2656

Chinese Science Bulletin Vol. 48 No. 24 December 2003

REVIEW
33. 34. 35. ment of a ngiosperms and some consideration on future studies, Acta Phytotax. Sin., 1998, 36(6): 558568. Frohlich, M. W., MADS about Gnetales, Proc. Natl. Acad. Sci. USA, 1999, 96: 8811 8813. Sun, G., Ji, Q., Dileher, D. L. et al., Archaefructaceae, a new basal angiosperm family, Science, 2002, 296: 899904. Hufford, L., The morphology and evolution of male repr oductive structures of Gnetales, Int. J. Plant Sci., 1996, 157(6 Suppl.): S95 S112. Endress, P. K., Structure and function of female and bisexual organ complexes in Gentales, Int. J. Plant Sci., 1996, 157(6 Suppl.): S113 S125. Donoghue, M. J., Doyle, J. A., Seed plant phylogeny: Demise of the Anthophyte hypothesis? Curr. Biol., 2000, 10: R106R109. Frohlich, M. W., Parker, D. S., The mostly male theory of flower evolutionary origins: From genes to fossils, Syst. Bot., 2000, 25(2): 155170. Vahala, T., Oxelman, B., Arnold, S. V., Two APETALA2-like genes of Picea abies are differentially expressed during development, J. Exp. Bot., 2001, 52: 1111 1115. Baum, D. A., The evolution of plant d evelopment, Curr. Opin. Plant Biol., 1998, 1: 7986. Endress, P. K., The Chloranthaceae: Reproductive structures and phylogenetic position, Bot. Jahrb. Syst., 1987, 109(2): 153226. Wu, Z., Lu, A., Tang, Y. et al., Synopsis of a new polyphyletic-polychronic-polytopic system of the angiosperms, Acta Phytotax. Sin., 2002, 40(4): 289322. Kramer, E. M., Irish, V. F., Evolution of the petal and stamen developmental programs: Evidence from comparative studies of the lower eudicots and basal angiosperms , Int. J. Plant Sci., 2000, 161: S29S40. Kramer, E. M., Irish, V. F., Evolution of genetic mechanisms controlling petal development, Nature, 1999, 399: 144148. Ma, H., Depamphilis, C., The ABCs of floral evolution, Cell, 2000, 101: 5 8. Cronk, Q. C. B., Plant evolution and development in a post-genomic context, Nat. Rev. Gen., 2001, 2: 607619. Lawton-Rauh, A. L., Alvarez-Buylla, E. R., Purugganan, M. D., Molecular evolution of flower development, Tree, 2000, 15(4): 144 149. Baum, D. A., Whitlock, B. A., Plant development: Genetic clues to petal evolution, Curr. Biol., 1999, 9: R525R527. Kramer, E. M., Stilio, V. S. D., Schluter, P. M., Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae, Int. J. Plant Sci., 2003, 164(1): 1 11. Purugganan, M. D., Suddith, J. I., Molecular population genetics of floral homeotic loci: Departures from the equilibrium-neutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana, Genetics, 1999, 151: 839848. Barrier, M., Robichaux, R. H., Purugganan, M. D., Accelerated regulatory gene evolution in an adaptive radiation, Proc. Natl. Acad. Sci. USA, 2001, 98(18): 1020810213. Lowman, A. C., Purugganan, M. D., Duplication of the Brassica oleracea APETALA1 floral homeotic gene and the evolution of domesticated cauliflower, J. Heredity, 1999, 90: 514520. Purugganan, M. D., Suddith, J. I., Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: Nonneutral evolution and naturally occurring variation in floral homeotic function, Proc. Natl. Acad. Sci. USA, 1998, 95: 81308134. Ford, V. S., Gottlieb, L. D., Bicalyx is a natural homeotic floral variant, Nature, 1992, 358: 671673. Mizukami, Y., Ma, H., Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA, Plant Mol. Biol., 1995, 28: 767784. 56. Tooke, F., Battey, N. H., A leaf-derived signal is a quantitative determinant of floral form in impatiens, Plant Cell, 2000, 12: 1837 1847. 57. Kater, M. M., Franken, J., Carney, K. J. et al., Sex determination in the monoecious species cucumber is confined to specific floral whorls, Plant Cell, 2001, 13: 481493. 58. Luo, D., Carpenter, R., Vincent, C. et al., Origin of floral asymmetry in Antirrhinum, Nature, 1996, 383: 794799. 59. Luo, D., Carpenter, R., Copsey, L. et al., Control of organ asymmetry in flowers of Antirrhinum, Cell, 1999, 99: 367376. 60. Hodin, J., Plasticity and constraints in development and evolution, Mol. Dev. Evol., 2000, 288: 1 20. 61. Theissen, G., Secret life of genes, Nature, 2002, 415: 741. 62. Doyle, J. A., Donoghue, M. J., Seed plant phylogeny and the origin of angiosperms: An experimental cladistic approach, Bot. Rev., 1986, 52: 321431. 63. Ambrose, B. A., Lerner, D. R., Ciceri, P. et al., Molecular and genetic analyses of the SILKY1 gene reveal conservation in floral organ specification between eudicots and monocots, Mol. Cell, 2000, 5: 569579. 64. Force, A., Lynch, M., Pickett, F. B. et al., Preservation of duplicate genes by complementary, degenerative mutations, Genetics, 1999, 151: 15311545. 65. Carroll, S. B., Endless forms: The evolution of gene regulation and morphological diversity, Cell, 2000, 101: 577580. 66. Mena, M., Ambrose, B. A., Meeley, R. B. et al., Diversification of C-function activity in maize flower development, Science, 1996, 274(5292): 15371540. 67. Greer, J. M., Puetz, J., Thomas, K. R. et al., Maintenance of functional equivalence during paralogous HOX gene evolution, Nature, 2000, 403: 661665. 68. Mattick, J. S., Gagen, M. J., The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAS in the development of complex organisms, Mol. Biol. Evol., 2001, 18(9): 1611 1630. 69. Koch, M. A., Weisshaar, B., Kroymann, J. et al., Comparative genomice and regulatory evolution: Conservation and function of the CHS and APETALA3 promoters, Mol. Biol. Evol., 2001, 18(10): 18821891. 70. Winter, K. U., Weiser, C., Kaufmann, K. et al., Evolution of class B floral homeotic proteins: Obligate heterodimerization originated from homodimerization, Mol. Biol. Evol., 2002, 19(5): 587596. 71. Ferrario, S., Immink, R. G. H., Shchennikova, A. et al., The MADS box gene FBP2 is required for SEPALLATA function in petunia, Plant Cell, 2003, 15: 914925. 72. Qiu, Y. L., Lee, J. Bernasconi-Quadroni, F. et al., The earliest angiosperms: Evidence from mitochondrial, plastmid and nuclear genomes, Nature, 1999, 402: 404407. 73. Kuzoff, R. K., Gasser, C. S., Recent progress in reconstructing angiosperm phylogeny, Trends Plant Sci., 2000, 5(8): 330336. 74. Soltis, P. S., Soltis, D. E., Chase, M. W., Angiosperm phylogeny inferred from multiple genes as a tool for comparaive biology, Nature, 1999, 402: 402404. 75. Baum, D. A., Doebley, J., Irish, V. F. et al., Response: Missing links: The genetic architecture of flower and floral dive rsification, Trends Plant Sci., 2002, 7(1): 3134. 76. Soltis, D. E., Soltis, P. S., Albert, V. A. et al., Missing links: The genetic architecture of flower and floral diversification, Trends Plant Sci., 2002, 7(1): 2231. 77. Arthur, W., The emerging conceptual framework of evolutionary developmental biology, Nature, 2002, 415: 757764. (Received May 21, 2003; accepted O ctober 10, 2003)

36.

37. 38.

39.

40. 41. 42.

43.

44. 45. 46. 47.

48. 49.

50.

51.

52.

53.

54. 55.

Chinese Science Bulletin Vol. 48 No. 24 December 2003

2657