The ABCs of floral evolution.

Because eudicots and monocots are on separate deep branches of the angiosperm phylogenetic tree, the strong genetic and molecular evidence supporting the conservation of the ABC model suggests that this model represents an ancient regulatory network and is likely to be generally applicable to most, if not all, angiosperms. This does not mean, however, that various modifications of specific components of the model cannot occur in different angiosperm lineages at different times, as we have discussed for some of the minor divergence of gene functions when duplicate genes have arisen to take the place of a single gene. In these cases, the sum of the duplicate genes can be equivalent of the single-copy ABC genes, and the general framework of the model remains intact.It is likely that the ABC MADS box genes have their origins in plants long before the appearance of angiosperms, on the basis of molecular clock estimates and phylogenetic analysis (Purugganan 1997xPurugganan, M.D. Mol. Evol. 1997; 45: 392–396Crossref | PubMed | Scopus (83)See all ReferencesPurugganan 1997). MADS box genes homologous to eudicot B and C function genes (and expressed in patterns consistent with these functions) have been isolated from the closest relatives of flowering plants, the nonflowering seed plants, the gymnosperms, including conifers (Figure 1Figure 1) (Rutledge et al. 1998xRutledge, R, Regan, S, Nicolas, O, Fobert, P, Cote, C, Bosnich, W, Kauffeldt, C, Sunohara, G, Seguin, A, and Stewart, D. Plant J. 1998; 15: 625–634Crossref | PubMedSee all ReferencesRutledge et al. 1998) and Gnetales (Winter et al. 1999xWinter, K.U, Becker, A, Munster, T, Kim, J.T, Saedler, H, and Theissen, G. Proc. Natl. Acad. Sci. USA. 1999; 96: 7342–7347Crossref | PubMed | Scopus (216)See all ReferencesWinter et al. 1999). Among all gymnosperms, Gnetales have until recently been considered the closest relatives of angiosperms; along with several extinct lineages, these plants have become known as the “Anthophytes” because of similarities in reproductive structure and development (Crane et al. 1995xCrane, P.R, Friis, E.M, and Pedersen, K.R. Nature. 1995; 374: 27–33Crossref | Scopus (465)See all ReferencesCrane et al. 1995). However, recent molecular studies indicate that all gymnosperms form a monophyletic group and that Gnetales are closest to conifers (Figure 1AFigure 1A) (16xQiu, Y.L, Lee, J, Bernasconi-Quadroni, F, Soltis, D.E, Soltis, P.S, Zanis, M, Zimmer, E.A, Chen, Z, Savolainen, V, and Chase, M.W. Nature. 1999; 402: 404–407Crossref | PubMed | Scopus (597)See all References, 20xWinter, K.U, Becker, A, Munster, T, Kim, J.T, Saedler, H, and Theissen, G. Proc. Natl. Acad. Sci. USA. 1999; 96: 7342–7347Crossref | PubMed | Scopus (216)See all References, 2xBowe, L.M, Coat, G, and dePamphilis, C.W. Proc. Natl. Acad. Sci. USA. 2000; 97Crossref | PubMed | Scopus (303)See all References, 4xChaw, S.-M, Parkinson, C.L, Cheng, Y, Vincent, T.M, and Palmer, J.D. Proc. Natl. Acad. Sci. USA. 2000; 97Crossref | PubMed | Scopus (319)See all References). This implies that the morphologically similar structures in angiosperms and Gnetales have evolved independently. The fact that gymnosperms have no flowers suggests that the ancestral B function homologs may regulate only male reproductive organs, and C function homologs may control both male and female reproductive organs. If this is indeed true, then the portion of the ABC model for reproductive organs may have been established and conserved since the time when gymnosperms and angiosperms shared a common ancestor, perhaps 300 million years ago or more (2xBowe, L.M, Coat, G, and dePamphilis, C.W. Proc. Natl. Acad. Sci. USA. 2000; 97Crossref | PubMed | Scopus (303)See all References, 4xChaw, S.-M, Parkinson, C.L, Cheng, Y, Vincent, T.M, and Palmer, J.D. Proc. Natl. Acad. Sci. USA. 2000; 97Crossref | PubMed | Scopus (319)See all References).The isolation of angiosperm and gymnosperm MADS box genes that exhibit strong sequence similarities to the ABC genes (Winter et al. 1999xWinter, K.U, Becker, A, Munster, T, Kim, J.T, Saedler, H, and Theissen, G. Proc. Natl. Acad. Sci. USA. 1999; 96: 7342–7347Crossref | PubMed | Scopus (216)See all ReferencesWinter et al. 1999) provides powerful tools to test evolutionary relationships of not only regulatory gene functions but also developmental structures. The study by Ambrose et al. 2000xAmbrose, B.A, Lerner, D.R, Ciceri, P, Padilla, C.M, Yanofsky, M.F, and Schmidt, R.J. Mol. Cell. 2000; 5: 569–579Abstract | Full Text | Full Text PDF | PubMedSee all ReferencesAmbrose et al. 2000 makes it clear that the ABC model may have predictive use for interpretation of relationship between floral organs of diverse angiosperms (see also Bowman 1997xBowman, J.L. J. Biosci. 1997; 22: 515–527CrossrefSee all ReferencesBowman 1997). Several angiosperm lineages (Amborella, Nymphaeales, Illiciales) are now known to branch earlier than the common ancestor of monocots and eudicots (Figure 1AFigure 1A). These include plants that produce flowers with tepals or “petaloid sepals”; therefore, although it may now be predicted that C function will be conserved, it is not yet clear whether distinct A and B functions are established in these basal groups. Perhaps a portion of Darwin's mystery may be solved by learning whether these basal angiosperms possess A and B functions and how angiosperms evolved distinct sepals and petals (Kramer et al. 1998xKramer, E.M, Dorit, R.L, and Irish, V.F. Genetics. 1998; 149: 765–783PubMedSee all ReferencesKramer et al. 1998). Further studies of the MADS box gene family in these basal angiosperms, other gymnosperms, and nonseed plants promise to generate new insights into floral evolution and development. *To whom correspondence should be addressed (e-mail: hxm16@psu.edu).