My work is largely focused on the evolution of ABC program, a genetic module that controls the establishment of floral organ identity. This model describes how the overlapping domains of three classes of genes function to establish floral organ identity by producing a combinatorial code such that A function alone encodes sepal identity; A and B function, petal identity; B and C function, stamen identity; and C function alone, carpel identity (figure below). Genetic analyses of mutations in A, B and C class genes from Arabidopsis and Antirrhinum indicate that this program is functioning similarly in both model species, despite their differences in floral morphology and phylogenetic position (Carpenter and Coen, 1990; Bowman et al., 1991). These mutants exhibit homeotic phenotypes, each displaying a
transformation of floral organ identity in two adjacent whorls. In mutants in the B group genes, for instance, petals are transformed into sepals and stamens, into carpels (Bowman et al., 1989). When the genes corresponding to the three classes of mutants were cloned it was found that Arabidopsis genes from each class are homologous to those in the corresponding classes of Antirrhinum (Coen and Meyerowitz, 1991). Furthermore, all but one of the so-called ABC genes are members of the MADS-box family of transcription factors, specifically MIKC-type MADS box genes (reviewed Theissen et al., 2000). Recently, an additional class of these genes, the SEPALLATAs (SEPs or E class genes) have been shown to be necessary for the proper functioning of the original ABC genes (Pelaz et al., 2000; Honma and Goto, 2001).
In a series of elegant genetic experiments using both mutants and lines exhibiting ectopic expression of the ABC genes, it has been shown that the identities of all the floral organs in an Arabidopsis flower are interchangeable and depend entirely on the ABC code expressed in the developing primordia (Bowman et al., 1991; Mizukami and Ma, 1992; Krizek and Meyerowitz, 1996). These findings have implications for the possible evolution of perianth organs. One can imagine that if the evolution of the ABC program predated the radiation of the angiosperms, the transition between, for instance, an entirely petaloid perianth and one with sepals and petals could be due to a simple shift in the B domain boundary (Bowman, 1997; Albert et al., 1998). Similarly, a lineage possessing petals could give rise to one without and, perhaps more importantly, vice versa. This “sliding boundary” model represents a conflict between the Darwinian gradualism embraced by traditional botanical studies and our modern understanding of the power of homeosis to radically alter morphology (Kramer and Irish, 2000; Kramer et al., 2003). Moreover, it suggests that although the differences among types of petaloid organs seem to indicate that they are independently derived, the pattern could be the product of a commonly inherited but differentially expressed petal identity program. On the whole, comparative studies suggest that while the ABC program is generally conserved, it is not a static entity and has been impacted significantly by patterns of gene duplication and divergence. The ABC genes originally identified in Arabidopsis are not immune to this phenomenon and may, in many respects, exhibit what could be considered derived characteristics. Moreover, across the angiosperms there are many examples of novel floral organ types that do not fit simply into the ABC model.
Currently, I am working to address several questions related to the evolution of the ABC program. These include:
How did a coincident group of duplications in each of the major floral organ identity gene lineages (AP1, AP3, AG and SEP) shape the evolution of the ABC program in the core eudicots?
How has the ancestral ABC program been modified in the lower eudicot order Ranunculales to produce the wide diversity of perianth morphologies observed in these genera?
References
Albert, V.A., Gustafsson, M.H.G., and Di Laurenzio, L. (1998). Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In Molecular Systematics of Plants, II, D. Soltis, P. Soltis, and J.J. Doyle, eds (New York: Chapman and Hall), pp. 349-374.
Bowman, J.L. (1997). Evolutionary conservation of angiosperm flower development at the molecular and genetic levels. Journal of Bioscience 22, 515-527.
Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. The Plant Cell 1, 37-52.
Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1991). Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1-20.
Carpenter, R., and Coen, E.S. (1990). Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes and Development 4, 1483-1493.
Coen, E.S., and Meyerowitz, E.M. (1991). The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37.
Honma, T., and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409, 525-529.
Kramer, E.M., Di Stilio, V.S., and Schluter, P. (2003). Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. IJPS 164, 1-11.
Kramer, E.M., and Irish, V.F. (2000). Evolution of the petal and stamen developmental programs: Evidence from comparative studies of the lower eudicots and basal angiosperms. Int J Plant Sci 161, S29-S40.
Krizek, B.A., and Meyerowitz, E.M. (1996). The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122, 11-22.
Mizukami, Y., and Ma, H. (1992). Ectopic expression of the floral homeotic gene agamous in transgenic arabidopsis plants alters floral organ identity. Cell 71, 119-131.
Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., and Yanofsky, M. (2000). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200-203.
Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Munster, T., Winter, K.-U., and
H., S. (2000). A short history of MADS-box genes in plants. Plant Molecular Biology 42,
115-149.
One of Elena’s major sources of distraction - Sam the Bear