Roles of MADS-box genes during carpel and ovule development in Arabidopsis

As is the case for other eukaryotes, the Arabidopsis genome contains many different gene families. These families are the result of extensive gene duplication that occurred during the evolution of Arabidopsis. Although most duplicated genes have evolved to acquire distinct roles, many still share overlapping functions reflecting their ancestral lineage. Such genetic redundancy greatly complicates functional characterization. Here we identify overlapping functions for four closely related MADS-box genes derived from a common ancestor: AGAMOUS (AG), SHATTERPROOF1 (SHP1), SHP2, and SEEDSTICK (STK). Studies on AG and SHP1/2 have been reported previously. AG is essential for development of the carpel, the female reproductive organ, while the SHP genes redundantly control seed dispersal. The expression data for these genes, together with their sequence similarity, suggest that they are likely to share redundant activities during carpel development. We show here that AG and SHP1/2 indeed act redundantly to specify carpel identity and that in an ap2 mutant flower, carpelloid features occurring on first whorl organs are completely suppressed only when AG, SHP1, and SHP2 are simultaneously inactivated. Our expression and functional characterization indicate that STK, which is expressed in ovules and seeds, is required for seed abscission and for funiculus morphogenesis. Significantly, STK and the other three other members of the AG clade act redundantly to promote ovule development, a landmark achievement of plant evolution that enabled seed plants to become the most successful group of land plants in nature. Lastly, we show that SEPALLATA factors, another class of redundant MADS-box proteins, interact with all members of AG clade to form ternary protein complexes involved in ovule development.