Why are orchid flowers so diverse? Reduction of evolutionary constraints by paralogues of class B floral homeotic genes

BACKGROUND: The nearly 30 000 species of orchids produce flowers of unprecedented diversity. However, whether specific genetic mechanisms contributed to this diversity is a neglected topic and remains speculative. We recently published a theory, the 'orchid code', maintaining that the identity of the different perianth organs is specified by the combinatorial interaction of four DEF-like MADS-box genes with other floral homeotic genes. SCOPE: Here the developmental and evolutionary implications of our theory are explored. Specifically, it is shown that all frequent floral terata, including all peloric types, can be explained by monogenic gain- or-loss-of-function mutants, changing either expression of a DEF-like or CYC-like gene. Supposed dominance or recessiveness of mutant alleles is correlated with the frequency of terata in both cultivation and nature. Our findings suggest that changes in DEF- and CYC-like genes not only underlie terata but also the natural diversity of orchid species. We argue, however, that true changes in organ identity are rare events in the evolution of orchid flowers, even though we review some likely cases. CONCLUSIONS: The four DEF paralogues shaped floral diversity in orchids in a dramatic way by modularizing the floral perianth based on a complex series of sub- and neo-functionalization events. These genes may have eliminated constraints, so that different kinds of perianth organs could then evolve individually and thus often in dramatically different ways in response to selection by pollinators or by genetic drift. We therefore argue that floral diversity in orchids may be the result of an unprecedented developmental genetic predisposition that originated early in orchid evolution.