Multicellular development and protein-protein interactions

The macroevolution of organs and tissues in higher plants and animals may have been contingent upon the expansion of numerous gene families encoding interacting proteins. For example, there are dozens of gene families encoding actin cytoskeletal proteins that elaborate intercellular structures influencing development. Once gene family members evolve compartmentalized expression, protein isovariants are free to coevolve new interacting partners that may be incompatible with other related protein networks. Ancient classes of actin isovariants and actin-binding proteins are clear examples of such coevolving networks. Ectopic expression and suppression studies were used to dissect these interactions. In higher plants, the ectopic expression of a reproductive actin isovariant in vegetative cell types causes aberrant reorganization of the F-actin cytoskeleton and bizarre development of most organs and tissues. In contrast, overexpression of vegetative actin in vegetative cell types has little effect. The extreme ectopic actin expression phenotypes are suppressed by the coectopic expression of reproductive profilin or actin depolymerizing factor (ADF/cofilin) isovariants, but not by the overexpression of vegetative profilin or ADF. These data provide evidence for the coevolution of organ-specific protein-protein interactions. Thus, understanding the contingent relationships between the evolution of organ-specific isovariant networks and organ origination may be key to explaining multicellular development.