Expansion of the polycomb system and evolution of complexity

Polycomb group (PcG) proteins regulate and maintain expression pattern of genes set early during development. Although originally isolated as regulators of homeotic genes, PcG members play a key role in epigenetic mechanisms that maintain the expression state of a large number of genes. All members of the two polycomb repressive complexes (PRC1 and PRC2) are conserved during evolution and while invertebrates generally have one gene for each of these, vertebrates have multiple homologues of them. It remains unclear, however, if different vertebrate PcG homologues have distinct or overlapping functions. We have identified and compared the sequence of PcG homologues in various organisms to analyze similarities and differences that shaped the evolutionary history of these proteins. Comparative analysis of the sequences led to the identification of several novel and signature motifs in the vertebrate homologues of these proteins, which can be directly used to pick respective homologues. Our analysis shows that PcG is an ancient gene group dating back to pre-bilaterian origin that has not only been conserved but also expanded during the evolution of complexity. The presence of unique motifs in each paralogue and its conservation for more than 500 Ma indicates their functional relevance and probable unique role. Although this does not rule out completely any overlapping function, our finding that these homologues only minimally overlap in their nuclear localization suggests that each PcG homologue has distinct function. We further propose distinct complex formation by the PcG members. Taken together, our studies suggest non-redundant and specific role of multiple homologues of PcG proteins in vertebrates and indicate major expansion event preceded by emergence of vertebrates that contributed as enhanced epigenetic resource to the evolution of complexity.