Uncoupled evolution of the Polycomb system and deep origin of non-canonical PRC1

Abstract

Polycomb group (PcG) proteins modulate chromatin states to silence gene transcription in plants and animals. Most PcG proteins function as part of distinct multi-subunit Polycomb repressive complexes (PRCs). Gene repression by the Polycomb system involves chromatin compaction by canonical PRC1 (cPRC1), mono-ubiquitylation of histone H2A (H2Aub1) by non-canonical PRC1 (ncPRC1) and tri-methylation of histone H3K27 (H3K27me3) by PRC2. Prevalent models for Polycomb repression emphasize a tight functional coupling between PRC1 and PRC2. However, whether this paradigm indeed reflects the evolution and functioning of the Polycomb system remains unclear. Here, we examined the relationship between cPRC1, ncPRC1 and PRC2 through a comprehensive analysis of their presence and evolution across the entire eukaryotic tree of life. We show that both PRC1 and PRC2 were present in the Last Eukaryotic Common Ancestor (LECA), but that their subsequent evolution is uncoupled. The identification of orthologs for ncPRC1-defining subunits in unicellular relatives of animals and of fungi suggests that the origin of ncPRC1 predates that of cPRC1, and we develop a scenario for the evolution of cPRC1 from ncPRC1. Our results demonstrate the independent evolution and function of PRC1 and PRC2 and show that crosstalk between these complexes is a secondary development in evolution.