Natural variation of H3K27me3 determines genes important for cell fate in the unicellular eukaryotic model Phaeodactylum tricornutum

In multicellular organisms, tri-methylation of lysine 27 of histone H3 (H3K27me3) was shown to be deposited by Polycomb Repressive Complex 2 (PRC2) to establish and maintain silencing, critical for cell fate and developmentally regulated processes. PRC2 complex is absent in both yeast Saccharomyces cerevisiae and S. pombe which initially suggested that PRC2 arose with the emergence of multicellularity. However, its discovery in several microalgae questions its role in this important class of organisms. Here, we show using mutants of the homologue of catalytic unit of PRC2, enhancer of zeste E(z) in the model diatom P. tricornutum (Pt), which presents different morphotypes (fusiform, triradiate, oval and cruciform) that Pt E(z) is responsible of di and tri-methylation of lysine 27. Indeed, H3K27me3 depletion causes the distortion of the morphology providing evidence for a role of H3K27me3 in cell differentiation in unicellular species. H3K27me3 genome wide profiling in fusiform and triradiate further revealed genes important for cell identity. These results suggest a role of PRC2 and its associated mark in cell fate in unicellular species and their ancestral function in a broad evolutionary context.