Polycomb Repressive Complex 2 in Eukaryotes—An Evolutionary Perspective

Abstract

Polycomb repressive complex 2 (PRC2) represents a group of evolutionarily conserved multi-subunit complexes that repress gene transcription by introducing trimethylation of lysine 27 on histone 3 (H3K27me3). PRC2 activity is of key importance for cell identity specification and developmental phase transitions in animals and plants. The composition, biochemistry, and developmental function of PRC2 in animal and flowering plant model species are relatively well described. Recent evidence demonstrates the presence of PRC2 complexes in various eukaryotic supergroups, suggesting conservation of the complex and its function. Here, we provide an overview of the current understanding of PRC2-mediated repression in different representatives of eukaryotic supergroups with a focus on the green lineage. By comparison of PRC2 in different eukaryotes, we highlight the possible common and diverged features suggesting evolutionary implications and outline emerging questions and directions for future research of polycomb repression and its evolution.

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

“…TEs are marked with DNA and H3K9 methylation that are associated with silencing in flowering plants 5 , animals, and fungi 6 . Yet, in distantly related eukaryotes TEs are instead marked by H3K27me3 deposited by the Polycomb Repressive Complex 2 (PRC2) [7][8][9][10][11] , an epigenetic mark associated with gene silencing in multicellular eukaryotes [12][13][14][15] . It was therefore proposed that the ancestral activity of PRC2 was the deposition of H3K27me3 to silence TEs 16 .To test this hypothesis we obtained mutants deprived of PRC2 activity and used genomics to analyze the role of PRC2 in extant species along the lineage of Archaeplastida.…”

The Importance of Networking: Plant Polycomb Repressive Complex 2 and Its Interactors

“…Throughout evolution, PRC2 may have recruited specific interactors in the plant cells to acquire novel and plant-specific activities that are key to the regulation of plant development and responses. Therefore, evolutionary studies to address why plants needed to invent these interactions, such as the ones currently carried out in ancestral plant species [ 169 ], will aid in clarifying PRC2’s phylogeny and elucidating its contribution to the evolution of plant development and adaptation [ 4 ]. The advancement in proteomic techniques, such as the affinity purification coupled to mass spectrometry (AP/MS) TAP assay [ 170 ], has proven to be crucial for revealing protein–protein interactions.…”

“…More recently, genome-wide enrichment of H3K27me3 in important crops, such as rice, maize, barley and oilseed rape, has been made available [ 14 , 16 , 172 ], demonstrating a similar epigenomic landscape but also special features in the deposition of this mark. Phylogenetic analyses also demonstrate a good conservation of the proteins of the complex and the possible existence of similar PRC2 subcomplexes [ 4 , 173 ]. However, much more research is needed to understand how PRC2’s functions are regulated in these species through the conservation of its protein network or through the formation of novel species-specific interactions.…”

“…PRC2 was first identified in Drosophila consisting of four core components: Enhancer of zeste (E(z)), a histone methyltransferase unit that catalyses H3K27me3; Extra sex combs (Esc), a WD40 domain protein scaffolding the interactions within the complex; Suppressor of zeste 12 (Su(z)12), a Zinc Finger protein that is essential for binding to nucleosomes; and Nuclear remodeling factor (Nurf55, also called p55), a Trp-Asp (WD) repeat protein involved in nucleosome remodelling [ 1 , 2 ]. After discovering PRC2 complexes in Drosophila as regulators of Hox genes expression, homologs of PRC2 subunits were identified in plants and other organisms [ 3 , 4 , 5 ]. In Arabidopsis thaliana ( Arabidopsis ), there are three E(z) homologs—CURLY LEAF (CLF), SWINGER (SWN) and MEDEA (MEA); three Su(z)12 homologs—EMBRYONIC FLOWER 2 (EMF2), VERNALIZATION 2 (VRN2) and FERTILIZATION-INDEPENDENT SEED 2 (FIS2); a single Esc homolog—FERTILIZATION-INDEPENDENT ENDOSPERM (FIE); and there are five Arabidopsis homologs of p55 protein—MULTICOPY SUPPRESSOR OF IRA (MSI) 1–5, but MSI1 is the only one demonstrated to be part of the PRC2 complex [ 6 , 7 ].…”

Transcriptional Stress Memory and Transgenerational Inheritance of Drought Tolerance in Plants

“…PcG genes were discovered in Drosophila ( Drosophila melanogaster ), and homologs of PcG components and their target genes have been identified in other eukaryotes including plants [ 173 , 174 , 175 , 176 ]. The role of the PRC2-mediated deposition of H3K27me3 has been studied in the context of developmental processes and environmental stress responses in plant model species including Arabidopsis [ 172 , 177 , 178 , 179 ].…”