Roles of Polycomb complexes in regulating gene expression and chromatin structure in plants

Abstract

The evolutionary conserved Polycomb Group (PcG) repressive system comprises two central protein complexes, PcG repressive complex 1 (PRC1) and PRC2. These complexes, through the incorporation of histone modifications on chromatin, have an essential role in the normal development of eukaryotes. In recent years, a significant effort has been made to characterize these complexes in the different kingdoms, and despite there being remarkable functional and mechanistic conservation, some key molecular principles have diverged. In this review, we discuss current views on the function of plant PcG complexes. We compare the composition of PcG complexes between animals and plants, highlight the role of recently identified plant PcG accessory proteins, and discuss newly revealed roles of known PcG partners. We also examine the mechanisms by which the repression is achieved and how these complexes are recruited to target genes. Finally, we consider the possible role of some plant PcG proteins in mediating local and long-range chromatin interactions and, thus, shaping chromatin 3D architecture.

Keywords: PRC1; PRC2; Polycomb Group; chromatin organization; gene repression; histone modifications.

Figure 1

A diverse repertoire of PRC1s. Schematic representation of PRC1 E3 modules in Drosophila, vertebrates, and Arabidopsis and accessory proteins found in canonical PRC1s (cPRC1s) and variant PRC1s (vPRC1s) in the different cases. Possible accessory proteins that have not been verified by AP–MS are indicated in a dotted background. The complete names of vertebrate accessory proteins that are not mentioned in the text are: AUTS2, autism susceptibility protein 2; BCOR, BCL-6 co-repressor; CK2, casein kinase 2; FBRS, fibrosin; L3MBTL2, lethal(3)malignant brain tumor-like protein 2; SKP1, S-phase kinase-associated protein 1; DCAF7, DDB1 and CUL4-Associated Factor 7; and WDR5, WD40-repeat protein 5.

Figure 2

PRC2 cores and accessory proteins. Schematic representation of PRC2 core components in Drosophila, vertebrates, and Arabidopsis and accessory proteins found in the different PRC2 sub-complexes. Possible accessory proteins that have not been verified by AP–MS are indicated in a dotted background.

Figure 3

Model for the two proposed PcG-mediated repressive mechanisms in plants. Before the recruitment of PcG complexes, PRC1-dependent genes are active, whereas PRC1-independent genes are repressed. Once PRC1 is targeted to active genes, chromatin becomes less accessible, and the transcription is downregulated. PRC2 then recognizes H2AK121ub marks and PRC1 components and mediates the transcriptional repression of these genes by promoting an inaccessible chromatin state, which is responsive to reactivation. Repressed genes are targeted only by PRC2, which maintains an inaccessible chromatin state.

Figure 4

Factors implicated in target site identification in plants. (A) TFs recognize their DNA binding motifs at PRE-like sequences of target sites. TFs that contain an EAR domain as a common feature participate in PRC2 and HDAC complex recruitment. While VAL factors act as a platform for the assembly of PRC1, PRC2, and HDAC (left panel), other TFs lead to the recruitment of PRC2 and HDAC independently of PRC1 activity (right panel). The ability of VAL factors and other PRC1 and PRC2 accessory proteins to bind histone modifications, such as H3K4me3, may stabilize the recruitment of the complexes to target genes. (B) An intronic lncRNA from the floral homeotic AGAMOUS (AG) gene, lncRNA-4, is expressed in leaves and interacts with CLF to deposit H3K27me3 histone marks into the AG locus. (C) The lncRNA APOLO mediates the formation of R-loops by sequence complementarity with its targets, which attract LHP1 and PRC2 core components.

Figure 5

PcG proteins and chromatin structure in plants. Different PcG proteins, such as EMF1, LHP1, or BAH proteins, may promote the formation of H3K27me3-marked domains, chromatin compaction, long-range chromatin loops, and phase-separated Polycomb bodies, which contribute to the maintenance of genes in a stable repressed state.