Dynamics of polycomb group marks in Arabidopsis.

Polycomb Group (PcG) histone-modifying system is key in maintaining gene repression, providing a mitotically heritable cellular memory. Nevertheless, to allow plants to transition through distinct transcriptional programs during development or to respond to external cues, PcG-mediated repression requires reversibility. Several data suggest that the dynamics of PcG marks may vary considerably in different cell contexts; however, how PcG marks are established, maintained, or removed in each case is far from clear. In this review, we survey the knowns and unknowns of the molecular mechanisms underlying the maintenance or turnover of PcG marks in different cell stages.

Binding by the Polycomb complex component BMI1 and H2A monoubiquitination shape local and long-range interactions in the Arabidopsis genome.

Three-dimensional (3D) chromatin organization is highly dynamic during development and seems to play a crucial role in regulating gene expression. Self-interacting domains, commonly called topologically associating domains (TADs) or compartment domains (CDs), have been proposed as the basic structural units of chromatin organization. Surprisingly, although these units have been found in several plant species, they escaped detection in Arabidopsis (Arabidopsis thaliana). Here, we show that the Arabidopsis genome is partitioned into contiguous CDs with different epigenetic features, which are required to maintain appropriate intra-CD and long-range interactions. Consistent with this notion, the histone-modifying Polycomb group machinery is involved in 3D chromatin organization. Yet, while it is clear that Polycomb repressive complex 2 (PRC2)-mediated trimethylation of histone H3 on lysine 27 (H3K27me3) helps establish local and long-range chromatin interactions in plants, the implications of PRC1-mediated histone H2A monoubiquitination on lysine 121 (H2AK121ub) are unclear. We found that PRC1, together with PRC2, maintains intra-CD interactions, but it also hinders the formation of H3K4me3-enriched local chromatin loops when acting independently of PRC2. Moreover, the loss of PRC1 or PRC2 activity differentially affects long-range chromatin interactions, and these 3D changes differentially affect gene expression. Our results suggest that H2AK121ub helps prevent the formation of transposable element/H3K27me1-rich long loops and serves as a docking point for H3K27me3 incorporation.

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

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.

EAR domain-containing transcription factors trigger PRC2-mediated chromatin marking in Arabidopsis.

Polycomb group (PcG) complexes ensure that every cell in an organism expresses the genes needed at a particular stage, time, or condition. However, it is still not fully understood how PcG complexes PcG-repressive complex 1 (PRC1) and PRC2 are recruited to target genes in plants. Recent findings in Arabidopsis thaliana support the notion that PRC2 recruitment is mediated by different transcription factors (TFs). However, it is unclear how all these TFs interact with PRC2 and whether they also recruit PRC1 activity. Here, by using a system to bind selected TFs to a synthetic promoter lacking the complexity of PcG target promoters in vivo, we show that while binding of the TF VIVIPAROUS1/ABSCISIC ACID-INSENSITIVE3-LIKE1 recapitulates PRC1 and PRC2 marking, the binding of other TFs only renders PRC2 marking. Interestingly, all these TFs contain an Ethylene-responsive element binding factor-associated Amphiphilic Repression (EAR) domain that triggers both HISTONE DEACETYLASE COMPLEX and PRC2 activities, connecting two different repressive mechanisms. Furthermore, we show that different TFs can have an additive effect on PRC2 activity, which may be required to maintain long-term repression of gene expression.