Histone H1 protects telomeric repeats from H3K27me3 invasion inArabidopsis

Abstract

Linker histones play a pivotal role in shaping chromatin architecture, notably through their globular H1 (GH1) domain that contacts the nucleosome and linker DNA. Yet, the interplay of H1 with chromatin factors along the epigenome landscape is poorly understood. Here, we report that Arabidopsis H1 favors chromatin compaction and H3K27me3 marking on a majority of Polycomb-targeted protein-coding genes while preventing H3K27me3 accumulation on telomeres and pericentromeric interstitial telomeric repeats (ITRs). These contrasting effects of H1 on H3K27me3 enrichment are associated with long-distance effects on the 3D organization of telomeres and ITRs. Mechanistically, H1 prevents ITRs from being invaded by Telomere Repeat Binding 1 (TRB1), a GH1-containing telomere component with an extra-telomeric function in targeting Polycomb to genes bearing telomeric motifs. We propose that reciprocal DNA binding of H1 and TRB1 to clustered telobox motifs prevents H3K27me3 accumulation on large chromosomal blocks, conferring a sequence-specific role to H1 in epigenome homeostasis.

Completing the TRB family: newly characterized members show ancient evolutionary origins and distinct localization, yet similar interactions

“…D) Telo -box motifs recruit Polycomb repressive complexes (PRC2) via interactions of PRC2 subunits with TRB (Zhou et al 2016; Zhou et al 2018, this study) CLF, CURLY LEAF; SWN, SWINGER; EMF2, EMBRYONIC FLOWER 2; VRN2, VERNALIZATION 2. E) Histone H1 prevents the invasion of H3K27me3 and TRB1 over telomeres and long interstitial telomeric regions (Teano et al 2020). F) TRB proteins, as subunits of the PEAT (PWO-EPCR-ARID-TRB) complex, are involved in heterochromatin formation and gene repression, but also have a locus-specific activating role, possibly through the promotion of histone acetylation (Tan et al 2018; Tsuzuki and Wierzbicki 2018; Mikulski et al 2019).…”

Polycomb Repressive Complex 2 in Eukaryotes—An Evolutionary Perspective

“…Several non-exclusive mechanisms can be envisaged, including changes in PRC2 catalytic activity or its genomic targeting. Dual H3K9me and H3K27me activities of E(z)-like proteins in ciliates [ 106 ], DNA methylation and/or H3K9me preventing H3K27me3 targeting to TEs in various eukaryotes [ 49 ] and recently reported prevention of H3K27me3 targeting to telomeric sequences by histone H1 in A. thaliana [ 307 ] may provide important hints.…”

Deposition and eviction of histone variants define functional chromatin states in plants

“…H1 is further involved in H3K27me3 homeostasis [46,47], as H1 favors H3K27me3 enrichment at Polycomb-regulated genes and prevents over-accumulation of H3K27me3 at interstitial telomeric repeats [47].…”

“…H3K27me3 plays a central role in gene expression control during development [48][49][50] and a common function of several histone variants seems to be the regulation of this repressive mark not only by ensuring maintenance at the replication fork [16,43] or preventing redistribution along the genome [46,47] but also by facilitating rapid H3K27me3 reprogramming [51,52]. An example for the latter is incorporation of the atypical histone variant H3.15 that lacks lysine 27 (Figure 1) and is induced upon wounding in roots.…”