Histone H1 protects telomeric repeats from H3K27me3 invasion in Arabidopsis

Abstract

AbstractLinker histones play a pivotal role in shaping chromatin architecture, notably through their globular H1 (GH1) domain that contacts the nucleosome and linker DNA. Yet, interplays of H1 with chromatin factors along the epigenome landscape are just starting to emerge. Here, we report that Arabidopsis H1 occupies and favors both chromatin compaction and H3K27me3 enrichment on a majority of Polycomb-target protein-coding genes. In contrast, H1 prevents H3K27me3 accumulation on telomeres and pericentromeric interstitial telomeric repeats (ITRs) while orchestrating long-distance interactions regulating the 3D organization of these chromosome regions. Mechanistically, H1 prevents ITRs from being invaded by Telomere Repeat Binding 1 (TRB1), a GH1-containing telomere component with extra-telomeric functions in Polycomb recruitment. Based on these findings, we propose that H1 represses H3K27me3 accumulation on large blocks of telomeric repeats by antagonizing TRB1 association to linker DNA, conferring to linker histones an additional and sequence-specific role in modulating H3K27me3 epigenome homeostasis.