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.
Telomeres, nucleoprotein structures at the ends of linear eukaryotic chromosomes, are crucial for the maintenance of genome integrity. In most plants, telomeres consist of conserved tandem repeat units comprising the TTTAGGG motif. Recently, non-canonical telomeres were described in several plants and plant taxons, including the carnivorous plant Genlisea hispidula (TTCAGG/TTTCAGG), the genus Cestrum (Solanaceae; TTTTTTAGGG), and plants from the Asparagales order with either a vertebrate-type telomere repeat TTAGGG or Allium genus-specific CTCGGTTATGGG repeat. We analyzed epigenetic modifications of telomeric histones in plants with canonical and non-canonical telomeres, and further in telomeric chromatin captured from leaves of Nicotiana benthamiana transiently transformed by telomere CRISPR-dCas9-eGFP, and of Arabidopsis thaliana stably transformed with TALE_telo C-33GFP. Two combinatorial patterns of telomeric histone modifications were identified: (i) an Arabidopsis-like pattern (A. thaliana, G. hispidula, Genlisea nigrocaulis, Allium cepa, Narcissus pseudonarcissus, Petunia hybrida, Solanum tuberosum, Solanum lycopersicum) with telomeric histones decorated predominantly by H3K9me2; (ii) a tobacco-like pattern (Nicotiana tabacum, N. benthamiana, C. elegans) with a strong H3K27me3 signal. Our data suggest that epigenetic modifications of plant telomere-associated histones are related neither to the sequence of the telomere motif nor to the lengths of the telomeres. Nor the phylogenetic position of the species plays the role; representatives of the Solanaceae family are included in both groups. As both patterns of histone marks are compatible with fully functional telomeres in respective plants, we conclude that the described specific differences in histone marks are not critical for telomere functions.
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