Histone H1 protects telomeric repeats from H3K27me3 invasion in Arabidopsis

• Published in: Cell reports (Cambridge) Vol. 42; no. 8; p. 112894
• Main Authors: Teano, Gianluca, Concia, Lorenzo, Wolff, Léa, Carron, Léopold, Biocanin, Ivona, Adamusová, Kateřina, Fojtová, Miloslava, Bourge, Michael, Kramdi, Amira, Colot, Vincent, Grossniklaus, Ueli, Bowler, Chris, Baroux, Célia, Carbone, Alessandra, Probst, Aline V., Schrumpfová, Petra Procházková, Fajkus, Jiří, Amiard, Simon, Grob, Stefan, Bourbousse, Clara, Barneche, Fredy
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 29-08-2023; Elsevier
• Subjects: 3D chromosome organization; Arabidopsis; Biochemistry, Molecular Biology; Botanics; chromatin accessibility; CP: Molecular biology; CP: Plants; Genomics; H3K27me3; Life Sciences; linker histone H1; Polycomb; telomere; Telomere Repeat Binding protein; TRB; Vegetal Biology; CP: Plants; Telomere Repeat Binding protein; Arabidopsis; TRB; 3D chromosome organization; chromatin accessibility; telomere; CP: Molecular biology; Polycomb; linker histone H1; H3K27me3
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2023.112894

While the pivotal role of linker histone H1 in shaping nucleosome organization is well established, its functional interplays with chromatin factors along the epigenome are just starting to emerge. Here we show that, in Arabidopsis, as in mammals, H1 occupies Polycomb Repressive Complex 2 (PRC2) target genes where it favors chromatin condensation and H3K27me3 deposition. We further show that, contrasting with its conserved function in PRC2 activation at genes, H1 selectively prevents H3K27me3 accumulation at telomeres and large pericentromeric interstitial telomeric repeat (ITR) domains by restricting DNA accessibility to Telomere Repeat Binding (TRB) proteins, a group of H1-related Myb factors mediating PRC2 cis recruitment. This study provides a mechanistic framework by which H1 avoids the formation of gigantic H3K27me3-rich domains at telomeric sequences and contributes to safeguard nucleus architecture.
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•H1 promotes PRC2 activity at a majority of genes•H1 limits PRC2 activity at telomeres and interstitial telomeric repeats (ITRs)•H1 orchestrates the spatial organization of telomeres and ITRs•PRC2 repression is achieved by restricting accessibility to TRB proteins
Teano et al. report that linker histone H1 and a group of H1-related telomeric proteins interplay to selectively influence the Polycomb repressive landscape at telomeric repeats in Arabidopsis. These findings provide a mechanistic framework by which H1 affects the epigenome and nuclear organization in a sequence-specific manner.