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The histone H3.1 variant regulates TONSOKU-mediated DNA repair during replication

Hossein Davarinejad, Yi-Chun Huang, Benoît Mermaz, Chantal LeBlanc, Axel Poulet, Geoffrey Thomson, Valentin Joly, Marcelo Muñoz, Alexis Arvanitis-Vigneault, Devisree Valsakumar, Gonzalo Villarino, Alex Ross, Benjamin H. Rotstein, Emilio I. Alarcón, J.S. Brunzelle, Philipp Voigt, Jie Dong, Jean‐François Couture, Yannick Jacob

2022Science67 citationsDOIOpen Access PDF

Abstract

The tail of replication-dependent histone H3.1 varies from that of replication-independent H3.3 at the amino acid located at position 31 in plants and animals, but no function has been assigned to this residue to demonstrate a unique and conserved role for H3.1 during replication. We found that TONSOKU (TSK/TONSL), which rescues broken replication forks, specifically interacts with H3.1 via recognition of alanine 31 by its tetratricopeptide repeat domain. Our results indicate that genomic instability in the absence of ATXR5/ATXR6-catalyzed histone H3 lysine 27 monomethylation in plants depends on H3.1, TSK, and DNA polymerase theta (Pol θ). This work reveals an H3.1-specific function during replication and a common strategy used in multicellular eukaryotes for regulating post-replicative chromatin maturation and TSK, which relies on histone monomethyltransferases and reading of the H3.1 variant.

Topics & Concepts

Histone H3BiologyDNA replicationOrigin recognition complexReplication factor CControl of chromosome duplicationGeneticsCell biologyHistoneGenome instabilityEukaryotic DNA replicationDNADNA damageGenomics and Chromatin DynamicsDNA Repair MechanismsEpigenetics and DNA Methylation