H3.1K27me1 maintains transcriptional silencing and genome stability by preventing GCN5-mediated histone acetylation

In plants, genome stability is maintained during DNA replication by the H3K27 methyltransferases ATXR5 and ATXR6, which catalyze the deposition of H3K27me1 on the replication-dependent H3.1 variant. Loss of H3.1K27me1 in atxr5 atxr6 mutants leads to heterochromatin defects, including transcriptional de-repression and genomic instability, but the molecular mechanisms involved remain largely unknown. In this study, we identified the conserved histone acetyltransferase GCN5 as a mediator of transcriptional de-repression and genomic instability in the absence of H3.1K27me1. GCN5 is part of a SAGA-like complex in plants and requires ADA2b and CHR6 to mediate the heterochromatic defects of atxr5 atxr6 mutants. Our results show that GCN5 acetylates multiple lysine residues on H3.1 variants, but that H3.1K27 and H3.1K36 play key roles in inducing genomic instability in the absence of H3.1K27me1. Overall, this work reveals a key molecular role for H3.1K27me1 in maintaining genome stability by preventing GCN5-dependent histone acetylation in plants. Examination of RNA seq and Rx ChiP seq of H3K27ac and H3K36ac in 4 different backgrounds col0, atxr5/6, gcn5. atxr5/6 gcn5