A plant histone H3.3-specific amino acid safeguards the deposition of H3K36 methylation for proper development and stress responses

Abstract

Histone variants are key regulators of chromatin function. The H3 variants H3.1 and H3.3 evolved independently in animals and plants and differ at amino acid position 31, where H3.1 contains alanine (A), whereas H3.3 carries serine (S) in animals or threonine (T) in plants. Although S and T can both be phosphorylated, the biological significance of plants having selectively adopted T over S remains unclear. Here, we report that H3.3T31 plays a critical role in plant development and stress responses by promoting H3K36me3 on H3.3. T31 prevents plant-specific H3K27 methyltransferases ATXR5 and ATXR6 from depositing H3K27me1, which otherwise inhibits the H3K36 methyltransferase EFS. The substitution of H3.3T31 with S or A increases ATXR5/6 activity and elevates H3K27me1, leading to reduced H3K36me3. Together, these findings suggest co-selection of the plant-specific H3.3T31 residue and ATXR5/6 to ensure the preferential accumulation of H3K27me1 on H3.1 and H3K36me3 on H3.3, thereby supporting chromatin function in plants.

Keywords: H3.1; H3.3; H3.3 G34R; H3.3 G34W; H3K27me1; H3K36me3; histone variant; oncohistone; plant development; stress response.