An Oryza-specific histone H4 variant predisposes H4 lysine 5 acetylation to modulate salt stress responses

Abstract

Paralogous variants of canonical histones guide accessibility to DNA and function as additional layers of genome regulation. Across eukaryotes, mechanism of action and functional significance of several variants of core histones are well-known except that of histone H4. Here we show that, a novel variant of H4 (H4.V) expressing tissue-specifically among Oryza members, mediated specific epigenetic changes contributing to salt tolerance. H4.V was incorporated to specific heterochromatic sites where it blocked deposition of active histone marks. Stress dependent re-distribution of H4.V enabled incorporation of active H4 Lysine5 Acetylation (H4K5Ac) marks. Mis-expression of H4.V led to defects in reproductive development and in mounting salt stress responses. H4.V formed homotypic nucleosomes and mediated these alterations by conferring distinct molecular properties to the nucleosomes, as seen with cryo-EM structures and biochemical assays. These results not only uncovered the presence of a H4 variant among plants, but also of a novel chromatin regulation that might have contributed to the adaptation of semi-aquatic Oryza members.