GCN5-mediated histone H3 acetylation orchestrates gene expression and plant development via H2A.Z

H2A.Z is a conserved histone variant that plays essential roles in various DNA-templated processes. Although both histone H3 acetylation and H2A.Z enrichment levels are important epigenetic marks that regulate gene expression, their functional interplay remains incompletely understood. This study integrates genetic, molecular, and genomic approaches to investigate how GCN5 - a conserved histone acetyltransferase - couples H3 acetylation with H2A.Z dynamics in Arabidopsis, and how this interplay shapes gene expression and plant development. We found that the increase in H2A.Z levels observed in the nrp1-1 nrp2-2 double mutant (defective in NAP1-RELATED PROTEIN 1 and 2) suppresses the morphological and molecular phenotypes of gcn5-7. Conversely, H2A.Z-depleted mutants aggravate these phenotypes of gcn5-7/c1. Notably, the reduction in H3 acetylation caused by GCN5 loss promotes the decrease in H2A.Z level, and this requires the function of NRPs. The integrated analysis of ChIP-Seq and RNA-Seq data revealed that the differential gene expression in the GCN5 deletion mutant is correlated with H2A.Z distribution and enrichment levels. Moreover, H2A.Z overaccumulation at genes in the nrp1-1 nrp2-2 mutant promotes increased H3 acetylation in a GCN5-dependent manner. In conclusion, our findings support a model in which GCN5-mediated H3 acetylation shapes H2A.Z occupancy, linking chromatin dynamics to precise gene expression control and proper plant development.