Chromatin crosstalk between HDA19 and NuA4 sets thresholds for stress gene activation in Arabidopsis

Histone acetylation by the plant NuA4 complex promotes high expression of growth-related genes while preventing gene body H2A.Z depletion and spurious activation of stress-responsive loci. How this NuA4-dependent chromatin state is modulated by histone deacetylases (HDACs) in plants remains unclear. Here, we investigate the interplay between NuA4 and HDACs in Arabidopsis by generating a collection of HDAC loss-of-function mutants in NuA4-proficient and NuA4-deficient backgrounds. Loss of individual HDACs did not rescue the severe growth defects of the NuA4(−) mutant; instead, most combinations further aggravated the phenotype, indicating that HDACs predominantly support rather than counteract NuA4 function. Focusing on the hda19-5 Atepl1b allele, we show that loss of HDA19 causes strong developmental defects and constitutive activation of biotic stress–responsive genes, but not canonical heat-response genes. 3′ RNA-seq and ChIP-seq reveal that upregulated genes in hda19-5 Atepl1b display increased H3K9ac and H2A.Zac with largely unchanged gene-body H2A.Z, and substantially overlap with genes induced in the NuA4-null Atepl1-2 mutant and in wild-type plants exposed to elevated temperature. Integration of our datasets with published HDA19 ChIP-seq maps shows that H2A.Zac is selectively increased at HDA19-bound H2A.Z peaks in hda19-5 Atepl1b , consistent with a direct role for HDA19 in H2A.Z deacetylation. However, elevated H2A.Zac is neither necessary nor sufficient for transcriptional activation, whereas changes in H3K9ac correlate strongly with gene induction. We propose that NuA4 and HDA19 cooperate to tune chromatin at stress-related loci, with H3K9 acetylation as the primary driver of transcription and H2A.Z acetylation acting as a modulatory mark that shapes stress gene responsiveness.