HDA19-mediated deacetylation of histone H3.3 lysine 27 and 36 regulates plant sensitivity to salt stress

Plants survive extreme environments through rapid chromatin reprogramming, while the epigenetic marks that confer this type of stress resilience remain poorly understood. Histone deacetylase HDA19 is a key epigenetic regulator in Arabidopsis, and hda19 deficient mutants are tolerant to several abiotic stresses. Through acetylome profiling, we identified a non-canonical K27/K36 di-acetylation mark on histone H3.3 among nine H3 variants as a key substrate of HDA19. The epigenetic mark accumulation decreased and increased in wild-type plants and hda19 mutants, whereas other known H3 marks were equally affected in response to salinity stress in both genotypes. Mimicking constitutive diacetylation of this H3K27/K36 mark led to the accumulation of stress resistance-mediating late embryogenesis abundant (LEA) proteins and induced salinity tolerance, similar to that observed in hda19 mutants. The loss of function mutants of lea7-1/lea29-1/rab18-1 abolished the salinity tolerance of hda19 . Our findings show that histone H3.3 K27/K36 di-acetylation mediates LEA protein accumulation, enabling plants to withstand environmental stresses.