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

Kotnik, Florian; Ueda, Minoru; Ito, Akihiro; Ishida, Junko; Takahashi, Satoshi; Sakai, Katsuyuki; Takagi, Hiroshi; Seidel, Julian et al. · Proc Natl Acad Sci U S A · 2026

basic_science · Level V

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Abstract

Plants survive extreme environments through rapid chromatin reprogramming, yet the epigenetic marks that confer stress resilience remain poorly understood. Histone deacetylase HDA19 is a key epigenetic regulator in Arabidopsis, and <i>hda19</i>-deficient mutants display tolerance to multiple abiotic stresses, including drought, heat, and salinity. Using lysine acetylome profiling, we identified a noncanonical K27/K36 diacetylation mark on histone H3.3, among nine H3 variants, as a specific substrate of HDA19. Under salinity stress, this mark decreased in wild-type plants but increased in <i>hda19</i> mutants, while other known H3 modifications were similarly affected in both genotypes. Mimicking constitutive diacetylation of H3.3K27/K36 through lysine-to-glutamine substitutions promoted accumulation of stress-responsive late embryogenesis abundant (LEA) proteins and conferred salinity tolerance in seedlings, phenocopying <i>hda19</i> mutants. Furthermore, generating the <i>lea7-1/lea29-1/rab18-1</i> triple mutant abolished <i>hda19</i>-dependent salinity tolerance, confirming the LEA proteins' role downstream of HDA19. Our findings demonstrate that H3.3K27/K36 diacetylation, modulated by HDA19, drives LEA protein accumulation and enables plants to withstand environmental stress, revealing a core mechanism of plant stress resilience.