S‐Nitrosylation of the histone deacetylase HDA19 stimulates its activity to enhance plant stress tolerance in Arabidopsis

Abstract

Arabidopsis histone deacetylase HDA19 is required for gene expression programs of a large spectrum of plant developmental and stress-responsive pathways. How this enzyme senses cellular environment to control its activity remains unclear. In this work, we show that HDA19 is post-translationally modified by Snitrosylation at 4 Cysteine (Cys) residues. HDA19 S-nitrosylation depends on the cellular nitric oxide level, which is enhanced under oxidative stress. We find that HDA19 is required for cellular redox homeostasis and plant tolerance to oxidative stress, which in turn stimulates its nuclear enrichment, S-nitrosylation and epigenetic functions including binding to genomic targets, histone deacetylation and gene repression. The Cys137 of the protein is involved in basal and stress-induced S-nitrosylation, and is required for HDA19 functions in developmental, stress-responsive and epigenetic controls. Together, these results indicate that Snitrosylation regulates HDA19 activity and is a mechanism of redox-sensing for chromatin regulation of plant tolerance to stress.

DELLA‐mediated gene repression is maintained by chromatin modification in rice

“…The IBM2 is a BAH domain‐containing protein, which was recently shown to recognize H3K27me3 (Zhang et al , 2023 ). HDA702 is orthologous to the Arabidopsis HDA19 (Hu et al , 2009 ), a primary plant HDAC with pleiotropic functions (Zheng et al , 2023 ). Their interaction with SLR1 was confirmed by Co‐immunoprecipitation (Co‐IP) of transiently transfected protoplasts and/or luciferase complementation assays in tobacco leaves (Appendix Fig S5 A and B).…”

Phytomelatonin: A key regulator of redox and phytohormones signaling against biotic/abiotic stresses

“…The stress-induced NO triggers the S-nitrosylation of histone deacetylase (HDA19) protein ( Fig. 4 ), which may repress the transcriptional level of genes responsible for plant tolerance or susceptibility [ 54 , 55 ]. Although NO and melatonin exhibit independent interaction through multiple signaling pathways, there is a certain degree of companionship [ 56 ].…”

Multifaceted functions of histone deacetylases in stress response

“…Proteomic data have identified arabidopsis HD2B and HD2C as targets of S-nitrosylation, which might affect their activity [55]. Recently, HDA19 was shown to be modified by S-nitrosylation which is enhanced under stress and promotes its deacetylase activity [56]. However, nitric oxide (NO) treatment increases histone acetylation in the plant [57,58], suggesting that S-nitrosylation is inhibitory for most HDACs catalytic activity.…”