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

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 S-nitrosylation 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 S-nitrosylation regulates HDA19 activity and is a mechanism of redox-sensing for chromatin regulation of plant tolerance to stress.

Histone deacetylase 9 interacts with SiHAT3.1 and SiHDA19 to repress dehydration responses through H3K9 deacetylation in foxtail millet.

Climate change inflicts several stresses on plants, of which dehydration stress severely affects growth and productivity. C4 plants possess better adaptability to dehydration stress; however, the role of epigenetic modifications underlying this trait is unclear. In particular, the molecular links between histone modifiers and their regulation remain elusive. In this study, genome-wide H3K9 acetylation (H3K9ac) enrichment using ChIP-sequencing was performed in two foxtail millet cultivars with contrasting dehydration tolerances (IC403579, cv. IC4-tolerant, and IC480117, cv. IC41-sensitive). It revealed that a histone deacetylase, SiHDA9, was significantly up-regulated in the sensitive cultivar. Further characterization indicated that SiHDA9 interacts with SiHAT3.1 and SiHDA19 to form a repressor complex. SiHDA9 might be recruited through the SiHAT3.1 recognition sequence onto the upstream of dehydration-responsive genes to decrease H3K9 acetylation levels. The silencing of SiHDA9 resulted in the up-regulation of crucial genes, namely, SiRAB18, SiRAP2.4, SiP5CS2, SiRD22, SiPIP1;4, and SiLHCB2.3, which imparted dehydration tolerance in the sensitive cultivar (IC41). Overall, the study provides mechanistic insights into SiHDA9-mediated regulation of dehydration stress response in foxtail millet.

The PIF1/PIF3-MED25-HDA19 transcriptional repression complex regulates phytochrome signaling in Arabidopsis.

Light signals are perceived by photoreceptors, triggering the contrasting developmental transition in dark-germinated seedlings. Phytochrome-interacting factors (PIFs) are key regulators of this transition. Despite their prominent functions in transcriptional activation, little is known about PIFs' roles in transcriptional repression. Here, we provide evidence that histone acetylation is involved in regulating phytochrome-PIFs signaling in Arabidopsis. The histone deacetylase HDA19 interacts and forms a complex with PIF1 and PIF3 and the Mediator subunit MED25. The med25/hda19 double mutant mimics and enhances the phenotype of pif1/pif3 in both light and darkness. HDA19 and MED25 are recruited by PIF1/PIF3 to the target loci to reduce histone acetylation and chromatin accessibility, providing a mechanism for PIF1/PIF3-mediated transcriptional repression. Furthermore, MED25 forms liquid-like condensates, which can compartmentalize PIF1/PIF3 and HDA19 in vitro and in vivo, and the number of MED25 puncta increases in darkness. Collectively, our study establishes a mechanism wherein PIF1/PIF3 interact with HDA19 and MED25 to mediate transcriptional repression in the phytochrome signaling pathway and suggests that condensate formation with Mediator may explain the distinct and specific transcriptional activity of PIF proteins.

The SNL-HDA19 histone deacetylase complex antagonizes HY5 activity to repress photomorphogenesis in Arabidopsis.

Reprogramming of the transcriptome during photomorphogenesis requires dynamic changes in chromatin and distribution of histone modifications. However, the chromatin-based regulation of this process remains to be elucidated. Here, we identify the conserved SWI-INDEPENDENT3 LIKE (SNL)-HISTONE DEACETYLASE19 (HDA19) deacetylase complex, including HDA19 and SNL1-SNL6, as a negative regulator of the light signaling pathway. Light-repression of HDA19 and SNLs expression is mediated by photoreceptors. HDA19 and SNLs are required for histone deacetylation and chromatin inactivation of PHYA gene. We further examined the interaction between SNL-HDA19 complex and ELONGATED HYPOCOTYL5 (HY5), and their antagonistic regulation on the expressions of target genes. The HDA19 deacetylase complex is recruited by HY5 to the chromatin regions of two positive light signaling genes, HY5 and B-BOX CONTAINING PROTEIN 22 (BBX22), thereby reduces the accessibility and histone acetylation and represses their expression. HDA19, SNL1, and HY5 associate with the same regulatory regions of HY5 and BBX22, and HY5 binding to these loci is enhanced upon SNL-HDA19 dysfunction. Our study reveals a crucial role for the HDA19 deacetylase complex in light signaling and demonstrates that the functional interplay between chromatin regulators and transcription factors regulates photomorphogenetic responses to the changing light environments.

The HDA19 histone deacetylase complex is involved in the regulation of flowering time in a photoperiod-dependent manner.

Chromatin modifications are known to affect flowering time in plants, but little is known about how these modifications regulate flowering time in response to environmental signals like photoperiod. In Arabidopsis thaliana, HDC1, a conserved subunit of the RPD3-like histone deacetylase (HDAC) complex, was previously reported to regulate flowering time via the same mechanism as does the HDAC HDA6. Here, we demonstrate that HDC1, SNLs and MSI1 are shared subunits of the HDA6 and HDA19 HDAC complexes. While the late-flowering phenotype of the hda6 mutant is independent of photoperiod, the hda19, hdc1 and snl2/3/4 mutants flower later than or at a similar time to the wild-type in long-day conditions but flower earlier than the wild-type in short-day conditions. Our genome-wide analyses indicate that the effect of hdc1 on histone acetylation and transcription is comparable with that of hda19 but is different from that of hda6. Especially, we demonstrate that the HDA19 complex directly regulates the expression of two flowering repressor genes related to the gibberellin signaling pathway. Thus, the study reveals a photoperiod-dependent role of the HDA19 HDAC complex in the regulation of flowering time.

Arabidopsis RPD3-like histone deacetylases form multiple complexes involved in stress response.

The Arabidopsis thaliana RPD3-type histone deacetylases have been known to form conserved SIN3-type histone deacetylase complexes, but whether they form other types of complexes is unknown. Here, we perform affinity purification followed by mass spectrometry and demonstrate that the Arabidopsis RPD3-type histone deacetylases HDA6 and HDA19 interact with several previously uncharacterized proteins, thereby forming three types of plant-specific histone deacetylase complexes, which we named SANT, ESANT, and ARID. RNA-seq indicates that the newly identified components function together with HDA6 and HDA19 and coregulate the expression of a number of genes. HDA6 and HDA19 were previously thought to repress gene transcription by histone deacetylation. We find that the histone deacetylase complexes can repress gene expression via both histone deacetylation-dependent and -independent mechanisms. In the mutants of histone deacetylase complexes, the expression of a number of stress-induced genes is up-regulated, and several mutants of the histone deacetylase complexes show severe retardation in growth. Considering that growth retardation is thought to be a trade-off for an increase in stress tolerance, we infer that the histone deacetylase complexes identified in this study prevent overexpression of stress-induced genes and thereby ensure normal growth of plants under nonstress conditions.

Histone deacetylase HDA19 interacts with histone methyltransferase SUVH5 to regulate seed dormancy in Arabidopsis.

Seed dormancy controls the timing of germination and plays a significant role in adaptation and evolution of seed plants. In this study, a yeast two-hybrid, pull-down assay and co-immunoprecipitation assay were used to ascertain the protein relationship of SUVH5 and HDA19. Both qRT-PCR and ChIP-qPCR were used to examine the molecular mechanism of how HDA19 and SUVH5 regulate seed dormancy. The results demonstrated that histone methyltransferase SUVH5 interacted with histone deacetylase HDA19 in vivo and in vitro. In addition, they showed that mutants of HDA19 could deepen seed dormancy, and that SUVH5 had the same effect. The hda19 suvh5 double mutant displayed a higher level of seed dormancy than the single mutants hda19 or suvh5. Moreover, the expression of seed dormancy-related genes increased in hda19, suvh5 and in hda19 suvh5 double mutant plants, which was associated with increased histone H3 acetylation (H3ac), but decreased histone H3 Lys 9 dimethylation (H3K9me2). ChIP assays proved that HDA19 could directly integrate into the chromatin of genes regulating seed dormancy. Taken together, our results show that HDA19 and SUVH5 work together and have a negative role in seed dormancy.