Nitric oxide coordinates growth, development, and stress response via histone modification and gene expression

Abstract

Nitric oxide (NO) is a signaling molecule with multiple regulatory functions in plant physiology and stress response. In addition to direct effects on transcriptional machinery, NO executes its signaling function via epigenetic mechanisms. We report that light intensity-dependent changes in NO correspond to changes in global histone acetylation (H3, H3K9 and H3K9/K14) in Arabidopsis (Arabidopsis thaliana) wild-type leaves, and that this relationship depends on S-nitrosoglutathione reductase (GSNOR) and histone deacetylase 6 (HDA6). The activity of HDA6 was sensitive to NO, demonstrating that NO participates in regulation of histone acetylation. ChIP-seq and RNA-seq analyses revealed that NO participates in the metabolic switch from growth and development to stress response. This coordinating function of NO might be particularly important in plant ability to adapt to a changing environment, and is therefore a promising foundation for mitigating the negative effects of climate change on plant productivity.

γ-Aminobutyrate (GABA) Regulated Plant Defense: Mechanisms and Opportunities

“…These result in lower levels of ROS, malondialdehyde (a product of ROS-mediated peroxidation of membrane polyunsaturated fatty acids and marker for the depletion of antioxidant systems), and protein carbonylation (product of protein peroxidation and a marker of oxidative damage), lower activities of NADPH oxidase, lipoxygenase and polyphenol oxidase, and restoration of ion homeostasis (electrolyte leakage), which is indicative of membrane stability. There is also evidence for the GABA-induced production of nitric oxide (NO) (Table 4), which could be associated with the enhancement of antioxidant defense, as well as regulation of epigenetic mechanisms and gene transcription [157,174,186]. The stress tolerance could also be related to GABA-induced changes in pathways associated with other phytohormones such as ABA (ABA receptors), ethylene (ACC oxidase, ACC synthase), PAs (arginine decarboxylase, free and conjugated forms, S-adenosylmethionine decarboxylase) and salicylate (Table 4) [60,156,172,175,187], which can regulate metabolic homeostasis and influence the expression of stress factors (miRNAs, transcription factors, heat shock proteins) with known and yet-to-be-determined functions [156,183,188].…”

Brassinosteroids Mitigate Cadmium Effects in Arabidopsis Root System without Any Cooperation with Nitric Oxide

“…Nitric oxide (NO) is a reactive nitrogen species which acts as signaling molecule coordinating development and stress response [ 32 ]. In rice ARs and LRs, Cd reduces NO levels, but the NO formed by sodium nitroprusside (SNP) decreases Cd uptake and enhances the NO-levels with this resulting into an alleviation of the morphological alterations induced by the heavy metal [ 33 ].…”

Histone Deacetylation Controls Xylem Vessel Cell Differentiation via Transcriptional Regulation of a Transcription Repressor Complex OFP1/4–MYB75–KNAT7–BLH6

“…Accordingly, we identified GSSG and GSH, important regulators of cellular thiol homeostasis, as inhibitors of VND7-based xylem vessel cell differentiation (Supplementary Figure 3). Recently, it has been reported that HDA6 is S-nitrosylated in response to NO via GSNO metabolism (Ageeva-Kieferle et al, 2021). This observation strongly suggests that HDAC, a crucial epigenomic regulator linking stress responses and gene expression (Mengel et al, 2017;Song et al, 2017;Ueda et al, 2017), is a key modulator of VND7-based transcriptional switching for xylem vessel cell differentiation (Supplementary Figure 11).…”

“…In addition, OFP1 and MYB75 expression has been reported to be increased in HDAC mutants; OFP1 and MYB75 are upregulated in srt1 srt2 and in hda19, respectively (Zhang et al, 2018;Ning et al, 2019). Moreover, the histone acetylation level was increased at the OFP1 gene locus in hda6 and in the MYB75 gene locus in hda19 (Ning et al, 2019;Ageeva-Kieferle et al, 2021), suggesting that OFP1 and MYB75 are targets of histone acetylation-based active regulation of gene expression. Further analysis of the contribution of HDA proteins to the regulation of OFP1 and MYB75 expression will provide insight into how the OFP1/4-MYB75-KNAT7-BLH6 transcriptional repression complex affects xylem vessel cell differentiation.…”

“…Therefore, we tested whether the negative effect of TSA and sirtinol on xylem vessel cell differentiation depends on protein S-nitrosylation or auxin response. For this, we co-treated VND7-VP16-GR seedlings with the nitric oxide scavenger 2-(4carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), which inhibits protein S-nitrosylation (Mengel et al, 2017;Ageeva-Kieferle et al, 2021), or with synthetic auxin 1-naphthaleneacetic acid (NAA). The inhibition of xylem vessel cell differentiation by TSA was not affected by the additional application of cPTIO (Supplementary Figure 4), and NAA did not inhibit the differentiation (Supplementary Figure 5), suggesting that the inhibitory effect on VND7-induced xylem vessel cell differentiation was not due to protein S-nitrosylation nor auxin response.…”