S-Nitrosoglutathione Reductase—The Master Regulator of Protein S-Nitrosation in Plant NO Signaling

Abstract

S-nitrosation has been recognized as an important mechanism of protein posttranslational regulations, based on the attachment of a nitroso group to cysteine thiols. Reversible S-nitrosation, similarly to other redox-base modifications of protein thiols, has a profound effect on protein structure and activity and is considered as a convergence of signaling pathways of reactive nitrogen and oxygen species. In plant, S-nitrosation is involved in a wide array of cellular processes during normal development and stress responses. This review summarizes current knowledge on S-nitrosoglutathione reductase (GSNOR), a key enzyme which regulates intracellular levels of S-nitrosoglutathione (GSNO) and indirectly also of protein S-nitrosothiols. GSNOR functions are mediated by its enzymatic activity, which catalyzes irreversible GSNO conversion to oxidized glutathione within the cellular catabolism of nitric oxide. GSNOR is involved in the maintenance of balanced levels of reactive nitrogen species and in the control of cellular redox state. Multiple functions of GSNOR in plant development via NO-dependent and -independent signaling mechanisms and in plant defense responses to abiotic and biotic stress conditions have been uncovered. Extensive studies of plants with down- and upregulated GSNOR, together with application of transcriptomics and proteomics approaches, seem promising for new insights into plant S-nitrosothiol metabolism and its regulation.

Thioredoxins: Emerging Players in the Regulation of Protein S-Nitrosation in Plants

“…S-nitrosoglutathione reductase (GSNOR) is an evolutionary conserved cytosolic enzyme that catalyzes an NADH-dependent reduction of GSNO, leading to the formation of glutathione disulfide (GSSG) and hydroxylamine ( Figure 1) [50]. By regulating GSNO levels through its irreversible degradation, GSNOR plays a critical role in the overall metabolism of RNS, in the homeostasis of intracellular levels of NO, and control of trans-nitrosation equilibrium between low-molecular weight and protein S-nitrosothiols [51,52]. According to the current enzyme classification, GSNOR belongs to class III of Zn-dependent medium-chain alcohol dehydrogenases (ADH3; EC 1.1.1.1); however, since GSNO has been uncovered as the most effective substrate of this enzyme both in vitro and in vivo, the enzyme designation as GSNOR has widely extended within the scientific literature.…”

“…GSNOR has been studied and characterized in multiple plant species, including important model plants and crops [52]. GSNOR is involved in numerous developmental processes and metabolic programs in plants via direct and indirect regulatory pathways of RNS homeostasis.…”

“…In addition to its direct role in GSNO catabolism, it may control the cellular redox state by affecting intracellular levels of NADH and GSH. Currently available experimental evidence delineates the importance of GSNOR in plant responses to diverse abiotic and biotic stress conditions [52,59,60]. Stress-induced modulations of GSNOR belong to important components of the ROS and RNS signaling cross-talk, mediated by nitrosative modifications of several key enzymes of their metabolism.…”

Regulation of physiological aspects in plants by hydrogen sulfide and nitric oxide under challenging environment

“…S ‐nitrosylation of proteins is involved in signaling responses to multiple abiotic stresses such as salinity, cold, drought, ozone and heavy metal toxicity, as it has been reported earlier (Camejo et al , Fancy et al ). Similarly, the attachment of the NO group to a tyrosine residue is called tyrosine nitration which is a ‘nitrosative stress marker’ in plants (Greenacre and Ischiropoulos , Corpas et al , b, Gong et al , Mata‐Pérez et al , Jahnová et al , Nabi et al ). NO also interacts with GSH to form S ‐nitrosoglutathione (GSNO), a non‐toxic and mobile form of NO that functions as key signaling molecule and regulates protein function and gene expression, contributing to fundamental processes in plants, such as development and the response to abiotic stresses (Begara‐Morales et al , Nabi et al ).…”

S-Nitrosothiol Signaling Is involved in Regulating Hydrogen Peroxide Metabolism of Zinc-Stressed Arabidopsis

“…The intracellular level of GSNO and, consequently, the intensity of SNO signalling are controlled by direct and selective processes like the NADPH-dependent thioredoxin reductase (NTR)-thioredoxin (TRX) system (Kneeshaw et al 2014, Umbreen et al 2018 and also by GSNO reductase activity (GSNOR, EC 1.2.1.1, Feechan et al 2005, Lee et al 2008, Chen et al 2009. The latter enzyme catalyses the NADH-dependent conversion of GSNO to GSSG and NH 3 (Jahnová et al 2019). GSNOR is encoded by a single gene (At5g43940), and the corresponding protein was detected in the cytosol, chloroplasts, mitochondria and peroxisomes of pea leaf cells using electron microscopy immunogold-labeling technique (Barroso et al 2013).…”