Oxidative post-translational modifications of plant antioxidant systems under environmental stress

Abstract

Plants are often subject to environmental challenges posed by abiotic and biotic stresses, which are increasing under the current climate change conditions, provoking a loss in crop yield worldwide. Plants must cope with adverse situations such as increasing temperatures, air pollution or loss of agricultural land due to salinity, drought, contamination, and pathogen attacks, among others. Plants under stress conditions increase the production of reactive oxygen-, nitrogen-, and sulphur species (ROS/RNS/RSS), whose concentrations must be tightly regulated. The enzymatic antioxidant system and metabolites are in charge of their control to avoid their deleterious effects on cellular components, allowing their participation in signalling events. As signalling molecules, reactive species are involved in plant responses to the environment through post-translational modifications (PTMs) of proteins, which, in turn, may regulate the structure, function, and location of the antioxidant proteins by oxidative/nitrosative/persulfure modifications of different amino acid residues. In this review, we examine the different effects of these post-translational modifications, which are emerging as a fine-tuned point of control of the antioxidant systems involved in plant responses to climate change, a growing threat to crop production.

FIGURE 1

Post‐translational cysteine modifications by reactive oxygen, nitrogen, and sulphur species (ROS, RNS, RSS) and glutathione (reduced GSH and oxidised GSSG). Cys oxidation of thiols (SH/S⁻) by ROS leads to the generation of highly reactive sulfenic acid (SOH), which can react with other thiols to generate disulfide bonds (S‐S), with GSH to glutathionylate (SSG) or with RSS to persulfidate (SSH), all of them reversible by thioredoxin (TRX) and/or glutaredoxin (GRX). Thiols also react with GSSG to glutathionylate, being reversed by GRX and possibly by TRX; with RNS to generate nitrosation (SNO), also reversible by TRX or peroxiredoxin (PRX); with fatty acids (FA) to acylate (SFA); or with HCN to cyanylate (SCN). Further oxidation of sulfenic acids to sulfinic (SO₂H) or sulfonic (SO₃H) are generally irreversible, with some exceptions, such as some PRXs reduced by sulfiredoxin (SRX) (see main text).

FIGURE 2

Main oxidative post‐translational modifications (oxiPTMs) in the plant antioxidant and redox system. The main oxiPTMs can affect cysteine/cysteine status of redox cysteine‐containing enzymes (in yellow) as thioredoxin (TRX), nucleoredoxin (NRX), glutaredoxin (GRX) and sulfiredoxin (SRX), as well as ROS scavenging enzymes (in blue) as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), monodehydro‐ and dehydro‐ascorbate reductases (MDHAR, DHAR), glutathione reductase (GR), peroxiredoxin (PRX), glutathione peroxidase (GPX). This Cys oxiPTMs include thiol oxidation to sulfenic, sulfinic, sulfonic or disulfide bonds (oxi), persulfidation (SSH), nitrosation (SNO), glutathionylation (SSG), cyanylation (SCN), and acylation by fatty acids (SFA and GlyFA). OxiPTMs also occur in methionine (MetO), tyrosine (TyrNO₂), lysine (acetylation: Acet or succinylation: Succ), or carbonyl groups of amino acids (C=O). Some of the oxiPTMs are reversible, regenerating the modified proteins to their reduced (red) states using reduced glutathione (GSH), SRX, NRX, TRX, or thioredoxin/ferredoxin‐ reductases (NTR, FTR) (see main text).