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Review

Cysteine Thiol-Based Oxidative Post-Translational Modifications Fine-Tune Protein Functions in Plants

by
Hongxin Li
1,
Xiaoyun Wang
2,
Ying Liu
1,
Peiyang Zhang
1,
Fuyuan Chen
1,
Na Zhang
1,
Bing Zhao
1,* and
Yang-Dong Guo
1,*
1
College of Horticulture, China Agricultural University, Beijing 100193, China
2
College of Plant Science and Technology, Beijing University of Agriculture, Beijing 102206, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(12), 2757; https://doi.org/10.3390/agronomy14122757
Submission received: 16 October 2024 / Revised: 12 November 2024 / Accepted: 19 November 2024 / Published: 21 November 2024
(This article belongs to the Special Issue Effects of Plant Hormones on Vegetable Adaptation and Mitigation of Abiotic Stress)
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Abstract

:
Post-translational modification is a prerequisite for the functions of intracellular proteins. Thiol-based oxidative post-translational modifications (OxiPTMs) mainly include S-sulfenylation, S-nitrosation, persulfidation, and S-glutathionylation. Reactive electrophilic species can reversibly or irreversibly oxidize redox-sensitive proteins, thereby exerting dual effects on plant growth, development, and environmental stress. Recent studies have shown that transcription factors (TFs) are main targets of OxiPTMs. The majority of TFs transmit redox signals by altering their transcriptional activity, while some non-transcription factors can also accept post-translational redox modifications. Here, we provide an overview of the known types of OxiPTMs, the reactive electrophilic species that induce OxiPTMs, and the significance of OxiPTMs in fine-tuning TF and non-TF proteins. This review will provide a more comprehensive understanding of the dynamic regulation of protein functions in response to stress.

1. Introduction

As the executors of biological functions, proteins undergo various forms of post-translational modifications (PTMs) that induce structural changes to enable specific functions to be carried out. PTMs modify the translated proteins, thus affecting their chemical properties to change the folding properties, spatial conformation, stability, subcellular localization, and protein–protein interactions. The highly diverse range of PTMs includes phosphorylation, ubiquitination, redox modification, SUMOylation, γ-carboxylation, methylation, glycosylation, acetylation, alkylation, hydroxylation, nitration, and nucleotide addition [1,2,3,4,5]. There is ample evidence for the significance of PTMs in plant growth and development as well as in the process of stress tolerance. Here, we focus on oxidative post-translational modifications (OxiPTMs), which can offer particular insight into the response of plants to stress, given that all forms of stress faced by plants cause secondary oxidative stress.
The active center and folding of a protein are crucial to its function, and involve the thiol (-SH) group of the cysteine (Cys) residue that plays a role in redox modification [6,7]. These thiol groups can be deprotonated to negatively charged thiolate (Cys-S−) to increase reactivity. The major redox modifications include S-sulfenylation, S-nitrosation, persulfidation, S-cyanylation, and S-glutathionylation. Reactive oxygen species (ROS), reactive nitrogen species (RNS), and reactive sulfur species (RSS) are chemically active and highly oxidative metabolites that mediate OxiPTMs (Figure 1). Reactive species have dual functions in plants, which can cause damage to biochemical processes by oxidizing biological macromolecules but also have critical physiological functions such as in signal transduction [8]. As secondary messengers, reactive species mediate multiple signaling pathways; regulate the protein sulfhydryl status, multiple antioxidant enzymes, hormones, and transcription factors (TFs); and can respond to environmental stress [8]. Redox regulation affects the redox state of many functional proteins to, in turn, regulate plant development and stress responses. TFs are a main target of OxiPTMs, which can change the transcriptional activity of target genes, thus transferring redox information to the nucleus to promote growth and development, resistance to stress, and the expression of other related genes. OxiPTMs also occur in proteins other than TFs, which mainly include kinases such as the serine/threonine protein kinase STN7 related to photosynthesis or plant protein tyrosine phosphatase 1 (PTP1) affecting plant growth and development [9,10]. These kinases are typically modified by OxiPTMs to enhance or decrease the activity of other related kinases, and to ensure that plants are not damaged by the external environment and can grow normally under fluctuating environments.
We here review the research advances on OxiPTMs in response to the accumulation of ROS, RNS, and RSS, demonstrating the significance of these modifications in fine-tuning the activities and functions of both TF and non-TF targets.

2. Major OxiPTMs in Plants

Reactive electrophilic species regulate plant life processes by the oxidative modification of redox-sensitive proteins. The major types of OxiPTMs that occur in plants are classified according to the involvement of ROS (S-sulfenylation and S-glutathionylation), RNS (S-nitrosation), and RSS (persulfidation) in Table 1.

2.1. ROS-Induced OxiPTMs

ROS represent reactive forms of oxygen that are only partially activated or reduced. ROS is therefore a general term used to describe oxygen-containing substances with very active and highly oxidative properties, including hydrogen peroxide (H2O2), superoxide anions (O2−), hydroxy radicals (·OH), and singlet oxygen (1O2), which are unavoidable products of plant growth, development, and metabolism [19,20,21,22,23,24]. ROS can be synthesized in different organelles through different pathways such as photosynthesis in chloroplasts [25,26], the last stage of the aerobic respiration pathway in mitochondria (oxidative phosphorylation) [27,28], and photorespiration in the peroxisome [27,29] and the plasma membrane oxidoreductase system [30,31]. During long-term evolution, plants not only acquired mechanisms to eliminate the toxic effects of ROS but also to exploit ROS by having them play an active role as signaling molecules. The main types of OxiPTMs that can be induced by ROS are S-sulfenylation and S-glutathionylation.

2.1.1. S-Sulfenylation

S-sulfenylation is a reversible modification process in which hydroxide reacts with the thiol group of specific Cys residues in a substrate protein to produce sulfenic acids. The chemical equation for S-sulfenylation can be expressed as follows: Cys-SH + H2O2 → Cys-SOH + H2O. S-sulfenylation plays an intermediate role in other redox modification pathways such as the formation of disulfide ethers (-SSR), disulfide bonds, S-glutathionylation, and peroxidation to sulfinic acid (SO2H) and sulfonic acid (SO3H) [32,33]. The formation of sulfonic acid can cause protein degradation or inactivation [34]. This reversible oxidation process controls the molecular thiol switch, which regulates protein activity, stability, conformational changes, interaction, and cell localization.
With the increasing study of H2O2 signal transduction, proteomics tools for identifying S-sulfenylation have been implemented and optimized in plants [11,35]. The initial workflow is to block free thiols in the extracted proteome, reduce oxidized Cys, and finally label the newly formed thiols [36,37,38]. However, these indirect proteomic methods can only be used to identify cysteine sulfenic acid (Cys-SOH) in vitro, albeit with some limitations. Cys-SOH detection technology is progressing rapidly. There are two main methods for identifying S-sulfenylated proteins selectively captured in Arabidopsis thaliana [11,12,39]. The first method involves the use of YAP1-based probes that were developed to capture S-sulfenylated proteins in plants [40] and a YAP1-based hyposulfenylated capture method coupled with a tandem affinity purification tag has been implemented [12,41]. Approximately 100 S-sulfenylated proteins were identified in early and late oxidative stress reactions, including 67 that had not been previously identified as being involved in OxiPTMs.
The other method involves a chemoselective DYn-2 probe based on alkynyl functionalization, which was developed to enable capturing information on the multiple redox changes of proteins that could not be obtained using previous analysis methods of protein-level capture. DYn-2 marks S-sulfenylated proteins in complete cells. Cell proteins are digested with trypsin, the labeled peptide is combined with azide biotin by a CuAAC reaction, and the peptide is affinity-purified on streptavidin resin, and is ultimately released through the light-splitting action of a biotin linker. The released DYn-2-modified peptide is then analyzed by mass spectrometry-based proteomics [11]. Subsequently, utilizing an enhanced 1-(pent-4-yn-1-yl)-1H-benzo[c][1,2] thiazin-4(3H)-one 2,2-dioxide (BTD)-derived probe, which exhibited superior reactivity compared to the DYn-2 probe, facilitated the comprehensive identification of 1394 proteins susceptible to S-sulfenylation. This achievement represented a substantial enlargement of the known S-sulfenylated proteome, surpassing the previous tally of 200 proteins [11,12,35].

2.1.2. S-Glutathionylation

S-glutathionylation is the process of forming mixed disulfides between glutathione and target protein Cys residues. The chemical equation for S-glutathionylation can be expressed as follows: Cys-SH + GSH→Cys-SSG. Owing to its regulatory effect on target protein function, S-glutathionylation is considered to be a form of OxiPTM. Glutathione is composed of three amino acids (γ-Glu-Cys-Gly) and acts as a rich soluble antioxidant in plant cells [42]. At physiological pH range, glutathione mainly exists in the reduced form (GSH); however, when stimulated by oxidation, it can be converted into the oxidized form glutathione disulfide (GSSG) [43,44]. The transition between the oxidized and reduced states of glutathione is crucial for normal cell metabolism and survival. Glutathione redox homeostasis is also a key factor in cell physiological metabolism, signal transduction, and transcriptional regulation [43,45,46]. GSH plays an essential role in various detoxification pathways, including the H2O2-regulated ascorbic acid glutathione cycle and the methylglyoxal-detoxified glyoxalase pathway [47,48]. The currently proposed mechanism of S-glutathionylation is based on redox reactions of thiol-containing proteins or GSH, which are usually induced by ROS [47,49].
There are six main reaction mechanisms for S-glutathionylation. The first is based on the thiol disulfide exchange between proteins containing thiol groups and GSSG. The second type involves intracellular ROS inducing the production of the intermediate protein-SOH or glutathione disulfonic acid, thereby resulting in modification. Other types include S-glutathionylation mediated by sulfonamide intermediates and the ROS-induced generation of sulfur free radicals, in which modification results from the recombination of free radicals or their reaction with thiol salts. The fifth type is the reaction of thiosulfinates with thiols to generate disulfide bonds and water, resulting in modification. The final type is S-glutathionylation catalyzed by glutathione [33,49,50,51,52].
The detection methods for S-glutathionylation are also constantly being explored and matured. From the initial 35S-Cys radiolabeling method [53] and biotin labeling method [54], proteomics methods have been continuously advanced and applied to the detection of S-glutathionylated proteins. Moreover, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF-MS) has recently been used to detect S-glutathionylated-modified proteins [55,56,57]. Protein S-glutathionylation modification can also be detected through the fluorescence of eosin-GSSG and sodium dodecyl sulfate-polyacrylamide gel electrophoresis (PAGE) [58]. With recent technological developments, anti-glutathione antibodies have also emerged. With a key advantage of the lack of requirement of pretreatment during the detection process, anti-glutathione antibodies can detect S-glutathionylated proteins under various physiological conditions. However, the sensitivity of anti-glutathione antibody is low and the accuracy of S-glutathionylation detection cannot be ensured [59]. S-glutathione can also be detected using a click reaction and proteomics. For the identification of S-glutathionylated proteins, the proteins extracted from cells are first enriched, followed by a series of click reactions with “clickable” probes [60]. The product is ultimately injected into a liquid chromatography (LC)-tandem mass spectrometry (MS/MS) detection system for proteomics analysis to identify the original S-glutathionylated protein.
Approximately 79 S-glutathionylated proteins were identified in Arabidopsis thaliana using the combination of GSH biotin labeling, two-dimensional PAGE, and MALDI-MS [13]. Another study identified 20 S-glutathionylated proteins in Arabidopsis, including triose phosphate isomerase and aldolase [54]. In addition, previous studies identified proteins with disulfide bonds by separating the total proteins of Arabidopsis and employing proteomics technology; however, the number of S-glutathionylated proteins identified was quite low [61]. Therefore, approximately 70 types of S-glutathionylated proteins are known in Arabidopsis, but their modified functions and modified sites remain unclear [13]. In addition, 25 S-glutathionylated proteins were identified in wheat seedlings using two-dimensional electrophoresis, immunoblotting, anti-GSH antibodies, and MALDI-TOF LC-MS/MS [14].

2.1.3. Disulfide Bonds

In plants, disulfide bonds are synthesized through the covalent crosslinking of sulfhydryl groups resident on the side chains of cysteine residues. This crosslinking mechanism stabilizes the folded conformation of proteins, thereby playing an indispensable role in the oxidative folding process of proteins. As a highly significant class of post-translational redox modifications, disulfide bonds hold immense importance for the functional modulation of proteins and the transmission of redox signals.
The formation of disulfide bonds in plants entails the participation of a diverse range of enzymes and proteins. Protein disulfide isomerase (PDI) and its protein homologues serve as pivotal catalysts, catalyzing the oxidation, reduction, and isomerization of protein disulfide bonds. PDI catalyzes the formation of disulfide bonds by harnessing the oxidative potential furnished by endoplasmic reticulum oxidoreductase (ERO1) [62]. The regulation of disulfide bonds is primarily governed by thioredoxin peroxidase (TPX), glutathione peroxidase (GPX), thioredoxin (TRX), and glutaredoxin (GRX) [63,64,65]. Upon exposure to hydrogen peroxide, TPX and GPX undergo an oxidation of their Cys residues, enabling them to relay cellular redox signals to downstream target proteins through disulfide bond exchange and protein–protein interactions [66]. Both the oxidized and reduced forms of TRX/GRX proteins can function as redox sensors, capable of responding to various environmental conditions [67,68]. Notably, TRXs possess the dual capability of reducing not only the disulfide bonds of target proteins but also their S-nitrosyl groups [67]. These oxidoreductases modify the oxidation or reduction state of disulfide bonds through their interactions with transcription factors. The transmission of redox signals is of paramount significant for the growth, development, and stress resistance of plants.

2.2. RNS-Induced OxiPTMs

RNS are derivatives centered on nitric oxide (NO) which play similar roles to NO in plants [69]. NO is a key signal component in various stress tolerance pathways and participates in the nitrogen cycle [70]. The major RNS in plants include free radicals such as ·NO and nitrogen dioxide (·NO2) radicals, along with the non-radical species S-nitrosothiols, peroxynitrite (ONOO−), nitroxyl anion (NO−), nitrate (NO3−), nitrosonium cation (NO+), dinitrogen trioxide (N2O3), dinitrogen tetroxide (N2O4), nitryl chloride (NO2Cl), and nitrous acid (HNO2) [71]. We here focus on ·NO as the most extensively studied signal molecule among RNS.
NO is a reactive free radical gas molecule. In plants, biological NO is chemically synthesized as a by-product of the arginine-dependent and nitrate-dependent pathways [72,73]. l-Arginine-dependent NO production involves nitric oxide synthase, which uses O2 and NADPH as substrates. The nitrate pathway (enzymatic pathway) utilizes different nitrate reductase (NR) enzymes, including cytoplasmic NR, mitochondrial NR, and plasma membrane-bound NR, as well as some specific classes of xanthine dehydrogenases/oxidases, to produce NO in various plant systems [72,74]. Initially, this free radical molecule was considered an air pollutant, but has since been shown to have important regulatory functions in the biochemical processes of plants and to play an important role in the response to abiotic and biotic stresses [75,76,77].
RNS accumulation can induce S-nitrosation (previously referred to as S-nitrosylation), which refers to the addition of an NO fraction to a rare, highly reactive Cys thiol to form S-nitrosothiol (SNO) in a manner similar to the more well-established PTMs [78,79,80]. The chemical equation for S-nitrosylation can be expressed as follows: Cys-SH + NO → Cys-SNO. S-nitrosation regulates protein function, localization, interactions, and degradation, resulting in a different structure after a conformational change [81,82]. Recent proteomics studied identified more than 2200 S-nitrosated proteins, with the majority identified from mammals [83]. S-nitrosated proteins in plants have been increasingly identified, mainly in Arabidopsis. Approximately 46 S-nitrosated proteins were identified from cultured Arabidopsis cell suspensions [15]. In specificity analysis, 11 mitochondrial proteins were identified as S-nitrosated and S-glutathionylated proteins [84]. Another study identified 62 endogenous S-nitrosated proteins from Arabidopsis seedlings [85]. The response of the S-nitrosated proteome to bacterial peptide flagellin was investigated using iodine-MS/MS labeling, leading to the identification of 35 S-nitrosated proteins [16]. A study in poplar leaves identified 172 S-nitrosated proteins and the S-nitrosation status of leaf proteins could be significantly altered after 1 h of ozone treatment, inducing rapid de-nitrosation and S-nitrosation in 32 proteins [82]. The S-nitrosated proteome of peanut plant root tips was analyzed under conditions of aluminum stress, and 402 S-nitrosated proteins were identified to cause programmed cell death, with a total of 551 S-nitrosation sites, including proteins involved in the regulation of various biological processes such as energy metabolism and the maintenance of cell wall function [86].

2.3. RSS-Induced OxiPTMs

RSS are redox-active sulfur compounds formed under oxidative stress conditions that may be able to initiate oxidation reactions [87]. RSS include thiyl radical (HS•), hydrogen persulfide (H2S2), persulfide radical (HS2•−), sulfite (SO32−), or sulfate (SO42−), among others [88,89,90,91]. Sulfur radicals accumulate in cells under oxidative stress formed by the reaction of sulfhydryl radicals with ROS [88]. We here focus on H2S, as the most extensively studied signaling molecule among RSS.
In plant cells, the main pathway for H2S production is through sulfite reductase in chloroplasts, through l-desulfurylase and d-desulfurylase in the cytosol, and through β-cyanoalanine synthase in the mitochondria [92]. Recent studies have shown that H2S is of great importance for plant growth and development, hormone signaling, and resistance to abiotic stresses [93]. H2S mainly exerts these functions by inducing the persulfidation of plant proteins as a specific form of OxiPTM.
Persulfidation involves the modification of cysteine residues (RSH) to persulfides (RSSH). The chemical equation for persulfidation can be expressed as follows: Cys-SH + H2S → Cys-SSH. Persulfides have higher nucleophilic activity compared to sulfhydryl groups, which consequently alters the reactivity of modified proteins [94]. This may explain the high prevalence of persulfidation, which affects a greater proportion of proteins than ROS- and RNS-induced PTMs [95,96]. With continuous advances in biological techniques, persulfides have been found to be widespread in plant cells [96]. A total of 106 putative persulfidated proteins were identified in Arabidopsis leaves, accounting for more than half of the 57 glycolytic proteins, half of the 84 tRNA amylated proteins, and one-seventh of 1471 abiotic stress-related proteins based on Gene Ontology enrichment results [97]. The analysis of S-sulfenylation in plants has also revealed a large number of persulfidated proteins, which exhibit functional changes in enzymatic activity, structure, and subcellular localization, and are reflected in various aspects of plant growth, development, and responses to abiotic stress [17,18,97]. Quantitative proteomic analyses identified 887 persulfidated proteins that were significantly induced by drought stress. The drought-induced persulfidated proteins were mainly involved in biological processes such as the stress response under oxidative stress and hydrogen peroxide catabolism, followed by protein degradation, the abiotic stress response, and the phenylpropanoid pathway. This suggests that persulfidation plays a highly essential role in plants coping with drought stress [98].

3. OxiPTM Fine-Tunes TF Function in Plants

TFs regulate the transcription process by assembling a DNA motif preceding the downstream target gene sequence. TFs are therefore essential for the basal transcription of genes regulating plant life activities and for inducing transcriptional changes required in the response to various environmental stimuli. ROS/RNS/RSS directly affect the activity of TFs in plants through S-sulfenylation, S-glutathionylation, S-nitrosation, and persulfidation [99,100]. These OxiPTMs can reprogram gene expression through the following main aspects: protein nuclear translocation, DNA binding capacity, protein–protein interactions, and protein hydrolysis.

3.1. OxiPTM Mediates Protein Nuclear Translocation

Salicylic acid (SA) is a phenolic phytohormone that plays a central role in defense signaling pathways by regulating antioxidant enzymes under various processes [101,102]. Recent studies have shown that NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1), as a defensive hormone receptor, has a primary function of balancing ROS production and clearance. NPR1 is the main regulatory factor for SA-dependent plant immune responses regulated by intracellular redox states [103]. Under normal conditions, NPR1 tends to exist intracellularly as an oligomer based on intramolecular disulfide bonds formed by Cys82 and Cys216. However, upon pathogen infection, the intramolecular disulfide bond is reduced by the reduction of TRX-H3/H5 and NPR1 is then shuttled into the nucleus as a monomer [104]. In the nucleus, NPR1 monomers interact with members of the TGA1 subfamily of the basic leucine zipper (bZIP) TF family to stimulate their DNA-binding activity [105], ultimately promoting the expression of downstream pathogen-associated genes.
WHIRLY1 is a DNA-binding protein located both in the chloroplast and in the nucleus with the same molecular weight in both regions [106]. Under normal conditions, WHIRLY1 forms 24 oligomers in the form of disulfide bonds that act as a bridge linking the cystoid and nucleus; however, in response to external environmental stimuli, alterations in the redox state of the photosynthetic machinery induce the mononucleation and translocation of WHIRLY1 into the nucleus [107]. In this way, the WHIRLY1 protein, as a chloroplast component of redox regulation, plays a unique role in retrograde signaling pathways leading to adaptation and immune responses.
Heat stress TFs (Hsfs) regulate the expression of genes that are induced under various abiotic stress conditions. Under cold stress, the heat-stimulated transcription factor 1 (HsfA1)–NPR1 complex is also regulated by OxiPTMs. Under low-temperature conditions, monomers released from cytoplasmic NPR1 oligomers in the presence of TRXH3 and TRXH5 are translocated to the nucleus and then interact with HsfA1 to promote the induction of HsfA1-regulated genes, resulting in low-temperature adaptation. The mechanism by which the NPR1–HsfA1 transcriptional complex promotes cold resistance in plants also involves the activation of HsfA1 target genes, including chaperone genes. These findings revealed novel regulatory pathways for cold acclimation mediated by NPR1 and HsfA1, and highlighted NPR1 as a bridge between cold and pathogen signaling to help plants better adapt to changing environments [108]. As another redox-sensitive TF, HsfA8 was induced by H2O2 treatment, and the nuclear translocation of HsfA8 was performed in a Cys24- and Cys269-dependent manner [109].

3.2. OxiPTMs Affect the DNA-Binding Properties of TFs

FLOWERING LOCUS C (FLC) plays a key role in flowering initiation in Arabidopsis and exerts a predominantly repressive effect on two flowering-promoting genes: FLOWERING LOCUS T (FT) and SUPPRESSOR OFOVEREXPRESSION OFCONSTANS 1 (SOC1) [110]. Among the four FLCs in heading Chinese cabbage, two (BraFLC1 and BraFLC3) directly affect the expression of the downstream genes BraSOC1 and BraFT by reducing their binding ability through persulfidation [111].
The TGA transcription factor FASCIATED EAR4 (FEA4) is a negative regulator of the redox state and developmental activity of the inflorescence meristem. A deficiency of FEA4 results in a significant increase in the size of the inflorescence apical meristem. The Cys site in FEA4 associated with the oxidative induction of dimer formation is Cys321. FEA4 interacts with maize CC-type GRX MALE STERILE TRANSFORMED ANTHER 1 (MSCA1) during maize ear development and its redox status is closely related to that of GRX. Because the key Cys321 residue of FEA4 is reduced by MSCA1, both the dimerization reaction of FEA4 and GRX mutation enhance the DNA-binding properties and transcriptional activity of FEA4 and auxin-related genes. This series of reactions leads to a stronger inhibition of the activity of the meristem at the top of the inflorescence [112].
With the continuous accumulation of NO, we previously identified the rapid induction of the C2H2 zinc finger-containing SNO REGULATORY GENE 1 (SRG1), which is a positive regulator of plant immunity [113]. SRG1 is also subject to post-translational redox regulation with Cys87 as its key modification site. The S-nitrosation at the Cys87 residue of SRG1 attenuates its DNA-binding activity and thus affects its transcriptional repression. Therefore, the formation of the SRG1–SNO complex may contribute to a negative feedback loop that attenuates the plant immune response to pathogens.
Cucurbitacin C (CuC), a triterpenoid secondary metabolite, improves the resistance of cucumber to insects and pathogens. Two basic helix-loop-helix TFs, Cs5G157230 and Cs5G156220, can control the expression of CuC biosynthetic genes [114], and their DNA-binding activity to the CuC biosynthesis gene Csa6G088690 promoter was increased by H2S persulfuration treatment, which improved the resistance of cucumber leaves to watermelon blast [115].

3.3. OxiPTMs Regulate Protein–Protein Interactions

Cross-talk between brassinosteroid (BR) and H2O2 is achieved through the post-translational redox regulation of the activity of the TF BRASSINAZOLE-RESISTANT1 (BZR1) [116,117]. The oxidation of BZR1 at Cys63 enhances its interaction with AUXIN RESPONSE FACTOR 6 (ARF6) and PHYTOCHROME INTERACTION FACTOR 4 (PIF4), key regulators of growth hormone and light signaling pathways, ultimately leading to the activation of growth-related genes. This suggests that OxiPTMs indirectly affect DNA-binding activity by influencing the interaction of BZR1 with other TFs [116].
NPR1 interacts with members of the TGA1 subfamily of the evolutionary branch 1 of the bZIP TF family in the nucleus, and activates their DNA-binding capacity [118]. Moreover, members of the TGA TF subfamily are subject to redox regulation. Under normal conditions, TGA1 forms an intramolecular disulfide bond between Cys260 and Cys266, and this oligomeric form blocks the interaction with NPR1. However, during pathogen infection, SA promotes the reduction of TGA1 by TRX through intracellular redox changes, interrupts the interaction with NPR1, and thus activates the DNA-binding capacity of TGA1 [105]. A similar redox-mediated interaction to that of NPR1 has been observed for TGA4 [119]. ROS and RNS cross-talk can also affect defense gene expression, which is mediated through post-translational redox modifications in the NPR1/TGA1 system.
The interaction between the plant hormone abscisic acid (ABA) and active substances such as ROS and RNS is important for the processes of plant growth and development, especially during seed germination and post-emergence development, and this process depends on post-translational redox modifications [120,121,122]. In general, ABA and H2S inhibit seed germination, while NO and H2O2 promote seed germination [65,123,124]. The S-nitrosation of ABI5 at the Cys153 residue facilitates its interaction with E3 ubiquitin ligase, leading to ubiquitin-mediated ABI5 protein hydrolysis, which attenuates the inhibition of seed germination and seedling formation [125].
Plants have evolved effective mechanisms for so-called “cold acclimation” specifically to enhance tolerance to cold stress in coping with cold climates. In Arabidopsis, a dehydration response element (DRE) with a core sequence of A/GCCGAC was identified as a cis-acting element that regulates the expression of desiccation-inducible genes [126,127], in which DREB1/CBF is an APETALA2/ETHYLENE-RESPONSIVE FACTOR (AP2/ERF) TF that binds to DREs and plays a major regulatory role in cold-induced gene expression [128]. Recent studies have highlighted the significance of redox regulation in plant frost resistance [68]. TRX-h2 was originally found to be localized in the cytoplasmic inner membrane; however, under low-temperature conditions, it enters the nucleus and reduces all dimerized CBF monomers by interacting with CBF. This results in functionally active monomeric CBF and promotes the expression of cold-regulated genes, conferring the plant with freeze resistance [68].
GT factors belong to the trihelix family of TFs, which bind to GT elements in light-regulated genes and promote the plant stress response and development [129]. A recent study showed that NO induced under high-temperature stress leads to S-nitrosation at the Cys324 or Cys347 site of GT-1. The S-nitrosation of GT-1 promotes its binding to the NO-responsive element in the HsfA2 promoter, which activates the expression of HsfA2 and enhances the expression of heat-responsive genes to result in heat tolerance [130].
The bZIP family is one of the largest families of transcriptional regulators, and recent studies have shown that the function of the Arabidopsis G-group bZIP TF is closely related to OxiPTMs. For example, Arabidopsis bZIP16, bZIP68, and G-box BINDING FACTOR1 (GBF1) can all respond to chloroplast redox changes under intense light irradiation [64,131,132].

3.4. OxiPTMs Mediate Proteolysis

High temperature and light have opposite functions on seed germination: high temperature inhibits seed germination, while light induces seed germination. Recently, the identification of the S-nitrosation of LONG HYPOCOTYL IN FAR-RED1 (HFR1) provided a mechanistic link between heat-controlled and light-controlled seed germination [133]. Light plays a stabilizing role for HFR1, which interacts with PIF1 to form a heterodimeric complex and attenuate its DNA-binding activity, thereby promoting seed germination in the light. However, high temperature triggers the S-nitrosation of HFR1 at Cys164, causing its degradation and the release of PIF1, which activates the expression of the CCCH-type zinc-finger protein SOMNUS, thereby altering ABA and gibberellic acid metabolism to subsequently suppress seed germination [133].
The TF ERFVII has emerged as an important regulator in plants during hypoxic stress. As a steady-state hypoxia sensor, ERFVII is characterized by a conserved N-terminal motif (MCGGAI[I/L]) that targets the N-terminal rule pathway of protein hydrolysis [134,135]. In the presence of methionine aminopeptidase, the N-terminal methionine is removed, exposing the Cys so that it is susceptible to redox modification. In the presence of ROS or RNS, the Cys residue is oxidized to sulfinic or sulfonic acid and is then arginylated and degraded by E3 ligase recognition [136]. However, under hypoxic conditions, N-terminal Cys oxidation is inhibited and ERFVII is not degraded, thus promoting the expression of its target genes.

4. OxiPTM Fine-Tunes the Functions of Kinases in Plants

OxiPTMs also participate in regulating the activities of various kinases to help plants adapt to changing environments and abiotic stress [137].
The fluctuation of natural light results in unbalanced photosynthetic electron fluxes; thus, chloroplasts are one of the primary locations of ROS production. Accordingly, many photosynthetic enzymes in plant chloroplasts are regulated by redox reactions to maintain a stable state. The serine/threonine-protein kinase STN7 is involved in the phosphorylation of the light-harvesting complex II protein, acting as a key regulator of the short-term and long-term response of the photosynthetic apparatus under adverse environmental conditions [138]. The activity of STN7 was reported to be regulated by the redox state of the plastoquinone pool and the Trx system. The overexpression of Trxm in tobacco deactivated STN7 through a redox-mediated mechanism [139]. Furthermore, LUMEN THIOL OXIDOREDUCTASE 1 (LTO1) was found to interact with the lumenal domain of STN7 both in vitro and in vivo, enabling the TRX-like domain of LTO1 to oxidize the lumenal Cys residues of STN7, ultimately regulating its kinase activity [10].
Oxidative stress is a common stress that affects plant growth and development under complex environmental conditions. The activity of PTP1 is regulated by the redox state. Specifically, H2O2 inactivates PTP1, which could be restored by dithiothreitol treatment. Moreover, the activity of MPK6 was significantly reduced by treatment with active PTP1, indicating that PTP1 may be the main target of Arabidopsis in response to oxidative stress [9]. Moreover, the 3′-phosphoadenosine 5′-phosphate (PAP) phosphatase SAL1 was reported to act as an oxidative stress sensor in plant chloroplasts. Chan et al. (2016) showed that oxidative stress triggered the dimerization between SAL1 monomeric subunits through Cys119–Cys119 intermolecular disulfide bonding, which stabilized the protein conformation and helped to form the Cys167–Cys190 intramolecular disulfide bond. The activity of SAL1 phosphatase was suppressed by dimerization and intramolecular disulfide formation, thereby regulating the expression of plastid redox-associated nuclear genes [140].
H2S is a critical gaseous signal in ABA-induced stomatal movement under abiotic stress. Recent evidence indicates that ABA stimulates the persulfidation of an important endogenous H2S enzyme, L-CYSTEINE DESULFHYDRASE1 (DES1), in a redox-dependent manner. In the presence of ABA, the Cys44 and Cys205 residues of DES1 protein could form persulfate by reacting with H2S to promote the enzyme activity of DES, resulting in the accumulation of H2S in guard cells [141]. Moreover, endogenous H2S was reported to trigger the persulfidation modification of two cysteine residues (Cys131 and Cys137) in SnRK2.6 protein, which altered the redox status and changed the protein structure. The persulfidation of SnRK2.6 further promoted its phosphorylation and binding ability to ABA response element-binding factor 2 (ABF2), a TF acting downstream of ABA signaling to trigger stomatal closure, thereby regulating the tolerance to drought stress [142]. The overproduction of H2S was also found to drive the persulfidation of NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG PROTEIN D (RBOHD) at Cys825 and Cys890 and enhanced its ROS-producing activity to trigger stomatal closure [141,143]. Furthermore, the redox states of Arabidopsis thaliana GLUTATHIONE PEROXIDASE 3 (AtGPX3) and the 2C-type protein phosphatase ABA INSENSITIVE 2 (ABI2) were found to be regulated by H2O2. In vitro, the oxidized AtGPX3 could transform the reduced ABI2 into the oxidized form and reduced its PP2C kinase activity, thus regulating stomatal movement under drought stress [63].
Another recent study showed that NO-induced S-nitrosation influenced ethylene synthesis and salt tolerance in tomatoes. As the last enzyme in the plant ethylene biosynthesis pathway, the enzymatic activation of ACO homolog 4 (ACOh4) was found to be activated by NO-induced S-nitrosation at Cys172, and the knockout of ACOh4 eliminated NO-induced ethylene biosynthesis. The researchers further showed that ACOh4 could positively influence K+/Na+ homeostasis under salt stress, which explains how NO promotes ethylene synthesis in response to salt stress [144].
OxiPTM also plays a certain role in regulating plant growth and development. Dual-specificity phosphatase STARCH EXCESS 4 (SEX4) protein is required for starch breakdown to sustain the growth of plants. SEX4 is a redox-regulated protein that is controlled by thioredoxins; in the oxidation state, the catalytic Cys198 residue and the Cys130 site within the phosphatase domain could form a disulfide bridge that inactivates SEX4 [145].
A definitive link has been established between the rapid accumulation of NO and the expression dynamics of Pattern-Triggered Immunity (PTI). Investigations have demonstrated that the recognition of pathogen-associated molecular patterns (PAMPs) by plant cell surface receptors elicits a swift accumulation of NO, ultimately resulting in the S-nitrosylation of cytosolic receptor-like kinase BIK1 at the Cys80 residue. This redox-mediated post-translational modification plays a pivotal role in promoting the phosphorylation, activation, and stabilization of BIK1. Additionally, the S-nitrosylated BIK1 exhibits enhanced interaction with RBOHD, a key mediator of extracellular oxidative bursts, thereby fostering the generation of reactive oxygen species (ROS) and orchestrating the plant immune response [146].
Stomatal movement plays a pivotal role in enabling plants to adapt to environmental stresses. HPCA1, a receptor kinase characterized by its leucine-rich repeat (LRR) motifs, primarily serves as a cell surface sensor for hydrogen peroxide, detecting extracellular hydrogen peroxide (eH2O2) to modulate plant stress responses. Upon the permeation of eH2O2 into the cell, HPCA1 undergoes oxidative post-translational modifications (OxiPTMs) within its extracellular domain, a process that culminates in autophosphorylation. This autophosphorylation event subsequently activates calcium ion channels located on the plasma membrane, leading to an elevation in cytosolic Ca²⁺ concentrations. Ultimately, this cascade of events triggers stomatal closure as a protective mechanism against external stressors [147].

5. Conclusions and Perspectives

In recent years, OxiPTMs have been increasingly studied, revealing their essential roles in plant life processes. Active-responsive species have emerged as signaling molecules and the cross-talk between such signaling molecules (e.g., ROS and RNS) or with different phytohormone signaling pathways (e.g., SA, BR, and ABA signaling) reflect the complexity of redox signaling in the regulation of the plant stress response and development (Figure 2). Moreover, with the development of technology, the combined use of techniques such as proteomics, chemical selection probes, and mass spectrometry has laid a solid foundation to better understand the functions and consequences of S-sulfenylation, S-glutathionylation, S-nitrosation, and persulfidation in plants [148,149,150]. Mercaptocysteine-based OxiPTM-mediated redox signaling can activate some TF or kinase functions through modifying protein nuclear translocation, DNA binding capacity, protein–protein interactions, and protein hydrolysis in Table 2.
The essence of these modifications is the reactivity of protein cysteine thiol groups (–SH). The upper part of the figure illustrates the oxidation states of sulfur (S) in proteins, ranging from thiol (−2) to sulfonic acid (+4). As the degree of oxidation increases, these reactions transition from reversible to irreversible. The lower part of the figure depicts the formation of major OxiPTMs. The initial reaction between thiol and H2O2 results in the formation of sulfenic acid (R-SOH; S-sulfenylation). Upon excessive exposure to H2O2, sulfenic acid (-SOH) can further oxidize to sulfinic acid (-SO2H; S-sulfinylation) and sulfonic acid (-SO3H; S-sulfonation). The formation of sulfonic acid is irreversible. -SOH can react with adjacent -SH groups within the same protein or from other proteins and glutathione (GSH), forming disulfide bonds (-SSR) and S-glutathionylated bonds (-SSG; S-glutathionylation), respectively. These disulfide bonds can be enzymatically reduced by thioredoxins (TRXs) or glutaredoxins (GRXs). S-nitrosylation can also be induced by NO, leading to the covalent addition of the NO group to reactive cysteine thiol (-SNO). S-nitrosylation can be reduced by TRXs (i.e., denitrosylation), or the NO group can be transferred to other protein thiols—a process termed “transnitrosylation”. Last, H2S can react with oxidized thiol derivatives (e.g., disulfides or -SOH) to form persulfides (-SSHs), a process called ‘persulfidation’ (or S-sulfhydration).
During plant growth and development or under oxidative stress, bursts of reactive oxygen, nitrogen, and sulfur species (ROS/RNS/RSS) could modify cysteine (Cys) thiols either through direct reactions with TFs and kinases or through pathways with redox-related transferases. Thiol-based OxiPTMs regulate TF functions through four main pathways: S-sulfenylation, S-nitrosation, persulfidation, and intra-/intermolecular disulfide bond formation. First, OxiPTMs can cause the translocation of a TF to the nucleus, thereby affecting transcriptional regulation. Second, OxiPTMs can induce conformational changes in TFs, thereby enhancing binding to the promoters of downstream target genes. Third, OxiPTMs can affect the interaction of TFs with other TFs. Fourth, OxiPTMs can control TF stability by regulating the interaction of a TF with the ubiquitin–proteasome system. Ultimately, all of these pathways lead to changes in the regulated expression of downstream target genes. Similarly, thiol-based OxiPTMs regulate kinase functions through three main pathways: S-nitrosation, persulfidation, and intra-/intermolecular disulfide bond formation. Kinase activity changes after oxidative modification and affects other post-translational modifications (including phosphorylation and ubiquitination) of downstream target proteins or the synthesis of metabolites (such as plant hormones).
To date, the majority of studies in this field have focused on the fine-tuning of OxiPTMs on TF functions rather than on their effects on other proteins; therefore, further investigations are needed on redox-mediated PTMs of non-TFs such as STN7, ABI2, and other kinases that play important roles in photosynthesis or ABA signaling pathways, as well as other proteins regulated by OxiPTMs that have yet to be identified [151]. In addition, currently, most research on OxiPTMs in plants is limited to the model species Arabidopsis; therefore, further attention should be paid to these effects in commercial crops to improve productivity and quality, resulting in more agronomically valuable crops. Since the redox state of cells is highly dynamic, many experiments related to the redox state cannot be effectively verified due to technical limitations, which greatly hinders the exploration of OxiPTMs, highlighting the need for specialized studies of the nuclear redox proteome. In particular, the cross-talk between signaling molecules mediating OxiPTMs and the apparent communication between different OxiPTMs remain to be elucidated, requiring further investigation in this area. Current research directions continue to be grounded in genomics, leveraging an array of novel technologies such as the chemoselective DYn-2 probe based on alkynyl functionalization and BTD-derived probes, to identify more modified proteins. This aligns well with previous research endeavors. Currently, there is a growing trend to integrate these technologies with forward and reverse genetics to specifically investigate the impact of these critical redox modification sites on the functions of transcription factors or kinases. Subsequently, through the use of CRISPR-Cas technology, genes are knocked out and then complemented with point mutations to precisely probe the functions of redox modification sites. In recent years, the advent of the novel CRISPR technology, Prime Editing (PE), has significantly enhanced the precision and efficiency of editing, achieving the aforementioned effects through base substitutions. Thus, it is evident that technological advancements have continuously propelled the progress of redox research in plants.

Author Contributions

B.Z. and Y.-D.G. conceived this project. H.L. wrote the manuscript. X.W., Y.L., P.Z., F.C. and N.Z. collected the references. B.Z. and Y.-D.G. revised the manuscript. All authors discussed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the grants from the Key Research and Development Program of Xinjiang Uygur autonomous region in China (2023B02017). We also appreciate the support from Beijing Agriculture Innovation Consortium (BAIC01-2024) and 2115 project of China Agricultural University.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 14 02757 g001
Figure 1. Overview of principal thiol-based OxiPTMs.
Figure 1. Overview of principal thiol-based OxiPTMs.
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Figure 2. Schematic diagram of the effects of cysteine thiol-based oxidative post-translational modifications (OxiPTMs) on plant transcription factors (TFs) and kinases.
Figure 2. Schematic diagram of the effects of cysteine thiol-based oxidative post-translational modifications (OxiPTMs) on plant transcription factors (TFs) and kinases.
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Table 1. The major OxiPTMs types in plants.
Table 1. The major OxiPTMs types in plants.
Reactive Electrophilic SpeciesSynthetic PathwaysOxiPTMsDetection MethodReferences
Reactive oxygen species (ROS)Photosynthesis in chloroplasts, the last stage of aerobic respiration pathway in mitochondria, photorespiration in peroxisome and plasma membrane oxidoreductase systemS-sulfenylation
S-glutathionylation		YAP1C probe
DYn-2 probe
BTD-based probe
LC–MS/MS
GS-biotin-labeling studies, 2D-PAGE followed by MALDI-MS
Immublot probe with anti-GSH antibodies and identified by MALDI-TOF and LC–MS/MS		[11,12,13,14]
Reactive nitrogen species (RNS)The arginine-dependent and nitrate-dependent pathways,S-nitrosationBSM and LC–MS/MS
Site-specific nitrosoproteomic approach		[15,16]
Reactive sulfur species (RSS)The function of
L-desulfurylase (L-CDES) and D-desulfurylase (D-CDES) in the cytosol and β-cyanoalanine synthase (CAS) in the mitochondria		PersulfidationModified BSM and LC–MS/MS
the tag-switch method		[17,18]
Table 2. Functional characterization of OxiPTM regulating TFs in plants.
Table 2. Functional characterization of OxiPTM regulating TFs in plants.
ProteinsSpeciesOxiPTMStress Condition/
Developmental Stage		Refs.
transcription factors
NPR1Arabidopsis thalianaDisulfide bondsImmune response[101,105]
WHIRLY1Arabidopsis thalianaDisulfide bondsAdaptation and immune response[106,107]
HsfA1- NPR1Arabidopsis thalianaDisulfide bondsCold stress[108,109]
BraFLC1,
BraFLC3		Chinese cabbage
(Brassica rapa L.)		PersulfidationFlowering transition[110,111]
FEA4Maize (Zea mays L.)Disulfide bondsFlower development[112]
SRG1Arabidopsis thalianaS-nitrosationImmune response[113]
Csa5G156220,
Csa5G157230		Cucumber
(Cucumis sativus L.)		PersulfidationImmune response[114,115]
BZR1Arabidopsis thalianaS-sulfenylationQuiescent center cell division and stomatal opening[116,117]
TGA1Arabidopsis thalianaDisulfide bondsImmune response[105,119]
ABI5Arabidopsis thalianaS-nitrosationSeed germination
and seedling growth		[120,125]
CBF1Arabidopsis thalianaDisulfide bondsCold stress[68,126,127,128]
GT-1Arabidopsis thalianaS-nitrosationHeat stress[129,130]
AtbZIP16,
AtbZIP68,
GBF1		Arabidopsis thalianaDisulfide bondHigh light exposure[64,131,132]
HFR1Arabidopsis thalianaS-nitrosationHeat stress[133]
ERFVIIArabidopsis thalianaS-sulfinylationCold stress[134,135,136]
Kinases
STN7Arabidopsis thalianaDisulfide bondsMaintain redox balance[138,139]
SAL1Arabidopsis thalianaDisulfide bondsRedox signaling transduction[140]
DES1Arabidopsis thalianaPersulfidationStomatal movement[141]
SnRK2.6Arabidopsis thalianaPersulfidationABA signaling transduction[142]
RBOHDArabidopsis thalianaPersulfidationStomatal movement[141,143]
GPX3
ABI2		Arabidopsis thalianaDisulfide bondsStomatal movement[63]
ACOh4Solanum lycopersicumS-nitrosationSalt Stress[144]
SEX4Arabidopsis thalianaDisulfide bondsStarch degradation to sustain plant growth[145]
BIK1Arabidopsis thalianaS-nitrosationImmune response[146]
HPCA1Arabidopsis thalianaDisulfide bondsStomatal movement[147]
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Li, H.; Wang, X.; Liu, Y.; Zhang, P.; Chen, F.; Zhang, N.; Zhao, B.; Guo, Y.-D. Cysteine Thiol-Based Oxidative Post-Translational Modifications Fine-Tune Protein Functions in Plants. Agronomy 2024, 14, 2757. https://doi.org/10.3390/agronomy14122757

AMA Style

Li H, Wang X, Liu Y, Zhang P, Chen F, Zhang N, Zhao B, Guo Y-D. Cysteine Thiol-Based Oxidative Post-Translational Modifications Fine-Tune Protein Functions in Plants. Agronomy. 2024; 14(12):2757. https://doi.org/10.3390/agronomy14122757

Chicago/Turabian Style

Li, Hongxin, Xiaoyun Wang, Ying Liu, Peiyang Zhang, Fuyuan Chen, Na Zhang, Bing Zhao, and Yang-Dong Guo. 2024. "Cysteine Thiol-Based Oxidative Post-Translational Modifications Fine-Tune Protein Functions in Plants" Agronomy 14, no. 12: 2757. https://doi.org/10.3390/agronomy14122757

APA Style

Li, H., Wang, X., Liu, Y., Zhang, P., Chen, F., Zhang, N., Zhao, B., & Guo, Y. -D. (2024). Cysteine Thiol-Based Oxidative Post-Translational Modifications Fine-Tune Protein Functions in Plants. Agronomy, 14(12), 2757. https://doi.org/10.3390/agronomy14122757

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