Antioxidant Potential of Glutathione and Crosstalk with Phytohormones
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This entry is adapted from the peer-reviewed paper 10.3390/plants12051133

Glutathione (GSH) is an abundant tripeptide that can enhance plant tolerance to biotic and abiotic stress. Its main role is to counter free radicals and detoxify reactive oxygen species (ROS) generated in cells under unfavorable conditions. Moreover, along with other second messengers (such as ROS, calcium, nitric oxide, cyclic nucleotides, etc.), GSH also acts as a cellular signal involved in stress signal pathways in plants, directly or along with the glutaredoxin and thioredoxin systems.

antioxidants abiotic stress reactive oxygen species glutathione

1. Introduction

The tripeptide thiol molecule glutathione (GSH) with an amino acid composition including cysteine, glutamic acid, and glycine is a common and widespread antioxidant in plants and plays an important role in stress response as a scavenger of free radicals. Reactive oxygen species (ROS) are a group of highly reactive molecules that are considered an unavoidable metabolic product of aerobic organisms, present in low and relatively stable amounts under normal physiological conditions. Oxidative stress occurs because of increased ROS accumulation or due to higher production and/or insufficient detoxification. Plants have evolved specific pathways and molecules to protect cells from ROS toxicity. GSH is one of the most critical components, being ubiquitous, present in different subcellular compartments, relatively abundant, and involved in a variety of cellular events, from the synthesis of DNA and proteins to cellular defense [1]. GSH is found in two forms: (1) the reduced form (GSH), considered one of the most important ROS scavengers, and (2) the oxidized form (GSSG), which then reverts to reduced glutathione by the enzyme glutathione reductase. There is a prevalence of GSH over GSSG under normal conditions. Cellular toxicity can be determined by the ratio of reduced versus oxidized glutathione [2].
Abiotic stress deriving from extreme temperatures, nutrient availability, water quality and accessibility, soil characteristics, unsuitable radiation, and toxic elements causes major crop loss [3]. Symptoms may be different and include withering, chlorosis, reduced growth, altered development, wilting, organ (e.g., leaf, flower, fruit) abscission, and rot/necrosis [4]. During stress conditions, ROS act in plants as transduction molecules that control different pathways. In addition to being biochemical products of the (stress) metabolism, NADPH oxidases (also named respiratory burst oxidase homologs, RBOHs) are a major source of ROS in stressed plants along with other oxidases and peroxidases [5]. The primary adaptive response to oxidative plant stress is an increase in antioxidant defense system activity [6]. This includes the participation of various antioxidants which are non-enzymatic such as GSH, ascorbic acid (AsA), tocopherols, phenols, other secondary metabolites, and inorganic amino acids, which have the common role of maintaining redox homeostasis [7]. In addition, several antioxidant enzymes, such as monodehydroascorbate reductase (MDHAR), glutathione reductase (GR), dehydroascorbate reductase (DHAR), glutathione S-transferase (GST), and glutathione peroxidase (GPX) are involved in these defense responses [8]. For instance, GSTs promote the conjugation of GST with xenobiotics, superoxide dismutases partition the superoxide radical in oxygen and hydrogen peroxide, catalases decompose hydrogen peroxide into water and oxygen, peroxidases (POD) catalyze the oxido-reduction between hydrogen peroxide and reductants, and MDHAR, DHAR, ascorbate peroxidase (APX), and GRs are members of the ascorbate–glutathione cycle that detoxifies hydrogen peroxidase [9] (Figure 1).
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Figure 1. A simplified view of the role of GSH in the redox homeostasis in plants following abiotic stress (such as extreme temperatures, drought, solar radiation, toxic elements, and poor soil conditions) and the subsequent cellular increase in common oxidants.
Phytohormones are molecules present in small amounts that can influence physiological processes in plants [10]. Phytohormones are chemical messengers that help in the management of cellular functions and signaling [11]. Auxins were the first discovered phytohormones [12] while strigolactones (SL) are the most recently identified [13]. Although classifications can be slightly different, the commonly recognized phytohormones are abscisic acid (ABA), brassinosteroids (BR), gibberellins (GA), jasmonates (JA), cytokinins (CK), auxins, salicylates (SA), strigolactones (SL), and ethylene (ETH) [11]. Some phytohormones mediate plant defense response to abiotic stress such as JA, ET, ABA, and SA [14]. Environmental conditions including wounding, cold, heat, salinity, and drought stresses mostly cause increases in abscisic acid levels; this is because abscisic acid is usually accountable for plant defense towards abiotic stresses [15].

2. GSH Biosynthesis

The biosynthesis of GSH encompasses two ATP-dependent stages (Figure 2). In the first, glutamate–cysteine ligase (GCL) catalyzes the reaction between glutamate and cysteine to produce γ-glutamylcysteine. By the addition of glycine to γ-glutamylcysteine, glutathione is produced via glutathione synthetase. The balance between GSH and GSSG is critical for preserving the cell’s homeostasis [2][16]. The availability of GCL and GS plays a crucial part in glutathione biosynthesis. GCL and GS are localized in the chloroplast and cytosol, respectively [17]. In Arabidopsis, glutamate–cysteine ligase and glutathione synthetase (GS) are encoded by the same gene (with different start sites), which produces proteins that are localized into the cytosol or transported to plastids [18]. Plant systems are unique in that they compartmentalize glutathione biosynthesis [2][19]. In plants, glutathione content is typically increased by over-expression of GCL rather than GS by increasing flux through the system. Arabidopsis seedlings treated with 5 mM H2O2 demonstrated an elevation in GCL function that ranged from GSH to GSSG form, as shown by immunoblot and activation experiments [20].
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Figure 2. Glutathione biosynthesis in plants.
Glutathione can also be described as a non-protein-reduced sulfur. GSH synthesis occurs in the cytosol, as well as in mitochondria, peroxisome, and chloroplasts (Figure 3) [21]. There are three amino acids initiating the reaction: glycine, cysteine, and glutamate. Two proteins catalyze the GSH synthesis (glutathione synthase (GSHS) and c-glutamylcysteine synthetase (cECS)). Plastids and cytosol are found in GSH while cECS is only found in plastids; because of this, in higher plants, the location of GSH creation is plastids [22].
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Figure 3. Diagrammatic illustration of biosynthesis pathways of glutathione in chloroplast, peroxysome, and mitochondria.
Under stress conditions, the transformation of reduced GSH into GSSG can happen inside various compartments through biochemical responses. The GSH-to-GSSG ratio is dependent mainly on the activity of glutathione reductase and also on glutathione peroxidases (GPX) [23]. Glutamate donates the carboxyl part and cysteine donates the amino part and, thus, the peptide bond connecting them is created. Subsequently, γ-glutamylcysteine accumulates glycine to contribute in glutathione synthesis. There is also the presence of a peptide bond between them. Glutathione synthetases (GS, GSH-S, GSH2) catalyze the formation of GSH. 

3. GSH as Regulatory and Antioxidant Molecule

It is well-known that GSH is an important antioxidant molecule [24]. In plants, the presence of GSH-specific peroxidases has been problematic because they, as indicated by GPXs in plants, show no reaction with GSH—only by means of TRXs (thioredoxins) [25]. GSH detoxifies lipid peroxides, methyl glyoxal, and pesticides in addition to H2O2 [26][27]. First, one ATP molecule is used by the GCL during the formation of glutamylcysteine from glutamate and cysteine. After that, glycine is transferred to the dipeptide catalyzed by GS and also requires another ATP molecule. It is interesting to note that oxidative stress (OS) can activate the nuclear factor erythroid 2-related factor 2, which controls GCL synthesis. As a result, oxidative stress increases GSH synthesis by promoting GCL action [28]. Glutamyl bonding, which makes GSH exceptionally robust and resilient to degradation by most proteases and peptidases, is one of the distinguishing physical features of GSH. The enzyme gamma-glutamyl transferase (GGT) breaks down the extracellularly situated GSH by removing gamma-glutamyl and, hence, produces cysteinylglycine or cysteinylglycine conjugates, which are further broken by dipeptidases [29].
Stress-instigated variations in GSH content as well as GSH/GSSG proportions could be due to a shift in GSH synthesis. The formation of cEC is mediated by cECS first and, subsequently, GSH synthetase adds a glycine to the dipeptide. The cECS is an administrative catalyst of glutathione amalgamation [30]. In addition to GSH, hGSH (homoglutathione) has been found in of the Fabaceae family [31], and in the Gramineae family, the presence of hmGSH (hydroxymethyl glutathione) is seen, but the biosynthetic pathway has not yet been determined [32]. The absorption of 35S via solute onto GSH as well as the augmented movement of the two proteins linked with GSH production showed that the cold-actuated expansion of maize in total glutathione (TG) concentrations is the direct consequence of a faster synthesis rate [33].
The linkage among antioxidants and ROS might provide metabolic contact points. These points are found in-between signals from metabolic pathways as well as those from the climate, directing the acceptance of processes of apoptosis [24]. The antioxidant activity framework, which includes the GSH/GSSG redox reaction, could have evolved to modulate redox signaling and the cellular redox state, as well as to organize gene expression [34].

4. Role of GSH under Abiotic Stress in Plant System

4.1. Oxidative Stress

GSH is the main antioxidant that directs abiotic stress reactions [35][36]. In cells, it additionally balances out redox homeostasis, invigorates stress-associated signals, promotes stress endurance, and detoxifies xenobiotics [37]. GSH initiates glutathionylation so that it can use oxidative stress for protein shielding [38][39]. In plants, this information could be utilized for the indication of stress markers to recognize necrotic cues [40]. Because of the abiotic stress, the GSH concentration additionally fluctuates inside various subcellular segments. Organelle-explicit varieties are shown by this tripeptide thiol during stress because of its assorted jobs within distinctive cell components. GSH maintains the declining interior climate inside cells and, furthermore, restricts uncontrolled oxidation of proteins and membranes [41].
During abiotic stress, vacuoles act as sinks for ROS. The rate-limiting enzyme GR which mediates the AsA–GSH cycle ensures elevated AsA concentrations in the vacuoles to easily scavenge phenoxy radicals [42]. The cat2 mutant competes with excessive GSH aggregation in the vacuoles to avoid the negative consequences of GSSG gathering. These include arrangement of necrosis, torpidity, and sores [43]. The overabundance of ROS in the vacuoles is detoxified by GSH during abiotic stress and for extraction of huge measure of GSH from cytoplasm goes about as a sink [44]. Glutathione combats various abiotic stresses by using its antioxidant defense machinery. Usually, it acts as a master antioxidant, as depicted in Figure 4.
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Figure 4. Glutathione‘s role as a master antioxidant in plant defense system.

4.2. Heat Stress

Heat stress negatively impacts plants’ performance. GSH application, however, improves plants’ ability to cope up with heat stress by modulating physiological and metabolic functioning, chiefly through the induction of antioxidant enzymes in combination with ROS scavenging. External GSH administration helped preserve leaf moisture content with enhanced antioxidant enzyme activity, thereby inducing resistance to heat stress in plants [45].

4.3. Cold Stress

Cold stress causes foliar chlorosis and a decline in the quality of the function and structure of cells and tissues by delaying leaf development, prolonging the cell cycle with reduced cell production, and stunting growth. To fight cold stress, external GSH administration was found to be beneficial via reducing lipid peroxidation and electrolyte leakage [46].
Low temperature changes the physiology of plants, causing damage to their cell membranes, changes in their lipid composition, chlorosis, and different enzyme activities that cause necrosis and even death in some cases [47][48]. The level of tolerance of the Pusa Sheetal cv. of tomato is decreased by cold stress. Exogenous GSH supplementation, however, has the tendency to raise the level of the tolerance [49]. 

4.4. Salinity Stress

Salinity stress gives rise to a decrease in water uptake, photosynthesis, and seed germination, nutritional imbalances, salt ion toxicity, and a general decline in agricultural output. Salinity stress can be treated with GSH administration. This improves plant growth, the fresh and dry masses of shoots and roots, and total yield. To counteract salinity stress, exogenous administration of GSH has boosted water usage efficiency (WUE), antioxidant enzyme activity, and levels of osmoprotectants [50].

4.5. Heavy Metal Stress

Heavy metal stress includes various heavy metals such as cadmium, nickel, lead, mercury, copper, zinc, etc. In general, heavy metal stress has harmful effects on plants, including reductions in growth, photosynthesis, and nutrient uptake, as well as changes to the water balance, chlorosis, and senescence. On the other hand, it has been found that applying glutathione to plants increases their ability to withstand stress by boosting their antioxidants, ROS scavenging, and photosynthetic pigment levels. Glutathione was applied exogenously to increase photosynthetic pigments and reduce oxidative damage in order to counteract the negative consequences of heavy metal stress [51].
Under Cd stress, plants increased the amount of GSH quickly and chelated Cd2+, thereby reducing the harm that Cd stress caused to the cytosol’s metabolic processes [52]. Under stress conditions, phytochelatin synthase (PCs) may transfer c-Glu-Cys to GSH, and subsequently form phytochelatin (PC) [53]. PC can, indeed, integrate Cd2+ directly, and can also lessen the harm of oxidative damage induced from heavy metals [54][55]. Moreover, GSH and PC enhance the majority of ABC transporters in the transfer of Cd [56][57]. 

4.6. Drought Stress

Drought frequently has limiting impacts on plants’ growth and developmental stages and induces growth inhibition and low total crop production [58]. Stomatal conductance, CO2 penetration, membrane electron transfer rate, photosynthesis, and carboxylation efficiency are hampered by drought, and this results in the production of ROS, which triggers oxidative damage. Exogenous supply of GSH attenuated drought stress in plants and was associated with enhanced photosynthesis as well as chlorophyll content and the activity of antioxidant enzymes [59].
GST (glutathione S-transferase) overexpression in Arabidopsis thaliana has a signaling function and controls plant growth by sustaining GSH pools. In comparison to the wild type, the mutated species atgstu17 produced more GSH and ABA. Additionally, adding exogenous GSH into wild-type plants increased their ABA concentration, produced a phenotype comparable to that of the variant, and improved their ability to withstand drought. The phytohormone ABA, which regulates stomatal aperture, inhibits transpiration rate, and regulates germination, was increased by GSH treatment [60].
In Ctenanthe setosa (Marantaceae), drought stress led to leaf rolling; this leaf rolling is regarded as an adaptability associated with increased GSH content as well as reduced GSSG concentration. The AsA–GSH cycle proteins and GSH levels were linked to the elimination of ROS. The stabilization of leaf moisture content was likewise linked to a higher GSH content, suggesting that it may play a role in preventing leaf rolling [61].

5. GSH Interaction with Phytohormones

Phytohormones such as ABA, SA, ET, and JA—which are fundamental for plant development regulation—are, by and large, available in near to the ground fixations but are also important for the improvement, generation, and endurance of plants, in addition to their roles as signaling molecules. Adjustment in phytohormonal concentrations under environmental stresses prompts an intricate crosstalk that assists the plants in undertaking the necessary versatile responses [62][63].

In plants, for the improvement of environmental stresses, the past studies on proteo-genomics additionally settled the GSH interchange in the company of ABA, along with SA [64][65]. In any case, at the transcriptional level, the outcome of phytohormones lying on GSH is still under investigation. At the transcriptional level, the current study focuses on illustrating the relationship between GSH and numerous phytohormones in samples of Arabidopsis with altered GSH content, such as the GSH-exhausted mutant, alongside the wild-type Col-0, the enhanced pad2-1 (treated with JA, SA, ABA, and ET), and the transgenic AtECS1 line with improved GSH content. 

Exogenous SA might, therefore, be used to mimic the state of plants after they have been exposed to biotic and abiotic stimuli that have resulted in increased endogenous SA levels. After SA treatment, the existence of enhanced GSH levels in AtECS1 may accordingly be worthwhile, as articulation of SA-interceded PR gene expression is caused by it, in contrast with the mutant plants and wild-type plants. Discernibly, the acceptance of the genes was not as substantial in pad2-1 in contrast with wild-type plants. In this way, GSH is found to be fundamental for plants in order to confer the resistance towards stress; furthermore, the upgraded GSH via SA signaling may provide protection against stress, as proven in transgenic tobacco from a past examination, which triggers the overexpressing γ-ECS [66].

6. Crosstalk between GSH and Jasmonate

Cross-resilience is the imposed resistance to extra abiotic and biotic challenges after focusing on a specific oxidative stress, and it is a limitless protective mechanism in higher plants. Pseudomonas syringae becomes impervious when Arabidopsis is treated to ozone in advance [67]. The pre-exposure of tobacco to ozone and ultra-violet light initiated protection from tobacco mosaic infection [68]. Various reports showed H2O2-prompted stress resistance [69][70]. Tobacco exhibited JA-actuated cross-resilience as well as ozone stress injuries [71]. The cross-resistance induced by JA is clarified by after-effects of upregulated JA-initiated metabolic genes of GSH. JA unequivocally invigorated gene expressions for GSH reuse and synthesis, conceivably prompting upgraded GSH synthesis, giving assurance towards ozone as well as towards oxidative stress.
Externally applied jasmonates significantly increased transcript modifications, although, under these conditions, no increase in GSH level was seen. GSH homeostasis remains a promising avenue of research and is expected to cover various applications. When there is zero GSH interest, if at that time JA improves the limit with respect to GSH synthesis, when a life form is subjected to oxidative stress, GSH synthesis is predicted to be quicker and more sensitive. [72] recommended that different regulatory “hardware” be engaged for signals of oxidative stress for the purpose of its detection and preparation. The signals originating from various oxidative stress events are frequency-modulated towards the nucleus, where gene expression is initiated, which determines cascade events. In both biotic and abiotic stressors, ROS, GSH, and redox status were hypothesized as focal segments of signal transmission [70]. In light of the fact that the results do not support reactive oxygen as measured by H2O2 decrease or perhaps the redox potential as measured by the GSH/GSSG ratio as signals framework, under oxidative stress, it is unclear if these putative signal molecules affect the outflow of GSH metabolic genes [70].

7. GSH interaction with Salicylic Acid

Plants experience a wide variety of stresses for the duration of their life in today’s threatening climate. To conquer these unfavorable circumstances, plants employ an assortment signaling molecules. The currently identified molecules are ROS, ABA, SA, ET, and JA, which are used by plants to combat different natural stress circumstances. Over the last two decades, GSH has acquired significance and has become an important molecule for plant scientists, particularly in the field of natural ecological stress organization. Albeit the role of GSH in safeguarding plants has been known for quite some time, a shortage of data still exists; furthermore, in regard to how the system of GSH partakes in this perplexing situation, the investigation shows an interchange in GSH by means of different signal-producing particles such as ABA, SA, and ET, utilizing genetic engineering to deal with, create, and build up transgenic tobacco, which is associated with overexpressing γ-ECS, resistance potential due to biotic/abiotic stresses, and improved GSH concentrations. Transcriptomic profiling distinguished genes as well as proteins identified with ET. SA was also associated with the potential related to stress resistance [73].
In plants, in responsive mechanisms instigated from different microbes, SA acts as a significant signaling molecule which plays a fundamental job [74]. Ongoing information points to the fact that, for regulating plant reactions towards numerous environmental stresses, SA additionally plays significant roles in response to environmental stresses include chilling, heat, salinity, and drought stresses. Conversely, abiotic resistance mediated through SA remains underappreciated, and investigations on SA-mediated abiotic resilience has primarily been conducted at the physical level. SA may have acted as a scavenger for eliminating ROS created during abiotic stress [75].
Antioxidant enzymatic frameworks (for example, peroxidase (POD), superoxide dismutases (SOD), as well as catalase (CAT)) as well as substances such as GSH and AsA have been linked to protection from ROS induced through stress conditions such as salt stress [76][77]. Earlier studies have shown that, SA strikingly increased AsA along with GSH levels as well as the gene that encodes the AsA–GSH cycle and its enzyme under cold stress conditions in maize, cucumber and rice, as well as in eggplant; researchers concluded that SA-prompted cold resistance has a significant role in the AsA–GSH cycle [78][79]. Various plant types have evolved immune processes to various biotic and abiotic stresses [80]. 

8. GSH Defense Enzymes in Crops

It has been suggested that the alkylation of the cysteine residue in GSH, proceeded by dissociation and oxidation to create alkenyl cysteine sulphoxide, is the first step in the production of taste precursors [81]. The catalytic activity of several GSH-dependent enzymes, such as GSTs and glyoxalase-I, use the tripeptide GSH as a detoxifying agent for both endogenous and exogenous toxins. In comparison, L-cystine conjugates are quickly metabolized in the vacuole from GSH conjugates, which are created by the catalytic properties of GSTs [82]. Alliinase or other such enzymes then proceed to metabolize cysteine conjugates to thiol and other related compounds in the cytosol following their efflux from the vacuole [83]. All of these events imply that GSTs, glyoxalase-I, and alliinase are interconnected. While analyzing the three enzymes’ activity in soluble vegetable extracts, a relationship between them was determined. The greatest GST activity was observed in onions, and then in Western blotting, a broad band for presumptive GST activity was recognized by anti-CmGSTF1 antiserum. The dissolved extraction, meanwhile, displayed the highest specified level of activity for onion glyoxalase-I, suggesting that the band may have partially been caused by the enzyme.
Detoxifying enzymes such as GSTs and glyoxalase-I serve a purpose for GSH. As a result, onion bulbs should exhibit the highest levels of these enzymes’ activity, which may indicate a connection between the two enzymes. Additionally, alliinase, a separate type of enzyme whose activity is relevant to sulfur compounds formed from GSH, demonstrated the highest degree of activity in onion bulbs [81]. The primary role of GSTs is the detoxification of endogenous and herbicidal toxins; hence, the presence of proteins in vegetables may improve food quality. Food quality may be connected with glyoxalase enzymes which detox harmful methylglyoxal.

9. GSH Role in Root Architecture and Root-Derived Changes in Shoots

In addition to modulating physiological and metabolic functioning in plant’s foliar parts, GSH takes part in modifying root traits and/or root-to-shoot signaling, thereby affecting shoot attributes. GSH’s involvement in root development is prevalent but its functions are poorly understood. Suppression in root growth, structural changes (length and cell division) in root apical meristem, and abnormalities in lateral root formation were observed when plants were treated with the GSH biosynthesis inhibitor buthionine sulfoximine (BSO) and Arabidopsis mutants lacking GSH biosynthesis (cad2, rax1, and rml1) [84]. The molecular mechanisms of GSH action were studied, and it was discovered that GSH deficiency affected the total ubiquitination of proteins and inhibited the transcriptional activation of early auxin-responsive genes as well as the auxin-related, ubiquitination-dependent degradation of Aux/IAA proteins. The ROS control of GSH, GSH’s active participation in cell proliferation, and GSH’s interactions with auxin suggest that GSH may modulate root development under stress conditions [85].

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Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Gyanendra Kumar Rai
,
Pradeep Kumar
,
Sadiya M. Choudhary
,
Hira Singh
,
Komal Adab
,
Rafia Kosser
,
Isha Magotra
,
Ranjeet Ranjan Kumar
,
Monika Singh
,
Rajni Sharma
,
Giandomenico Corrado
,
Youssef Rouphael
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Update Date: 07 Apr 2023
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