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Antioxidant Potential of Glutathione and Crosstalk with Phytohormones: Comparison
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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).
).
/media/item_content/202304/642f7e9f04061plants-12-01133-g001.png
/media/item_content/202304/642f7d1cd8b84plants-12-01133-g001.png
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]. /media/item_content/202304/642f7d35e3608plants-12-01133-g002.png
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].
/media/item_content/202304/642f7d5617529plants-12-01133-g003.png
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.
/media/item_content/202304/642f7d6e8239bplants-12-01133-g004.png
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].

References

  1. Deneke, S.M. Thiol-based antioxidants. Curr. Top. Cell. Regul. 2001, 36, 151–180.
  2. Noctor, G.; Mhamdi, A.; Chaouch, S.; Han, Y.; Neukermans, J.; Marquez-Garcia, B.; Queval, G.; Foyer, C.H. Glutathione in plants: An integrated overview. Plant Cell Environ. 2012, 35, 454–484.
  3. Canter, L.W. Environmental Impact of Agricultural Production Activities, 1st ed.; CRC Press: Boca Ration, FL, USA, 2018; p. 400.
  4. Cook, D.; Fowler, S.; Fiehn, O.; Thomashow, M.F. A prominent role for the CBF cold response pathway in configuring the lowtemperature metabolome of Arabidopsis. Proc. Natl. Acad. Sci. USA 2004, 101, 15243–15248.
  5. Yadav, S.K. Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot. 2010, 76, 167–179.
  6. Fatma, M.; Iqbal, N.; Sehar, Z.; Alyemeni, M.N.; Kaushik, P.; Khan, N.A.; Ahmad, P. Methyl jasmonate protects the PS II system by maintaining the stability of chloroplast D1 protein and accelerating enzymatic antioxidants in heat-stressed wheat plants. Antioxidants 2021, 10, 1216.
  7. Hasanuzzaman, M.; Bhuyan, M.H.M.B.; Zulfiqar, F.; Raza, A.; Mohsin, S.M.; Mahmud, J.A.; Fujita, M.; Fotopoulos, V. Reactive oxygen species and antioxidant defence in plants under abiotic stress: Revisiting the crucial role of a universal defence regulator. Antioxidants 2020, 9, 681.
  8. Hasanuzzaman, M.; Mahmud, J.A.; Anee, T.I.; Nahar, K.; Islam, M.T. Drought stress tolerance in wheat: Omics approaches in understanding and enhancing antioxidant defense. In Abiotic Stress-Mediated Sensing and Signaling in Plants: An Omics Perspective; Zargar, S.M., Zargar, M.Y., Eds.; Springer: Singapore, 2018; pp. 267–307.
  9. Nahar, K.; Rhaman, M.S.; Parvin, K.; Bardhan, K.; Marques, D.N.; García-Caparrós, P.; Hasanuzzaman, M. Arsenic-induced oxidative stress and antioxidant defense in plants. Stresses 2022, 2, 179–209.
  10. Davies, P.J. The Plant Hormones: Their nature, occurrence and functions. In Plant Hormones: Biosynthesis, Signal Transduction, Action! Davies, P.J., Ed.; Springer Science & Business Media Press: New York, NY, USA, 2004; pp. 1–15.
  11. Fleet, C.; Williams, M.E.; Gibberellins. Teaching Tools in plant biology: Lecture notes. Plant Cell 2011, 110. Available online: www.plantcell.org/cgi/doi/101105/tpc (accessed on 5 November 2022).
  12. Went, F. Auxin, the plant growth-hormone Avena sativa. Bot. Rev. 1935, 1, 162–182.
  13. Gomez-Roldan, V.; Fermas, S.; Brewer, P.B.; Puech-Pagès, V.; Dun, E.A.; Pillot, J.-P.; Letisse, F.; Matusova, R.; Danoun, S.; Portais, J.-C.; et al. Strigolactone inhibition of shoot branching. Nature 2008, 455, 189–194.
  14. Bari, R.; Jones, J.D. Role of plant hormones in plant defence responses. Plant Mol. Biol. 2009, 69, 473–488.
  15. Zhang, J.; Jia, W.; Yang, J.; Ismail, A.M. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res. 2006, 97, 111–119.
  16. Meister, A. Glutathione biosynthesis and its inhibition. In Biothiols Part B: Thiols in Signal Transduction and Gene Regulation; Packer, L., Ed.; Academic Press: San Diego, CA, USA, 1995; pp. 26–30.
  17. Hell, R.; Bergmann, L. c-glutamylcysteine synthetase in higher plants: Catalytic properties and subcellular localization. Planta 1990, 180, 603–612.
  18. Wachter, A.; Wolf, S.; Steininger, H.; Bogs, J.; Rausch, T. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: Implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J. 2005, 41, 15–30.
  19. Galant, A.; Preuss, M.L.; Cameron, J.; Jez, J.M. Plant glutathione biosynthesis: Diversity in biochemical regulation and reaction products. Front. Plant Sci. 2011, 2, 45.
  20. Hicks, L.M.; Cahoon, R.E.; Bonner, E.R.; Rivard, R.S.; Sheffield, J.; Jez, J.M. Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 2007, 19, 2653–2661.
  21. Zechmann, B.; Muller, M. Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma 2010, 246, 15–24.
  22. Pasternak, M.; Lim, B.; Wirtz, M.; Hell, R.; Cobbett, C.S.; Meyer, A.J. Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J. Cell Mol. Biol. 2008, 53, 999–1012.
  23. Mahmood, Q.; Ahmad, R.; Kwak, S.S.; Rashid, A.; Anjum, N.A. Ascorbate and glutathione: Pro-tectors of plants in oxidative stress. In Ascorbate–Glutathione Pathway and Stress Tolerance in Plants; Springer: New, York, NY, USA, 2010; pp. 209–229.
  24. Foyer, C.H.; Noctor, G. Redox homeostasis and antioxidant signalling: A metabolic link between stress perception and physiological responses. Plant Cell 2005, 17, 1866–1875.
  25. Navrot, N.; Collin, V.; Gualberto, J.; Gelhaye, E.; Hirasawa, M.; Rey, P.; Knaff, D.B.; Issakidis, E.; Jacquot, J.P.; Rouhier, N. Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol. 2006, 142, 1364–1379.
  26. Rausch, T.; Gromes, R.; Liedschulle, V.; Muller, I.; Bogs, J.; Galovic, V.; Wachter, A. Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biol. 2007, 9, 565–572.
  27. Yadav, S.K.; Singla-Pareek, S.L.; Sopory, S.K. An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metab. Drug Interact 2008, 23, 51–68.
  28. Lian, G.; Gnanaprakasam, J.R.; Wang, T.; Wu, R.; Chen, X.; Liu, L.; Shen, Y.; Yang, M.; Yang, J.; Chen, Y.; et al. Glutathione de novo synthesis but not recycling process coordinates with glutamine catabolism to control redox homeostasis and directs murine T cell differentiation. eLife 2018, 7, e36158.
  29. Deponte, M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta (BBA)-Gen. Subj. 2013, 1830, 3217–3266.
  30. Ruegsegger, A.; Brunold, C. Effect of cadmium on c-glutamylcysteine synthesis in maize seedlings. Plant Physiol. 1992, 99, 428–433.
  31. Klapheck, S. Homoglutathione: Isolation, quantification and occurrence in legumes. Physiol. Plant 1988, 74, 727–732.
  32. Klapheck, S.; Chrost, B.; Starke, J.; Zimmermann, H. c-Glutamylcysteinylserine–a new homologue of glutathione in plants of the family Poaceae. Bot Acta 1991, 105, 174–179.
  33. Kocsy, G.; Galiba, G.; Brunold, C. Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol. Plant 2001, 113, 158–164.
  34. Noctor, G.; Foyer, C.H. Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49, 249–279.
  35. Banerjee, A.; Roychoudhury, A. Abiotic stress, generation of reactive oxygen species, and their consequences: An overview. In Revisiting the Role of Reactive Oxygen Species (ROS) in Plants: ROS Boon or Bane for Plants? Singh, V., Singh, S., Tripathi, D., Prasad, S.M., Chauhan, D.K., Eds.; Wiley: New York, NY, USA, 2018; pp. 23–50.
  36. Banerjee, A.; Roychoudhury, A. Effect of salinity stress on growth and physiology of medicinal plants. In Medicinal Plants and Environmental Challenges; Ghorbanpour, M., Varma, A., Eds.; Springer International Publishing AG: Cham, Switzerland, 2018; pp. 177–188.
  37. Schmitt, F.J.; Renger, G.; Friedrich, T.; Kreslavski, V. Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim. Biophys. Acta (BBA)-Bioenerg. 2014, 1837, 385–848.
  38. Zaffagnini, M.; Bedhomme, M.; Lemaire, S.D.; Trost, P. The emerging roles of protein glutathionylation in chloroplasts. Plant Sci. 2012, 185, 86–96.
  39. Banerjee, A.; Roychoudhury, A. The gymnastics of epigenomics in rice. Plant Cell Rep. 2018, 37, 25–49.
  40. Banerjee, A.; Roychoudhury, A. Abscisic-acid-dependent basic leucine zipper (bZIP) transcription factors in plant abiotic stress. Protoplasma 2017, 254, 3–16.
  41. Banerjee, A.; Roychoudhury, A. Role of Glutathione in Plant Abiotic Stress Tolerance. In Reactive Oxygen, Nitrogen and Sulfur Species in Plants; Hasanuzzaman, M., Fotopoulos, V., Nahar, K., Fujita, M., Eds.; Wiley: New York, NY, USA, 2019; Volume I, pp. 159–172.
  42. Koffler, B.E.; Luschin-Ebengreuth, N.; Stabentheiner, E.; Singla, M. Compartment specific response of antioxidants to drought stress in Arabidopsis. Plant Sci. 2014, 227, 133–144.
  43. Queval, G.; Jaillard, D.; Zechmann, B.; Noctor, G. Increased intra-cellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ. 2011, 34, 21–32.
  44. Zechmann, B. Compartment-specific importance of glutathione during abiotic and biotic stress. Front. Plant Sci. 2014, 5, 566.
  45. Ding, X.; Jiang, Y.; He, L.; Zhou, Q.; Yu, J.; Hui, D.; Huang, D. Exogenous Glutathione Improves High Root-Zone Temperature Tolerance by Modulating Photosynthesis, Antioxidant and Osmolytes Systems in Cucumber Seedlings. Sci. Rep. 2016, 6, 35424.
  46. Yao, M.; Ge, W.; Zhou, Q.; Zhou, X.; Luo, M.; Zhao, Y.; Wei, B.; Ji, S. Exogenous Glutathione Alleviates Chilling Injury in Postharvest Bell Pepper by Modulating the Ascorbate-Glutathione (AsA-GSH) Cycle. Food Chem. 2021, 352, 129458.
  47. Singh, H.; Kumar, P.; Chaudhary, S.; Edelstein, M. Tomato Grafting: A Global Perspective. HortSci 2017, 52, 1328–1336.
  48. Ruelland, E.; Vaultier, M.N.; Zachowski, A.; Hurry, V. Cold signalling and cold acclimation in plants. Adv. Bot. Res. 2009, 49, 35–150.
  49. Gul, N.; Ahmad, P.; Wani, T.A.; Tyagi, A.; Aslam, S. Glutathione improves low temperature stress tolerance in Pusa Sheetal cultivar of Solanum lycopersicum. Sci. Rep. 2022, 12, 1–13.
  50. Rehman, H.U.; Alharby, H.F.; Bamagoos, A.A.; Abdelhamid, M.T.; Rady, M.M. Sequenced Application of Glutathione as an Antioxidant with an Organic Biostimulant Improves Physiological and Metabolic Adaptation to Salinity in Wheat. Plant Physiol. Biochem. 2021, 158, 43–52.
  51. Alamri, S.; Kushwaha, B.K.; Singh, V.P.; Siddiqui, M.H.; Al-Amri, A.A.; Alsubaie, Q.D.; Ali, H.M. Ascorbate and Glutathione Independently Alleviate Arsenate Toxicity in Brinjal but Both Require Endogenous Nitric Oxide. Physiol. Plant. 2021, 173, 276–286.
  52. Marrs, K.A. The functions and regulation of glutathione S transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47, 127–158.
  53. Thangavel, P.; Long, S.; Minocha, R. Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension cultures under cadmium and zinc stress. Plant Cell Tissue Organ. Cult. 2007, 88, 201–216.
  54. Schützendübel, A.; Schwanz, P.; Teichmann, T.; Gross, K.; Langenfeld-Heyser, R.; Godbold, D.L.; Polle, A. Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol. 2001, 127, 887–898.
  55. Schutzendubel, A.; Polle, A. Plant responses to abiotic stresses: Heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 2002, 53, 1351–1365.
  56. Bovet, L.; Feller, U.; Martinoia, E. Possible involvement of plant ABC transporters in cadmium detoxification: A cDNA sub-microarray approach. Environ. Int. 2005, 31, 263–267.
  57. Rauser, W.E. Phytochelatins and related peptides-structure, biosynthesis, and function. Plant Physiol. 1995, 109, 1141–1149.
  58. Kumar, P.; Rouphael, Y.; Cardarelli, M.; Colla, G. Vegetable grafting as a tool to improve drought resistance and water use efficiency. Front. Plant Sci. 2017, 8, 1130.
  59. Koh, Y.S.; Wong, S.K.; Ismail, N.H.; Zengin, G.; Duangjai, A.; Saokaew, S.; Phisalprapa, P.; Tan, K.W.; Goh, B.H.; Tang, S.Y. Mitigation of Environmental Stress-Impacts in Plants: Role of Sole and Combinatory Exogenous Application of Glutathione. Front. Plant Sci. 2021, 12, 791205.
  60. Chen, J.H.; Jiang, H.W.; Hsieh, E.J.; Chen, H.Y.; Chien, C.T.; Hsieh, H.L.; Lin, T.P. Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol. 2012, 158, 340–351.
  61. Saruhan, N.; Terzi, R.; Saglam, A.; Kadioglu, A. The relationship between leaf rolling and ascorbate-glutathione cycle enzymes in apoplastic and symplastic areas of Ctenanthe setosa subjected to drought Stress. Biol. Res. 2009, 42, 315–326.
  62. Grant, M.; Jones, J. Hormone (dis)harmony moulds plant health and disease. Science 2009, 324, 750–752.
  63. Pieterse, C.M.; Leon-Reyes, A.; Vander Ent, S.; Van Wees, S.C. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 2009, 5, 308–316.
  64. Ghanta, S.; Datta, R.; Bhattacharyya, D.; Kumar, D.; Sinha, R.; Hazra, S.; Mazumdar, A.B. Chattopadhyay, Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. J. Plant Physiol. 2014, 171, 940–950.
  65. Kumar, D.; Datta, R.; Hazra, S.; Sultana, A.; Mukhopadhyay, R.; Chattopadhyay, S. Transcriptomic profling of Arabidopsis thaliana mutant pad2.1 in response to combined cold and osmotic stress. PLoS ONE 2015, 10, e0122690.
  66. Ghanta, S.; Bhattacharyya, D.; Sinha, R.; Banerjee, A.; Chattopadhyay, S. Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway. Planta 2011, 233, 895–910.
  67. Sharma, Y.K.; León, J.; Raskin, I.; Davis, K.R. Ozoneinduced responses in Arabidopsis thaliana—The role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc. Natl. Acad. Sci. USA 1996, 93, 5099–5104.
  68. Yalpani, N.; Enyedi, A.J.; León, J.; Raskin, I. Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 1994, 193, 372–376.
  69. Prasad, T.K.; Anderson, M.D.; Stewart, C.R. Localization and characterization of peroxidases in the mitochondria of chilling-acclimated maize seedlings. Plant Physiol. 1995, 108, 1597–1605.
  70. Foyer, C.H.; Lopez-Delgado, H.; Dat, J.F.; Scott, I.M. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol. Plant 1997, 100, 241–254.
  71. Örvar, B.L.; McPherson, J.; Ellis, B.E. Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J. 1997, 11, 203–212.
  72. Hausladen, A.; Alscher, R.G. Glutathione. In Antioxidants in Higher Plants; Alscher, R., Ed.; CRC Press: Boca Raton, FL, USA, 1993; pp. 1–30.
  73. Chattopadhyay, S. Interplay among glutathione, salicylic acid, and ethylene to combat environmental stresses. In Drought Stress Tolerance in Plants; Springer: Cham, Switzerland, 2016; Volume 1, pp. 145–161.
  74. Snyman, M.; Cronjé, M.J. Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. J. Exp. Bot. 2008, 59, 2125–2132.
  75. Horváth, E.; Szalai, G.; Janda, T. Induction of abiotic stress tolerance by salicylic acid signaling. J. Plant Growth Regul. 2007, 26, 290–300.
  76. Carillo, P.; Mastrolonardo, G.; Nacca, F.; Parisi, D.; Verlotta, A.; Fuggi, A. Nitrogen metabolism in durum wheat under salinity: Accumulation of proline and glycine betaine. Funct. Plant Biol. 2008, 35, 412–426.
  77. Carillo, P.; Parisi, D.; Woodrow, P.; Pontecorvo, G.; Massaro, G.; Annunziata, M.G.; Fuggi, A.; Sulpice, R. Salt induced accumulation of glycine betaine is inhibited by high light in durum wheat. Funct. Plant Biol. 2011, 38, 139–150.
  78. Kang, H.M.; Saltveit, M.E. Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol. Plant. 2002, 115, 571–576.
  79. Chen, S.; Liu, Z.; Cui, J.; Ding , J.; Xia, X.; Liu, D.; Yu, J. Alleviation of chilling-induced oxidative damage by salicylic acid pretreatment and related gene expression in eggplant seedlings. Plant Growth Regul. 2011, 65, 101–108.
  80. Wang, G.; Hui, Z.; Li, F.; Zhao, M.; Zhang, J.; Wang, W. Improvement of heat and drought photosynthetic tolerance in wheat by over accumulation of glycine betaine. Plant Biotechnol. Rep. 2010, 4, 213–222.
  81. Granroth, B. Biosynthesis and decomposition of cysteine derivatives in onion and other Allium species. Ann. Acad. Sci. Fenn. Chem. 1970, 154, 71.
  82. Coleman, J.O.D.; Randall, R.; Blakeklaff, M.M.A. Detoxification of xenobiotics in plant cells by glutathione conjugation and vacuolar compartmentalization: A fluorescent assay using monochlorobimane. Plant Cell Environ. 1997, 20, 449–460.
  83. Kiddle, G.A.; Bennett, R.N.; Hick, A.J.; Wallsgrove, R.M. C-Slyase activities in leaves of crucifers and non-crucifers, and the characterization of three classes of C-S lyase activities from oil seed rape (Brassica napus L.). Plant Cell Environ. 1999, 22, 433–445.
  84. Gao, H.; Yu, C.; Liu, R.; Li, X.; Huang, H.; Wang, X.; Zang, C.; Jiang, N.; Li, X.; Cheng, S.; et al. The Glutathione S-Transferase PtGSTF1 improve Biomass Production and Salt Tolerance through Regulating Xylem Cell Proliferation, Ion Homeostasis and Reactive Oxygen Species Scavenging in Poplar. Int. J. Mol. Sci. 2022, 23, 11288.
  85. Pasternak, T.; Palme, K.; Paponov, I.A. Glutathione enhances auxin sensitivity in Arabidopsis roots. Biomolecules 2020, 10, 1550.
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