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MINI REVIEWpublished: 07 June 2018doi: 10.3389/fpls.2018.00751Edited by:Kendal Hirschi,Baylor College of Medicine,United StatesReviewed by:Toshiro Shigaki,The University of Tokyo, JapanRaju Kandel,Arizona State University, United States*Correspondence:Smita Kumarsmitabiochem@gmail.comSpecialty section:This article was submitted toPlant Traffic and Transport,a section of the journalFrontiers in Plant ScienceReceived: 15 February 2018Accepted: 16 May 2018Published: 07 June 2018Citation:Kumar S and Trivedi PK (2018)Glutathione S-Transferases: Rolein Combating Abiotic StressesIncluding Arsenic Detoxificationin Plants. Front. Plant Sci. 9:751.doi: 10.3389/fpls.2018.00751Glutathione S-Transferases: Role inCombating Abiotic StressesIncluding Arsenic Detoxification inPlantsSmita Kumar* and Prabodh K. TrivediCouncil of Scientific and Industrial Research–National Botanical Research Institute, Lucknow, IndiaArsenic (As), naturally occurring metalloid and a potential hazardous material, is foundin low concentrations in the environment and emerges from natural sources andanthropogenic activities. The presence of As in ground water, which is used for irrigation,is a matter of great concern since it affects crop productivity and contaminates foodchain. In plants, As alters various metabolic pathways in cells including the interactionof substrates/enzymes with the sulfhydryl groups of proteins and the replacementof phosphate in ATP for energy. In addition, As stimulates the generation of freeradicals and reactive oxygen species (ROS), resulting in oxidative stress. GlutathioneS-transferases (GSTs) quench reactive molecules with the addition of glutathione(GSH) and protect the cell from oxidative damage. GSTs are a multigene family ofisozymes, known to catalyze the conjugation of GSH to miscellany of electrophilicand hydrophobic substrates. GSTs have been reported to be associated with plantdevelopmental processes and are responsive to multitude of stressors. In past, severalstudies suggested involvement of plant GST gene family in As response due to therequirement of sulfur and GSH in the detoxification of this toxic metalloid. This reviewprovides updated information about the role of GSTs in abiotic and biotic stresses withan emphasis on As uptake, metabolism, and detoxification in plants. Further, the geneticmanipulations that helped in enhancing the understanding of the function of GSTs inabiotic stress response and heavy metal detoxification has been reviewed.Keywords: abiotic stress, arsenic, detoxification, glutathione, heavy metals, oxidative stressINTRODUCTIONArsenic (As) is a ubiquitous environmental contaminant, present in earth’s crust and naturally inrocks, soil, water, air, plants, and animals (Kumar et al., 2015b). Increased level of As in soil anddrinking water has been identified in numerous countries across the world where As in drinkingwater exceeds the permissible limit established by World Health Organization (Sinha et al., 2013).In addition to human activities such as use of agricultural pesticides, chemicals, coal-fired powerplants, smelting, and mining, most of the As flux comes through natural sources including volcanicFrontiers in Plant Science | www.frontiersin.org 1 June 2018 | Volume 9 | Article 751Kumar and Trivedi Plant Glutathione S-Transferase and Stressaction, forest fires, erosion of rocks, and low-temperaturevolatilization (Neumann et al., 2010). Arsenic exists in differentoxidation states and forms, of which inorganic form ofgeological origin is more toxic and present in ground watercausing contamination of drinking water around the world(Lizama et al., 2011). Arsenic is a food chain contaminantand leads to severe health problems in the humans (Zhaoet al., 2011). Due to human health endangerment and lossin plant productivity, several studies have been carried out tounderstand the mechanisms/processes involved in As uptake andtranslocation in plant tissues. In addition, the intricate nexusof signaling pathways controlling heavy metal stress tolerancein plants have been studied (Kumar and Trivedi, 2016a). Inpast, using genome-wide expression analysis, several key Asresponsive genes related to the molecular mechanisms underlyingAs uptake and detoxification have been identified (Chakrabartyet al., 2009; Kumar and Trivedi, 2016b; Lindsay and Maathuis,2017) and characterized.During heavy metal exposure, phytochelatins (PCs) are themost copious class of non-protein thiols (NPTs) synthesizedutilizing both cysteine (Cys) and GSH (Hasan et al., 2017).This in turn, increases the sulfur requirement as observed bygeneral induction of pathways related to sulfur metabolismduring exposure to heavy metals (Kumar et al., 2011, 2015a; Leaoet al., 2014; Dixit et al., 2015a,b, 2016; Hernández et al., 2015;Khare et al., 2017). Several regulatory factors including smallRNAs have also been documented to be involved in regulatingplant As stress response (Kumar et al., 2017). Therefore, currentunderstanding of the genes participating in heavy metal stressresponse has put forth an area of research to understand themechanisms and regulation of oxidative stress in plants. In thiscontext, glutathione S-transferases (GSTs) finds an importantmention as members of this family quench reactive moleculesand catalyze the conjugation of GSH to an array of hydrophobicand electrophilic substrates, thus, protecting the cell fromoxidative burst. Members of this family were first discoveredfor their potential of metabolizing an array of toxic exogenouscompounds, i.e., xenobiotics via GSH conjugation (Cumminset al., 2011). GSTs have been implicated in several cellularprocesses (Chronopoulou and Labrou, 2009; Nianiou-Obeidatet al., 2017). Studies suggest that GSTs could protect the plantsfrom different abiotic stresses (Ding et al., 2017) including heavymetal stress (Zhang et al., 2013), and damage of ultra-violet (UV)radiations (Liu and Li, 2002).Though, the involvement of members of GST family has beenreported in plant development and abiotic stresses (NianiouObeidat et al., 2017), limited information is available aboutthe involvement of this family in combating As stress. Amongdifferent classes of GSTs, role of Lambda class GSTs has beenreported in As stress response (Kumar et al., 2013a,b) inaddition to plant growth and development. Thus, functionalcharacterization and analysis of regulatory aspects of geneexpression of GST gene family members could help inenhancing the understanding about their role in As responseand detoxification as well as evolving strategies for developingAs tolerant and As-free crops through biotechnological tools infuture.GLUTATHIONE S-TRANSFERASEThe GSTs are a super family of enzymes that are notable for theirrole in phase II detoxification reactions. It is well documentedthat GSTs conjugate GSH to an array of electrophilic compoundsof exogenous and endogenous origins (Cummins et al., 2011).GSTs have been reported in all the organisms including bacteriaand fungi (Frova, 2006; Perperopoulou et al., 2017). In plants,GSTs have been exhaustively studied in terms of herbicidedetoxification and specific members of this family have beenreported to provide tolerance toward herbicide in major cropspecies (Chronopoulou et al., 2017). Studies suggest that GSTssafeguard the cells against chemical-induced toxicity and providetolerance by catalyzing S-conjugation between the thiol groupof GSH and electrophilic moiety in the hydrophobic and toxicsubstrate (Deavall et al., 2012). After conjugation, the conjugateis either sequestered into the vacuoles or are exported from thecells by putative membrane ATP-dependent pump systems.Apart from herbicide detoxification, involvement of GSTsin hormone biosynthesis, tyrosine degradation, and peroxidebreakdown (Oakley, 2011), stress signaling proteins (Loyall et al.,2000), nodule function (Dalton et al., 2009), and non-catalyticallyacting as flavonoid-binding proteins (Mueller et al., 2000) havebeen reported. In recent years, involvement of GSTs in differentprocesses such as modulation of cell signaling kinases, formationand modulation of ion channels, oxidation-reduction reactions,and the post-translational glutathionylation of proteins havebeen outlined (Dixon et al., 2010). The level of functionaldiversification in GSTs makes them remarkable in studying theevolutionary aspects of gene family and opens up an avenue toidentify the multiple roles of GSTs in plant development andresponse to environmental cues.DIFFERENT CLASSES AND CATALYTICMECHANISM OF GSTsThough the classification and nomenclature of GSTs inplants and animals are conundrum, however, they have beendistinctly categorized into three families; cytosolic, microsomal,and mitochondrial GSTs (also referred as kappa-class GSTs)(Figure 1). According to the evolutionary and sequence diversity,microsomal GSTs have been identified to be the integralmembrane proteins and are known as Membrane-AssociatedProteins in Eicosanoid and Glutathione Metabolism (MAPEGs).The cytosolic GSTs are profusely present and have been dividedinto divergent classes based on their genesis, catalytic amino-acidresidue, sequence similarity, and substrate specificity (Labrouet al., 2015). These distinct evolutionary classes include Alpha,Beta, Dehydroascorbate reductases (DHARs), Delta, Epsilon, Mu,Omega, Pi, Phi, Sigma, Tau, Theta, and Zeta. Among theseclasses, only six classes have been functionally characterized inplants (Figure 1). The identified classes in plants include DHARs,Elongation factor 1 gamma (EF1G), Lambda (GSTL), Phi (GSTF),Tau (GSTU), Tetrachlorohydroquinone dehalogenase (TCHQD),Theta (GSTT), and Zeta (GSTZ) (Mohsenzadeh et al., 2011).Among different classes, Phi and Tau class GSTs are plant-specificFrontiers in Plant Science | www.frontiersin.org 2 June 2018 | Volume 9 | Article 751Kumar and Trivedi Plant Glutathione S-Transferase and StressFIGURE 1 | Different classes of glutathione S-transferase.and predominantly present, whereas the smaller Theta and Zetaclasses, having restricted xenobiotic activity, are also found inanimals. The soluble form of GSTs has been investigated toexist as dimers. The active site in each subunit is known tobe composed of two definite functional regions. One region istermed as G-site, which is hydrophilic in nature and binds thephysiological substrate GSH, and another region is the H-site,which assists in binding of electrophilic substrates by providinga hydrophobic environment (Frova, 2003).GSTs AND STRESS RESPONSEGlutathione S-transferases are known to express at differentstages of plant development. Studies suggest that expression ofGSTs is induced by various environmental stimuli, includingbiotic stresses such as fungal elicitors and pathogen attack (Chenet al., 2013), abiotic stresses such as cold (Kim et al., 2011),drought (Xu et al., 2015), H2O2 (Levine et al., 1994), hormonetreatments (Wagner et al., 2002; Xu et al., 2002), heavy metals(Dubey et al., 2010; Rai et al., 2011), phosphate starvation (Ezakiet al., 1995; Shukla et al., 2015), salt (Jia et al., 2016), andwounding (Reymond et al., 2000). To study the stress responseof GSTs at transcriptional level in plants, a comprehensive studywas carried out on Arabidopsis cell-suspension culture. Analysissuggested an early stress induced changes in the expressionof genes with functional redundancy and precise involvementof GSTs in the oxidative stress protection (Sappl et al., 2009).It has been observed that one member of Arabidopsis Phi classGST (AtGSTF2) is associated with the regulation of bindingand transport of defense-related compounds in planta (Dixonet al., 2011). Also, the over expression of AtGSTF2 has beenfound to provide tolerance toward phenol stress in plants(Xu et al., 2017). In a study, chloroplast antioxidant defensesystem was shown to be enhanced due to increased expressionof genes encoding DHAR and GST enzymes (Martret et al.,2011). In addition, molecular docking of one of the tomatoGST member, SlGSTU5, and ligand suggested that the activity ofSlGSTs could be enhanced by the use of safeners for the purposeof crop improvement and stress defiance (Islam et al., 2017).It has been well documented that GSTs assist in regulatingoxidative stress metabolism. AtGSTU17 has been found toregulate light signaling and modulating different aspects ofplant development (Chen et al., 2012). Also, negative role ofAtGSTU17 toward drought and salt stresses has been determinedby the mutant analysis. Intriguingly, increased accumulation ofABA and GSH inducing resistance toward drought stress hasbeen observed in mutant plants (Chen et al., 2012). Similarly,GmGSTU4 expressing transgenic tobacco plants were observedto provide tolerance toward salt stress and herbicide alachlor.Furthermore, increased production of protective metabolitessuch as trehalose and proline were identified in GmGSTU4expressing transgenic lines in comparison to the wild typeplants under salt stress (Kissoudis et al., 2015). The geneticmanipulation that has been carried out to improve stresstolerance in plants through different classes of GSTs has beensummarized in Table 1. Thus, functional characterization ofdifferent classes of GSTs is an interesting area of research,which could help in developing the crop varieties with improvedresilience toward the range of environmental stresses.GSTs AND HEAVY METAL STRESSGlutathione S-transferases are responsive toward different heavymetals including arsenic. Studies suggest that As induces theFrontiers in Plant Science | www.frontiersin.org 3 June 2018 | Volume 9 | Article 751Kumar and Trivedi Plant Glutathione S-Transferase and StressTABLE 1 | Transgenic plants developed using glutathione S-transferase.S. No. Source Target Manipulation Outcome Reference1. Nicotiana tabacum Nicotiana tabacum Silencing Significantly increased resistance tofungal infection was observedHernández et al., 20092. Nicotiana benthamiana Nicotiana benthamiana Silencing Significant decrease in the viral RNAaccumulationChen et al., 20133. Oryza sativa Oryza sativa Over expression Enhanced germination and growthrate at low temperature and undersubmergenceTakesawa et al., 20024. Lycopersicon esculentum Arabidopsis thaliana Over expression Enhanced resistance toward salt andosmotic stressXu et al., 20155. Oryza sativa Arabidopsis thaliana Over expression Increased tolerance toward salinityand oxidative stress. Reducedsensitivity toward plant hormones,auxin, and abscisic acid.Sharma et al., 20146. Glycine max Arabidopsis thaliana Over expression Enhanced resistance toward saltstressChan and Lam, 20147. Glycine soja Nicotiana tabacum Over expression Increased drought and salt tolerance Ji et al., 20108. Juglans regia Nicotiana tabacum Over expression Enhanced tolerance toward chillingstressYang et al., 20169. Trichoderma virens Nicotiana tabacum Over expression Increased tolerance toward cadmiumstressDixit et al., 201110. Oryza sativa Arabidopsis thaliana Over expression Increased tolerance toward differentabiotic stresses including heavymetals, drought, salt, and cold stressKumar et al., 2013b11. Pyrus pyrifolia Nicotiana tabacum Over expression Increased tolerance toward drought,salt, and cadmium stresses.Liu et al., 201312. Suaeda salsa Oryza sativa Over expression Enhanced resistance toward salt,paraquat, and chilling stressZhao and Zhang, 200613. Limonium bicolor Nicotiana tabacum Over expression Increased tolerance toward salt stress Diao et al., 201114. Glycine max Nicotiana tabacum Over expression Enhanced resistance toward salinitystressKissoudis et al., 201515. Nicotiana tabacum Dianthus superbus Over expression Increased tolerance toward drought,light, and heavy metal stressLim et al., 2005generation of Reactive Oxygen Species (ROS) leading to oxidativestress and lipid peroxidation in plants (Shukla et al., 2018).Arsenic toxicity induces the synthesis of phytochelatins (PCs),produced non-translationally from GSH (Schmöger et al., 2000;Dhankher, 2005). Heavy metal(oid) exposure to plants increasesGSH content, which has been correlated with the feedbackinduction and increased expression of genes encoding membersof GST and glutathione peroxidases (GPX) gene families underAs stress (Shri et al., 2009). PCs make complexes with As, whichis further sequestered into the vacuoles through ABCC1/ABCC2transporters. Involvement of GSTs in As detoxification throughPC synthesis has been summarized in Figure 2. Apart fromAs stress, induction of different classes of GSTs have beenobserved in response to other heavy metals in plants (Sapplet al., 2009; Lin et al., 2013). For example, different membersof Phi class induce on Copper (Cu) and Aluminum (Al)exposure in Arabidopsis (Ezaki et al., 2000). Interestingly, afungus Trichoderma virens GST (TvGST) has been observed toprovide tolerance toward Cadmium (Cd) stress (Dixit et al.,2011). Also, over expression of one member of tobacco Tauclass GST (Nt107) in Dianthus superbus plants unveil increasedCu accumulation in comparison to wild type plants (Lim et al.,2005).Methylation of As is generally regarded as one of themain detoxification mechanism and have a key role in Asgeochemical cycle. Studies have reported that microorganismstransform few inorganic forms of As to organic forms andvice versa by the process of methylation or demethylation(Bentley and Chasteen, 2002). The presence of As resistance(ars) operons have been found in the bacteria and archaea,which provide tolerance toward As stress. A soil bacterium,Arsenicibacter rosenii, has been identified to encode an efficientenzyme for the As methylation and volatilization (Huanget al., 2016). Similarly, heterologous expression of arsM fromRhodopseudomonas palustris has been observed to enhancetolerance toward As(III) stress in E. coli by the conversionof As to methylated forms (Qin et al., 2006). Very recently,genetically engineered Rhizobium-legume symbiont expressingAs(III) S-adenosylmethionine methyltransferase (arsM) genefrom alga Chlamydomonas reinhardtii showed methylation andsubsequently volatilization of As (Zhang et al., 2017). Thesestudies suggest the potential role of legume-rhizobia symbiontsand other engineered bacterium for As bioremediation. Thus,this microbial-mediated transformation of As is an essentialarea of research as it contributes to the global cycling of Asin the environment. The in depth understanding about AsFrontiers in Plant Science | www.frontiersin.org 4 June 2018 | Volume 9 | Article 751Kumar and Trivedi Plant Glutathione S-Transferase and StressFIGURE 2 | Schematic model representing the GST-mediated As detoxification in plants. gGlu, glutamate; Cys, cysteine; gECS, g-glutamylcysteine synthetase; Gly,glycine; GS, glutathione synthetase; GSH, glutathione; X, xenobiotics; GST, glutathione S-transferase; PCS, phytochelatin synthase; PC, phytochelatins; As, arsenic;PC-As, phytochelatin arsenic complex; T, ABCC1/ABCC2 vacuolar transporters.volatilization would provide sustainable ways to detoxify As andreduce contamination.These studies provide a platform to study distinct andoverlapping roles of different members of GST gene family. It willbe interesting to identify the regulatory mechanisms underlyingmolecular and biochemical responses of different classes of GSTs.The modulation in the expression and redundancy of GSTsascertain its enigmatic roles in plant growth and development.LAMBDA CLASS GSTs AND As STRESSNumerous studies have suggested the heterogeneity of GST genefamily with an assertion of diversion of different classes intosub-classes with diverse functions. The diversified functions ofdifferent classes of plant GSTs have been explored but still limitedinformation is available for the involvement of GSTs in Asdetoxification. As per recent reports, members of Lambda classGSTs have been reported to play important role in As stressresponse and detoxification. Genome-wide analysis suggests thepresence of three members from Lambda class in Arabidopsis,poplar, and Triticum aestivum (Lan et al., 2009; Dixon et al.,2011). Very recently, genome-wide analysis identified 90 GSTsin tomato, which were categorized into ten different classes.Among different classes, Tau and Lambda classes were found tobe numerous in tomato in comparison to other plant species.The expression profiling showed up regulation of group of genesin response to different stress conditions (Islam et al., 2017). Inrice, GST multigene family was first analyzed on the basis ofESTs as well as unfinished genomic sequence. This analysis ledto the identification of 59 members of GST gene family (Soranzoet al., 2004). Subsequently, Jain et al. (2010) reanalyzed riceGST gene family through updated annotation and suggested thepresence of 84 members in rice genome. The study showed theirspecificity toward different tissues and stages of plant growthand development in addition to their responsiveness towardhormones and different stress conditions (Jain et al., 2010).However, these analyses did not identify Lambda class (GSTLs)in rice. Later, genome-wide analysis of rice Lambda gene familyidentified three members (OsGSTL1, OsGSTL2, and OsGSTL3),which were named as In2-1 proteins in rice genome database(Kumar et al., 2013a).It has been established that all GSTs exist as dimeric proteinsand have serine in the active site, however, DHARs and Lambdaclass GSTs are monomeric, and possess catalytic cysteine inactive site (Wagner et al., 2002; Dixon et al., 2011). Thisunique characteristic of GSTLs help in the substitution ofamino acid in active site residues forming mixed disulfideswith thiol group rather than promoting formation of reactivethiolate anion of GSH. Another accountability of GSTLs is thereduction of disulfide bonds instead of GSH transfer activity,as found in other GSTs. Due to these structural changes, theunambiguous functions of GSTLs have not been able to decipher.However, specific GSTLs have been reported to be responsive toxenobiotic compounds such as herbicides and pharmaceuticals(Theodoulou et al., 2003; Hu, 2014). In context of identificationand characterization of rice GSTLs, genome-wide expressionanalysis have suggested differential expression of OsGSTLs atvarious stages of plant development as well as under stressconditions (Kumar et al., 2013a). Furthermore, over expressionof OsGSTL2 in Arabidopsis have been discern to enhance the rateof germination and causes early bolting, which explicitly suggestsits involvement in plant growth and development (Kumar et al.,2013b). Moreover, the forbearance of transgenic lines towardFrontiers in Plant Science | www.frontiersin.org 5 June 2018 | Volume 9 | Article 751Kumar and Trivedi Plant Glutathione S-Transferase and Stressdifferent abiotic stresses such as cold, drought, salt, and heavymetals affirms its role in stress tolerance. Remarkable toleranceof transgenic plants toward As stress, attributes its importance inAs detoxification in plants (Kumar et al., 2013b).Another aspect of GSTLs is their association with homeostasisof flavanols. Studies have described that flavonols and theirderivatives are likely the substrate for GSTLs, which tightly bindto these small molecules (Dixon et al., 2011). It has been suggestedthat GSTLs can recycle GSH adducts of oxidized flavonols backto the parent flavonols, maintaining the antioxidant pools. Dueto the involvement of flavonols in biotic and abiotic stresses(Hernandez et al., 2004), it can be proposed that GSTLs playpivotal role in stress response. Interestingly, at subcellular level,different members of GSTLs show differential localization. Fewmembers of Arabidopsis and wheat Lambda class GSTs (AtGSTL1,TaGSTL1, and TaGSTL3) have been identified to be localized incytosol, whereas others (AtGSTL2 and TaGSTL2) are chloroplastlocalized (Dixon et al., 2002). It has also been suggested that themembers, which are localized in cytoplasm are strongly inducedby stress conditions (Theodoulou et al., 2003). Despite of theexhaustive information available about GST super family, still theknowledge about the presence and diverse functions of GSTs islacking.CONCLUSION AND FUTUREPERSPECTIVESAbiotic stresses including the heavy metal stress profusely arrestscrop yield and productivity. Among different heavy metals, Asis considered to be the most hazardous material not only interms of plant growth and development but also due to its illeffects on human health. In the recent past, several studies haverevealed metal responsive genes and their genetic manipulationshave suggested strategies to develop different crop varietieswith improved stress tolerance and avoidance. GST is one suchmultigene family, which has been studied in detail and hasbeen notable for its role in herbicide detoxification. Though thisancient gene family has been exhaustively studied in differentorganisms, still the information available about its sequencesand gene organization understates its functional diversity. Recentbiotechnological advances have revealed diverse functions ofthis isozyme family, but unveiling the precise physiologicalrole of GSTs is still vexed. Considering this, it is imperativeto comprehend the functional polymorphism and geneticvariation, which might be the reason for gene duplication anddiversification of GST gene family. In addition, genome editingis an approach in which a specific target gene can be engineeredby adding, deleting or replacing the nucleotides. Recently, thescientific breakthrough, clustered regularly interspaced shortpalindromic repeats (CRISPR)-Cas (CRISPR associated protein)system has gained momentum for genome editing in plants.Using CRISPR-Cas9 in human and mouse cells, genome-wide,targeted loss-of-function pooled screens have been studied thathas provided information about the inactivated genomic lociand strategies that modulate transcriptional activities (Shalemet al., 2015). Apart from other genes, glutathione S-transferaseMu class gene (GSTM1) from the human genome has beenedited using CRISPR-Cas9 system (Sanjana et al., 2014). Inthis perspective, it is important to understand how CRISPRCas9 system can help in the crop improvement by harnessingthe precision of genome editing of GSTs in different plantspecies. Therefore, intensive studies are required to explore themultifactorial role of GSTs in plant development and stressresponse.The identification of GSTLs raises gripping questionsregarding their occurrence and functions. One of the questionsis about the prevalence of Lambda class GSTs in plant genome.GSTLs have been identified to be the smallest clade of GSTsuperfamily. As per the analysis, In2-1 proteins were identifiedto be the Lambda class GSTs in rice, which were missing in therice genome database (Kumar et al., 2013a), so, the questionarises that whether these In2-1 proteins in different plant speciesare the putative GSTLs? Another positive correlation of In2-1proteins and GSTLs is that both lack GST activity as observed insoybean and maize (McGonigle et al., 2000), which invokes thatIn2-1 protein could probably be the unidentified and undefinedGSTLs.Other crucial question concerns the mode of action andmechanism of GSTLs in As stress. Intriguingly, Lambdaclass GSTs has structural similarity with Omega GSTs ofmammals, which plays pivotal role in As biotransformationin humans. Both the classes share number of conservedresidues in the N-terminal GSH binding domain and possess adistinct structural feature of N-terminal extension (Theodoulouet al., 2003). A unique characteristic of presence of catalyticcysteine in the active site help them in thioltransferase activityinstead of GSH transfer activity. In addition, this active sitemotif assists in methylation of inorganic toxic form, As(III),to organic form monomethylarsonic acid (MMA) (Dixonet al., 2002). Therefore, such similarity perceives the roleof Lambda GSTs in As methylation and/or volatilization inplants.Consequently, these unique properties of GSTs make themimportant and interesting area of research for the functionalcharacterization. In particular, functions of all GST membersincluding Lambda class GSTs need to be explored becauseof its importance in As stress response. Overall, GSTs haveconsiderable agronomic potential not only in herbicide tolerancebut also in heavy metal stress detoxification.AUTHOR CONTRIBUTIONSAll authors listed have made a substantial, direct and intellectualcontribution to the work, and approved it for publication.ACKNOWLEDGMENTSSK thankfully acknowledges Department of Science andTechnology, Government of India, for the DST-INSPIRE FacultyAward. PKT acknowledges Council of Scientific and IndustrialResearch (CSIR), New Delhi for financial support as NetworkProject (BSC-0107).Frontiers in Plant Science | www.frontiersin.org 6 June 2018 | Volume 9 | Article 751Kumar and Trivedi Plant Glutathione S-Transferase and StressREFERENCESBentley, R., and Chasteen, T. G. (2002). Microbial methylation of metalloids:arsenic, antimony, and bismuth. Microbiol. Mol. Biol. 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