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Glutathione S-transferase: a versatile protein family

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Abstract

Glutathione-S transferase (GST) is a most ancient protein superfamily of multipurpose roles and evolved principally from gene duplication of an ancestral GSH binding protein. They have implemented in diverse plant functions such as detoxification of xenobiotic, secondary metabolism, growth and development, and majorly against biotic and abiotic stresses. The vital structural features of GSTs like highly divergent functional topographies, conserved integrated architecture with separate binding pockets for substrates and ligand, the stringent structural fidelity with high Tm values (50º–60º), and stress-responsive cis-regulatory elements in the promoter region offer this protein as most flexible plant protein for plant breeding approaches, biotechnological applications, etc. This review article summarizes the recent information of GST evolution, and their distribution and structural features with emphasis on the assorted roles of Ser and Cys GSTs with the signature motifs in their active sites, alongside their recent biotechnological application in the area of agriculture, environment, and nanotechnology have been highlighted.

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Fig. 1
Fig. 2

Vaish et al. 2018)

Fig. 3

adopted from Vaish et al. 2018)

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Abbreviations

GST:

Glutathione S-Transferase

GSH:

Glutathione;

TCHQD:

Tetrachloro-hydroquinone dehalogenase

EF1B γ:

Elongation factor 1B gamma

DHAR:

Dehydroascorbate reductases

GHRs:

Glutathionyl-hydroquinone reductases

mPGES-2 s:

Microsomal prostaglandin E synthase type 2

Cyt P450s:

Cytochrome P450s

SMV:

Soybean Mosaic Virus

BaMV:

Bamboo Mosaic Virus

ROS:

Reactive Oxygen Species

POD:

Peroxidases

SOD:

Superoxide Dismutase

GPOX:

Glutathione Peroxidase

Ka/Ks ratio:

Nonsynonymous/ Synonymous Mutation

AsA:

Ascorbic Acid

GSTU:

Tau GST

GSTF:

Phi GST

References

  • Abdallah IB, Tlili N, Martinez-Force E, Pérez Rubio AG, Perez-Camino MC, Albouchi A, Boukhchina S (2015) Content of carotenoids, tocopherols, sterols, triterpenes and aliphatic alcohols, and volatile compounds in six walnuts (Juglans regia L.) varieties. Food Chem 173:972–978

    CAS  PubMed  Google Scholar 

  • Ahmad L, Rylott EL, Bruce NC, Edwards R, Grogan G (2017) Structural evidence for Arabidopsis glutathione transferase at GSTF2 functioning as a transporter of small organic ligands. FEBS Open Bio 7:122–132

    CAS  PubMed  Google Scholar 

  • Ali Z, Zhang DY, Xu ZL, Xu L, Yi JX, He XL, Huang YH, Liu XQ, Khan AA, Trethowan RM, Ma HX (2012) Uncovering the salt response of soybean by unraveling its wild and cultivated functional genomes using tag sequencing. PLoS ONE 7:e48819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Apic G, Gough J, Teichmann SA (2001) Domain combinations in archaeal, eubacterial, and eukaryotic proteomes. J Mol Biol 310:311–325

    CAS  PubMed  Google Scholar 

  • Armstrong RN (1998) Mechanistic imperatives for the evolution of glutathione transferases. Current Op in Chem Biol 2:618–623

    CAS  Google Scholar 

  • Axarli I, Dhavala P, Papageorgiou AC, Labrou NE (2009) Crystallographic and functional characterization of the fluorodifen-inducible glutathione transferase from Glycine max reveals an active site topography suited for diphenylether herbicides and a novel L-site. J Mol Biol 385:984–1002

    CAS  PubMed  Google Scholar 

  • Babu M, Gagarinova AG, Brandle JE, Wang A (2008) Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection. J Gen Virol 89:1069–1080

    CAS  PubMed  Google Scholar 

  • Bai Y, Luo Q, Zhang W, Miao L, Xu J, Li H, Liu J (2013) Highly ordered protein nanorings designed by accurate control of glutathione S-transferase self-assembly. J Am Chem Soc 135:10966–10969

    CAS  PubMed  Google Scholar 

  • Banday ZZ, Nandi AK (2018) Arabidopsis thaliana GLUTATHIONE S-TRANSFERASE THETA 2 interacts with RSI1/FLD to activate systemic acquired resistance: GSTT2 interacts with FLD and regulates SAR. Mol Plant Pathol 19:464–475

    CAS  PubMed  Google Scholar 

  • Basantani M, Srivastava A (2007) Plant glutathione transferases: a decade falls short. Can J Bot 85:443–456

    CAS  Google Scholar 

  • Basantani M, Srivastava A, Sen S (2011) Elevated antioxidant response and induction of tau-class glutathione S-transferase after glyphosate treatment in Vigna radiata (L.) Wilczek. Pesti Biochem Physiol 99:111–117

    CAS  Google Scholar 

  • Benekos K, Kissoudis C, Nianiou-Obeidat I, Labrou N, Madesis P, Kalamaki M, Makris A, Tsaftaris A (2010) Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J Biotechnol 150:195–201

    CAS  PubMed  Google Scholar 

  • Board PG, Baker RT, Chelvanayagam G, Jermiin LS (1997) Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem J 328:929–935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Board PG, Taylor MC, Coggan M, Parker MW, Lantum HB, Anders MW (2003) Clarification of the role of key active site residues of glutathione transferase Zeta/maleylacetoacetate isomerase by a new spectrophotometric technique. Biochem J 374:731–737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cairrao E, Couderchet M, Soares AMVM, Guilhermino L (2004) Glutathione-S-transferase activity of Fucus spp. as a biomarker of environmental contamination. Aquatic Toxicol 70:277–286

    CAS  Google Scholar 

  • Chen IC, Huang IC, Liu MJ, Wang ZG, Chung SS, Hsieh HL (2007) Glutathione S -transferase interacting with far-red insensitive 219 is involved in phytochrome A-mediated signaling in Arabidopsis. Plant Physiol 143:1189–1202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen IH, Chiu MH, Cheng SF, Hsu YH, Tsai CH (2013) The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic Virus. New Phytol 199:749–757

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Huang H, Wei S, Huang Z, Wang X, Zhang C (2017) Investigating the mechanisms of glyphosate resistance in goosegrass (Eleusine indica (L.) Gaertn.) by RNA sequencing technology. Plant J 89:407–415

    CAS  PubMed  Google Scholar 

  • Chi Y, Cheng Y, Vanitha J, Kumar N, Ramamoorthy R, Ramachandran S, Jiang S (2011) Expansion Mechanisms and Functional Divergence of the Glutathione S Transferase Family in Sorghum and Other Higher Plants. DNA Res 18:1–16

    CAS  PubMed  Google Scholar 

  • Chothia C, Gough J, Vogel C, Teichmann SA (2003) Evolution of the protein repertoire. Science 300:1701–1703

    CAS  PubMed  Google Scholar 

  • Chronopoulou E, Madesis P, Tsaftaris A, Labrou NK (2012) Cloning and characterization of a biotic-stress-inducible glutathione transferase from phaseolus vulgaris. Planta 235:1253–1269

    CAS  PubMed  Google Scholar 

  • Chronopoulou E, Ataya FS, Pouliou F, Perperopoulou F, Georgakis N, Nianiou-Obeidat I et al (2017a) Structure evolution and functional roles of plant glutathione transferases. Glutathione in plant growth, development, and stress tolerance. Springer, London, pp 195–213

    Google Scholar 

  • Chronopoulou E, Georgakis N, Nianiou-Obeidat I, Madesis P, Perperopoulou F, Pouliou F et al (2017b) Plant glutathione transferases in abiotic stress response and herbicide resistance. Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, London, pp 215–233

    Google Scholar 

  • Chronopoulou EG, Vlachakis D, Papageorgiou AC, Ataya FS, Labrou NE (2019) Structure-based design and application of an engineered glutathione transferase for the development of an optical biosensor for pesticides determination. Biochimica Biophysica Acta 1863:565–576

    CAS  Google Scholar 

  • Cicero LL, Madesis P, Tsaftaris A, Piero ALR (2015) Tobacco plants over-expressing the sweet orange tau glutathione transferases (CsGSTUs) acquire tolerance to the diphenyl ether herbicide fluorodifen and to salt and drought stresses. J Phytochem 116:69–77

    Google Scholar 

  • Conn S, Curtin C, Zier AB, Franco C, Zhang W (2008) Purification, molecular cloning, and characterization of glutathione S-transferases (GSTs) from pigmented Vitis vinifera L. cell suspension cultures as putative anthocyanin transport proteins. J Experimental Botany 59:3621–3634

    CAS  Google Scholar 

  • Csiszar J, Horvath E, Vary Z, Galle A, Bela K, Brunner S, Tari I (2014) Glutathione transferase supergene family in tomato: salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid. Plant Physiol Biochem 78:15–26

    CAS  PubMed  Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1998) Purification of multiple glutathione transferases involved in herbicide detoxification from wheat (Triticum aestivum L.) treated with the safener fenchlorazole-ethyl. Pestic Biochem Physiol 59:35–49

    Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292

    CAS  PubMed  Google Scholar 

  • Cummins I, Wortley DJ, Sabbadin F, He Z, Coxon CR, Straker HE, Sellars JD, Knight K, Edwards L, Hughes D, Kaundun SS, Hutchings SJ, Steel PG, Edwards R (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci 110:5812–5817

    CAS  PubMed  Google Scholar 

  • da Fonseca RR, Johnson WE, O’Brien SJ, Vasconcelos V, Antunes A (2010) Molecular evolution and the role of oxidative stress in the expansion and functional diversification of cytosolic glutathione transferases. BMC Evol Biol 10:281

    PubMed  PubMed Central  Google Scholar 

  • Dalton DA, Boniface C, Turner Z, Lindah A, Kim HJ, Jelinek L, Govindarajulu M, Finger RE, Taylor CG (2009) Physiological roles of glutathione S-transferases in soybean root nodules. Plant Physiol 150:521–530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding N, Wang A, Zhang X, Wu Y, Wang R, Cui H, Huang R, Luo Y (2017) Identification and analysis of glutathione S-transferase gene family in sweet potato reveal divergent GST-mediated networks in aboveground and underground tissues in response to abiotic stresses. BMC Plant Biol 17:225

    PubMed  PubMed Central  Google Scholar 

  • Dixit P, Mukherjee PK, Sherkhane PD, Kale SP, Eapen S (2011) Enhanced tolerance and remediation of anthracene by transgenic tobacco plants expressing a fungal glutathione transferase gene. J Hazardous Mat 192:270–276

    CAS  Google Scholar 

  • Dixon DP, Edwards R (2009) Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J Biol Chem 284:21249–21256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Current Op in Plant Biol 1:258–266

    CAS  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Boil 3:1–3004

    Google Scholar 

  • Dixon DP, Lapthorn A, Madesis P, Mudd EA, Day A, Edwards R (2008) Binding and glutathione conjugation of porphyrinogens by plant glutathione transferases. J of Biolog Chem 283:20268–20276

    CAS  Google Scholar 

  • Dixon DP, Hawkins T, Hussey PJ, Edwards R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60:1207–1218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350

    CAS  PubMed  Google Scholar 

  • Dixon DP, Sellars JD, Edwards R (2011) The Arabidopsis phi class glutathione transferase AtGSTF2: binding and regulation by biologically active heterocyclic ligands. Biochem J 438:63–70

    CAS  PubMed  Google Scholar 

  • Du J, Ren J, Ye X, Hou A, Fu W, Mei F, Liu Z (2018) Genome-wide identification and expression analysis of the glutathione S-transferase (GST) family under different developmental tissues and abiotic stresses in Chinese Peer. J Preprints 6:62

    Google Scholar 

  • Edward PL, Lee N, Watson D, Ray FR (1980) Glutathion-S-transferase is present in a variety of microorganisms. Chemosphere 9:565–569

    Google Scholar 

  • Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: with multiple functions in sickness and in health. Trends Plant Sci 5:193–198

    CAS  PubMed  Google Scholar 

  • Frear DS, Swanson HR (1970) Biosynthesis of S-(4-ethylamino-6-isopropylamino- 2-s-triazino) glutathione: partial purification and properties of a glutathione S-transferase from corn. Phytochemistry 9:2123–2132

    CAS  Google Scholar 

  • Frova C (2003) The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol Plant 119:469–479

    CAS  Google Scholar 

  • Gallé A, Csiszár J, Secenji M, Tari I, Györgyey J, Dudits D, Erdei L (2005) Changes of glutathione S-transferase activities and gene expression in Triticum aestivum during polyethylene-glycol induced osmotic stress. Acta Biologica Szegediensis 49:95–96

    Google Scholar 

  • Gallé Á, Czékus Z, Bela K, Horváth E, Ördög A, Csiszár J, Poór P (2019) Plant glutathione transferases and light. Front Plant Sci 9:1944

    PubMed  PubMed Central  Google Scholar 

  • Gao J, Chen B, Lin H, Liu Y, Wei Y, Chen F, Li W (2020) Identification and characterization of the glutathione S-Transferase (GST) family in radish reveals a likely role in anthocyanin biosynthesis and heavy metal stress tolerance. Gene 743:144484

    CAS  PubMed  Google Scholar 

  • Georgakis N, Poudel N, Papageorgiou AC, Labrou NE (2020) Comparative structural and functional analysis of phi class glutathione transferases involved in multiple-herbicide resistance of grass weeds and crops. Plant Physiol. Biochem 149:266–276

    CAS  PubMed  Google Scholar 

  • Gong H, Jiao Y, Hu WW, Pua EC (2005) Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro, Plant Mol. Biol 57:53–66

    CAS  Google Scholar 

  • Gunning V, Tzafestas K, Sparrow H, Johnston EJ, Brentnall AS, Potts JR, Rylott EL, Bruce NC (2014) Arabidopsis glutathione transferasesU24 andU25 exhibit arange of detoxification activities with the environmental pollutant and explosive, 2,4,6-trinitrotoluene. Plant Physiol 165:854–865

    CAS  PubMed  PubMed Central  Google Scholar 

  • Han XM, Yang ZL, Liu YJ, Yang HL, Zeng QY (2018) Genome-wide profiling of expression and biochemical functions of the Medicago glutathione S-transferase gene family. Plant Physiol et Biochem 126:126–133

    CAS  Google Scholar 

  • Herv’E C, Groisillier A, Thierry TT, Boyen C (2008) New members of the glutathione transferase family discovered in red and brown algae. Biochem J 412:535–544

    Google Scholar 

  • Horváth E, Bela K, Papdi C, Gallé Á, Szabados L, Tari I, Jolán C (2015) The role of Arabidopsis glutathione transferase F9 gene under oxidative stress in seedlings. Acta Biol Hungarica 66:406–418

    Google Scholar 

  • Hu B, Zhao J, Lai B, Qin Y, Wang H, Hu G (2016) LcGST4 is an anthocyanin-related glutathione S-transferase gene in Litchi chinensis Sonn. Plant Cell Rep 35:831–843

    CAS  PubMed  Google Scholar 

  • Islam S, Sajib SD, Jui ZS, Arabia S, Islam T (2019) Genome-wide identification of glutathione S-transferase gene family in pepper, its classification, and expression profiling under different anatomical and environmental conditions. Scientific Reports 9:9101

    PubMed  PubMed Central  Google Scholar 

  • Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of glutathione S-transferases during development and stress responses in rice. BMC Genomics 11:73

    PubMed  PubMed Central  Google Scholar 

  • Jepson VJ, Lay DC, Holt SW, Bright J, Andrew J (1994) Cloning and characterization of maize herbicide safener-induced cDNAs encoding subunits of glutathione S-transferase isoforms I. II and IV Plant Mol Bio 26:1855–1866

    CAS  Google Scholar 

  • Jiang HW, Liu MJ, Chen IC, Huang CH, Chao LY, Hsieh HL (2010) A Glutathione S-transferase regulated by light and hormones participates in the modulation of arabidopsis seedling development. Plant Physiol 154:1646–1658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kampranis SC, Damianova R, Atallah M, Toby G, Kondi G, Tsichlis PN, Makris AM (2000) A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast. J Biol Chem 275:29207–29216

    CAS  PubMed  Google Scholar 

  • Kayum MA, Nath UK, Park JI, Biswas MK, Choi EK, Song JY, Kim HT, Nou IS (2018) Genome-wide identification, characterization, and expression profiling of glutathione S-transferase (GST) family in pumpkin reveals likely role in cold-stress tolerance. Genes 9:84

    PubMed Central  Google Scholar 

  • Ki M, Yeo KB, Pack SP (2013) Surface immobilization of protein via biosilification catalyzed by silicatein fused to glutathione S-transferase (GST). Bioprocess Biosyst Eng 36:643–648

    CAS  PubMed  Google Scholar 

  • Kissoudis C, Kalloniati C, Pavli O, Flemetakis E, Labrou NE, Madesis P, Skaracis G, Tsaftaris A, Nianiou-Obeidat I (2015) Stress inducible GmGSTU4 shapes transgenic tobacco plants metabolome towards increased salinity tolerance. Acta Physiol Plant 37:102

    Google Scholar 

  • Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114

    CAS  PubMed  Google Scholar 

  • Kitamura S, Akita Y, Ishizaka H, Narumia I, Tanaka A (2012) Molecular characterization of an anthocyanin-related glutathione S-transferase gene in cyclamen. J Plant Physiol 169:636–642

    CAS  PubMed  Google Scholar 

  • Koonin EV, Mushegian AR, Tatusov RL, Altschul SF, Bryant SH, Bork P, Valencia A (1994) Eukaryotic translation elongation factor 1c contains a glutathione transferase domain - study of a diverse, ancient protein superfamily using motif search and structural modeling. Protein Sci 3:2045–2054

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kou M, Liu YJ, Li ZY, Zhang YG, Tang W, Yan H, Wang X, Chen XG, Su ZX, Arisha MH, Li Q, Ma DF (2019) A novel glutathione S-transferase gene from sweetpotato, IbGSTF4, is involved in anthocyanin sequestration. Plant Physiol and Biochem 135:395–403

    CAS  Google Scholar 

  • Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:751

    PubMed  PubMed Central  Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Expression of a rice Lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazardous Materials 248–249:228–237

    Google Scholar 

  • Labrou NE, Papageorgiou AC, Pavli O, Flemetakis E (2015) Plant GSTome: structure and functional role in xenome network and plant stress response. Current Op in Biotechnol 32:186–194

    CAS  Google Scholar 

  • Lallement PA, Brouwer B, Keech O, Hecker A, Rouhier N (2014a) The still mysterious roles of cysteine-containing glutathione transferases in plants. Front Pharmacol 5:192

    PubMed  PubMed Central  Google Scholar 

  • Lallement PA, Meux E, Gualberto JM, Prosper P, Didierjean C, Saul F, Haouz A, Rouhier N, Hecker A (2014b) Structural and enzymatic insights into Lambda glutathione transferases from populus trichocarpa, monomeric enzymes constituting an early divergent class specific to terrestrial plants. Biochem J 462:39–52

    CAS  PubMed  Google Scholar 

  • Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lan T, Wang XR, Zeng QY (2013) Structural and functional evolution of positively selected sites in pine glutathione s-transferase enzyme family. J of Biol Chem 288:24441–24451

    CAS  Google Scholar 

  • Lederer B, Böger P (2003) Binding and protection of porphyrins by glutathione S-transferases of Zea mays L. Biochem Biophys Acta 1621:226–233

    CAS  PubMed  Google Scholar 

  • Li D, Xu L, Pang S, Liu Z, Wang K, Wang C (2017) Variable levels of glutathione S-transferases are responsible for the differential tolerance to metolachlor between maize (Zea mays) shoots and roots. J Agric Food Chem 65:39–44

    CAS  PubMed  Google Scholar 

  • Licciardello C, Agostino N, Traini A, Recupero GR, Frusciante L, Chiusano ML (2014) Characterization of the glutathione S-transferase gene family through ESTs and expression analyses within common and pigmented cultivars of Citrus sinensis (L) Osbeck. BMC Plant Biol 14:39

    PubMed  PubMed Central  Google Scholar 

  • Liu YJ, Han XM, Ren LL, Yang HL, Zeng QY (2013) Functional divergence of the glutathione S-transferase supergene family in Physcomitrella patens reveals complex patterns of large gene family evolution in land plants. Plant Physiol 161:773–786

    CAS  PubMed  Google Scholar 

  • Liu HJ, Tang ZX, Han XM, Yang ZL, Zhang FM, Yang HL, Liu YJ, Zeng QY (2015) Divergence in enzymatic activities in the soybean GST supergene family provides new insight into the evolutionary dynamics of whole-genome duplicates. Mol Biol Evol 32:2844–2859

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lv F, Zhou J, Zeng L, Xing D (2015) β-cyclocitral upregulates salicylic acid signalling to enhance excess light acclimation in Arabidopsis. J Exp Bot 66:4719–4732

    CAS  PubMed  Google Scholar 

  • Marrs KA (1996) The functions and regulation of Glutathione S-transferases in plants. Annu Rev Plant Physiol 47:127–158

    CAS  Google Scholar 

  • Martin JL (1995) Thioredoxin—a fold for all reasons. Structure 3:245–250

    CAS  PubMed  Google Scholar 

  • McGonigle B, Keeler SJ, Lau S-MC, Koeppe MK, O’Keefe DP (2000) A genomics approach to the comprehensive analysis of the glutathione s-transferase gene family in soybean and maize. Plant Physiol 124:1105–1120

    CAS  PubMed  PubMed Central  Google Scholar 

  • McGuinness M, Mazurkiewicz V, Brennan E, Dowling D (2007) Dechlorination of pesticides by a specific bacterial glutathione S -transferase, BphKLB400: Potential for Bioremediation. Eng Life Sci 7:611–615

    CAS  Google Scholar 

  • Moons A (2003) Osgstu3 and osgtu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett 553:427–432

    CAS  PubMed  Google Scholar 

  • Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitam And Horm 72:155–202

    CAS  Google Scholar 

  • Morales A, O'Rourke JA, Van M, Mortel DE (2013) Transcriptome analyses and virus induced gene silencing identify genes in the Rpp4-mediated Asian soybean rust resistance pathway. Funct Plant Biol 40:1029–1047

    CAS  PubMed  Google Scholar 

  • Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ, Berger S (2008) General detoxification and stress responses are mediated by oxi- dized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20:768–785

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakka S, Jugulam M, Peterson D, Asif M (2019) Herbicide resistance: Development of wheat production systems and current status of resistant weeds in wheat cropping systems. The Crop J 7:750–760

    Google Scholar 

  • Nianiou-Obeidat I, Madesis P, Kissoudis C, Voulgari G, Chronopoulou E, Tsaftaris A, Labrou NE (2017) Plant glutathione transferase-mediated stress tolerance: functions and biotechnological applications. Plant Cell Rep 36:791–805

    CAS  PubMed  Google Scholar 

  • Oakley AJ (2005) Glutathione transferases: new functions. Curr Opin Struct Biol 15:716–723

    CAS  PubMed  Google Scholar 

  • Oliveira TIS, Oliveira M, Viswanathan S, Barroso MF, Barreiros L, Nunes OC, Rodrigues JA, de Lima-Neto P, Mazzetto SE, Morais S, Delerue-Matos C (2013) Molinate quantification in environmental water by a glutathione-S-transferase based biosensor. Talanta 106:249–254

    CAS  PubMed  Google Scholar 

  • Öztetik E (2008) A Tale of Plant Glutathione S-Transferases: Since 1970. Bot Rev 74:419–437

    Google Scholar 

  • Oztetik E, Kockar F, Alper M, Iscan M (2015) Molecular characterization of zeta class glutathione S-transferases from Pinus brutia Ten. J Genet 94:417–423

    CAS  PubMed  Google Scholar 

  • Pandey T, Singh SK, Chhetri G, Tripathi T, Singh AK (2015) Characterization of a highly ph stable Chi Class Glutathione S-Transferase from Synechocystis PCC 6803. PLoS ONE 10:e0126811

    PubMed  PubMed Central  Google Scholar 

  • Paternolli C, Ghisellini P, Nicolini C (2002) Development of immobilization techniques of cytochrome P450-GST fusion protein. Colloids Surf B 23:305–311

    CAS  Google Scholar 

  • Pégeot H, Koh CS, Petre B, Mathiot S, Duplessis S, Hecker A, Didierjean C, Rouhier N (2014) The poplar Phi class glutathione transferase: expression, activity and structure of GSTF1. Front Plant Sci 5:712

    PubMed  PubMed Central  Google Scholar 

  • Pégeot H, Mathiot S, Perrot T, Gense F, Hecker A, Didierjean C, Rouhier N (2017) Structural plasticity among glutathione transferase Phi members: natural combination of catalytic residues confers dual biochemical activities. FEBS J 284:2442–2463

    PubMed  Google Scholar 

  • Peragón J, Amores-Escobar MT (2018) Olive tree glutathione S-transferase and its response against the herbicides oxyfluorfen and glyphosate. Sci Hortic 231:194–200

    Google Scholar 

  • Plomion C, Aury J, Amselem J et al (2018) Oak genome reveals facets of long lifespan. Nature Plants 4:440–452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prade L, Hof P, Bieseler B (1997) Dimer interface of glutathione S-transferase rom Arabidopsis thaliana: influence of the G site architecture on the dimer interface and implications for classification. Biol Chem 378:317–320

    CAS  PubMed  Google Scholar 

  • Puglisi I, Lo Cicero L, Lo Piero AR (2013) The glutathione S-transferase gene superfamily: an in silico approach to study the post translational regulation. Biodegradation 24:471–485

    CAS  PubMed  Google Scholar 

  • Rawat B, Mishra KK, Barman U, Arora L, Pal D, Paily RP (2020) Two-Dimensional MoS2-based electrochemical biosensor for highly selective detection of glutathione. IEEE Sensors J 1:1. https://doi.org/10.1109/JSEN.2020.2978275

    Article  Google Scholar 

  • Rezaei MK, Shobbar ZS, Shahbazi M, Abedini R, Zare S (2013) Glutathione S-transferase (GST) family in barley: Identification of members, enzyme activity, and gene expression pattern. J Plant Physiol 170:1277–1284

    CAS  PubMed  Google Scholar 

  • Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    CAS  PubMed  Google Scholar 

  • Safarpour H, Safarnejad MR, Tabatabaei M, Mohsenifar A, Rad F, Basirat M, Shahryari F, Hasanzadeh F (2012) Development of a quantum dots FRET-based biosensor for efficient detection of Polymyxa betae. Biochem Cell Biol 2012(34):507–515

    Google Scholar 

  • Sharma R, Sahoo A, Devendran R, Jain M (2014) Over-expression of a rice tau class glutathione s transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PLoS ONE 9:e92900

    PubMed  PubMed Central  Google Scholar 

  • Shi HY, Li ZH, Zhang YX, Chen L, Xiang DY, Zhang YF (2014) Two pear glutathione S-transferases genes are regulated during fruit development and involved in response to salicylic acid, Auxin, and glucose signaling. PLoS ONE 9:e89926

    PubMed  PubMed Central  Google Scholar 

  • Singh S (2015) Cytoprotective and regulatory functions of glutathione S-transferases in cancer cell proliferation and cell death. Cancer Chemother Pharmacol 75:1–15

    CAS  PubMed  Google Scholar 

  • Singh BR, Shaw RW (1988) Selective inhibition of oat glutathione-S-transferase activity by tetrapyrroles. FEBS Lett 234:379–382. https://doi.org/10.1016/0014-5793(88)80120-0

    Article  CAS  Google Scholar 

  • Singhal SS, Singh SP, Singhal P, Horne D, Singhal J, Awasthi S (2015) Antioxidant role of glutathione S-transferases: 4-hydroxynonenal, a key molecule in stress-mediated signaling. Toxicol Appl Pharmacol 289:361–370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skopelitou K, Muleta AW, Papageorgiou AC, Chronopoulou E, Labrou NE (2015) Catalytic features and crystal structure of a tau class glutathione transferase from glycine max specifically upregulated in response to soybean mosaic virus infections. Biochem Biophys Acta 1854:166–177

    CAS  PubMed  Google Scholar 

  • Smith AP, Nourizadeh SD, Peer WA, Xu J, Bandyopadhyay A, Murphy AS, Goldsbrough PB (2003) Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. Plant J 36:433–442

    CAS  PubMed  Google Scholar 

  • Soranzo N, Gorla MS, Mizzi L, De TG, Frova C (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271:511–521

    CAS  PubMed  Google Scholar 

  • Su T, Xu J, Li Y, Lei L, Zhao L, Yang H, Feng J, Liu G, Ren D (2011) Glutathione-indole-3- acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23:364–380

    PubMed  PubMed Central  Google Scholar 

  • Sylvestre-Gonon E, Law SR, Schwartz M, Robe K, Keech O, Didierjean C, Dubos C, Rouhier N, Hecker A (2019) Functional, Structural and Biochemical Features of Plant Serinyl-Glutathione Transferases. Front Plant Sci 10:608

    PubMed  PubMed Central  Google Scholar 

  • Sylvestre-Gonon E, Schwartz M, Girardet JM, Hecker A, Rouhier N (2020) Is there a role for tau glutathione transferases in tetrapyrrole metabolism and retrograde signalling in plants?. Phil. Trans. R, Soc, p B37520190404

    Google Scholar 

  • Takusagawa F (2013) Microsomal prostaglandin E synthase type2 (mPGES2) is a glutathione dependent heme protein, and di thiothreitol dissociates the bound heme to produce active prostaglandin E2 synthase in vitro. J Biol Chem 288:10166–10175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Hoagland KD, Siegfried BD (1998) Uptake and bioconcentration of atrazine by selected freshwater algae. Environ Toxicol Chem 17:1085–1090

    CAS  Google Scholar 

  • Tanikawa N, Ohmiya Y, Ohkubo H, Hashimoto K, Kangawa K, Kojima M, Ito S, Watanabe K (2002) Identification and characterization of a novel type of membrane- associated prostaglandin Esynthase. Biochem Biophys Res Commun 291:884–889

    CAS  PubMed  Google Scholar 

  • Thom R, Dixon DP, Edwards R, Cole DJ, Lapthorn AJ (2001) The structure of a zeta class glutathione S-transferase from Arabidopsis thaliana: characterisation of a GST with novel active-site architecture and a putative role in tyrosine catabolism. J Mol Biol 308:949–962

    CAS  PubMed  Google Scholar 

  • Tiwari V, Patel MK, Chaturvedi AK, Mishra A, Jha B (2016) Functional characterization of the Tau Class Glutathione-S-Transferases Gene (SbGSTU) promoter of Salicornia brachiata under salinity and osmotic stress. PLoS ONE 2:e0148494

    Google Scholar 

  • Vaish S, Awasthi P, Tiwari S, Tiwari SK, Basantani MK (2018) In silico genome-wide identification and characterization of glutathione S-transferase gene family in Vigna radiata (L.) Wilczek. Genome 61:311–322

    CAS  PubMed  Google Scholar 

  • Vijayakumar H, Thamilarasan SK, Shanmugam A, Natarajan SK, Jung HJ, Park JI, Kim H, Chung MY, Nou Ill S (2016) Glutathione transferases superfamily: cold-inducible expression of distinct GST genes in Brassica oleracea. Int J Mol Sci 17:1211

    PubMed Central  Google Scholar 

  • Wang H, Sun S, Ge W, Zhao L, Hou B, Wang K et al (2020) Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 368:6493

    Google Scholar 

  • Warner JR, Behlen LS, Copley SD (2008) A trade-off between catalytic power and substrate inhibition in TCHQ dehalogenase. Biochemistry 47:3258–3265

    CAS  PubMed  Google Scholar 

  • Wongsantichon J, Ketterman AJ (2005) Alternative splicing of glutathione S-transferases. Methods Enzymol 401:100–116

    CAS  PubMed  Google Scholar 

  • Xu XY, Fan R, Zheng R, Li CM, Yu DY (2011) Proteomic analysis of seed germination under salt stress in soybeans. J Zhejiang Univ Sci B 12:507–517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Xing XJ, Tian YS, Peng RH, Xue Y, Zhao W, Yao QH (2014) Transgenic arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS ONE 10:e0136960

    Google Scholar 

  • Xu J, Tian YS, Xing XJ, Xu ZS, Zhu B, Fu XY, Peng RH, Yao QH (2017) Enhancement of phenol stress tolerance in transgenic Arabidopsis plants overexpressing glutathione S-transferase. Plant Growth Regul 82:37–45

    CAS  Google Scholar 

  • Yamada T, Komoto J, Watanabe K, Ohmiya Y, Takusagawa F (2005) Crystal structure and possible catalytic mechanism of microsomal prostaglandin E synthase type2 (mPGES-2). J Mol Bio 348:1163–1176

    CAS  Google Scholar 

  • Yang HL, Zhao YR, Wang CL, Yang ZL, Zeng QY, Lu H (2009) Molecular characterization of a dehydroascorbate reductase from Pinus bungeana. J Integr Plant Biol 51:993–1001

    CAS  PubMed  Google Scholar 

  • Yang Q, Liu YJ, Zeng QY (2014) Biochemical functions of the glutathione transferase supergene family of Larix kaempferi. Plant Physiol and Biochem 7:99–107

    Google Scholar 

  • Yang G, Xu Z, Peng S, Sun Y, Jia C, Zhai M (2016) In planta characterization of a tau class glutathione S-transferase gene from Juglans regia (JrGSTTau1) involved in chilling tolerance. Plant Cell Rep 35:681–692

    CAS  PubMed  Google Scholar 

  • Zeng QY, Lu H, Wang XR (2005) Molecular characterization of a glutathione transferase from Pinus tabulaeformis (Pinaceae). Biochimie 87:445–455

    CAS  PubMed  Google Scholar 

  • Zettl R, Schell J, Palme K (1994) Photoaffinity labeling of Arabidopsis thaliana plasma membrane vesicles by 5-azido-[7-3H] indole-3-acetic acid: identification of a glutathione S-transferase. Proc Natl Acad Sci 91:689–693

    CAS  PubMed  Google Scholar 

  • Zhang W, Luo Q, Miao L, Hou C, Bai Y, Dong Z, Xu J, Liu J (2012) Self-assembly of glutathione S-transferase into nanowires. Nanoscale 4:5847–5851

    CAS  PubMed  Google Scholar 

  • Zhang H, Yang Y, Ma K, Shi C, Chen W, Liu D (2020) A novel sigma class glutathione S-transferase gene in freshwater planarian Dugesia japonica: cloning, characterization and protective effects in herbicide glyphosate stress. Ecotoxicology 29:295–304

    CAS  PubMed  Google Scholar 

  • Zheng K, Board PG, Fei X, Sun Y, Lv S, Yan G, Liu J, Shen J, Luo G (2008) A novel selenium containing glutathione transferase zeta1-1, the activity of which surpasses the level of some native glutathione peroxidases. Int J Biochem Cell Biol 40:2090–2097

    CAS  PubMed  Google Scholar 

  • Zhu JH, Li HL, Guo D, Wang Y, Dai HF, Mei WL, Peng SQ (2016) Transcriptome-wide identification and expression analysis of glutathione S-transferase genes involved in flavonoids accumulation in Dracaena cambodiana. Plant Physiol and Biochem S0981–942830:182–186

    Google Scholar 

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Vaish, S., Gupta, D., Mehrotra, R. et al. Glutathione S-transferase: a versatile protein family. 3 Biotech 10, 321 (2020). https://doi.org/10.1007/s13205-020-02312-3

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