Skip to main content
SpringerLink
Log in

Structure, Evolution and Functional Roles of Plant Glutathione Transferases

  • Chapter
  • First Online:
Glutathione in Plant Growth, Development, and Stress Tolerance

Abstract

Plant cytosolic glutathione transferases (EC 2.5.1.18, GSTs) are essential enzymes involved in multiple and diverse functions which are crucial to xenobiotic detoxification, hormone signalling, redox homeostasis, plant metabolism, growth regulation and adaptation to abiotic and biotic stresses. GSTs are capable of catalysing the conjugation of reduced glutathione (γ-L-Glu-L-Cys-Gly; GSH), via the sulphydryl group, to electrophilic centres on a vast number of molecules, both endogenous and xenobiotic, including herbicides, leading to their detoxification. Recent progress of plant proteomics, genomics and transcriptomics projects has allowed the identification, classification and evolutionary analysis of a large number of GST isoenzymes and has provided new knowledge and insights into their in planta function and catalytic role. This chapter focuses on plant GSTs and attempts to give an overview of their evolution, catalytic function and structural biology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • AlJabr AM, Hussain A, Rizwan-Ul-Haq M, Al-Ayedh H (2017) Toxicity of plant secondary metabolites modulating detoxification genes expression for natural red palm weevil pesticide development. Molecules 22:169

    Article  Google Scholar 

  • Allocati N, Casalone E, Masulli M, Ceccarelli I, Carletti E, Parker MW, Di Ilio C (1999) Functional analysis of the evolutionarily conserved proline 53 residues in Proteus mirabilis glutathione S-transferase B1-1. FEBS Lett 445:347–350

    Google Scholar 

  • Allocati N, Federici L, Masulli M, Di Ilio C (2009) Glutathione transferases in bacteria. FEBS J 276:58–75

    Article  CAS  PubMed  Google Scholar 

  • Armstrong RN (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. A useful review of GSTs from an evolutionary perspective. Chem Res Toxicol 10:2–18

    Article  CAS  PubMed  Google Scholar 

  • Arora PK, Bae H (2014) Role of dehalogenases in aerobic bacterial degradation of chlorinated aromatic compounds. J Chem 2014:1–10

    Google Scholar 

  • Axarli I, Dhavala P, Papageorgiou AC, Labrou NE (2009a) 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

    Article  CAS  PubMed  Google Scholar 

  • Axarli I, Dhavala P, Papageorgiou AC, Labrou NE (2009b) Crystal structure of Glycine max glutathione transferase in complex with glutathione: investigation of the mechanism operating by the tau class glutathione transferases. Biochem J 422:247–256

    Article  CAS  PubMed  Google Scholar 

  • Axarli I, Muleta AW, Vlachakis D, Kossida S, Kotzia G, Maltezos A, Dhavala P, Papageorgiou AC, Labrou NE (2016) Directed evolution of tau class glutathione transferases reveals a site that regulates catalytic efficiency and masks co-operativity. Biochem J 473:559–570

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bathige SDNK, Umasuthan N, Revathy KS, Lee Y, Kim S, Cho MY, Park M-A, Whang I, Lee J (2014) A mu class glutathione S-transferase from manila clam Ruditapes philippinarum (RpGSTμ): cloning, mRNA expression, and conjugation assays. Comp Biochem Physiol C Toxicol Pharmacol 162:85–95

    Article  CAS  PubMed  Google Scholar 

  • Belchik M, Xun L (2011) S-glutathionyl-(chloro)hydroquinone reductases: a new class of glutathione transferases functioning as oxidoreductases. Drug Metab Rev 43:307–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Board P, Menon D (2013) Glutathione transferases, regulators of cellular metabolism and physiology. Biochemica et Biophysica Acta 1830:3267–3288

    Article  CAS  Google Scholar 

  • Chan C, Lam H-M (2014) A putative lambda class glutathione S-transferase enhances plant survival under salinity stress. Plant Cell Physiol 55:570–579

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Chen X, Dou W, Wang L, Yin H, Guo S (2016) GST(phi) gene from macrophyte Lemna minor is involved in cadmium exposure responses. Chinese J Oceanol and Limnology 34:342–353

    Google Scholar 

  • Cho HY, Kong KH (2007) Study on the biochemical characterization of herbicide detoxification enzyme, glutathione S-transferase. Biofactors 30:281–287

    Article  CAS  PubMed  Google Scholar 

  • Cho HY, Maeng SJ, Cho HJ, Choi YS, Chung JM, Lee S, Kim HK, Kim JH, Eom C-Y, Kim Y-G, Guo M, Jung HS, Kang BS, Kim S (2015) Assembly of multi-tRNA synthetase complex via heterotetrameric glutathione transferase-homology domains. J Biol Chem 290:29313–29328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chronopoulou E, Madesis P, Asimakopoulou B, Platis D, Tsaftaris A, Labrou NE (2012) Catalytical and structural diversity of the fluazifop-inducible glutathione transferases from Phaseolus vulgaris. Planta 235:1253–1269

    Article  CAS  PubMed  Google Scholar 

  • Chronopoulou E, Madesis P, Tsaftaris A, Labrou NE (2014) Cloning and characterization of a biotic-stress-inducible glutathione transferase from Phaseolus vulgaris. Appl Biochem Biotechnol 172:595–609

    Article  CAS  PubMed  Google Scholar 

  • Chronopoulou E, Kontouri K, Chantzikonstantinou M, Pouliou F, Perperopoulou F, Voulgari G, Bosmali E, Axarli I, Nianiou-Obeidat I, Madesis P, Tsaftaris A, Labrou EN (2015) Plant glutathione transferases: structure, antioxidant catalytic function and in planta protective role in biotic and abiotic stress. Curr Chem Biol 8:58–75

    Article  Google Scholar 

  • Csiszar J, Horvath E, Vary Z, Galle A, Bela K, Brunner S et al (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

    Article  CAS  PubMed  Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1997) Purification of multiple glutathione transferases involved in herbicide detoxification from wheat (Triticum aestivum L.) treated with the safener fenchlora-zole-ethyl. Pestic Biochem Physiol 59:35–49

    Article  CAS  Google Scholar 

  • Cummins I, Bryant DN, Edwards R (2009) Safener responsiveness and multiple herbicide resistance in the weed black-grass (Alopecurus myosuroides). Plant Biotechnol J 7:807–820

    Article  CAS  PubMed  Google Scholar 

  • Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280

    Article  CAS  PubMed  Google Scholar 

  • Dirr H, Reinemer P, Huber R (1994) X-ray crystal structures of cytosolic glutathione S-transferases – implications for protein architecture, substrate recognition and catalytic function. Eur J Biochem 220:645–661

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Edwards R (2010a) Glutathione transferases. The Arabidopsis Book 8:e0131. https://doi.org/10.1199/tab.0131

    Article  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Edwards R (2010b) Roles for stress-inducible lambda glutathione transferases in flavonoid metabolism in plants as identified by ligand fishing. J Biol Chem 285:36322–36329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Cummins L, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification system in plants. Curr Opin Plant Biol 1:258–266

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Cole DJ, Edwards R (2000) Characteristics of a zeta class GST from Arabidopsis thaliana with a putative role in tyrosine catabolism. Arch Biochem Biophys 384:407–412

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Davis BG, Edwards E (2002a) Functional divergence in the glutathione transferase superfamily in plants. J Biol Chem 277:30859–30869

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002b) Plant glutathione transferases. Genome Biol 3:1–10

    Google Scholar 

  • Dixon DP, McEwen AG, Lapthorn AJ, Edwards R (2003) Forced evolution of a herbicide detoxifying glutathione transferase. J Biol Chem 278:23930–23935

    Article  CAS  PubMed  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 Biol Chem 283:20268–20276

    Article  CAS  PubMed  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

    Article  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Dueckersho K, Mueller S, Mueller MJ, Reinders J (2008) Impact of cyclopentenone-oxylipins on the proteome of Arabidopsis thaliana. Biochim Biophys Acta 1784:1975–1985

    Article  Google Scholar 

  • Edwards R, Dixon DP (2000) The role of glutathione transferases in herbicide metabolism. In: Cobb AH, Kirkwood RC (eds) Herbicides and their mechanisms of action. Sheffield Academic Press, Sheffield, pp 38–71

    Google Scholar 

  • Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods Enzymol 401:169–186

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Frova C (2006) Glutathione transferases in the genomics era: new insights and perspectives. Biomol Eng 23:149–169

    Article  CAS  PubMed  Google Scholar 

  • George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin-induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318

    Google Scholar 

  • Ginsberg G, Smolenski S, Hattis D, Guyton KZ, Johns DO, Sonawane B (2009) Genetic polymorphism in glutathione transferases (GST): population distribution of GSTM1, T1, and P1 conjugating activity. J Toxicol Environ Health B Crit Rev 12:389–439

    Article  CAS  PubMed  Google Scholar 

  • Gonneau M, Mornet R, Laloue MA (1998) Nicotiana plumbaginifolia protein labeled with an azido cytokinin agonist is a glutathione S-transferase. Physiol Plant 103:114–124

    Google Scholar 

  • Gunning V, Tzafestas K, Sparrow H, Johnston EJ, Brentnall AS, Potts JR, Rylott EL, Bruce NC (2014) Arabidopsis glutathione transferases U24 and U25 exhibit a range of detoxification activities with the environmental pollutant and explosive, 2,4,6-trinitrotoluene. Plant Physiol 165:854–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huberts DH, van der Klei IJ (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta 1803:520–525

    Article  CAS  PubMed  Google Scholar 

  • Ivarsson Y, Mannervik B (2007) Combinatorial protein chemistry in three dimensions: a paradigm for the evolution of glutathione transferases with novel activities. In Awasthi YC (ed) Toxicology of glutathione transferases, CRC Press, Boca Raton, Florida; pp 213-231. Please provide publisher name and location for Ivarsson and Mannervik (2007) and Jacquot et al. (2013).Were added

    Google Scholar 

  • Jacquot JP, Dietz KJ, Rouhier N, Meux E, Lallement PA, Selles B, Hecker A. Redox regulation in plants: glutathione and “redoxin” related families. U. Jakob and D. Reichmann (eds.), Oxidative stress and redox regulation. 2013; Springer, Dordrecht, pp. 213–231

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeffery CJ (2009) Moonlighting proteins- an update. Mol BioSyst 5:345–350

    Article  CAS  PubMed  Google Scholar 

  • Jia B, Sun M, Sun X, Li R, Wang Z, Wu J, Wei Z, DuanMu H, Xiao J, Zhu Y (2016) Overexpression of GsGSTU13 and SCMRP in Medicago sativa confers increased salt-alkaline tolerance and methionine content. Physiol Plant 156:176–189

    Article  CAS  Google Scholar 

  • Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2016) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101

    Google Scholar 

  • Kampranis SC, Damianova R, Atallah M et al (2000) A novel plant glutathione S-transferase/peroxidase suppresses bax lethality in yeast. J Biol Chem 275:29207–29216

    Article  CAS  PubMed  Google Scholar 

  • Kao CW, Bakshi M, Sherameti I, Dong S, Reichelt M, Oelmüller R, Yeh KW (2016) A Chinese cabbage (Brassica campetris subsp. Chinensis) τ-type glutathione-S-transferase stimulates Arabidopsis development and primes against abiotic and biotic stress. Plant Mol Biol 92:643–659

    Article  CAS  PubMed  Google Scholar 

  • Kapoli P, Axarli IA, Platis D, Fragoulaki M, Paine M, Hemingwayb J, Vontas J, Labrou EN (2008) Engineering sensitive glutathione transferase for the detection of xenobiotics. Biosens Bioelectron 24:498–503

    Article  CAS  PubMed  Google Scholar 

  • Karpusas M, Axarli I, Chiniadis L, Papakyriakou A, Bethanis K, Scopelitou K, Clonis YD, Labrou NE (2013) The interaction of the chemotherapeutic drug chlorambucil with human glutathione transferase A1-1: kinetic and structural analysis. PLoS One 8:e56337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Differential expression of rice lambda class GST gene family members during plant growth, development, and in response to stress conditions. Plant Mol Biol Rep 31:569–580

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Labudda M, Azam FMS (2014) Glutathione-dependent responses of plants to drought: a review. Acta Soc Bot Pol 83:3–12

    Article  CAS  Google Scholar 

  • Lallement P-A, Brouwer B, Keech O, Hecker A, Rouhier N (2014a) The still mysterious roles of cysteine-containing glutathione transferases in plants. Front Pharmacol 5:1–22

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Lallement PA, Meux E, Gualberto JM, Dumarcay S, Favier F, Didierjean C, Saul F, Haouz A, Morel-Rouhier M, Gelhaye E, Rouhier N, Hecker A (2015) Glutathionyl-hydroquinone reductases from poplar are plastidial proteins that deglutathionylate both reduced and oxidized glutathionylated quinones. FEBS Lett 589:37–44

    Article  CAS  PubMed  Google Scholar 

  • Lam LK, Zhang Z, Board PG, Xun L (2012) Reduction of benzoquinones to hydroquinones via spontaneous reaction with glutathione and enzymatic reaction by S-glutathionyl-hydroquinone reductases. Biochemistry 51:5014–5021

    Article  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

    Article  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 Biol Chem 288:24441–24451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H-C, Toung Y-PS TY-SL, Tu C-PD (1995) A molecular genetic approach for the identification of essential residues in human glutathione S-transferase function in Escherichia coli. J Biol Chem 270:99–109

    Article  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

    Article  CAS  PubMed  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

    Google Scholar 

  • Liu H, He J, Zhao R, Chi C, Bao Y (2015) A novel biomarker for marine environmental pollution of pi-class glutathione S-transferase from Mytilus coruscus. Ecotoxicol Environ Saf 118:47–54

    Article  CAS  PubMed  Google Scholar 

  • Lu WD, Atkins WA (2004) Novel antioxidant role for ligandin behavior of glutathione S-transferases: attenuation of the photodynamic effects of hypericin. Biochemistry 43:12761–12769

    Article  CAS  PubMed  Google Scholar 

  • Mannervik B, Danielson UH (1988) Glutathione transferases: structure and catalytic activity. CRC Crit Rev Biochem 23:283–337

    Article  CAS  PubMed  Google Scholar 

  • Mashiyama ST, Malabanan MM, Akiva E, Bhosle R, Branch MC et al (2014) Large-scale determination of sequence, structure, and function relationships in cytosolic glutathione transferases across the biosphere. PLoS Biol 12:1–19

    Article  Google Scholar 

  • Meyer DJ, Crease DJ, Ketterer B (1995) Forward and reverse catalysis and product sequestration by human glutathione S-transferases in the reaction of GSH with dietary aralkyl isothiocyanates. Biochem J 306:565–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohsenzadeh S, Esmaeili M, Moosavi F, Shahrtash M, Saffari B, Mohabatkar H (2011) Plant glutathione S-transferase classification, structure and evolution. African J Biotech 10:8160–8165

    Article  CAS  Google Scholar 

  • Morel M, Meux E, Mathieu Y, Thuillier A, Chibani K, Harvengt L et al (2013) Xenomic networks variability and adaptation traits in wood decaying fungi. Microb Biotechnol 6:248–263

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuefeind T, Huber R, Dasenbrock H, Prade L, Bieseler B (1997a) Crystal structure of herbicide-detoxifying maize glutathione S-transferase-I in complex with lactoylglutathione: evidence for an induced- fit mechanism. J Mol Biol 274:446–453

    Google Scholar 

  • Neuefeind T, Huber R, Reinemer P, Knäblein J, Prade L, Mann K, Bieseler B (1997b) Cloning, sequencing, crystallization and X-ray structure of glutathione S-transferase-III from Zea mays Var. mutin: a leading enzyme in detoxification of maize herbicides. J Mol Biol 274:577–587

    Article  CAS  PubMed  Google Scholar 

  • Parbhoo N (2013) Topologically conserved hydrophobic residues of the thioredoxin C-subdomain stabilise GSTs. WIReDSpace

    Google Scholar 

  • Pearson WR (2005) Phylogenies of glutathione transferase families. Methods Enzymol 401:186–204

    Article  CAS  PubMed  Google Scholar 

  • Pickett CB, Lu AYH (1989) Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem 58:743–764

    Article  CAS  PubMed  Google Scholar 

  • Polekhina G, Board PG, Blackburn AC, Parker MW (2001) Crystal structure of maleylacetoacetate isomerase/glutathione transferase zeta reveals the molecular basis for its remarkable catalytic promiscuity. Biochemistry 40:1567–1576

    Article  CAS  PubMed  Google Scholar 

  • Reinemer P, Prade L, Hof P, Neuefeind T, Huber R, Zettl R, Palme K, Schell J, Jkoelln I, Bartunik H, Bieseler B (1996) An inducible glutathione S-transferase in soybean hypocotyl is localized in the apoplast. Plant Physiol 3:1185–1190

    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

    Article  CAS  PubMed  Google Scholar 

  • Roxas VP, Smith RK Jr, 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

    Article  CAS  PubMed  Google Scholar 

  • Rushmore TH, Pickett CB (1993) Glutathione S-transferases, structure, regulation, and therapeutic implications. J Biol Chem 268:11475–11478

    CAS  PubMed  Google Scholar 

  • Schröder P (2001) The role of glutathione and glutathione S-transferase in plant reaction and adaptation to xenobiotics. Plant Ecophysiol 2:155–183

    Article  Google Scholar 

  • Shaokui W, Kun W, Qingbo Y, Xueying L, Zhengbin L, Xiaoyan L, Ruizhen Z, Haitao Z, Guojun D, Qian Q, Guiquan Z, Xiangdong F (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954

    Google Scholar 

  • Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non- mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Hashimoto N, Nakayama I, Nakao T, Mizutani H, Unai T (1995) A novel isourazole herbicide, fluthiacet-methyl, is a potent inhibitor of protoporphyrinogen oxidase after isomerization by glutathione S-transferase. Plant Cell Physiol 36:625–632

    CAS  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 7:539

    Article  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. Biochim Biophys Acta 1854:166–177

    Article  CAS  PubMed  Google Scholar 

  • Skopelitou K, Muleta AW, Papageorgiou AC, Chronopoulou EG, Pavli O, Flemetakis E, Skaracis GN, Labrou NE (2017) Characterization and functional analysis of a recombinant tau class glutathione transferase GmGSTU2-2 from Glycine max. Int J Biol Macromol 94:802–812

    Article  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

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Talalay P, De Long MJ, Prochaska HJ (1988) Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc Natl Acad Sci U S A 85:8261–8265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thom R, Cummins I, Dixon DP, Edwards R, Cole DJ, Lapthorn AJ (2002) Structure of a tau class glutathione S-transferase from wheat active in herbicide detoxification. Biochemistry 41:7008–7020

    Article  CAS  PubMed  Google Scholar 

  • Tzafestas K, Razalan MM, Gyulev I, Mazari AM, Mannervik B, Rylott EL, Bruce NC (2016) Expression of a drosophila glutathione transferase in Arabidopsis confers the ability to detoxify the environmental pollutant, and explosive, 2,4,6-trinitrotoluene. New Phytol. https://doi.org/10.1111/nph.14326

  • Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Liu Y-J, Zeng Q-Y (2014) Biochemical functions of the glutathione transferase supergene family of Larix kaempferi. Plant Physiol Biochem 77:99–107

    Google Scholar 

  • Zettl R, Schell J, Palme K (1994) Photoaffinity labelling 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 U S A 91:689–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

FSA and NEL extend their appreciation to the International Scientific Partnership Program (ISPP) at King Saud University for funding this research work through ISPP# 0071.

Author information

Authors and Affiliations

  1. Laboratory of Enzyme Technology, Department of Biotechnology, School of Food, Biotechnology and Development, Agricultural University of Athens, 75 Iera Odos Street, GR-11855, Athens, Greece

    Evangelia Chronopoulou, Fotini Pouliou, Fereniki Perperopoulou, Nikolaos Georgakis, Elisavet Ioannou & Nikolaos E. Labrou

  2. Department of Biochemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Farid S. Ataya

  3. Laboratory of Genetics and Plant Breeding, School of Agriculture, Forestry and Natural Environment Aristotle University of Thessaloniki, P.O. Box 261, Thessaloniki, GR-54124, Greece

    Irini Nianiou-Obeidat

  4. Institute of Applied Biosciences, CERTH, 6th km Charilaou-Thermis Road, P.O. Box 361, Thermi, GR-57001, Thessaloniki, Greece

    Panagiotis Madesis

Authors
  1. Evangelia Chronopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farid S. Ataya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fotini Pouliou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fereniki Perperopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nikolaos Georgakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Irini Nianiou-Obeidat
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Panagiotis Madesis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Elisavet Ioannou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nikolaos E. Labrou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nikolaos E. Labrou .

Editor information

Editors and Affiliations

  1. Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, Bangladesh

    Mohammad Anwar Hossain

  2. Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh

    Mohammad Golam Mostofa

  3. Department of Plant Breeding, CEBAS-CSIC, Murcia, Murcia, Spain

    Pedro Diaz-Vivancos

  4. Department of Botany, University of Otago, Dunedin, Otago, New Zealand

    David J Burritt

  5. Department of Applied Biological Science, Kagawa University, Kagawa, Japan

    Masayuki Fujita

  6. RIKEN Center for Sustainable Resource Science, Signaling Pathway Research Unit, Yokohama, Japan

    Lam-Son Phan Tran

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Chronopoulou, E. et al. (2017). Structure, Evolution and Functional Roles of Plant Glutathione Transferases. In: Hossain, M., Mostofa, M., Diaz-Vivancos, P., Burritt, D., Fujita, M., Tran, LS. (eds) Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-66682-2_9

Download citation

Publish with us

Policies and ethics

Search

Navigation