Skip to main content
SpringerLink
Log in

Plant Glutathione Transferases in Abiotic Stress Response and Herbicide Resistance

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

Abstract

Plant responses and adaptations to stress conditions are of great interest for both basic and applied science, and represent the key factors for the improvement of economically important crops worldwide. Glutathione S-transferases (GSTs, EC. 2.5.1.18) are multifunctional enzymes encoded by a highly divergent ancient gene family. GSTs catalyze the conjugation of tripeptide glutathione (GSH) with endogenous electrophilic compounds (secondary metabolites, hydroperoxides) and xenobiotics, such as herbicides, leading to their cellular detoxification. Therefore, GSTs are implicated in metabolism-based herbicide resistance in crop weeds. This chapter discusses the involvement of plant GSTs in abiotic stress response with focus on metabolism-based herbicide resistance and attempts to give an overview of their catalytic roles and in planta function.

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

  • 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 

  • Axarli I, Muleta AW, Chronopoulou EG, Papageorgiou AC, Labrou NE (2017) Directed evolution of glutathione transferases towards a selective glutathione-binding site and improved oxidative stability. BBA(General Subjects) 1861:3416–3428

    Article  CAS  Google Scholar 

  • Bakkali Y, Ruiz-Santaella JP, Osuna MD, Wagner J, Fischer AJ, De Prado R (2007) Late watergrass (Echinochloa phyllopogon): mechanisms involved in the resistance to fenoxaprop-p-ethyl. J Agr Food Chem 55:4052–4058

    Article  CAS  Google Scholar 

  • Bakshi S, Dewan D (2013) Status of transgenic cereal crops: a review. Clon Transgen 3:119

    Google Scholar 

  • Banday ZZ, Nandi AK (2017) Arabidopsis thaliana GLUTATHIONE-S-TRANSFERASE THETA 2 interacts with RSI1/FLD to activate systemic acquired resistance. Mol Plant Pathol. https://doi.org/10.1111/mpp.12538

  • Benbrook CM (2012) Impacts of genetically engineered crops on pesticide usein the U.S. the first sixteen years. Environ Sci Eur 24:24

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Bilang J, Sturm A (1995) Cloning and characterization of a glutathione S-transferase that can be photolabeled with 5-azido-indole-3-acetic acid. Plant Physiol 109:253–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowler C, Van Camp W, Van Montagu M, Inze D (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218

    Article  CAS  Google Scholar 

  • Burla B, Pfrunder S, Nagy R, Francisco RM, Lee Y, Martinoia E (2013) Vacuolar transport of abscisic acid glucosyl ester is mediated by ATP-binding cassette and proton-antiport mechanisms in Arabidopsis. Plant Physiol 163:1446–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan C, Lam HM (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 

  • Cho HY, Kong KH (2005) Molecular cloning, expression, and characterization of a phi-type glutathione S-transferase from Oryza sativa. Pestic Biochem Phys 83:29–36

    Article  CAS  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 

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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cummins I, Moss S, Cole DJ, Edwards R (1997b) Glutathione transferases in herbicide-resistant and herbicide-susceptible black-grass (Alopecurus myosuroides). Pest Manag Sci 51:244–250

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Cummins I, O’Hagan D, Jablonkai I, Cole DJ, Hehn A, Werck-Reichhart D, Edwards R (2003) Cloning, characterization and regulation of a family of phi class glutathione transferases from wheat. Plant Mol Biol 52:591–603

    Article  CAS  PubMed  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 

  • 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 Nat Acad Sci USA 110:5812–5817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. CMLS 57:779–795

    Article  CAS  PubMed  Google Scholar 

  • Del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837

    Article  PubMed  CAS  Google Scholar 

  • Deng F, Hatzios KK (2002a) Characterization and safener induction of multiple glutathione S-transferases in three genetic lines of rice. Pestic Biochem Phys 72:24–39

    Article  CAS  Google Scholar 

  • Deng F, Hatzios KK (2002b) Purification and characterization of two glutathione S-transferase isozymes from indica-type rice involved in herbicide detoxification. Pestic Biochem Phys 72:10–23

    Article  CAS  Google Scholar 

  • Deng F, Nagao A, Shim I, Usui K (1997) Induction of glutathione S-trasnferase isozymes in rice shoots treated with a combination of petilachlor and fenclorim. J Weed Sci Tech 42:277–288

    Article  CAS  Google Scholar 

  • DeRidder BP, Goldsbrough PB (2006) Organ-specific expression of glutathione S-transferases and the efficacy of herbicide safeners in Arabidopsis. Plant Physiol 140:167–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixit P, Mukherjee PK, Ramachandran V, Eapen S (2011) Glutathione transferase from Trichoderma Virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6:e16360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon D, Cole DJ, Edwards R (1997) Characterisation of multiple glutathione transferases containing the GST I subunit with activities toward herbicide substrates in maize (Zea mays). Pestic Sci 50:72–82

    Article  CAS  Google Scholar 

  • Dixon DP, Cole DJ, Edwards R (1999) Dimerisation of maize glutathione transferases in recombinant bacteria. Plant Mol Biol 40:997–1008

    Article  CAS  PubMed  Google Scholar 

  • Dixon DP, Laphtorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.3001–3004.3010

    Article  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 

  • Dubey AK, Kumar N, Sahu N, Verma PK, Ranjan R, Chakrabarty D, Behera SK, Mallick S (2016) Response of two rice cultivars differing in their sensitivity towards arsenic, differs in their expression of glutaredoxin and glutathione S-transferase genes and antioxidant usage. Ecotoxicol Environ Saf 124:393–405

    Article  CAS  PubMed  Google Scholar 

  • Duhoux A, Carrère S, Gouzy J, Bonin L, Délye C (2015) RNA-Seq analysis of rye-grass transcriptomic response to an herbicide inhibiting acetolactate-synthase identifies transcripts linked to non-target-site-based resistance. Plant Mol Biol 87:473–487

    Article  CAS  PubMed  Google Scholar 

  • Duhoux A, Carrère S, Duhoux A, Délye C (2017) Transcriptional markers enable identification of rye-grass (Lolium sp.) plants with non-target-site-based resistance to herbicides inhibiting acetolactate-synthase. Plant Sci 257:22–36

    Article  CAS  PubMed  Google Scholar 

  • Duke SO (2011) Glyphosate degradation in glyphosate-resistant and-susceptible crops and weeds. J Agric Food Chem 59:5835–5841

    Article  CAS  PubMed  Google Scholar 

  • Feng PCC, CaJacob CA, Martino-Catt SJ, Cerny RE, Elmore GA, Heck GR, Huang J, Kruger WM, Malven M, Miklos JA, Padgette SR (2010) Glyphosate-resistant crops: developing the next generation products. In: Nandula VK (ed) Glyphosate resistance in crops and weeds: history, development, and management. Wiley, Hoboken

    Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ, Psip PP (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Fuerst EP, Gronwald JW (1986) Induction of rapid metabolism of metolachlor in sorghum (Sorghum bicolor) shoots by Cga-92194 and other antidotes. Weed Sci 34:354–361

    CAS  Google Scholar 

  • Funke T, Han H, Healy-Fried ML, Fischer M, Schonbrunn E (2006) Molecular basis for the herbicide resistance of roundup ready crops. Proc Nat Acad Sci USA 103:13010–13015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray SB, Brady SM (2016) Plant developmental responses to climate change. Dev Biol 419:64–77

    Article  CAS  PubMed  Google Scholar 

  • Green JM (2014) Current state of herbicides in herbicide-resistant crops. Pest Manag Sci 70:1351–1357

    Article  CAS  PubMed  Google Scholar 

  • Hatton PJ, Cummins I, Cole DJ, Edwards R (1999) Glutathione transferases involved in herbicide detoxification in the leaves of Setaria faberi (giant foxtail). Physiol Plant 105:9–16

    Article  CAS  Google Scholar 

  • Hatzios KK, Burgos N (2004) Metabolism-based herbicide resistance: regulation by safeners. Weed Sci 52:454–467

    Article  CAS  Google Scholar 

  • Heap I (2014) Global perspective of herbicide-resistant weeds. Pest Manag Sci 70:1306–1315

    Article  CAS  PubMed  Google Scholar 

  • Inupakutika MA, Sengupta S, Devireddy AR, Azad RK, Mittler R (2016) The evolution of reactive oxygen species metabolism. J Exp Bot 67:5933–5943

    Article  CAS  PubMed  Google Scholar 

  • Irzyk GP, Fuerst EP (1993) Purification and characterization of a glutathione-s-transferase from benoxacor-treated maize (Zea mays). Plant Physiol 102:803–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Yang Y, Jia LX, Lin JL, Liu Y, Pan B, Lin Y (2016) Biological responses of wheat (Triticum aestivum) plants to the herbicide simetryne in soils. Ecotoxicol Environ Saf 127:87–94

    Article  CAS  PubMed  Google Scholar 

  • Karavangeli M, Labrou NE, Clonis YD, Tsaftaris A (2005) Development of transgenic tobacco plants overexpressing maize glutathione S-transferase I for chloroacetanilide herbicides phytoremediation. Biomol Eng 22:121–128

    Article  CAS  PubMed  Google Scholar 

  • Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32

    Article  PubMed  CAS  Google Scholar 

  • Kasote DM, Katyare SS, Hegde MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci 11:982–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaundun SS (2014) Resistance to acetyl-CoA carboxylase-inhibiting herbicides. Pest Manag Sci 70:1405–1417

    Article  CAS  PubMed  Google Scholar 

  • Kissoudis C, Kalloniati C, Flemetakis E, Madesis P, Labrou NE, Tsaftaris A, Nianiou-Obeidat I (2015a) Maintenance of metabolic homeostasis and induction of cytoprotectants and secondary metabolites in alachlor treated GmGSTU4 overexpressing tobacco plants, as resolved by metabolomics. Plant Biotechnol Rep 9:287–296

    Article  Google Scholar 

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

    Article  CAS  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

    Google Scholar 

  • Kleinman Z, Rubin B (2017) Non-target-site glyphosate resistance in Conyza bonariensis is based on modified subcellular distribution of the herbicide. Pest Manag Sc 73:246–253

    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 

  • Labrou NE, Muharram MM, Abdelkader MS (2016) Delineation of the structural and functional role of Arg111 in GSTU4-4 from Glycine max by chemical modification and site-directed mutagenesis. Biochim Biophys Acta 1864:1315–1321

    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 

  • Lambert DM, Larson JA, Roberts RK, English BC, Zhou XV, Falconer LL, Hogan RJ Jr, Johnson JL, Reeves JM (2017) Resistance is futile: estimating the costs of managing herbicide resistance as a first-order Markov process and the case of U.S. upland cotton producers. Agric Econ 48:1–10

    Article  Google Scholar 

  • Le Martret B, Poage M, Shiel K, Nugent GD, Dix PJ (2011) Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J 9:661–673

    Article  PubMed  CAS  Google Scholar 

  • Li G, Wu SG, Yu RX, Cang T, Chen LP, Zhao XP, Cai LM, Wu CX (2013) Identification and expression pattern of a glutathione S-transferase in Echinochloa crus-galli. Weed Res 53:314–321

    Google Scholar 

  • Li D, Gao Q, Li X, Pang S, Liu Z, Wang C, Tan W (2016) Characterization of glutathione S-transferases in the detoxification of metolachlor in two maize cultivars of differing herbicide tolerance. Pestic Biochem Physiol. https://doi.org/10.1016/j.pestbp.2016.12.003

  • 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

    Google Scholar 

  • Liu XF, Li JY (2002) Characterization of an ultra-violet inducible gene that encodes glutathione S-transferase in Arabidopsis thaliana. Acta Genet Sinica 29:458–465

    Google Scholar 

  • Liu D, Liu Y, Rao J, Wang G, Li H, Ge F, Chen C (2013) Overexpression of the glutathione S-transferase gene from Pyrus pyrifolia fruit improves tolerance to abiotic stress in transgenic tobacco plants. Mol Biol (Mosk) 47:591–601

    Article  CAS  Google Scholar 

  • Lo Cicero L, Madesis P, Tsaftaris A, Lo Piero AR (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. Phytochemistry 116:69–77

    Article  CAS  PubMed  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-Transferasesin plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  CAS  PubMed  Google Scholar 

  • McGonigle B, Lau SMC, Jennings LD, O’Keefe DP (1998) Homoglutathione selectivity by soybean glutathione S-transferases. Pestic Biochem Physiol 62:15–25

    Article  CAS  Google Scholar 

  • McGonigle B, Keeler SJ, Lan SMC, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milligan AS, Daly A, Parry MAJ, Lazzeri PA, Jepson I (2001) The expression of a maize glutathione S-transferase gene in transgenic wheat confers herbicide tolerance, both in planta and in vitro. Mol Breed 7:301–315

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M (2015) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252:461–475

    Article  CAS  PubMed  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. https://doi.org/10.1007/s00299-017-2139-7

  • Padgette SR, Kolacz KH, Delannay X, Re DB, Lavallee BJ, Tinius CN, Rhodes WK, Otero YI, Barry GF, Eichholtz DA, Peschke VM, Nida DL, Taylor NB, Kishore GM (1995) Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci 35:1451–1461

    Article  CAS  Google Scholar 

  • Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci 8:581

    Article  PubMed  PubMed Central  Google Scholar 

  • Pang S, Duan L, Liu Z, Song X, Li X, Wang C (2012) Co-induction of a glutathione-s-transferase, a glutathione transporter and an ABC transporter in maize by xenobiotics. PLoS One 7:e40712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park AE, Kim IS, Do H, Jeon BW, Lee CW, Roh SJ, Shin SC, Park H, Kim YS, Kim YH, Yoon HS, Lee JH, Kim HW (2016) Structure and catalytic mechanism of monodehydroascorbate reductase, MDHAR, from Oryza sativa L. japonica. Sci Rep 6:33903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perry ED, Moschini G, Hennessey DA (2016) Testing for complementarity: glyphosate tolerant soybeans and conservation tillage. Am J Agric Econ 98:765–784

    Article  Google Scholar 

  • Popelka M, Tuinstra M, Weil F (2010) Discovering genes for abiotic stress tolerance in crop plants. Clifford. Wiley-Blackwell Ames, Aiowa

    Google Scholar 

  • Rao Madhava KV, Raghavendra AS, Reddy Janardhan K (2006) Physiology and molecular biology of stress tolerance in plants. Springer Netherlands, Dordrecht

    Book  Google Scholar 

  • Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    Article  CAS  PubMed  Google Scholar 

  • Rossini L, Jepson I, Greenland AJ, Gorla MS (1996) Characterization of glutathione S-transferase isoforms in three maize inbred lines exhibiting differential sensitivity to alachlor. Plant Physiol 112:1595–1600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234

    Article  CAS  PubMed  Google Scholar 

  • Saidi I, Chtourou Y, Djebali W (2014) Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J Plant Physiol 171:85–91

    Article  CAS  PubMed  Google Scholar 

  • Sammons RD, Gaines TA (2014) Glyphosate resistance: state of knowledge. Pest Manag Sci 70:1367–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samsel A, Seneff S (2013) Glyphosate’s suppression of cytochrome P450 enzymes and amino acid biosynthesis by the gut microbiome: pathways to modern diseases. Entropy 15:1416–1463

    Article  CAS  Google Scholar 

  • Schröder P (2001) The role of glutathione and glutathione S-transferase in plant reaction and adaptation to xenobiotics. Kluwer, Dordrecht

    Book  Google Scholar 

  • Schröder P, Scheer CE, Diekmann F, Stampfl A (2007) How plants cope with foreign compounds – translocation of xenobiotic glutathione conjugates in roots of barley (Hordeum vulgare). Environ Sci Pollut R 14:114–122

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016a) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143

    PubMed  PubMed Central  Google Scholar 

  • Singh R, Singh S, Parihar P, Mishra RK, Tripathi DK, Singh VP, Chauhan DK, Prasad SM (2016b) Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front Plant Sci 7:1299

    PubMed  PubMed Central  Google Scholar 

  • Skipsey M, Andrews CJ, Townson JK, Jepson I, Edwards R (1997) Substrate and thiol specificity of a stress-inducible glutathione transferase from soybean. FEBS Lett 409:370–374

    Article  CAS  PubMed  Google Scholar 

  • Skipsey M, Cummins I, Andrews CJ, Jepson I, Edwards R (2005) Manipulation of plant tolerance to herbicides through co-ordinated metabolic engineering of a detoxifying glutathione transferase and thiol cosubstrate. Plant Biotechnol J 3:409–420

    Article  CAS  PubMed  Google Scholar 

  • Skipsey M, Knight KM, Brazier-Hicks M, Dixon DP, Steel PG, Edwards R (2011) Xenobiotic responsiveness of Arabidopsis thaliana to a chemical series derived from a herbicide safener. J Biol Chem 286:32268–32276

    Article  CAS  PubMed  PubMed Central  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 

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

    Article  CAS  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 

  • Tripathi A, Indoliya Y, Tiwari M, Tiwari P, Srivastava D, Verma PK, Verma S, Gautam N, Chakrabarty D (2014) Transformed yeast (Schizosaccharomyces pombe) overexpressing rice tau class glutathione S-transferase (OsGSTU30 and OsGSTU41) shows enhanced resistance to hexavalent chromium. Metallomics 6:1549–1557

    Article  CAS  PubMed  Google Scholar 

  • Viger PR, Eberlein CV, Fuerst EP, Gronwald JW (1991) Effects of Cga-154281 and temperature on metolachlor absorption and metabolism, glutathione content, and glutathione-S-transferase activity in corn (Zea mays). Weed Sci 39:324–328

    CAS  Google Scholar 

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

    Article  PubMed Central  CAS  Google Scholar 

  • Walsh MJ, Powles SB (2014) Management of herbicide resistance in wheat cropping systems: learning from the Australian experience. Pest Manag Sci 70:1324–1328

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Xing XJ, Tian YS, Peng RH, Xue Y, Zhao W, Yao QH (2015) Transgenic Arabidopsis plants expressing tomato glutathione s-transferase showed enhanced resistance to salt and drought stress. PLoS One 10:e0136960

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang G, Wang Y, Xia D, Gao C, Wang C, Yang C (2014) Overexpression of a GST gene (ThGSTZ1) from Tamarix hispida improves drought and salinity tolerance by enhancing the ability to scavenge reactive oxygen species. Plant Cell Tissue Organ Cult 117:99–112

    Article  CAS  Google Scholar 

  • Yang Q, Deng W, Li X, Yu Q, Bai L, Zheng M (2016a) Target-site and non-target-site based resistance to the herbicide tribenuron-methyl in flixweed (Descurainia sophia L.) BMC Genomics 17:551

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang G, Xu Z, Peng S, Sun Y, Jia C, Zhai M (2016b) 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

    Article  CAS  PubMed  Google Scholar 

  • Yu Q, Powles S (2014) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:1106–1118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan JS, Tranel PJ, Stewart CN Jr (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13

    Article  CAS  PubMed  Google Scholar 

  • Zhang O, Riechers DE (2004) Proteomic characterization of herbicide safener-induced proteins in the coleoptile of Triticum tauschii seedlings. Proteomics 4:2058–2071

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Lin CY, Shen ZC (2011) Development of transgenic glyphosate-resistant rice with G6 gene encoding 5-enolpyruvylshikimate-3-phosphate synthase. Agri Sci China 10:1307–1312

    Article  CAS  Google Scholar 

Download references

Acknowledgement

We acknowledge support by the research project for excellence IKY/SIEMENS; Grants4Targets 2016-2-25, funded by Bayer CropScience AG; the ISPP#0071 program, funded by King Saud University; and the IKY program “Strengthening Postdoctoral Researchers” (1st Cycle), funded by the National Strategic Reference Framework (ESPA) 2014-2020.

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, Nikolaos Georgakis, Fereniki Perperopoulou, Fotini Pouliou, Eleni Vasilopoulou, Elisavet Ioannou & Nikolaos E. Labrou

  2. 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

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

    Panagiotis Madesis

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

    Farid S. Ataya

Authors
  1. Evangelia Chronopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nikolaos Georgakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Irini Nianiou-Obeidat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Panagiotis Madesis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fereniki Perperopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fotini Pouliou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eleni Vasilopoulou
    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. Farid S. Ataya
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. 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). Plant Glutathione Transferases in Abiotic Stress Response and Herbicide Resistance. 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_10

Download citation

Publish with us

Policies and ethics

Search

Navigation