Plant Adaptation to Stress Conditions: The Case of Glutathione S-Transferases (GSTs)

  • Evangelia Stavridou
  • Georgia Voulgari
  • Irini Bosmali
  • Evangelia G. Chronopoulou
  • Luca Lo Cicero
  • Angela Roberta Lo Piero
  • Nikolaos E. Labrou
  • Athanasios Tsaftaris
  • Irini Nianiou-Obeidat
  • Panagiotis MadesisEmail author


Plants, unlike animals, are anchored to one place and, therefore, forced to sustain any environmental condition present. Unfavourable environmental conditions include abiotic (extreme temperatures, water deficits, floods, salinity, light intensities) and biotic (pests, viral, bacterial and fungal diseases) stress factors. Both types of stresses induce the production of reactive oxygen species (ROS), which damage macromolecules such as proteins, lipids, nucleic acids and cell structures like membranes. The effect of each stress factor depends on its intensity. When the stress is severe and the production of ROS is high, it might result to plant death. To avoid such event, plants have developed advanced physiological and chemical defence mechanisms of stress avoidance and/or tolerance, which allow growth only when the environmental conditions are optimum for each species, like in the case of seed dormancy. Plants have also evolved specific enzymatic defence mechanisms, including enzymes like catalase, peroxidase, super oxide dismutase and glutathione transferases. These defence mechanisms help plants either to avoid adverse environmental conditions or to combat their negative effects. A major defence mechanism involves the action of antioxidant enzymes. Glutathione transferases (GSTs) are antioxidant enzymes of great importance for the detoxification of plants from toxic compounds. GSTs have also important involvement in plant stress tolerance against biotic and abiotic stress tolerance like extreme heat, cold, salt and herbicides.


Glutathione transferase GST Oxidative stress Herbicide detoxification Salinity Water deficit High and low temperatures Heavy metal stress Tolerance mechanisms 


  1. Ahammed GJ, Gao CJ, Ogweno JO, Zhou YH, Xia XJ, Mao WH, Shi K, Yu JQ (2012) Brassinosteroids induce plant tolerance against phenanthrene by enhancing degradation and detoxification in Solanum lycopersicum L. Ecotoxicol Environ Saf 80:28–36. Scholar
  2. Ahsan H, Ali A, Ali R (2003) Oxygen free radicals and systemic autoimmunity. Clin Exp Immunol 131:398–404. Scholar
  3. Alvarez S, Berla BM, Sheffield J, Cahoon RE, Jez JM, Hicks LM (2009) Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9:2419–2431. Scholar
  4. Amini F, Ehsanpour AA, Hoang QT, Shin JS (2007) Protein pattern changes in tomato under in vitro salt stress. Russ J Plant Physiol 54:464–471. Scholar
  5. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396. Scholar
  6. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544. Scholar
  7. 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. Scholar
  8. 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. Biochim Biophys Acta – Gen Subj 1861:3416–3428. Scholar
  9. 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 Agric Food Chem 55:4052–4058. Scholar
  10. Basantani M, Srivastava A (2007) Plant glutathione transferases—a decade falls short. Can J Bot 85:443–456. Scholar
  11. Basu S, Roychoudhury A, Saha PP, Sengupta DN (2009) Differential antioxidative responses of indica rice cultivars to drought stress. Plant Growth Regul 60:51–59. Scholar
  12. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. Scholar
  13. Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34. Scholar
  14. 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. Scholar
  15. Bowler C, Van Camp W, Van Montagu M, Inzé D, Asada K (1994) Superoxide dismutase in plants superoxide dismutase in plants. CRC Crit Rev Plant Sci 13:199–218CrossRefGoogle Scholar
  16. Boyer JS (1982) Plant productivity and environment. Science 218:443–448. Scholar
  17. Chan C, Lam H (2017) A putative lambda class glutathione S -transferase enhances plant survival under salinity stress. Plant Cell Physiol 55:570–579. Scholar
  18. Chen J-H, Jiang H-W, Hsieh E-J, Chen H-Y, Chien C-T, Hsieh H-L, Lin T-P (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351. Scholar
  19. Cho H-Y, Kong K-H (2005) Molecular cloning, expression, and characterization of a phi-type glutathione S-transferase from Oryza sativa. Pestic Biochem Physiol 83:29–36. Scholar
  20. Choi YI, Noh EW, Kim HJ, Shim D (2013) Overexpression of poplar GSTU51 confers selective tolerance to both mercury and methyl viologen but not to CDNB or cadmium in transgenic poplars. Plant Biotechnol Rep 7:175–184. Scholar
  21. Chronopoulou EG, Labrou NE (2009) Glutathione transferases: emerging multidisciplinary tools in red and green biotechnology. Recent Pat Biotechnol 3:211–223CrossRefPubMedGoogle Scholar
  22. 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. Scholar
  23. 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. Scholar
  24. Cia MC, Guimarães ACR, Medici LO, Chabregas SM, Azevedo RA (2012) Antioxidant responses to water deficit by drought-tolerant and -sensitive sugarcane varieties. Ann Appl Biol 161:313–324. Scholar
  25. Cox A, Venkatachalam P, Sahi S, Sharma N (2017) Plant physiology and biochemistry reprint of: silver and titanium dioxide nanoparticle toxicity in plants: a review of current research. Plant Physiol Biochem 110:33–49. Scholar
  26. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163. Scholar
  27. Csiszár J, Horváth E, Váry Z, Gallé Á, 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. Scholar
  28. 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. Scholar
  29. 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. Scholar
  30. Cummins I, Wortley DJ, Sabbadin F et al (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci U S A 110:5812–5817. Scholar
  31. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795. Scholar
  32. Deeba F, Pandey AK, Ranjan S, Mishra A, Singh R, Sharma YK, Shirke PA, Pandey V (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol Biochem 53:6–18. Scholar
  33. DeLano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 Newsl Protein Crystallogr 40:82–92Google Scholar
  34. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335. Scholar
  35. Deng F, Hatzios KK (2002) Purification and characterization of two glutathione S-transferase isozymes from indica-type rice involved in herbicide detoxification. Pestic Biochem Physiol 72:10–13. Scholar
  36. Deng F, Jelesko J, Cramer CL, Wu J, Hatzios KK (2003) Use of an antisense gene to characterize glutathione S-transferase functions in transformed suspension-cultured rice cells and calli. Pestic Biochem Physiol 75:27–37. Scholar
  37. Diao G, Wang Y, Wang C, Yang C (2011) Cloning and functional characterization of a novel glutathione S-transferase gene from Limonium bicolor. Plant Mol Biol Rep 29:77–87. Scholar
  38. Dill GM, Cajacob CA, Padgette SR (2008) Glyphosate-resistant crops: adoption, use and future considerations. Pest Manag Sci 64:326–336. Scholar
  39. Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109. Scholar
  40. 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. Scholar
  41. Dixit G, Singh AP, Kumar A, Singh PK, Kumar S, Dwivedi S, Trivedi PK, Pandey V, Norton GJ, Dhankher OP, Tripathi RD (2015) Sulfur mediated reduction of arsenic toxicity involves efficient thiol metabolism and the antioxidant defense system in rice. J Hazard Mater 298:241–251. Scholar
  42. Dixon (2010) Glutathione transferases. In: The Arabidopsis book. American Society of Plant Biologists, p e0131CrossRefPubMedPubMedCentralGoogle Scholar
  43. Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants: identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869. Scholar
  44. Dixon DP, McEwen AG, Lapthorn AJ, Edwards R (2003) Forced evolution of a herbicide detoxifying glutathione transferase. J Biol Chem 278:23930–23935. Scholar
  45. 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. Scholar
  46. 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. Scholar
  47. Dong Y, Li C, Zhang Y, He Q, Daud MK, Chen J, Zhu S (2016) Glutathione S-transferase gene family in Gossypium raimondii and G. arboreum: comparative genomic study and their expression under salt stress. Front Plant Sci 7:139. Scholar
  48. Droog F (1997) Plant glutathione S -transferases, a tale of theta and tau. J Plant Growth Regul 16:95–107CrossRefGoogle Scholar
  49. Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665. Scholar
  50. Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127:918–927. Scholar
  51. Ezaki B, Suzuki M, Motoda H, Kawamura M, Nakashima S (2004) Mechanism of gene expression of Arabidopsis in response to aluminum stress 1. Sci Technol 134:1672–1682. Scholar
  52. Fones H, Preston GM (2012) Reactive oxygen and oxidative stress tolerance in plant pathogenic pseudomonas. FEMS Microbiol Lett 327:1–8. Scholar
  53. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic Interface between stress perception and physiological responses. Plant Cell 17:1866–1875. Scholar
  54. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:862–905. Scholar
  55. Foyer CH, Descourvières P, Kunert KJ, Descourvieres P (1994) Protection against oxygen radicals- an important defense mechanism studied in transgenic plants. Plant Cell Environ 17:507–523. Scholar
  56. 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 9:2123–2132CrossRefGoogle Scholar
  57. Frova C (2003) The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol Plant 119:469–479. Scholar
  58. Frova C (2006) Glutathione transferases in the genomics era: new insights and perspectives. Biomol Eng 23:149–169. Scholar
  59. Gallé Á, Csiszár J, Secenji M, Guóth A, Cseuz L, Tari I, Györgyey J, Erdei L (2009) Glutathione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit. J Plant Physiol 166:1878–1891. Scholar
  60. Gallé Á, Csiszár J, Secenji M, Erdei L, Benyo D, Györgyey J, Tari I (2011) Induction and regulation of glutathione transferases in wheat species exposed to PEG induced osmotic stress. Acta Biol Szeged 55:79–80. Scholar
  61. Gallé Á, Csiszár J, Secenji M, Guóth A, Cseuz L, Tari I, Györgyey J, Erdei L (2013) Drought response strategies during grain filling in wheat. J Plant Physiol 170:1389–1399CrossRefPubMedGoogle Scholar
  62. 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. Scholar
  63. Gietler M, Nykiel M, Zagdańska BM (2016) Changes in the reduction state of ascorbate and glutathione, protein oxidation and hydrolysis leading to the development of dehydration intolerance in Triticum aestivum L. seedlings. Plant Growth Regul 79:287–297. Scholar
  64. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. Scholar
  65. 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. Scholar
  66. Gupta NK, Agarwal S, Agarwal VP, Nathawat NS, Gupta S, Singh G (2013) Effect of short-term heat stress on growth, physiology and antioxidative defence system in wheat seedlings. Acta Physiol Plant 35:1837–1842. Scholar
  67. Gür A, Demirel U, Özden M, Kahraman A, Opur O (2010) Diurnal gradual heat stress affects antioxidant enzymes, proline accumulation and some physiological components in cotton (Gossypium hirsutum L.) Afr J Biotechnol 9:1008–1015. Scholar
  68. Hameed A, Bibi N, Akhter J, Iqbal N (2011) Differential changes in antioxidants, proteases, and lipid peroxidation in flag leaves of wheat genotypes under different levels of water deficit conditions. Plant Physiol Biochem 49:178–185. Scholar
  69. He F, Liu Q, Zheng L, Cui Y, Shen Z, Zheng L (2015) RNA-Seq analysis of rice roots reveals the involvement of post-transcriptional regulation in response to cadmium stress. Front Plant Sci 6:1–16. Scholar
  70. Hernandez JA, Ferrer MA, Jimenez A, Barcelo AR, Sevilla F (2001) Antioxidant systems and O2.-/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831. Scholar
  71. Hernandez I, Alegre L, Munne-Bosch S (2004) Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol 24:1303–1311. Scholar
  72. Herschbach C, van Der Zalm E, Schneider A, Jouanin L, De Kok LJ, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar overexpressing gamma-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124:461–473. Scholar
  73. Hu T (2014) A glutathione s-transferase confers herbicide tolerance in rice. Crop Breed Appl Biotechnol 14:76–81. Scholar
  74. Hu Y, Burucs Z, von Tucher S, Schmidhalter U (2007) Short-term effects of drought and salinity on mineral nutrient distribution along growing leaves of maize seedlings. Environ Exp Bot 60:268–275. Scholar
  75. Hu T, Qv X, Xiao G, Huang X (2009) Enhanced tolerance to herbicide of rice plants by over-expression of a glutathione S-transferase. Mol Breed 24:409–418. Scholar
  76. Iannelli MA, Pietrini F, Fiore L, Petrilli L, Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol Biochem 40:977–982. Scholar
  77. 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. Scholar
  78. Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832. Scholar
  79. Ji W, Zhu Y, Li Y, Yang L, Zhao X, Cai H, Bai X (2010) Over-expression of a glutathione S-transferase gene, GsGST, from wild soybean (Glycine soja) enhances drought and salt tolerance in transgenic tobacco. Biotechnol Lett 32:1173–1179. Scholar
  80. Jia B, Sun M, Sun X et al (2016) Overexpression of GsGSTU13 and SCMRP in Medicago sativa confers increased salt-alkaline tolerance and methionine content. Physiol Plant 156:176–189. Scholar
  81. Jozefczak M, Keunen E, Schat H et al (2014) Differential response of Arabidopsis leaves and roots to cadmium: glutathione-related chelating capacity vs antioxidant capacity. Plant Physiol Biochem 83:1–9. Scholar
  82. 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. Scholar
  83. 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. Scholar
  84. Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. Scholar
  85. Khare R, Kumar S, Shukla T, Ranjan A, Trivedi PK (2017) Differential sulphur assimilation mechanism regulates response of Arabidopsis thaliana natural variation towards arsenic stress under limiting sulphur condition. J Hazard Mater 337:198–207. Scholar
  86. Kim SD, Lee JH, Hur EH et al (2011) Influence of GST gene polymorphisms on the clearance of intravenous busulfan in adult patients undergoing hematopoietic cell transplantation. Biol Blood Marrow Transplant 17:1222–1230. Scholar
  87. Kissoudis C, Kalloniati C, Flemetakis E, Madesis P, Labrou NE, Tsaftaris A, Nianiou-Obeidat I (2015a) Stress-inducible GmGSTU4 shapes transgenic tobacco plants metabolome towards increased salinity tolerance. Acta Physiol Plant 37:1–11. Scholar
  88. Kissoudis C, Kalloniati C, Flemetakis E, Madesis P, Labrou NE, Tsaftaris A, Nianiou-Obeidat I (2015b) 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. Scholar
  89. Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiol Plant 34:75–86. Scholar
  90. Kumar S, Asif M, Chakrabarty D (2013a) Differential expression of rice lambda class GST gene family members during plant growth, development, and in response to stress conditions. Plant Mol Biol 31:569–580CrossRefGoogle Scholar
  91. Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013b) Expression of a rice lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazard Mater 248–249:228–237. Scholar
  92. 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. Scholar
  93. Lallement PA, Brouwer B, Keech O, Hecker A, Rouhier N (2014) The still mysterious roles of cysteine-containing glutathione transferases in plants. Front Pharmacol 5:1–22. Scholar
  94. Lan T, Yang Z-L, Yang X, Liu Y-J, Wang X-R, Zeng Q-Y (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766. Scholar
  95. Lane A, Jarvis A (2007) Changes in climate will modify the geography of crop suitability: agricultural biodiversity can help with adaptation. SAT eJ 4:1–12. Scholar
  96. Lappartient AC, Touraine B (1997) Glutathione-mediated regulation of ATP sulfurylase activity, SO42− uptake, and oxidative stress response in intact canola roots. Plant Physiol 114:177–183CrossRefPubMedPubMedCentralGoogle Scholar
  97. 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. Scholar
  98. Light GG, Mahan JR, Roxas VP, Allen RD (2005) Transgenic cotton (Gossypium hirsutum L.) seedlings expressing a tobacco glutathione S-transferase fail to provide improved stress tolerance. Planta 222:346–354. Scholar
  99. Lim JD, Hahn SJ, Yu CY, Chung IM (2005) Expression of the glutathione S-transferase gene (NT107) in transgenic Dianthus superbus. Plant Cell Tissue Organ Cult 80:277–286. Scholar
  100. Lin CY, Trinh NN, Lin CW, Huang HJ (2013) Transcriptome analysis of phytohormone, transporters and signaling pathways in response to vanadium stress in rice roots. Plant Physiol Biochem 66:98–104. Scholar
  101. Liu XF, Li JY (2002) Characterization of an ultra-violet inducible gene that encodes glutathione S-transferase in Arabidopsis thaliana. Acta Genet Sin 29:458–460PubMedGoogle Scholar
  102. 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 47:515–523. Scholar
  103. 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. Scholar
  104. Lo Cicero L, Catara V, Strano CP, Bella P, Madesis P, Lo Piero AR (2017) Over-expression of CsGSTU promotes tolerance to the herbicide alachlor and resistance to Pseudomonas syringae pv. tabaci in transgenic tobacco. Biol Plant 61:169–177. Scholar
  105. Mahan JR, Mauget SA (2005) Antioxidant metabolism in cotton seedlings exposed to temperature stress in the field. Crop Sci 45:2337–2345. Scholar
  106. Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158. Scholar
  107. McGonigle B, Lau SMC, O’Keefe DP (1997) Endogenous reactions and substrate specificity of herbicide metabolizing enzymes. In: Regulation of enzymatic systems detoxifying xenobiotics in plants, NATO ASI Series. Kluwer Academic Publishers, Dordrecht, pp 9–18CrossRefGoogle Scholar
  108. McGonigle B, Keeler SJ, Cindy Lau S-M, Koeppe MK, O 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. Scholar
  109. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. Scholar
  110. Milligan AS, Daly A, Parry MAJ, Lazzeri PA, Jepson I, Al H (2001) The expression of a maize glutathione S -transferase gene in transgenic wheat confers herbicide tolerance, both in planta and in vitro. Mol Breed 7:301–315CrossRefGoogle Scholar
  111. Mishra P, Bhoomika K, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive indica rice (Oryza sativa L.) seedlings. Protoplasma 250:3–19. Scholar
  112. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. Scholar
  113. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462. Scholar
  114. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. Scholar
  115. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. Scholar
  116. Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856. Scholar
  117. Molassiotis A, Fotopoulos V (2011) Oxidative and nitrosative signaling in plants. Plant Signal Behav 6:210–214. Scholar
  118. Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481. Scholar
  119. 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. Scholar
  120. Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitam Horm 72:155–202. Scholar
  121. Nahakpam S, Shah K (2011) Expression of key antioxidant enzymes under combined effect of heat and cadmium toxicity in growing rice seedlings. Plant Growth Regul 63:23–35. Scholar
  122. Nair PMG, Chung IM (2014) Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsis thaliana. Environ Sci Pollut Res 21:8858–8869. Scholar
  123. Nakka S, Godar AS, Thompson CR, Peterson DE, Jugulam M (2017) Rapid detoxification via glutathione S-transferase (GST) conjugation confers a high level of atrazine resistance in palmer amaranth (Amaranthus palmeri). Pest Manag Sci 73:2236–2243. Scholar
  124. 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. Scholar
  125. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279. Scholar
  126. Norton GJ, Douglas A, Lahner B et al (2014) Genome wide association mapping of grain arsenic, copper, molybdenum and zinc in rice (Oryza sativa L.) grown at four international field sites. PLoS One 9:1–12. Scholar
  127. Nutricati E, Miceli A, Blando F, De Bellis L (2006) Characterization of two Arabidopsis thaliana glutathione S-transferases. Plant Cell Rep 25:997–1005. Scholar
  128. Pang S, Ran Z, Liu Z, Song X, Duan L, 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 7:1–5. Scholar
  129. Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172. Scholar
  130. Pei D (2012) Cloning and expression of a tomato glutathione S- transferase (GST) in Escherichia coli. Afr J Biotechnol 11:6402–6408. Scholar
  131. Peñuelas J (2008) An increasingly scented world. New Phytol 180(4):735–738CrossRefPubMedGoogle Scholar
  132. Perez-Lopez U, Robredo A, Lacuesta M, Sgherri C, Mun A, Pe U, Navari-izzo F, Mena-petite A (2009) The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2 use. Physiol Plant 135:29–42. Scholar
  133. Pimm SL (2009) Climate disruption and biodiversity. Curr Biol 19:R595–R601. Scholar
  134. Popelka M, Tuinstra M, Weil CF (2009) Discovering genes for abiotic stress tolerance in crop plants. In: Jenks MA, Wood AJ (eds) Genes for plant abiotic stress. Blackwell Publishing Ltd, Ames, pp 281–302CrossRefGoogle Scholar
  135. Powles SB, Yu Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347. Scholar
  136. Qi YC, Liu WQ, Qiu LY, Zhang SM, Ma L, Zhang H (2010) Overexpression of glutathione S-transferase gene increases salt tolerance of Arabidopsis. Russ J Plant Physiol 57:233–240. Scholar
  137. Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731. Scholar
  138. Rampino P, Mita G, Fasano P, Borrelli GM, Aprile A, Dalessandro G, De Bellis L, Perrotta C (2012) Novel durum wheat genes up-regulated in response to a combination of heat and drought stress. Plant Physiol Biochem 56:72–78. Scholar
  139. Rao KVM, Raghavendra AS, Reddy KJ (2006) Physiology and molecular biology of stress tolerance in plants. Springer Science & Business Media, NetherlandsGoogle Scholar
  140. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375. Scholar
  141. Rentel MC, Knight MR, Kingdom U (2004) Oxidative stress-induced calcium signaling. Plant Physiol 135:1471–1479. Scholar
  142. Reymond P (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–720. Scholar
  143. 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. Scholar
  144. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073. Scholar
  145. Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151. Scholar
  146. 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. Scholar
  147. Ryu HY, Kim SY, Park HM, You JY, Kim BH, Lee JS, Nam KH (2009) Modulations of AtGSTF10 expression induce stress tolerance and BAK1-mediated cell death. Biochem Biophys Res Commun 379:417–422. Scholar
  148. Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Cervilla LM, Blasco B, Rios JJ, Rosales MA, Romero L, Ruiz JM (2010) Genotypic differences in some physiological parameters symptomatic for oxidative stress under moderate drought in tomato plants. Plant Sci 178:30–40. Scholar
  149. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Harvey Millar A, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68. Scholar
  150. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658CrossRefPubMedGoogle Scholar
  151. Seckin B, Turkan I, Sekmen AH, Ozfidan C (2010) The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barleygrass) and Hordeum vulgare L. (cultivated barley). Environ Exp Bot 69:76–85. Scholar
  152. Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ Exp Bot 99:141–149. Scholar
  153. Shao H-B, Chu L-Y, Jaleel CA, Zhao C-X (2008) Water-deficit stress-induced anatomical changes in higher plants. C R Biol 331:215–225. Scholar
  154. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26. Scholar
  155. 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 9:1–11. Scholar
  156. Sievers F, Wilm A, Dineen D et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. Scholar
  157. 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. Scholar
  158. 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, Proteins Proteomics 1854:166–177. Scholar
  159. 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 94:802–812CrossRefPubMedGoogle Scholar
  160. Smith AP, Nourizadeh SD, Peer WA, Xu J, Bandyopadhyay A, Murphy AS, PBG Ã (2003) Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. Plant J 36:433–442. Scholar
  161. Sun W, Xu X, Zhu H, Liu A, Liu L, Li J, Hua X (2010) Comparative transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. Plant Cell Physiol 51:997–1006. Scholar
  162. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699. Scholar
  163. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270. Scholar
  164. Takesawa T, Ito M, Kanzaki H, Kameya N, Nakamura I (2002) Over-expression of glutathione ζ glutathione S-transferase in transgenic rice enhances germination and growth at low temperature. Mol Breed 9:93–101CrossRefGoogle Scholar
  165. 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. Scholar
  166. Türkan I, Bor M, Özdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Sci 168:223–231. Scholar
  167. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122. Scholar
  168. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539CrossRefPubMedGoogle Scholar
  169. Vij S, Tyagi AK (2007) Emerging trends in the functional genomics of the abiotic stress response in crop plants. Plant Biotechnol J 5:361–380CrossRefPubMedGoogle Scholar
  170. Voss I, Sunil B, Scheibe R, Raghavendra AS (2013) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol 15:713–722. Scholar
  171. 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. Scholar
  172. Wang LP, Qi YC, Zhao YX, Zhang H (2002) Cloning and sequencing of GST gene of Suaeda salsa and its expression characteristics. J Plant Physiol Mol Biol 28:133–136Google Scholar
  173. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14. Scholar
  174. Xu F, Lagudah ES, Moose SP, Riechers DE (2002) Tandemly duplicated safener-induced glutathione S-transferase genes from Triticum tauschii contribute to genome- and organ-specific expression in hexaploid wheat. Society 130:362–373. Scholar
  175. Xu J, Xing XJ, Tian YS, Peng RH, Xue Y, Zhao W, Yao QH, Zhang H (2015a) Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS One 10:1–16. Scholar
  176. Xu Z, Jiang Y, Zhou G (2015b) Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front Plant Sci 6:1–17. Scholar
  177. Xu J, Tian YS, Xing XJ, Peng RH, Zhu B, Gao JJ, Yao QH (2016) Over-expression of AtGSTU19 provides tolerance to salt, drought and methyl viologen stresses in Arabidopsis. Physiol Plant 156:164–175. Scholar
  178. 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. Scholar
  179. Zhang C-H, Wu Z-Y, Ju T, Ge Y (2013) Purification and identification of glutathione S-transferase in rice root under cadmium stress. Rice Sci 20(3):173–178CrossRefGoogle Scholar
  180. Zhang JZ, Creelman RA, Zhu J-K (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135:615–621. Scholar
  181. Zhao FJ, McGrath SP (2009) Biofortification and phytoremediation. Curr Opin Plant Biol 12:373–380. Scholar
  182. Zhao F, Zhang H (2006) Salt and paraquat stress tolerance results from co-expression of the Suaeda salsa glutathione S-transferase and catalase in transgenic rice. Plant Cell Tissue Organ Cult 86:349–358. Scholar
  183. Zhao F, Liu W, Zhang S (2009) Different responses of plant growth and antioxidant system to the combination of cadmium and heat stress in transgenic and non-transgenic Rice. J Integr Plant Biol 51:942–950. Scholar
  184. Zinta G, Abdelgawad H, Domagalska MA et al (2014) Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels. Glob Chang Biol 20:3670–3685. Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Evangelia Stavridou
    • 1
  • Georgia Voulgari
    • 1
  • Irini Bosmali
    • 1
  • Evangelia G. Chronopoulou
    • 2
  • Luca Lo Cicero
    • 3
  • Angela Roberta Lo Piero
    • 3
  • Nikolaos E. Labrou
    • 2
  • Athanasios Tsaftaris
    • 4
  • Irini Nianiou-Obeidat
    • 5
  • Panagiotis Madesis
    • 1
    Email author
  1. 1.Institute of AgrobiotechnologyCERTHThessalonikiGreece
  2. 2.Laboratory of Enzyme Technology, Department of Agricultural BiotechnologyAgricultural University of AthensAthensGreece
  3. 3.Department of Genetics and Plant Breeding, School of AgricultureAristotle University of ThessalonikiThessalonikiGreece
  4. 4.Dipartimento di ScienzedelleProduzioniAgrarie e Alimentari (DISPA)Università di CataniaCataniaItaly
  5. 5.Perrotis CollegeAmerican Farm SchoolThessalonikiGreece

Personalised recommendations