Russian Journal of Plant Physiology

, Volume 64, Issue 6, pp 876–882 | Cite as

Expressions of glutathione-related genes and activities of their corresponding enzymes in leaves of tomato exposed to heavy metal

  • D. Kısa
Research Papers


Plant development depends on the environmental conditions, and the accumulation of heavy metals in plant tissues causes various molecular and biochemical changes in plant life cycles. Plants have developed a number of detoxification mechanisms to tolerate oxidative damages in the unsuitable environments. GR and GST involved with glutathione are the key antioxidant defense enzymes in response to heavy metals stress. In the present study, mRNA expressions and activities of GR and GST enzymes are investigated in the leaves of tomato (Lycopersicon esculentum Mill.) increasing doses of Cd, Cu, and Pb. The transcriptional expression of GR and GST was analyzed by real-time quantitative PCR. GR and GST genes are induced compared to control in leaves of tomato by the application of heavy metals. The expression of GR usually significantly increased except for 10 ppm of Pb which there was no significant change in the low dose. The GST transcript significantly raised in all treatment of heavy metals. The highest expression of GR and GST was observed in the application of 20 and 50 ppm of Pb, respectively. The enzyme activities of GR and GST significantly increased by the application of Cd, Cu, and Pb, but GR activity remained constant at 50 ppm of Cu compared to control in leaves of tomato. The results presented in this study indicate that the transcript expressions show a correlation with enzymes activities with small differences because post-transcriptional factors might affect the enzymes activities.


Lycopersicon esculentum cadmium copper gene expression glutathione reductase glutathione S-transferase heavy metal lead 



glutathione reductase


glutathione S-transferase


reactive oxygen species


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  1. 1.
    Bertoli, A.C., Cannata, M.G., Carvalho, R., Bastos, A.R.R., Freitas, M.P., and Augusto, A.S., Lycopersicon esculentum submitted to Cd stressful conditions in nutrition solution: nutrient contents and translocation, Ecotoxicol. Environ. Saf., 2012, vol. 86, pp. 176–181.CrossRefGoogle Scholar
  2. 2.
    Yadav, S.K., Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants, S. Afr. J. Bot., 2010, vol. 76, pp. 167–179.CrossRefGoogle Scholar
  3. 3.
    Gratao, P.L., Polle, A., Lea, P.J., and Azevedo, R.A., Making the life of heavy metal-stressed plants a little easier, Mycorrhiza, 2006, vol. 17, pp. 1–10.CrossRefGoogle Scholar
  4. 4.
    Trivedi, D.K., Gill, S.S., Yadav, S., and Tuteja, N., Genome-wide analysis of glutathione reductase (GR) genes from rice and Arabidopsis, Plant Signal. Behav., 2013, vol. 8, pp. 1–7.CrossRefGoogle Scholar
  5. 5.
    Chamseddine, M., Wided, B.A., Guy, H., Marie-Edith, C., and Fatma, J., Cadmium and copper induction of oxidative stress and antioxidative response in tomato (Solanum lycopersicon) leaves, Plant Growth Regul., 2009, vol. 57, pp. 89–99.CrossRefGoogle Scholar
  6. 6.
    Edwards, R., Dixon, D.P., and Walbot, V., Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health, Trends Plant Sci., 2000, vol. 5, pp. 193–198.CrossRefPubMedGoogle Scholar
  7. 7.
    Romero-Puertas, M.C., Corpas, F.J., Sandalio, L.M., Leterrier, M., Rodriguez-Serrano, M., Rio, L.A., and Palma, J.M., Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme, New Phytol., 2006, vol. 170, pp. 43–52.CrossRefPubMedGoogle Scholar
  8. 8.
    Yannarelli, G.G., Fernandez-Alvarez, A.J., Santa-Cruz, D.M., and Tomaro, M.L., Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress, Phytochemistry, 2007, vol. 68, pp. 505–512.CrossRefPubMedGoogle Scholar
  9. 9.
    Kim, S.H., Kim, S.J., Lee, J.S., and Lee, Y.M., Acute effects of heavy metals on the expression of glutathione-related antioxidant genes in the marine ciliate Euplotes crassus, Mar. Pollut. Bull., 2014, vol. 85, pp. 455–462.CrossRefPubMedGoogle Scholar
  10. 10.
    Eroglu, A., Dogan, Z., Kanak, E.G., Atli, G., and Canli, M., Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism, Environ. Sci. Pollut. Res., 2015, vol. 22, pp. 3229–3237.CrossRefGoogle Scholar
  11. 11.
    He, G., Guan, C.N., Chen, Q.X., Gou, X.J., Liu, W., Zeng, Q.Y., and Lan, T., Genome-wide analysis of the glutathione S-transferase gene family in Capsella rubella: identification, expression, and biochemical functions, Front. Plant Sci., 2016, vol. 7, pp. 1–14.Google Scholar
  12. 12.
    Yousuf, P.Y., Hakeem, K.U.R., Chandna, R., and Ahmad, P., Role of glutathione reductase in plant abiotic stress, in Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability, Ahmad, P. and Prasad, M.N.V., Eds., New York: Springer-Verlag, 2012, pp. 149–158.CrossRefGoogle Scholar
  13. 13.
    Goupil, P., Souhuir, D., Ferjani, E., Faure, O., Hitmi, A., and Ledoigt, G., Expression of stress related genes in tomato plants exposed to arsenic and chro mium in nutrient solution, J. Plant Physiol., 2009, vol. 166, pp. 1446–1452.CrossRefPubMedGoogle Scholar
  14. 14.
    Carlberg, I. and Mannervik, B., Purification and characterization of the flavoenzyme glutathione reductase from rat liver, J. Biol. Chem., 1975, vol. 250, pp. 5475–5480.PubMedGoogle Scholar
  15. 15.
    Habig, W.H., Pabst, M.J., and Jakoby, W.B., Glutathione S-transferases. The first enzymatic step in mercapturic acid formation, Biol. Chem., 1974, vol. 249, pp. 7130–7139.Google Scholar
  16. 16.
    Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method, Methods, 2001, vol. 25, pp. 402–408.CrossRefPubMedGoogle Scholar
  17. 17.
    Garnik, E.Y., Belkov, V.I., Trasenko, V.I., Korzun,M.A., and Konstantinov, Y.M., Glutathione reductase gene expression depends on chloroplast signals in Arabidopsis thaliana, Biochemistry (Moscow), 2016, vol. 81, pp. 364–372.CrossRefGoogle Scholar
  18. 18.
    Wang, J., Jiang, Y., Chen, S., Xia, X., Shi, K., Zhou, Y., Yu, Y., and Yu, J., The different responses of glutathione-dependent detoxification pathway to fungicide chlorothalonil and carbendazim in tomato leaves, Chemosphere, 2010, vol. 79, pp. 958–965.CrossRefPubMedGoogle Scholar
  19. 19.
    Waschke, A., Sieh, D., Tamasloukht, M., Fischer, K., Mann, P., and Franken, P., Identification of heavy metal-induced genes encoding glutathione S-transferases in the arbuscular mycorrhizal fungus Glomus intraradices, Mycorrhiza, 2006, vol. 17, pp. 1–10.CrossRefPubMedGoogle Scholar
  20. 20.
    Brunet, J., Varrault, G., Zuily-Fodil, Y., and Repellin, A., Accumulation of lead in the roots of grass pea (Lathyrus sativus L.) plants triggers systemic variation in gene expression in the shoots, Chemosphere, 2009, vol. 77, pp. 1113–1120.CrossRefPubMedGoogle Scholar
  21. 21.
    Csiszar, J., Horvath, E., Vary, Z., Galle, A., Bela, K., and Brunner, S., 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., 2014, vol. 78, pp. 15–26.CrossRefPubMedGoogle Scholar
  22. 22.
    Mortel, J.E.V.D., Schat, H., Moerland, P.D., Themaat, E.V.L.V., Ent, S.V.D., Blankestɩjn, H., Ghandɩlyan, A., and Tsiatsiani, S., Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens, Plant Cell Environ., 2008, vol. 31, pp. 301–324.CrossRefPubMedGoogle Scholar
  23. 23.
    Han, J., Won, E.J., Hwang, D.S., Rhee, J.S., Kim, I.C., and Lee, J.S., Effect of copper exposure on GST activity and on the expression of four GSTs under oxidative stress condition in the monogonont rotifer, Brachionus koreanus, Comp. Biochem. Physiol., 2013, vol. 158, pp. 91–100.Google Scholar
  24. 24.
    Ahn, S.Y., Kim, S.A., and Yun, H.K., Glutathione Stransferase genes differently expressed by pathogeninfection in Vitis flexuosa, Plant Breed. Biotech., 2016, vol. 4, pp. 61–70.CrossRefGoogle Scholar
  25. 25.
    Dobrakowski, M., Pawlas, N., Hudziec, E., Kozlowska, A., Mikolajczyk, A., Birkner, E., and Kasperczyk, S., Glutathione, glutathione-related enzymes, and oxidative stress in individuals with subacute occupational exposure to lead, Environ. Toxicol. Pharmacol., 2016, vol. 45, pp. 235–240.PubMedGoogle Scholar
  26. 26.
    Gratao, P.L., Monteiro, C.C., Tezotto, T., Carvalho, R.F., Alves, L.R., Peters, L.P., and Azevedo, R.A., Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants, Biometals, 2015, vol. 28, pp. 803–816.CrossRefPubMedGoogle Scholar
  27. 27.
    Meena, M., Zehra, A., Dubey, M.K., Aamir, M., Gupta, V.K., and Upadhyay, R.S., Comparative evaluation of biochemical changes in tomato (Lycopersicon esculentum Mill.) infected by Alternaria alternata and its toxic metabolites (TeA, AOH, and AME), Front. Plant Sci., 2016, vol. 7, pp. 1–14.CrossRefGoogle Scholar
  28. 28.
    Woo, S., Yum, S., Park, H.S., Lee, T.K., and Ryu, J.C., Effects of heavy metals on antioxidants and stressresponsive gene expression in Javanese medaka (Oryzias javanicus), Comp. Biochem. Physiol., 2009, vol. 149, pp. 289–299.Google Scholar
  29. 29.
    Mazzucotelli, E., Mastrangelo, A.M., Crosatti, C., Guerra, D., Stanca, A.M., and Cattivelli, L., Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription, Plant Sci., 2008, vol. 174, pp. 420–431.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  1. 1.Faculty of Science and Arts, Department of BiologyGaziosmanpasa UniversityTokatTurkey

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