Skip to main content
SpringerLink
Log in

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

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

GR:

glutathione reductase

GST:

glutathione S-transferase

ROS:

reactive oxygen species

References

  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.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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. 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.

    Chapter  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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. 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.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Science and Arts, Department of Biology, Gaziosmanpasa University, 60250, Tokat, Turkey

    D. Kısa

Authors
  1. D. Kısa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Kısa.

Additional information

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kısa, D. Expressions of glutathione-related genes and activities of their corresponding enzymes in leaves of tomato exposed to heavy metal. Russ J Plant Physiol 64, 876–882 (2017). https://doi.org/10.1134/S1021443717060048

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443717060048

Keywords

Search

Navigation