Skip to main content
SpringerLink
Log in

Interactive effects of zinc and nickel on the glutathione system state in Mimulus guttatus plants

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

Abstract

To determine whether the enhanced stress tolerance of ZnSO4 with NiSO4-treated Mimulus guttatus Fischer ex DC. plants was associated with the glutathione (GR-GSH) system, we investigated the changes in glutathione redox state (reduced (GSH), oxidized (GSSG) forms, total reduced (GSHt) glutathione, and GSH/GSSG ratio) and in the enzymatic activities of glutathione reductase (GR) and peroxidatic glutathione S-transferases (GST). The 6-week-old plants were grown in water culture during 4 weeks on a modified Rorison’s medium with ZnSO4 (50, 100, and 200 μM) and NiSO4 (20 and 80 μM) in a condition of separate or simultaneous supply of the components. Dry biomass accumulations of roots and shoots were not influenced by the examined treatments. The positive correlations between the total external concentrations of ZnSO4 and NiSO4 and the total Zn and Ni contents in roots and leaves were found. It was determined that the MDA content was higher in the ZnSO4-treated plants than in the NiSO4-treated ones. The supplementation of the ZnSO4-treated plants with varied concentrations of NiSO4 decreased the Zn-induced increase in the MDA levels. The inverse proportionality between the MDA and pigment levels in leaves was found. The Zn-Ni interactions were shown to induce the decreases in the GR activity, the total peroxidatic GST activity, and the GSH/GSSG ratio in roots. However, in leaves, the GR activity and the GSH/GSSG ratio were significantly increased and the total peroxidatic GST activity was decreased. The supplementation of the ZnSO4-treated plants with varied concentrations of NiSO4 restored the Zn-induced reduction in the GSHt levels in roots and decreased the Zn-induced increase in the GSSG levels in leaves, which resulted in more reduced state of the intracellular environment. It was likely to cause a decrease of the MDA level. Thus, our studies on the Zn−Ni interactions identified the antagonizing role of Ni in Zn toxicity by the GR-GSH system.

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

APX:

ascorbate peroxidase

CAT:

catalase

Chl:

chlorophylls

DTNB:

5,5′-dithiobis(2-nitrobenzoic acid)

GSH:

reduced glutathione

GSSG:

oxidized glutathione

GSHt:

total reduced glutathione

GSH/GSSG:

GSH-to-GSSG ratio

GR:

glutathione reductase

GST:

glutathione S-transferase

GR-GSH system:

glutathione system

HM:

heavy metals

SOD:

superoxide dismutase

TNB:

5-thio-2-nitrobenzoic acid

References

  1. Anjum, N.A., Ahmad, I., Mohmood, I., Pacheco, M., Duarte, A.C., Pereira, E., Umarc, S., Ahmad, A., Khan, N.A., Iqbal, M., and Prasad, M.N.V., Modulation of glutathione and its related enzymes in plants' responses to toxic metals and metalloids–a review, Environ. Exp. Bot., 2012, vol. 75, pp. 307–324.

    CAS  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. Krämer, U., Metal hyperaccumulation in plants, Annu. Rev. Plant Biol., 2010, vol. 61, pp. 517–534.

    Article  PubMed  Google Scholar 

  4. Nadgórska-Socha, A., Kafel, A., Kandziora-Ciupa, M., Gospodarek, J., and Zawisza-Raszka, A., Accumulation of heavy metals and antioxidant responses in Vicia faba plants grown on monometallic contaminated soil, Environ. Sci. Pollut. Res., 2013, vol. 20, pp. 1124–1134.

    Article  Google Scholar 

  5. Aravind, P. and Prasad, M.N.V., Cadmium–zinc interactions in a hydroponic system using Ceratophylum demersum L.: adaptive ecophysiology, biochemistry and molecular toxicology, Braz. J. Plant Physiol., 2005, vol. 17, pp. 3–20.

    Article  CAS  Google Scholar 

  6. Seregin, I.V. and Kozhevnikova, A.D., Physiological role of nickel and its toxic effects on higher plants, Russ. J. Plant Physiol., 2006, vol. 53, pp. 257–277.

    Article  CAS  Google Scholar 

  7. Gill, S.S., Anjum, N.A., Hasanuzzaman, M., Gill, R., Trivedi, D.K., Ahmad, I., Pereira, E., and Tuteja, N., Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations, Plant Physiol. Biochem., 2013, vol. 70, pp. 204–212.

    Article  CAS  PubMed  Google Scholar 

  8. Gechev, T.S., van Breusegem, F., Stone, J.M., Denev, I., and Laloi, C., Reactive oxygen species as signals that modulate plant stress responses and programmed cell death, BioEssays, 2006, vol. 28, pp. 1091–1101.

    Article  CAS  PubMed  Google Scholar 

  9. Gill, S.S. and Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 2010, vol. 48, pp. 909–930.

    Article  CAS  PubMed  Google Scholar 

  10. Noctor, G., Mhamdi, A., Chaouch, S., Han, Y., Neukermans, J., Marquez-Garcia, B., Queval, G., and Foyer, C.H., Glutathione in plants: an integrated overview, Plant Cell Environ., 2012, vol. 35, pp. 454–484.

    Article  CAS  PubMed  Google Scholar 

  11. Mhamdi, A., Hager, J., Chaouch, S., Queval, G., Han, Y., Taconnat, L., Saindrenan, P., Gouia, H., Issakidis-Bourguet, E., Renou, J.-P., and Noctor, G., Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways, Plant Physiol., 2010, vol. 153, pp. 1144–1160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tilstone, G.H. and Macnair, M.R., Multiple metal tolerance to nickel in Mimulus guttatus Fischer ex DC., S. Afr. J. Sci., 2001, vol. 97, pp. 539–544.

    CAS  Google Scholar 

  13. Wu, C.A., Lowry, D.B., Cooley, A.M., Wright, K.M., Lee, Y.W., and Willis, J.H., Mimulus is an emerging model system for the integration of ecological and genomic studies, Heredity, 2008, vol. 100, pp. 220–230.

    Article  CAS  PubMed  Google Scholar 

  14. Bashmakova, E.B., Pashkovskii, P.P., Radyukina, N.L., and Kuznetsov, Vl.V., Possible mechanism of iron deficit development in Mimulus guttatus plants exposed to joint action of nickel and zinc salts, Russ. J. Plant Physiol., 2015, vol. 62, pp. 761–771.

    Article  CAS  Google Scholar 

  15. Golubkina, N.A., Fluorimetric method for selenium determination, Zh. Anal. Khim., 1995, vol. 50, pp. 492–497.

    Google Scholar 

  16. Heath, R.L. and Packer, L., Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.

    Article  CAS  PubMed  Google Scholar 

  17. Lichtenthaler, H.K., Chlorophylls and carotenoids: pigments of photosynthetic biomembranes, Methods Enzymol., 1987, vol. 148, pp. 350–382.

    Article  CAS  Google Scholar 

  18. Griffith, O.W., Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine, Anal. Biochem., 1980, vol. 106, pp. 207–212.

    Article  CAS  PubMed  Google Scholar 

  19. Smith, I.K., Vierheller, T.L., and Thorne, C.A., Assay of glutathione reductase in crude tissue homogenates using 5,5’-dithiobis(2-nitrobenzoic acid), Anal. Biochem., 1988, vol. 175, pp. 408–413.

    Article  CAS  PubMed  Google Scholar 

  20. Esen, A., A simple method for quantitative, semiquantitative, and qualitative assay of protein, Anal. Biochem., 1978, vol. 89, pp. 264–273.

    Article  CAS  PubMed  Google Scholar 

  21. Gaullier, J.M., Lafontant, P., Valla, A., Bazin, M., Giraud, M., and Santus, R., Glutathione peroxidase and glutathione reductase activities toward glutathionederived antioxidants, Biochem. Biophys. Res. Commun., 1994, vol. 203, pp. 1668–1674.

    Article  CAS  PubMed  Google Scholar 

  22. Chen, C., Huang, D., and Liu, J., Functions and toxicity of nickel in plants: recent advances and future prospects, Clean, 2009, vol. 37, pp. 304–313.

    CAS  Google Scholar 

  23. Gajewska, E., Skłodowska, M., Słaba, M., and Mazur, J., Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots, Biol. Plant., 2006, vol. 50, pp. 653–659.

    CAS  Google Scholar 

  24. Yusuf, M., Fariduddin, Q., Hayat, S., and Ahmad, A., Nickel: an overview of uptake, essentiality and toxicity in plant, Bull. Environ. Contam. Toxicol., 2011, vol. 86, pp. 1–17.

    Article  CAS  PubMed  Google Scholar 

  25. Caregnato F.F., Koller C.E., MacFarlane G.R., and Moreira, J.C.F., The glutathione antioxidant system as a biomarker suite for the assessment of heavy metal exposure and effect in the grey mangrove, Avicennia marina (Forsk.) Vierh, Mar. Pollut. Bull., 2008, vol. 56, pp. 1119–1127.

    Article  CAS  PubMed  Google Scholar 

  26. Siripornadulsil, S., Traina, S., Verma, D.P.S., and Sayre, R.T., Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae, Plant Cell, 2002, vol. 14, pp. 2837–2847.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Miteva, L.P.-E., Ivanov, S.V., and Aleksieva, V.S., Alterations in glutathione pool and some related enzymes in leaves and roots of pea plants treated with the herbicide glyphosate, Russ. J. Plant Physiol., 2010, vol. 57, pp. 131–136.

    Article  CAS  Google Scholar 

  28. Rao, K.V.M. and Sresty, T.V.S., Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses, Plant Sci., 2000, vol. 157, pp. 113–128.

    Article  Google Scholar 

  29. Di Baccio, D., Kopriva, S., Sebastiani, L., and Rennenberg, H., Does glutathione metabolism have a role in the defence of poplar against zinc excess? New Phytol., 2005, vol. 167, pp. 73–80.

    Article  CAS  PubMed  Google Scholar 

  30. Freeman, J.L., Persans, M.W., Nieman, K., Albrecht, C., Peer, W., Pickering, I.J., and Salt, D.E., Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators, Plant Cell, 2004, vol. 16, pp. 2176–2191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, ul. Botanicheskaya 35, Moscow, 127276, Russia

    E. B. Bashmakova, P. P. Pashkovskiy, N. L. Radyukina & Vl. V. Kuznetsov

Authors
  1. E. B. Bashmakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. P. Pashkovskiy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. L. Radyukina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vl. V. Kuznetsov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. B. Bashmakova.

Additional information

Published in Russian in Fiziologiya Rastenii, 2016, Vol. 63, No. 5, pp. 668–678.

The article was translated by the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bashmakova, E.B., Pashkovskiy, P.P., Radyukina, N.L. et al. Interactive effects of zinc and nickel on the glutathione system state in Mimulus guttatus plants. Russ J Plant Physiol 63, 626–635 (2016). https://doi.org/10.1134/S1021443716050022

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443716050022

Keywords

Search

Navigation