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Glutathione in adaptation of Arabidopsis thaliana to cadmium stress

  • Published:
Biologia Plantarum

Abstract

The role of glutathione (GSH) in the adaptation of wild type Arabidopsis thaliana plants to Cd stress was investigated. The nutrient solution (control or containing 50 or 100 μM Cd) was supplemented with buthionine sulfoximine (BSO; 50, 100, 500 μM, to decrease the GSH content in plants) or GSH (50, 100, 500 μM, to increase its content in plants) in order to find how GSH content could regulate Cd stress responses. BSO application did not influence plant biomass, while exogenous GSH (especially 500 μM) reduced root biomass. BSO (500μM) in combination with Cd (100 μM) increased Cd toxicity on root growth (by over 50 %), most probably due to reduced GSH content and phytochelatin (PC) accumulation (by over 96 %). On the other hand, combination of exogenous GSH (500 μM) with Cd (100 μM) was also more toxic to plants than Cd alone despite a significant increase in GSH and PC accumulation (up to 2.7 fold in the roots). This fact could indicate that the natural content of endogenous GSH in wild type A. thaliana plants is sufficient for Cd-tolerance. A decrease in this GSH content led to decreased Cd-tolerance of the plants but an increase in GSH content did not enhance Cd-tolerance, and it showed even toxic effect on the plants.

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Abbreviations

BSO:

buthionine sulfoximine

DTNB:

5,5’-dithiobis-2-nitrobenzoic acid

GSB:

glutathione S-bimane

GSH:

reduced glutathione

GSSG:

oxidized glutathione

MCB:

monochlorobimane

PC:

phytochelatin

ROS:

reactive oxygen species

References

  • Anderson, M.E.: Determination of glutathione and glutathione disulfides in biological samples. — Meth. Enzymol. 113: 548–555, 1985.

    Article  CAS  PubMed  Google Scholar 

  • Armstrong, J.S., Jones, D.P.: Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2 overexpressing HL60 cells. — FASEB J. 16: 1263–1265, 2002.

    CAS  PubMed  Google Scholar 

  • Belmonte, M.F., Ambrose, S.J., Ross, A.R.S., Abrams, S.R., Stasolla, C.: Improved development of microspore-derived embryo cultures of Brassica napus cv Topaz following changes in glutathione metabolism. — Physiol. Plant. 127: 690–700, 2006.

    Article  CAS  Google Scholar 

  • Ben Ammar, W., Mediouni, C., Tray, B., Ghorbel, M.H., Jemal, F.: Glutathione and phytochelatin contents in tomato plants exposed to cadmium. — Biol. Plant. 52: 314–320, 2008.

    Article  CAS  Google Scholar 

  • Cobbett, C.S., May, M.J., Howden, R., Rolls, B.: The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. — Plant J. 16: 73–78, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Cobbett, C.S, Meagher, R.B.: Arabidopsis and genetic potential for the phytoremediation of toxic elemental and organic pollutants. — In: Somerville, C.R., Meyerowitz, E.M. (ed.): The Arabidopsis Book. Pp. 1–22. American Society of Plant Biologists, Rockville 2002.

    Google Scholar 

  • Espunya, M.C., Díaz, M., Moreno-Romero, J., MartÍnez, M.C.: Modification of intracellular levels of glutathione-dependent formaldehyde dehydrogenase alters glutathione homeostasis and root development. — Plant Cell Environ. 29: 1002–1011, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Fricker, M.D., May, M., Meyer, A.J., Sheard, N., White, N.S.: Measurement of glutathione levels in intact roots of Arabidopsis. — J. Microscopy 198: 162–173, 2000.

    Google Scholar 

  • Gussarsson, M., Asp, H., Adalsteinsson, S., Jensén, P.: Enhancement of cadmium effects on growth and nutrient composition of birch (Betula pendula) by buthionine sulphoximine (BSO). — J. exp. Bot. 47: 211–215, 1996.

    Article  CAS  Google Scholar 

  • Howden, R., Cobbett, C.S.: Cadmium-sensitive mutants of Arabidopsis thaliana. — Plant Physiol. 99: 100–107, 1992.

    Article  Google Scholar 

  • Howden, R., Goldsbrough, P.B., Andersen, C.R., Cobbett, C.S.: Cadmium-sensitive cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. — Plant Physiol. 107: 1059–1066, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Jamaï, A., Tommasini, R., Martinoia, E., Delrot, S.: Characterization of glutathione uptake in broad bean leaf protoplasts. — Plant Physiol. 111: 1145–1152, 1996.

    PubMed  Google Scholar 

  • Lee, S., Moon, J.S., Ko, T.-S., Petros, D., Goldsbrough, P.B., Korban, S.S.: Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. — Plant Physiol. 131: 656–663, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Maksymiec, W., Krupa, Z.: The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. — Environ. exp. Bot. 57: 187–894, 2006.

    Article  CAS  Google Scholar 

  • Markovska, Y.K., Gorinova, N.I., Nedkovska, M.P., Miteva, K.M.: Cadmium-induced oxidative damage and antioxidant responses in Brassica juncea plants. — Biol. Plant. 53: 151–154, 2009.

    Article  CAS  Google Scholar 

  • May, M.J., Leaver, C.J.: Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. — Plant Physiol. 103: 621–627, 1993.

    CAS  PubMed  Google Scholar 

  • Maughan, S., Foyer, C.H.: Engineering and genetic approaches to modulating the glutathione network in plants. — Physiol. Plant. 126: 382–397, 2006.

    Article  CAS  Google Scholar 

  • Peterson, A.G., Oliver, D.J.: Leaf-targeted phytochelatin synthase in Arabidopsis thaliana. — Plant Physiol. Biochem. 44: 885–892, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Rouhier, N., Lemaire, S.D., Jacquot, J.-P.: The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. — Annu. Rev. Plant Biol. 59: 143–166, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Fernández, R., Fricker, M., Corben, L.B., White, N.S., Sheard, N., Leaver, C.J., Van Montagu, M., Inzé, D., May, M.J.: Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. — Proc. nat. Acad. Sci. USA 94: 2745–2750, 1997.

    Article  PubMed  Google Scholar 

  • Schat, H., Llugany, M., Vooijs, R., Hartey-Hittaker, J., Bleeker, P.M.: The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. — J. exp. Bot. 53: 2381–2392, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Semane, B., Cuypers, A., Smeets, K., Van Belleghem, F., Horemans, N., Schat, H., Vangronsveld, J.: Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. — Physiol. Plant. 129: 519–528, 2007.

    Article  CAS  Google Scholar 

  • Senda, K., Ogawa, K.: Induction of PR-1 accumulation accompanied by runaway cell death in the lsd1 mutant of Arabidopsis is dependent on glutathione levels but independent of the redox state of glutathione. — Plant Cell Physiol. 45: 1578–1585, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Skórzyńska-Polit, E., Drążkiewicz, M., Krupa, Z.: The activity of the antioxidative system in cadmium-treated Arabidopsis thaliana. — Biol. Plant. 47: 71–78, 2003/4.

    Article  Google Scholar 

  • Szalai, G., Kellős, T., Galiba, G., Kocsy, G.: Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. — J. Plant Growth Regul. 28: 66–80, 2009.

    Article  CAS  Google Scholar 

  • Vatamaniuk, O.K., Mari, S., Lu, Y.P., Rea, P.A.: Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC-synthase-catalysed transpeptidation of glutathione and related thiol peptides. — J. biol. Chem. 275: 31451–31459, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Vernoux, T., Wilson, R.C., Seeley, K.A., Reichheld, J.-P., Muroy, S., Brown, S., Maughan, S.C., Cobbett, C.S., Van Montagu, M., Inzé, D., May, M.J., Sung, Z.R.: The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. — Plant Cell 12: 97–109, 2000.

    Google Scholar 

  • Wójcik, M., Tukiendorf, A.: Cadmium uptake, localization and detoxification in Zea mays. — Biol. Plant. 49: 237–245, 2005.

    Article  Google Scholar 

  • Wójcik, M., Tukiendorf, A.: Response of wild type of Arabidopsis thaliana to copper stress. — Biol. Plant. 46: 79–84, 2003.

    Article  Google Scholar 

  • Xiang, C., Werner, B.L., Christensen, E.M., Oliver, D.J.: The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. — Plant Physiol. 126: 564–574, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, Y.L., Pilon-Smiths, E.A.H., Tarun, A.S., Jouanin, L., Terry, N.: Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. — Plant Physiol. 119: 73–79, 1999a.

    Article  CAS  Google Scholar 

  • Zhu, Y.L., Pilon-Smiths, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L., Terry, N.: Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. — Plant Physiol. 121: 1169–1177, 1999b.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by State Committee for Scientific Research (KBN), grant No. 3 P04C.050.22. We thank Tomasz Piersiak for an excellent technical assistance in confocal microscopy.

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  1. Department of Plant Physiology, Maria Curie-Skłodowska University, Akademicka 19, 20-033, Lublin, Poland

    M. Wójcik & A. Tukiendorf

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  1. M. Wójcik
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  2. A. Tukiendorf
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Correspondence to M. Wójcik.

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Wójcik, M., Tukiendorf, A. Glutathione in adaptation of Arabidopsis thaliana to cadmium stress. Biol Plant 55, 125–132 (2011). https://doi.org/10.1007/s10535-011-0017-7

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  • DOI: https://doi.org/10.1007/s10535-011-0017-7

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