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Glutathione metabolism in Urtica dioica in response to cadmium based oxidative stress

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Biologia Plantarum

Abstract

To investigate the antioxidative response of glutathione metabolism in Urtica dioica L. to a cadmium induced oxidative stress, activities of glutathione reductase (GR), glutathione-S-transferase (GST), and glutathione peroxidase (GSH-Px), content of reduced (GSH) and oxidized (GSSG) glutathione, lipid peroxidation (LPO), and also accumulation of Fe, Zn, Mn, Cu besides Cd were determined in the roots, stems, and leaves of plants exposed to 0 (control), 0.045, and 0.09 mM CdCl2 for 58 h. Whereas the Cd content continuously increased in all organs, the Fe, Zn, Mn, and Cu content decreased in dependence on the applied Cd concentration and incubation time. The Cd treatment resulted in increased GR and GST activities in all organs, however, GSH-Px activity was dependent on Cd concentration and plant organ. The GSH/GSSG ratio maintained above the control level in the stems at both Cd concentrations. The LPO was generally close to the control values in the roots and stems but it increased in the leaves especially at 0.09 mM Cd.

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Abbreviations

GR:

glutathione reductase

GSH:

reduced glutathione

GSH-Px:

glutathione peroxidase

GSSG:

oxidized glutathione

GST:

glutathione-S-transferase

LPO:

lipid peroxidation

MDA:

malondialdehyde

ROS:

reactive oxygen species

References

  • Andresen, E., Küpper, H.: Cadmium toxicity in plants. — In Sigel, A., Sigel, H., Sigel, R.K.O. (ed.): Cadmium: From Toxicity to Essentiality. Metal Ions in Life Sciences. Vol. 13. Pp 395–413. Springer, Dordrecht 2013.

    Chapter  Google Scholar 

  • Aravind, P., Prasad, M.N.V.: Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate glutathione cycle and glutathione metabolism. — Plant Physiol. Biochem. 43: 107–116, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Baker, A.J.M., Brooks, R.: Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. — Biorecovery 1: 81–126, 1989.

    CAS  Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Buege, J.A., Aust, S.D.: Lactoperoxidase-catalyzed lipid peroxidation of microsomal and artificial membranes. — Biochim. biophys. Acta. 444: 192–201, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Chaoui, A., Mazhoudi, S., Ghorbal, M.H., El Ferjani, E.: Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). — Plant Sci. 127: 139–147, 1997.

    Article  CAS  Google Scholar 

  • Chardonnens, A.N., Ten Bookum, W. M., Kuijper, L.D., Verkleij, J.A., Ernst, W.H.: Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris. — Physiol. Plant. 104: 75–80, 1998.

    Article  CAS  Google Scholar 

  • Clemens, S.: Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. — Biochimie 88: 1707–1719, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Cummins, I., Cole, D.J., Edwards, R.: Purification of multiple glutathione transferases involved in herbicide detoxification from wheat (Triticum aestivum L.) treated with the safener fenchlorazole-ethyl. — Pestic. Biochem. Physiol. 59: 35–49, 1997.

    Article  CAS  Google Scholar 

  • Cuypers, A., Plusquin, M., Remans, T., Jozefczak, M., Keunen, E., Gielen, H., Smeets, K.: Cadmium stress: an oxidative challenge. — Biometals 23: 927–940, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Dixit, V., Pandey, V., Shyam, R.: Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). — J. exp. Bot. 52: 1101–1109, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Ernst, W.H.O., Nelissen, H.J.M.: Life-cycle phases of a zincand cadmium-resistant ecotype of Silene vulgaris in risk assessment of polymetallic mine soils. — Environ. Pollut. 107: 329–338, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Foyer, C.H., Lopez-Delgado, H., Dat, J.F., Scott, I.M.: Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. — Physiol. Plant. 100: 241–254, 1997.

    Article  CAS  Google Scholar 

  • Foyer, C.H., Noctor, G.: Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. — Plant Cell Environ. 28: 1056–1071, 2005.

    Article  CAS  Google Scholar 

  • Gallego, S.M., Benavídes, M.P., Tomaro, M.L.: Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. — Plant Sci. 121: 151–159, 1996.

    Article  CAS  Google Scholar 

  • Gill, S., Tuteja, N.: Cadmium stress tolerance in crop plants. — Plant Signal Behav. 6: 215–222, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Gjorgieva, D., Kadifkova Panovska, T., Ruskovska, T., Baceva, K., Stafilov, T.: Influence of heavy metal stress on antioxidant status and DNA damage in Urtica dioica. — Biomed. Res. Int. 2013: 1–6, 2013.

    Article  Google Scholar 

  • Gomez, L.D., Noctor, G., Knight, M.R., Foyer, C.H.: Regulation of calcium signalling and gene expression by glutathione. — J. exp. Bot. 55: 1851–1859, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Grzam, A., Tennstedt, P., Clemens, S., Hell, R., Meyer, A.J.: Vacuolar sequestration of glutathione-S-conjugates outcompetes a possible degradation of the glutathione moiety by phytochelatin synthase. — FEBS Lett. 580: 6384–6390, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Habig, W.H., Cabot, M.J., Jarkoby, W.B.: Glutathione Stransferase. The first enzymatic step in mercapturic acid formation. — J. biol. Chem. 249: 7130–7139, 1974.

    CAS  PubMed  Google Scholar 

  • Halliwell, B., Gutteridge, J.M. (ed.): Free Radicals in Biology and Medicine. — Oxford University Press, Oxford 1999.

    Google Scholar 

  • Hart, J.J., Welch, R.M., Norvell, W.A., Sullivan, L.A., Kochian, L.V.: Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. — Plant Physiol. 116: 1413–1420, 1998.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hipps, N.A., Davies, M.J., Dodds, P., Buckley, G.P.: The effects of phosphorus nutrition and soil pH on the growth of some ancient woodland indicator plants and their interaction with competitor species. — Plant Soil 271: 131–141, 2005.

    Article  CAS  Google Scholar 

  • Iannelli, M.A., Pietrini, F., Fiore, L., Petrilli, L., Massacci, A.: Antioxidant response to cadmium in Phragmites australis plants. — Plant Physiol. Biochem. 40: 977–982, 2002.

    Article  CAS  Google Scholar 

  • Kahle, H.: Response of roots of trees to heavy metals. — Environ. exp. Bot. 33: 99–119, 1993.

    Article  Google Scholar 

  • Leita, L., Contin, M., Maggioni, A.: Distribution of cadmium and induced Cd-binding proteins in roots, stems and leaves of Phaseolus vulgaris. — Plant Sci. 77: 139–147, 1991.

    Article  CAS  Google Scholar 

  • Li, F.T., Qi, J.M., Zhang, G.Y., Lin, L.H., Fang, P.P., Tao, A.F., Xu, J.T.: Effect of cadmium stress on the growth, antioxidative enzymes and lipid peroxidation in two kenaf (Hibiscus cannabinus L.) plant seedlings. — J. integr. Agr. 12: 610–620, 2013.

    Article  Google Scholar 

  • Lopez, E., Arce, C., Oset-Gasque, M., Canadas, S., Gonzalez, M.: Cadmium induces reactive oxygen species generation and lipid peroxidation in cortical neurons in culture. — Free Radical Biol. Med. 40: 940–951, 2006.

    Article  CAS  Google Scholar 

  • Marchiol, L., Leita, L., Martin, M., Peressotti, A., Zerbi, G.: Physiological responses of two soybean cultivars to cadmium. — J. Environ. Qual. 25: 562–566, 1996.

    Article  CAS  Google Scholar 

  • Marquez-Garcia, B., Horemans, N., Torronteras, R., Cordoba, F.: Glutathione depletion in healthy cadmium-exposed Erica andevalensis. — Environ. exp. Bot. 75: 159–166, 2012.

    Article  CAS  Google Scholar 

  • Marrs, K.A.: The functions and regulation of glutathione Stransferases in plants. — Annu. Rev. Plant Biol. 47: 127–158, 1996.

    Article  CAS  Google Scholar 

  • Massey, V., Williams, C.H.: On the reaction mechanism of yeast glutathione reductase. — J. biol. Chem. 240: 4470–4480, 1965.

    CAS  PubMed  Google Scholar 

  • Mates, J.M., Sanchez-Jimenez, F.M.: Role of reactive oxygen species in apoptosis: implications for cancer therapy. — Int. J. Biochem. cell. Biol. 32: 157–170, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Mehra, R.K., Tripathi, R.D. (ed.): Environmental Pollution and Plant Responses. — CRC Press, Boca Raton 1999.

    Google Scholar 

  • Mohamed, A., Castagna, A., Ranieri, A., Sanita di Toppi, L.: Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. — Plant Physiol. Biochem. 57: 15–22, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Mohanpuria, P., Rana, N.K., Yadav, S.K.: Cadmium induced oxidative stress influence on glutathione metabolic genes of Camellia sinensis (L.) O. Kuntze. — Environ. Toxicol. 22: 368–374, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Paglia, D.E., Valentine, W.N.: Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. — J. Lab. Clin. Med. 70: 158–169, 1967.

    CAS  PubMed  Google Scholar 

  • Pereira, G.J.G., Molina, S.M.G., Lea, P.J., Azevedo, R.A.: Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. — Plant Soil 239: 123–132, 2002.

    Article  CAS  Google Scholar 

  • Perrin, D., Watt, A.: Complex formation of zinc and cadmium with glutathione. — Biochim. biophys. Acta 230: 96–104, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Pietrini, F., Iannelli, M.A., Pasqualini, S., Massacci, A.: Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. — Plant Physiol. 133: 829–837, 2003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rauser, W.E.: Phytochelatins and related peptides. Structure, biosynthesis, and function. — Plant Physiol. 109: 1141–1149, 1995.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saidi, I., Ayouni, M., Dhieb, A., Chtourou, Y., Chaïbi, W., Djebali, W.: Oxidative damages induced by short-term exposure to cadmium in bean plants: Protective role of salicylic acid. — S. Afr. J. Bot. 85: 32–38, 2013.

    Article  CAS  Google Scholar 

  • Sanita di Toppi, L., Gabbrielli, R.: Response to cadmium in higher plants. — Environ. exp. Bot. 41: 105–130, 1999.

    Article  Google Scholar 

  • Sbartai, H., Djebar, M.R., Sbartai, I., Berrabbah, H.: Bioaccumulation of cadmium and zinc in tomato (Lycopersicon esculentum L.). — Compt. Rend. Biol. 335: 585–593, 2012.

    Article  CAS  Google Scholar 

  • Schickler, H., Caspi, H.: Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. — Physiol. Plant. 105: 39–44, 1999.

    Article  CAS  Google Scholar 

  • Schützendübel, A., Schwanz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R., Godbold, D.L., Polle, A.: Cadmiuminduced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. — Plant Physiol. 127: 887–898, 2001.

    Article  PubMed Central  PubMed  Google Scholar 

  • Shen, G., Zhu, C., Du, Q., Shangguan, L.: Ascorbateglutathione cycle alteration in cadmium sensitive rice mutant cadB-1. — Rice Sci. 19: 185–192, 2012.

    Article  Google Scholar 

  • Siedlecka, A., Krupa, Z.: Cd/Fe interaction in higher plants — its consequences for the photosynthetic apparatus. — Photosynthetica 36: 321–331, 1999.

    Article  CAS  Google Scholar 

  • Sneller, F.E.C., Van Heerwaarden, L.M., Kraaijeveld-Smit, F.J.L., Ten Bookum, W.M., Koevoets, P.L.M., Schat, H., Verkleij, J.A.C.: Toxicity of arsenate in Silene vulgaris, accumulation and degradation of arsenate-induced phytochelatins. — New Phytol. 144: 223–232, 1999.

    Article  CAS  Google Scholar 

  • Souguir, D., Ferjani, E., Ledoigt, G., Goupil, P.: Sequential effects of cadmium on genotoxicity and lipoperoxidation in Vicia faba roots. — Ecotoxicology 20: 329–336, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Srivalli, S., Khanna-Chopra, R.: Role of glutathione in abiotic stress tolerance. — In: Khan, N.A., Singh, S., Umar, S. (ed.): Sulfur Assimilation and Abiotic Stress in Plants. Pp. 207–225. Springer, Berlin — Heidelberg 2008.

    Chapter  Google Scholar 

  • Stroinski, A.: Some physiological and biochemical aspects of plant resistance to cadmium effect. I. Antioxidative system. — Acta Physiol. Plant. 21: 175–188, 1999.

    Article  CAS  Google Scholar 

  • Sun, Q., Ye, Z.H., Wang, X.R., Wong, M.H.: Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. — J. Plant Physiol. 164: 1489–1498, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Teare, J.P., Punchard, N.A., Powell, J.J., Lumb, P.J., Mitchell, W.D., Thompson, R.P.: Automated spectrophotometric method for determining oxidized and reduced glutathione in liver. — Clin. Chem. 39: 686–689, 1993.

    CAS  PubMed  Google Scholar 

  • Vestena, S., Cambraia, J., Ribeiro, C., Oliveira, J. A., Oliva, M.A.: Cadmium-induced oxidative stress and antioxidative enzyme response in water hyacinth and salvinia. — Braz. J. Plant Physiol. 23: 131–139, 2011.

    Article  CAS  Google Scholar 

  • Vitoria, A.P., Lea, P.J., Azevedo, R.A.: Antioxidant enzymes responses to cadmium in radish tissues. — Phytochemistry 57: 701–710, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Vogeli-Lange, R., Wagner, G.: Relationship between cadmium, glutathione and cadmium-binding peptides (phytochelatins) in leaves of intact tobacco seedlings. — Plant Sci. 114: 11–18, 1996.

    Article  Google Scholar 

  • Vogl, S., Picker, P., Mihaly-Bison, J., Fakhrudin, N., Atanasov, A.G., Heiss, E. H., Kopp, B.: Ethnopharmacological in vitro studies on Austria’s folk medicine. — J. Ethnopharmacol. 149: 750–771, 2013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wagner, G.J.: Accumulation of cadmium in crop plants and its consequences to human health. — Adv. Agron. 51: 173–212, 1993.

    Article  CAS  Google Scholar 

  • Wu, F.-Z., Yang, W.-Q., Zhang, J., Zhou, L.-Q.: Effects of cadmium stress on growth and nutrient accumulation, distribution and utilization in Osmanthus fragrans var. thunbergii. — Chin. J. Plant Ecol. 34: 1220–1226, 2010.

    Google Scholar 

  • Yannarelli, G.G., Fernandez-Alvarez, A.J., Santa-Cruz, D.M., Tomaro, M.L.: Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. — Phytochemistry 68: 505–512, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Zenk, M.: Heavy metal detoxification in higher plants — a review. — Gene 179: 21–30, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C., Yin, X., Gao, K., Ge, Y., Cheng, W.: Nonprotein thiols and glutathione S-transferase alleviate Cd stress and reduce root-to-shoot translocation of Cd in rice. — J. Soil Sci. Plant Nutr. 176: 626–633, 2013.

    Article  CAS  Google Scholar 

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  1. Faculty of Science, Department of Chemistry, University of Dokuz Eylul, 35160, Buca, Izmir, Turkey

    L. Tarhan & B. Kavakcioglu

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  1. L. Tarhan
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Tarhan, L., Kavakcioglu, B. Glutathione metabolism in Urtica dioica in response to cadmium based oxidative stress. Biol Plant 60, 163–172 (2016). https://doi.org/10.1007/s10535-015-0570-6

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  • DOI: https://doi.org/10.1007/s10535-015-0570-6

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