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Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress

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Abstract

The activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione S-transferase (GST) as well as proline content were studied in leaves and roots of 14 day-old pea plants treated with NiSO4 (10, 100, 200 µm) for 1, 3, 6 and 9 days. Exposure of pea plants to nickel (Ni) resulted in the decrease in CuZnSOD as well as total SOD activities in both leaves and roots. The activity of APX in leaves of plants treated with 100 and 200 µm Ni increased following the 3rd day after metal application, while in roots at the end of the experiment the activity of this enzyme was significantly reduced. In both organs CAT activity generally did not change in response to Ni treatment. The activity of GST in plants exposed to high concentrations of Ni increased, more markedly in roots. In both leaves and roots after Ni application accumulation of free proline was observed, but in the case of leaves concentration of this amino acid increased earlier and to a greater extent than in roots. The results indicate that stimulation of GST activity and accumulation of proline in the tissues rather than antioxidative enzymes are involved in response of pea plants to Ni stress.

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Abbreviations

APX:

ascorbate peroxidase

CAT:

catalase

CDNB:

1-chloro-2,4-dinitrobenzene

GSH:

reduced glutathione

GST:

glutathione S-transferase

NBT:

nitro blue tetrazolium

ROS:

reactive oxygen species

SOD:

superoxide dismutase

References

  • Ali G., Srivastava P.S., Iqbal M. 1998. Morphogenic response and proline content in Bacopa monniera cultures grown under copper stress. Plant Sci., 138: 191–195.

    Article  CAS  Google Scholar 

  • Alia, Pardha Saradhi P. 1991. Proline accumulation under heavy metal stress. J. Plant Physiol., 138: 554–558.

    CAS  Google Scholar 

  • Alia, Prasad K.V.S.K., Paraha Saradhi P. 1995. Effect of zinc on free radicals and proline in Brassica and Cajanus. Phytochemistry, 39: 45–47.

    Article  CAS  Google Scholar 

  • Atta-Aly M.A. 1999. Effect of nickel addition on the yield and quality of parsley leaves. Sci. Hort., 82: 9–24.

    Article  CAS  Google Scholar 

  • Baccouch S., Chaoui A., El Ferjani E. 1998. Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots. Plant Physiol. Biochem., 36: 689–694.

    Article  CAS  Google Scholar 

  • Baccouch S., Chaoui A., El Ferjani E. 2001. Nickel toxicity induces oxidative damage in Zea mays roots. J. Plant Nutr., 24: 1085–1097.

    Article  CAS  Google Scholar 

  • Bandurska H. 2001. Does proline accumulated in leaves of water deficit stressed barley plants confine cell membrane injuries? II. Proline accumulation during hardening and its involvement in reducing membrane injuries in leaves subjected to severe osmotic stress. Acta Physiol. Plant., 23: 483–490.

    CAS  Google Scholar 

  • Barnett N.M., Naylor A.W. 1966. Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiol., 41: 1222–1230.

    PubMed  CAS  Google Scholar 

  • Bates L.S., Waldren R.P., Teare I.D. 1973. Rapid determination of free proline for water-stress studies. Plant Soil, 39: 205–207.

    Article  CAS  Google Scholar 

  • Bolwell G.P., Wojtaszek P. 1997. Mechanisms for the generation of reactive oxygen species in plant defense-a broad perspective. Physiol. Mol. Plant Pathol., 51: 347–366.

    Article  CAS  Google Scholar 

  • Boominathan R., Doran P.M. 2002. Ni-induced oxidative stress in roots of the Ni hyper-accumulator, Alyssum bertolonii. New Phytol., 156: 205–215.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen C.T., Chen L.-M., Lin C.C., Kao C.H. 2001. Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Sci., 160: 283–290.

    Article  CAS  PubMed  Google Scholar 

  • Chen Y.X., He Y.F., Luo Y.M., Yu Y.L., Lin Q., Wong M.H. 2003. Physiological mechanism of plant roots exposed to cadmium. Chemosphere, 50: 789–793.

    Article  PubMed  CAS  Google Scholar 

  • Cuypers A., Vangronsveld J., Clijsters H. 2000. Biphasic effect of copper on ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol. Plant., 110: 512–517.

    Article  CAS  Google Scholar 

  • Davis D.G., Swanson H.R. 2001. Activity of stress-related enzymes in the perennial weed leafy spurge (Euphorbia esula L.). Environ. Exp. Bot., 46: 95–108.

    Article  CAS  Google Scholar 

  • Dhindsa R.S., Plumb-Dhindsa P., Thorpe T.A. 1981. Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J. Exp. Bot., 32: 93–101.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Elia M.R., Borraccino G., Dipierro S. 1992. Soluble ascorbate peroxidase from potato tubers. Plant Sci., 85: 17–21.

    Article  CAS  Google Scholar 

  • Eskew D.L., Welch R.M., Cary E.E. 1983. Nickel: an essential micronutrient for legumes and possibly all higher plants. Science, 222: 621–623.

    Article  CAS  PubMed  Google Scholar 

  • Gabbrielli R., Pandolfini T., Espen L., Palandri M.R. 1999. Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings exposed to Ni2+ toxicity. J. Plant Physiol., 155: 639–645.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gzik A. 1996. Accumulation of proline and pattern of ∞-amino acids in sugar beet plants in response to osmotic, water and salt stress. Environ. Exp. Bot., 36: 29–38.

    Article  CAS  Google Scholar 

  • Habig W.H., Pabst M.J., Jakoby W.B. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem., 246: 7130–7139.

    Google Scholar 

  • Hartzendorf T., Rolletschek H. 2001. Effect of NaCl-salinity on amino acid and carbohydrate contents of Phragmites australis. Aquat. Bot., 69: 195–208.

    Article  CAS  Google Scholar 

  • Hoagland D.R., Arnon D.I. 1938. The water-culture method for growing plants without soil. Circ. Calif. Univ. Agric. Exp. Stn., 347: 1–39.

    CAS  Google Scholar 

  • Kasprzak K.S., Bal W., Karaczyn A.A. 2003. The role of chromatin damage in nickel-induced carcinogenesis. A review of recent developments. J. Environ. Monit., 5: 183–187.

    Article  PubMed  CAS  Google Scholar 

  • L’Huillier L., d’Auzac J., Durand M., Michaud-Ferrière N. 1996. Nickel effects on two maize (Zea mays) cultivars: growth, structure, Ni concentration, and localization. Can. J. Bot., 74: 1547–1554.

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Małecka A., Jarmuszkiewicz W., Tomaszewska B. 2001. Antioxidative defense to lead stress in subcellular compartments of pea root cells. Acta Biochim. Pol., 48: 687–698.

    PubMed  Google Scholar 

  • Marrs K.A. 1996. The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 47: 127–158.

    Article  PubMed  CAS  Google Scholar 

  • Marrs K.A., Walbot V. 1997. Expression and RNA splicing of the maize glutathione S-transferase Bronze2 gene is regulated by cadmium and other stresses. Plant Physiol., 113: 93–102.

    Article  PubMed  CAS  Google Scholar 

  • Matysik J., Alia, Bhalu B., Mohanty P. 2002. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr. Sci., 82: 525–532.

    CAS  Google Scholar 

  • Mauch F., Dudler R. 1993. Differential induction of distinct glutathione S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol., 102: 1193–1201.

    Article  PubMed  CAS  Google Scholar 

  • McCord J.M., Fridovich I. 1969. Superoxide dismutase. An enzymatic function for erythro-cuprein (hemocuprein). J. Biol. Chem., 244: 6049–6055.

    PubMed  CAS  Google Scholar 

  • Minami M., Yoshikawa H. 1979. A simplified assay method of superoxide dismutase activity for clinical use. Clin. Chim. Acta, 92: 337–342.

    Article  PubMed  CAS  Google Scholar 

  • Nagalakshmi N., Prasad M.N.V. 2001. Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci., 160: 291–299.

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y., Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol., 22: 867–880.

    CAS  Google Scholar 

  • Pandey N., Sharma C.P. 2002. Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci., 163: 753–758.

    Article  CAS  Google Scholar 

  • Pandey N., Sharma C.P. 2003. Chromium interference in iron nutrition and water relations of cabbage. Environ. Exp. Bot., 49: 195–200.

    Article  CAS  Google Scholar 

  • Parida B.K., Chhibba I.M., Nayyar V.K. 2003. Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci. Hort., 98: 113–119.

    Article  CAS  Google Scholar 

  • Prohaska J. 1983. Changes in tissue growth, concentrations of copper, iron, cytochrome oxidase and superoxide dismutase subsequent to dietary or genetic copper deficiency in mice. J. Nutr., 113: 2048–2058.

    PubMed  CAS  Google Scholar 

  • Samarakoon A.B., Rauser W.E. 1979. Carbohydrate levels and photoassimilate export from leaves of Phaseolus vulgaris exposed to excess cobalt, nickel, and zinc. Plant Physiol., 63: 1165–1169.

    Article  PubMed  CAS  Google Scholar 

  • Sandalio L.M., Dalurzo H.C., Gómez M., Romero-Puertas M.C., del Río L.A. 2001. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J. Exp. Bot., 52: 2115–2126.

    PubMed  CAS  Google Scholar 

  • Sharma S.S., Schat H., Vooijs R. 1998. In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry, 49: 1531–1535.

    Article  PubMed  CAS  Google Scholar 

  • Sudhakar C., Lakshmi A., Giridarakumar S. 2001. Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci., 161: 613–619.

    Article  CAS  Google Scholar 

  • Tewari R.K., Kumar P., Sharma P.N., Bisht S.S. 2002. Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci., 162: 381–388.

    Article  CAS  Google Scholar 

  • Tripathy B.C., Bhatia B., Mohanty P. 1981. Inactivation of chloroplast photosynthetic electron-transport activity by Ni2+. Biochim. Biophys. Acta, 638: 217–224.

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Weckx J.E.J., Clijsters H.M.M. 1997. Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol. Biochem., 35: 405–410.

    CAS  Google Scholar 

  • Zajc A., Neuefeind T., Prade L., Reinemer P., Huber R., Bieseler B. 1999. Herbicide detoxification by glutathione S-transferases as implicated from X-ray structures. Pestic. Sci., 55: 248–252.

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Physiology and Biochemistry, University of Łód, Banacha 12/16, 90-237, Łód, Poland

    Ewa Gajewska & Maria Skłodowska

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  1. Ewa Gajewska
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  2. Maria Skłodowska
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Correspondence to Ewa Gajewska.

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Gajewska, E., Skłodowska, M. Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27, 329–340 (2005). https://doi.org/10.1007/s11738-005-0009-3

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  • DOI: https://doi.org/10.1007/s11738-005-0009-3

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