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Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves

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Abstract

Influence of 100 μM Ni on growth, Ni accumulation,\(\ \hbox{O}_{2}^{\cdot-}\), H2O2 and lipid peroxides contents as well as the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (POD) and glutathione peroxidase (GSH-Px) were studied in the leaves of wheat plants on the 3rd, 6th and 9th days after treatment. Exposure of the plants to Ni for only 3 days led to almost 200-fold increase in this metal concentration in the leaf tissue but later the rate of Ni accumulation was much slower. Length and fresh weight of the leaves were substantially reduced, up to 25% and 39%, respectively at the end of experiment. Visible symptoms of Ni toxicity: chlorosis and necrosis were observed following the 3rd day. Treatment with Ni resulted in the increase in\( \ \hbox{O}_{2}^{\cdot -}\) and H2O2 contents in the leaves. Both showed their highest values, approximately 250% of those of the control, on the 3rd day and then their levels decreased but still markedly exceeded the control values. SOD and CAT activities decreased significantly in response to Ni treatment, however a several-fold increase in APX and POD activities was found. No significant changes in lipid peroxides content were observed in the leaves after Ni application. The activity of GSH-Px showed a 29% induction on the 3rd day. Our results indicated that despite prolonged increases in\( \ \hbox{O}_{2}^{\cdot-}\) and H2O2 levels, oxidative damage, measured as the level of lipid peroxidation, did not occur in the leaves of Ni-treated wheat.

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Abbreviations

APX:

ascorbate peroxidase

CAT:

catalase

GSH:

reduced glutathione

GSH-Px:

glutathione peroxidase

MBTH:

3-methyl-2-benzothiazolinone hydrazone

NBT:

nitro blue tetrazolium

POD:

guaiacol peroxidase

ROS:

reactive oxygen species

SOD:

superoxide dismutase

TBARS:

thiobarbituric acid reacting substances

References

  • Aroca R, Irigoyen JJ, Sánchez-Díaz M (2003). Drought enhances maize chilling tolerance. II. Photosynthetic traits and protective mechanisms against oxidative stress. Physiol Plant 117:540–549

    Article  PubMed  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 

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

    Article  CAS  Google Scholar 

  • Bradford MM (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 

  • Capaldi DJ, Taylor KE (1983). A new peroxidase color reaction: oxidative coupling of 3-methyl-2-benzothiazolinone hydrazone (MBTH) with its formaldehyde azine. Application to glucose and choline oxidases. Anal Biochem 129:329–336

    Article  PubMed  CAS  Google Scholar 

  • Chen L-M, Lin CC, Kao CH (2000). Copper toxicity in rice seedlings: Changes in antioxidative enzyme activities, H2O2 level, and cell wall peroxidase activity in roots. Bot Bull Acad Sin 41:99–103

    CAS  Google Scholar 

  • Cho U-H, Park J-O (2000). Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9

    Article  PubMed  CAS  Google Scholar 

  • Delisle G, Champoux M, Houde M (2001). Characterization of oxalate oxidase and cell death in Al-sensitive and tolerant wheat roots. Plant Cell Physiol 42:324–333

    Article  PubMed  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA. (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 

  • Díaz J, Bernal A, Pomar F, Merino F (2001). Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 161:179–188

    Article  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 

  • Doke N (1983). Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357

    Article  CAS  Google Scholar 

  • Drązkiewicz M, Skórzyńska-Polit E, Krupa Z (2004). Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. BioMetals 17:379–387

    Article  PubMed  Google Scholar 

  • Edwards R (1996). Characterisation of glutathione transferases and glutathione peroxidases in pea (Pisum sativum). Physiol. Plant. 98:594–604

    Article  CAS  Google Scholar 

  • Faltin Z, Camoin L, Ben-Hayyim G, Perl A, Beeor-Tzahar T, Strosberg AD (1998). Cysteine is the presumed catalytic residue of Citrus sinensis phospholipid hydroperoxide glutathione peroxidase over-expressed under salt stress. Physiol Plant 104:741–746

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–339

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M, Słaba M, Mazur J. 2006. Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant (in press)

  • Gaspar T, Penel C, Hagege D, Greppin H (1991). Peroxidases in plant growth, differentiation, and development processes. In: Łobarzewski J, Greppin H, Penel C, Gaspar T (eds). Biochemical, Molecular and Physiological Aspects of Plant Peroxidases. University M. Curie-Skłodowska, Lublin, Poland, pp. 249–280

    Google Scholar 

  • Gonnelli C, Galardi F, Gabbrielli R (2001). Nickel and copper tolerance and toxicity in three Tuscan populations of Silene paradoxa. Physiol Plant 113:507–514

    Article  CAS  Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo A (2005). Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    Article  CAS  Google Scholar 

  • Hao F, Wang X, Chen J (2006). Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000). Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950). The water-culture method for growing plants without soil. Circ Calif Univ Agric Exp Stn 347:1–39

    Google Scholar 

  • Hodgson MA, Fridovich I (1975). The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: inactivation of the enzyme. Biochemistry 14:5294–5303

    Article  PubMed  CAS  Google Scholar 

  • Hopkins J, Tudhope GR (1973). Glutathione peroxidase in human red cells in health and disease. Br J Hematol 25:563–575

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kehrer JP (2000). The Haber–Weiss reaction and mechanisms of toxicity. Toxicology 149:43-50

    Article  PubMed  CAS  Google Scholar 

  • Krupa Z, Siedlecka A, Maksymiec W, Baszyński T (1993). In vivo response of photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity. J Plant Physiol 142:664–668

    CAS  Google Scholar 

  • Kuo MC, Kao CH (2004). Antioxidant enzyme activities are upregulated in response to cadmium in sensitive, but not in tolerant, rice (Oryza sativa L.) seedlings. Bot Bull Acad Sin 45:291–299

    CAS  Google Scholar 

  • Madhava Rao KV, Sresty TVS (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  PubMed  CAS  Google Scholar 

  • Maehly AC, Chance B (1954). The assay of catalases and peroxidases. In: Glick D (eds). Methods of biochemical analysis vol. 1. Interscience Publishers Inc, New York, pp. 357–425

    Chapter  Google Scholar 

  • McCord JM, 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 

  • Munné-Bosch S, Alegre L (2002). The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57

    Article  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 CP (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 V, Dixit V, Shyam R (2005). Antioxidative responses in relation to growth of mustard (Brassica juncea cv. Pusa Jaikisan) plants exposed to hexavalent chromium. Chemosphere 61:40–47

    Article  PubMed  CAS  Google Scholar 

  • Parida BK, Chhibba IM, Nayyar VK (2003). Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci Hort 98:113–119

    Article  CAS  Google Scholar 

  • Roeckel-Drevet P, Gagne G, Tourvieille de Labrouhe D, Dufaure J-P, Nicolas P, Drevet JR (1998). Molecular charactrization, organ distribution and stress-mediated induction of two glutathione peroxidase-encoding mRNAs in sunflower (Helianthus annuus). Physiol Plant 103:385–394

    Article  CAS  Google Scholar 

  • Samarakoon AB, Rauser WE (1979). Carbohydrate levels and photoassimilate export from leaves of Phaseolus vulgaris exposed to excess cobalt, nickel, and zinc. Plant Physiol 63:1165–1169

    PubMed  CAS  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey RS (2001). Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

    Article  CAS  Google Scholar 

  • Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A, Vangronsveld J (2005). Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444

    Article  PubMed  CAS  Google Scholar 

  • Weckx JEJ, Clijsters HMM (1997). Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 35:405–410

    CAS  Google Scholar 

  • Yagi K (1976). A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15:212–216

    Article  PubMed  CAS  Google Scholar 

  • Zeller S, Feller U (1999). Long-distance transport of cobalt and nickel in maturing wheat. Eur J Agron 10:91–98

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was partly supported by University of Łódź Grant No. 505/429. The authors are grateful to Dr. Z. Nita (Hodowla Roślin Strzelce Sp. z o.o., Poland) for supplying the wheat seeds.

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Correspondence to Ewa Gajewska.

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Gajewska, E., Skłodowska, M. Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20, 27–36 (2007). https://doi.org/10.1007/s10534-006-9011-5

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