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Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress

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Abstract

The present study aims to elucidate the role of antioxidative enzyme in the adaptive responses of metal-accumulators (Thlaspi caerulescens and Brassica juncea) and non-accumulator plant (Nicotiana tabacum) to Cadmium stress. When seedlings of plants were grown in hydroponic condition for a period of 4 days in the presence of 200 or 400 μM CdCl2, photosynthetic rate, transpiration rate and stomatal conductance in metal-accumulators decreased more slowly than that in tobacco. MDA content and electrolyte leakage increased with elevated Cd concentration and exposure time in all plant species, while the oxidative damage in tobacco was more serious than that in metal-accumulators. The activities of SOD and CAT in metal-accumulators were significantly higher than that in tobacco under normal condition, whereas there was no significant difference in the activity of POD between Indian mustard and tobacco. The activities of antioxidative enzymes increased rapidly in metal-accumulators in response to the Cd treatments, especially SOD and CAT. In tobacco, CAT activity declined rapidly by exposure to the Cd treatment, though the activity of SOD and POD was enhanced, indicating that the antioxidative enzymes in tobacco could not fully scavenge ROS generated by Cd toxicity. These results collectively indicate that the enzymatic antioxidation capacity is one of the important mechanisms responsible for metal tolerance in metal-accumulator plant species.

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Abbreviations

Cd:

cadmium

ROS:

reactive oxygen species

MDA:

malondialdehyde

SOD:

superoxide dismutase

CAT:

catalase

POD:

peroxidase

EC:

electrical conductivity

References

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  PubMed  CAS  Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, pp 85–108

    Google Scholar 

  • Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  • Boominathan R, Doran PM (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator Thlaspi caerulescens. Biotechnol Bioeng 83:158–167

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Bradford MM (1976) 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

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • De Vos CH, Schat H (1991) Free radicals and heavy metal tolerance. In: Rozema J, Verkleij JAC (eds) Ecological responses to environmental stress. Kluwer, Dordrecht, pp 1–30

    Google Scholar 

  • Fatima RA, Ahmad M (2005) Certain antioxidant enzymes of Allium cepa as biomarkers for the detection of toxic heavy metals in wastewater. Sci Total Environ 346:256–273

    Article  PubMed  CAS  Google Scholar 

  • Foster JG, Hess JL (1980) Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol 66:482–487

    Article  PubMed  CAS  Google Scholar 

  • Gallego SM, Benavides MP, Tomaro ML (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 

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

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetic and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Hendry GAF, Brocklebank KJ (1985) Iron-induced oxygen radical metabolism in waterlogged plants. New Phytol 101:199–206

    Article  CAS  Google Scholar 

  • Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309

    Article  PubMed  CAS  Google Scholar 

  • Kaiser W (1976) The effect of hydrogen peroxide on CO2 fixation of isolated chloroplast. Biochem Biophys Acta 440:476–482

    Article  PubMed  CAS  Google Scholar 

  • Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant and soil 200:241–250

    Article  CAS  Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kimd TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    Article  PubMed  CAS  Google Scholar 

  • León AM, Palma JM, Corpas FJ, Gómez M, Romero-Puertas MC, Chatterjee D, Mateos RM, del Rio LA, Sandalio LM (2002) Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820

    Article  Google Scholar 

  • MacRae EA, Ferguson IB (1985) Changes in catalase activity and hydrogen peroxide concentration in plants in response to low temperature. Physiol Plant 65:51–56

    Article  CAS  Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga scenedesmus. Ecotoxicol Environ Safety 55:64–69

    Article  PubMed  CAS  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    PubMed  CAS  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MN (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37

    Article  PubMed  CAS  Google Scholar 

  • Mittal R, Dubey RS (1991) Behaviour of peroxidases in rice: changes in enzyme activity and isoforms in relation to salt tolerance. Plant Physiol Biochem 29:31–40

    CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610

    Article  PubMed  CAS  Google Scholar 

  • Nickel RS, Cunningham BA (1969) Improved peroxidase assay method using Ieuco 2,3,6-trichlcroindophenol and application to comparative measurements of peroxidase catalysis. Anal Biochem 27:292–299

    Article  PubMed  CAS  Google Scholar 

  • Papazoglou EG, Karantounias GA, Vemmos SN, Bouranis DL (2005) Photosynthesis and growth responses of giant reed (Arundo donax L.) to the heavy metals Cd and Ni. Environ Int 31:243–249

    Article  PubMed  CAS  Google Scholar 

  • Piquery L, Davoine C, Huault C, Billard JP (2000) Senescence of leaf sheaths of ryegrass stubble: changes in enzyme activities related to H2O2 metabolism. Plant Growth Regul 30:71–77

    Article  CAS  Google Scholar 

  • Poschenrieder C, Barcelo J (1999) Water relations in heavy metal stressed plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. From molecules to ecosystems. Springer, Berlin, pp 207–229

    Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    Article  CAS  Google Scholar 

  • Radotic K, Ducic T, Mutavdzic D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environ Exp Bot 44:105–113

    Article  PubMed  CAS  Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodríguez-Serrano M, Gómez M, del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol. 164:1346–1357

    Article  PubMed  CAS  Google Scholar 

  • Salin ML (1987) Toxic oxygen species and protective systems of the chloroplast. Physiol Plant 72:681–689

    Article  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    PubMed  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schutzendubel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in scots pine roots. Plant Physiol 127:887–898

    Article  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 

  • Shaw BP (1995) Effects of mercury and cadmium on the activities of antioxidative enzymes in the seedlings of Phaseolus aureus. Biol Plant 37:587–596

    Article  CAS  Google Scholar 

  • Singh S, Eapen S, D’Souza SF (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246

    Article  PubMed  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 

  • Smirnoff N (1995) Antioxidant systems and plant response to the environment. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. Bios Scientific, Oxford, pp 217–243

    Google Scholar 

  • Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germination seedling of mung bean (Phaseolus vulgarize): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89

    Article  CAS  Google Scholar 

  • Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot 60:468–476

    Article  CAS  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Wada H, Koshiba T, Matsui T, Sato M (1998) Involvement of peroxidase in differential sensitivity to γ-radiation in seedlings of two Nicotiana species. Plant Sci 132:109–119

    Article  CAS  Google Scholar 

  • Zhou QX, Wei SH, Zhang QR (2006) Ecological remediation. China Environmental Science, Beijing, p 246

    Google Scholar 

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Acknowledgements

This research was supported by the National High Technology Planning Program of China (Grant nos. 2006AA10Z407 and 2007AA021404) and the China National Natural Sciences Foundation (Grant nos. 30570146).

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Correspondence to Yuxiu Zhang.

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Responsible Editor: Juan Barcelo.

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Wang, Z., Zhang, Y., Huang, Z. et al. Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil 310, 137–149 (2008). https://doi.org/10.1007/s11104-008-9641-1

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