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Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in Lens culinaris medic. Seedlings through modulation of antioxidant enzyme activities

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Abstract

The effect of calcium (Ca) on lentil (Lens culinaris Medic.) seedlings exposed to cadmium (Cd) stress was studied by investigating plant growth and antioxidant enzyme activities. Plants were grown for 14 days in full-strength Hoagland nutrient media supplemented with Cd concentrations of 0, 10, 20, and 40 μM, and on corresponding medium supplied with 5 mM Ca(NO3)2 prior to Cd addition. Increasing Cd led to accumulation of metal and reduced the fresh weight of the shoots more strongly than that of the roots. Cd concentrations of 20 and 40 μM were selected to study its toxic effect on seedlings. Activities of superoxide dismutase, ascorbate peroxidase, catalase, dehydroascorbate reductase, and glutathione reductase decreased at much higher magnitude in the shoots than those observed in the roots under Cd exposure. Failure of antioxidant defense in scavenging of reactive oxygen species was evidenced by abnormal rise in H2O2, resulting in enhancement of lipid peroxidation and membrane electrolyte leakage as the marks of Cd-induced oxidative stress in lentil seedlings. Ca priming in the media significantly reduced the Cd accumulation and considerably alleviated the adverse impact of Cd treatment by modulating the antioxidant enzyme activity. Mitigation of Cd-induced stress by Ca application was strongly suggested by declining levels of H2O2 and consequent lowering of oxidative damage of membrane. Consequently, this enhanced fresh mass of plant parts as the sign of Ca-mediated normal growth in Cd-treated lentil seedlings.

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References

  • Akibode S, Maredia M. 2011. Global and regional trends in production, trade and consumption of food legume crops. Draft Report, March 27, 2011

    Google Scholar 

  • Anjum NA, Umar S, Iqbal M, Khan NA. 2011. Cadmium causes oxidative stress in mung bean by affecting the antioxidant enzyme system and ascorbate-glutathione cycle metabolism. Russ. J. Plant Physiol. 58: 92–99

    Article  CAS  Google Scholar 

  • Bandeolu E, Eyidogan F, Yücel M, Öktem HA. 2004. Antioxidant responses of shoots and roots of lentil to NaCl-salinity stress. Plant Growth Regul. 42: 69–77

    Article  Google Scholar 

  • Beyer WF, Fridovich I. 1987. Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal. Biochem. 161: 559–566

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Carlberg I, Mannervik B. 1985. Glutathione reductase. In M Alton, eds, Methods in Enzymology, Academic Press, San Diego, pp 484–490

    Google Scholar 

  • Chance B, Maehly AC. 1955. Assay of catalases and peroxidases. Methods Enzymol. 2: 764–817

    Article  Google Scholar 

  • Chen YL, Huang RF, Xiao YM, Lu P, Chen J, Wang XC. 2004. Extracellular calmodulin-induced stomatal closure is mediated by heterotrimeric G protein and H2O2. Plant Physiol. 136: 4096–4103

    Article  PubMed  CAS  Google Scholar 

  • Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H. 2001. Detoxification of cadmium in tobacco plants: Formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213: 45–50

    Article  PubMed  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 

  • DalCorso G, Farinati S, Furini A. 2010. Regulatory networks of cadmium stress in plants. Plant Signal. Behav. 5: 663–667

    Article  PubMed  CAS  Google Scholar 

  • De Pinto MC, De Gara L. 2004. Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J. Exp. Bot. 55: 2559–2569

    Article  PubMed  Google Scholar 

  • Dionisio-Sese M, Tobita S. 1998. Antioxidant responses of rice seedlings to salinity stress. Plant Sci. 135: 1–9

    Article  CAS  Google Scholar 

  • FAOSTAT. 2008. Available at: http://faostat.fao.org/

  • Gautam S, Pandey SN. 2008. Growth and biochemical responses of nickel toxicity on leguminous crop (Lens esculantum) grown in alluvial soil. Res. Environ. Life Sci. 1: 25–28

    Google Scholar 

  • Gong M, Chen SN, Song YQ, Li ZG. 1997. Effect of calcium and calmodulin on intrinsic heat tolerance in relation to antioxidant systems in maize seedlings. Aust. J. Plant Physiol. 24: 371–379

    Article  CAS  Google Scholar 

  • Hirschi KD. 2004. The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol. 136: 2438–2442

    Article  PubMed  CAS  Google Scholar 

  • Hodges DM, Delong JM, Forney CF, Prange RK. 1999. Improving the thiobarbituric acid-reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604–611

    Article  CAS  Google Scholar 

  • Hu X, Jiang M, Zhang J, Zhang A, Lin F, Tan M. 2007. Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants. New Phytol. 173: 27–38

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Huang B. 2001. Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J. Exp. Bot. 52: 341–349

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Yang YY, Lee Y. 2002. Pb and Cd uptake in rice roots. Physiol. Plant. 116: 368–372

    Article  CAS  Google Scholar 

  • Kiran Y, Sahin A. 2006. The effects of cadmium on seed germination, root development and mitotic of root tip cells of lentil (Lens culinaris Medik.). World J. Agric. Sci. 2: 196–200

    Google Scholar 

  • Lechowski Z, Bialczyk J. 1993. Calcium mediated cytokinin action on chlorophyll synthesis in isolated embryo of Scots pine. Biol. Plant. 35: 53–62

    Article  CAS  Google Scholar 

  • Mandal SM, Bhattacharyya R. 2012. Rhizobium-Legume symbiosis: A model system for the recovery of metal-contaminated agricultural land, In A Zaidi, PA Wani, MS Khan, eds, Toxicity of heavy metals in legumes and bioremediation, Springer-Verlag Wien, pp 115–118

  • 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 

  • Muehlbauer FJ, Cho S, Sarker S, McPhee KE, Coyne CJ, Rajesh PN, Ford R. 2006. Application of biotechnology in breeding lentil for resistance to biotic and abiotic stress. Euphytica 147: 149–156

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Noctor G, Foyer CH. 1998. Ascorbate and glutathione: Keeping active oxygen under control. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–279

    Article  CAS  Google Scholar 

  • Ortega-Villasante C, Rellán-Álvarez ZZ, Del Campo FF, Carpena-Ruiz RO, Hernández LE. 2005. Cellular damage induced by Cd and mercury in Medicago sativa. J. Exp. Bot. 56: 2239–2251

    Article  PubMed  CAS  Google Scholar 

  • Ouzounidou G, Moustakas M, Eleftherious EP. 1997. Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves. Arch. Environ. Contam. Toxicol. 32: 154–160

    Article  PubMed  CAS  Google Scholar 

  • Rentel MC, Knight MR. 2004. Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135: 1471–1479

    Article  PubMed  CAS  Google Scholar 

  • Rivetta A, Negrini N, Cocucci M. 1997. Involvement of Ca 2+-calmodulin in Cd 2+ toxicity during early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ. 20: 600–608

    Article  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM. 2009. Cellular responses of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150: 229–243

    Article  PubMed  Google Scholar 

  • Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Rio LA, Sandalio LM. 2004. Cd-induced subcellular accumulation of O2- and H2O2 in pea leaves. Plant Cell Environ. 27: 1122–1134

    Article  CAS  Google Scholar 

  • Roy BK, Prasad R, Gunjan. 2010. Heavy metal accumulation and changes in metabolic parameters in Cajanas cajan grown in mine spoil. J. Environ. Biol. 31: 567–573

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Schützendübel A, Polle A. 2002. Plant responses to abiotic stresses: heavy metal- induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53: 1351–1365

    Article  PubMed  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Sakran AM, Basalah MO, Ali HM. 2012. Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. Int. J. Mol. Sci. 13: 6604–6619

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N. 2005. Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol. 22: 19–25

    Article  CAS  Google Scholar 

  • Talukdar D. 2011a. The aneuploid switch: Extra-chromosomal effect on antioxidant defense through trisomic shift in Lathyrus sativus L. Ind. J. Fund. Appl. Life Sci. 1: 263–273

    Google Scholar 

  • Talukdar D. 2011b. Isolation and characterization of NaCltolerant mutations in two important legumes, Clitoria ternatea L. and Lathyrus sativus L.: Induced mutagenesis and selection by salt stress. J. Med. Plants Res. 5: 3619–3628

    CAS  Google Scholar 

  • Talukdar D. 2011c. Flower and pod production, abortion, leaf injury, yield and seed neurotoxin levels in stable dwarf mutant lines of grass pea (Lathyrus sativus L.) differing in salt stress responses. Int. J. Curr. Res. 2: 46–54

    Google Scholar 

  • Talukdar D. 2012a. Flavonoid-deficient mutants in grass pea (Lathyrus sativus L.): Genetic control, linkage relationships, and mapping with aconitase and S nitrosoglutathione reductase isozyme loci. The Scientific World Journal 2012: Article ID 345983, 11 pages, doi:1 0.1100/2012/345983

  • Talukdar D. 2012b. Ascorbate deficient semi-dwarf asfL1 mutant of Lathyrus sativus exhibits alterations in antioxidant defense. Biol. Plant. 56: 675–682

    Article  CAS  Google Scholar 

  • Talukdar D. 2012c. An induced glutathione deficient mutant in grass pea (Lathyrus sativus L.): Modifications in plant morphology, alterations in antioxidant activities and increased sensitivity to cadmium. Biorem. Biodiv. Bioavail. 6: 75–86

    Google Scholar 

  • Talukdar D. 2012d. Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol. Mol. Biol. Plants DOI:10.1007/s12298-012-0140-8.

  • Talukdar D. 2013. Bioaccumulation and transport of arsenic in different genotypes of lentil (Lens culinaris Medik.). International Journal of Pharma and Bio Sciences 4: (B) 694–701

    Google Scholar 

  • Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X. 2011. Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84: 63–69

    Article  PubMed  CAS  Google Scholar 

  • Uraguchi S, Fujiwara T. 2012. Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5: 5

    Article  Google Scholar 

  • Vernoux T, Wilson RC, Seeley KA, Reichheld J-P, Muroy S, et al.2000. The ROOT MERISTEMLESS/CADMIUM SENSITIVE 2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97–109

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang CQ, Chen M, Wang BS. 2007. Betacyanin accumulation in the leaves of C3 halophyte Suaeda salsa L. is induced by watering roots with H2O2. Plant Sci. 172: 1–7

    Article  CAS  Google Scholar 

  • Wang CQ, Song H. 2009. Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep. 28: 1341–1349

    Article  PubMed  CAS  Google Scholar 

  • Williams PC, Bhatty RS, Deshpande SS, Hussein LA, Savage GP. 1994. Improving nutritional quality of cool season food legumes. In FJ Muehlbauer, WJ Kaiser, eds, Expanding the Production and Use of Cool Season Food Legumes, Kluwer Academic Publishers, Dordrecht, pp 113–129

    Chapter  Google Scholar 

  • Yang T, Poovaiah BW. 2003. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 8: 505–512

    Article  PubMed  CAS  Google Scholar 

  • Yau SK, Erskine W. 2000. Diversity of boron-toxicity tolerance in lentil growth and yield. Genet. Res. Crop Evol. 47: 55–61

    Article  Google Scholar 

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  1. Plant Cell and Stress Biology Laboratory, Department of Botany, R.P.M. College, University of Calcutta, Uttarpara, Hooghly, 712258, India

    Dibyendu Talukdar

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Talukdar, D. Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in Lens culinaris medic. Seedlings through modulation of antioxidant enzyme activities. J. Crop Sci. Biotechnol. 15, 325–334 (2012). https://doi.org/10.1007/s12892-012-0065-3

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