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Oxidative stress induced by cadmium in Nicotiana tabacum L.: effects on growth parameters, oxidative damage and antioxidant responses in different plant parts

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Abstract

Tobacco (Nicotiana tabacum L.) is a tolerant species that accumulates cadmium. We studied the effect of Cd (0, 10, 25, 50, 100 μM) on growth parameters, chlorophyll and proline contents, enzymatic antioxidative response and lipid peroxidation of tobacco plants grown in hydroponic culture for 11 days to clarify the strategy of plant response against oxidative stress caused by this heavy metal. Cadmium accumulated more in roots than in shoots. Plant growth was not significantly affected by the cadmium concentrations used. Young leaves were more affected, showing visible chlorosis and a significant decrease in chlorophyll content at high Cd concentrations. Dry weight of both leaves and roots increased indicating a lower capacity for roots to absorb water. An increase in malondialdehyde levels was observed, indicating that lipid peroxidation occurred as a result of ROS formation. The activity of guaiacol peroxidase in leaves increased, indicating that it was very important in the scavenging of H2O2, while superoxide dismutase activity only increased in old leaves. Ascorbate peroxidase showed constant activity levels in tobacco leaves, suggesting that the ascorbate–glutathione pathway was less important as a defense mechanism.

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References

  • Aebi HE (1983) Catalase. In: Bergmeyer US (ed) Methods in enzymatic analysis. Verlag-Chemie, Weinheim, pp 273–277

    Google Scholar 

  • Ali MB, Yu KW, Hahn EJ, Paek KY (2005) Differential responses of anti-oxidants enzymes, lipoxygenase activity ascorbate content and the production of saponins in tissue cultured root of mountain Panax ginseng C.A. Mayer and Panax quinquefolium L. in bioreactor subjected to methyl jasmonate stress. Plant Sci 169:83–92

    Article  CAS  Google Scholar 

  • Ammar W, Nouairi I, Zarrouk M, Ghorbel M, Jemal F (2008) Antioxidative response to cadmium in roots and leaves of tomato plants. Biol Plant 52:727–731

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Barcelo J, Poschenrieder C (2004) Structural and ultrastructural changes in heavy metal exposed to plants. In: Prasad MNV (ed) Heavy metal stress in plants. Springer, Berlin, pp 223–248

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Burzyński M, Żurek A (2007) Effects of copper and cadmium on photosynthesis in cucumber cotyledons. Photosynthetica 45:239–244

    Article  Google Scholar 

  • Chen CM, Liu MC (2006) Ecological risk assessment on a cadmium contaminated soil landfill—a preliminary evaluation based on toxicity tests on local species and site-specific information. Sci Total Environ 359:120–129

    Article  PubMed  CAS  Google Scholar 

  • Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793

    Article  PubMed  CAS  Google Scholar 

  • Clijsters H, Cuypers A, Vangronsveld J (1999) Physiological responses to heavy metals in higher plants: defence against oxidative stress. Z Naturforsch (C) 54:730–734

    CAS  Google Scholar 

  • Costa G, Spitz E (1997) Influence of cadmium on soluble carbohydrates, free amino acids, protein content of in vitro cultured Lupinus albus. Plant Sci 128:131–140

    Article  CAS  Google Scholar 

  • Cuypers A, Vangronsveld J, Clijsters H (2002) Peroxidases in roots and primary leaves of Phaseolus vulgaris copper and zinc phytotoxicity: a comparison. J Plant Physiol 159:869–876

    Article  CAS  Google Scholar 

  • DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280

    Article  PubMed  CAS  Google Scholar 

  • Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

  • Gajewska E, Sklodowska M, Slaba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659

    Article  CAS  Google Scholar 

  • Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanassov A, Herzig R (2007) Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity. Environ Pollut 145:161–170

    Article  PubMed  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  Google Scholar 

  • Guo TR, Zhang GP, Zhou MX, Wu FB, Chen JX (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248

    Article  CAS  Google Scholar 

  • Hernandez-Allica J, Becerril JM, Garbisu C (2008) Assessment of the phytoextraction potential of high biomass crop plants. Environ Pollut 152:32–40

    Article  PubMed  CAS  Google Scholar 

  • Jimenez A, Hernandez JA, delrio LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    PubMed  CAS  Google Scholar 

  • Maurya R, Prasad SM, Gopal R (2008) LIF technique offers the potential for the detection of cadmium-induced alteration in photosynthetic activities of Zea Mays L. J Photochem Photobiol C Photochem Rev 9:29–35

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  Google Scholar 

  • Mourato MP, Martins LL, Campos-Andrada MP (2009) Physiological responses of Lupinus luteus to different copper concentrations. Biol Plant 53:105–111

    Article  CAS  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of gluthatione homeostasis and signalling. J Exp Bot 53:1283–1304

    Article  PubMed  CAS  Google Scholar 

  • Nouairi I, Ben Ammar W, Ben Youssef N, Ben Miled DD, Ghorbal M, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiol Plant 31:237–247

    Article  CAS  Google Scholar 

  • Pereira GJG, Molina SMG, Lea PJ, Azevedo RA (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. Plant Soil 239:123–132

    Article  CAS  Google Scholar 

  • Poschenrieder C, Barcelo J (2004) Water relations in heavy metal stressed plants. In: Prasad MNV (ed) Heavy metal stress in plants. Springer, Berlin, pp 249–270

    Google Scholar 

  • Romero-Puertas MC, Palma JM, Gomez M, Del Rio LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686

    Article  CAS  Google Scholar 

  • Rubio MC, Gonzalez EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115:531–540

    Article  PubMed  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez 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 

  • Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482

    Article  CAS  Google Scholar 

  • Schutzendubel 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  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, Dubey RS (1998) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plant 40:121–130

    Article  Google Scholar 

  • Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550

    Article  CAS  Google Scholar 

  • Shi GR, Cai QS (2008) Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46:627–630

    Article  CAS  Google Scholar 

  • Shi GR, Cai QS, Liu QQ, Wu L (2009) Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes. Acta Physiol Plant 31:969–977

    Article  CAS  Google Scholar 

  • Siedlecka A, Krupa Z, Samuelsson G, Oquist G, Gardestrom P (1997) Primary carbon metabolism in Phaseolus vulgaris plants under Cd/Fe interaction. Plant Physiol Biochem 35:951–957

    CAS  Google Scholar 

  • Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Rem Sens Environ 81:337–354

    Article  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 

  • Stolt JP, Sneller FEC, Bryngelsson T, Lundborg T, Schat H (2003) Phytochelatin and cadmium accumulation in wheat. Environ Exp Bot 49:21–28

    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 

  • Wagner GJ, Yeargan R (1986) Variation in cadmium accumulation potential and tissue distribution of cadmium in tobacco. Plant Physiol 82:274–279

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Zhang YX, Huang ZB, Huang L (2008) Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil 310:137–149

    Article  CAS  Google Scholar 

  • Yannarelli GG, Gallego SM, Tomaro ML (2006) Effect of UV-B radiation on the activity and isoforms of enzymes with peroxidase activity in sunflower cotyledons. Environ Exp Bot 56:174–181

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by Fundação para a Ciência e Tecnologia project PPCDT/AMB/55312/2004. Nicotiana tabacum Virginia var. K 326 seeds were kindly provided by Agrotab. The UIQA (Unidade de Investigação Química Ambiental) is grant aided by the FCT (Fundação para a Ciência e Tecnologia). The authors acknowledge the assistance of Dr. Giles Atkinson in reviewing the manuscript.

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Correspondence to Miguel Pedro Mourato.

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Communicated by G. Klobus.

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Martins, L.L., Mourato, M.P., Cardoso, A.I. et al. Oxidative stress induced by cadmium in Nicotiana tabacum L.: effects on growth parameters, oxidative damage and antioxidant responses in different plant parts. Acta Physiol Plant 33, 1375–1383 (2011). https://doi.org/10.1007/s11738-010-0671-y

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