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Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress

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Biologia Plantarum

Abstract

The effects of cadmium on physiological and ultrastructural characteristics were evaluated in 6-d-old seedlings of two Brassica napus L. cultivars Zheda 619 and ZS 758. Results show that Cd at lower concentration (100 μM) stimulated the seedling growth but at higher concentration (500 μM) inhibited the growth of both cultivars, decreased content of photosynthetic pigments, activities of antioxidant enzymes, and increased the content of malondialdehyde and reactive oxygen species. Cd content in different parts of seedlings was higher in ZS 758 than in Zheda 619. Electron micrographs illustrated that 500 μM Cd severely damaged the leaf and root tip cells of both cultivars. Under Cd stress, the size and number of starch grains, plastoglobuli, and lipid bodies in the chloroplasts increased. In the root tip cells, enlarged vacuoles, diffused cell walls, and undeveloped mitochondria were detected.

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Abbreviations

APX:

ascorbate peroxidase

CAT:

catalase

Car:

carotenoids

Chl:

chlorophyll

GR:

glutathione reductase

MDA:

malondialdehyde

POD:

peroxidase

SOD:

superoxide dismutase

TSP:

total soluble proteins

References

  • Aebi, H.: Catalase in vitro. — Methods Enzymol. 105: 121–126, 1984.

    CAS  PubMed  Google Scholar 

  • Ali, B., Wang, B., Ali, S., Ghani, M.A., Hayat, M.T., Yang, C., Xu, L., Zhou, W.J.: 5-Aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity and ultrastructural changes under cadmium stress in Brassica napus L. — J. Plant Growth Regul. in press, 2013a. DOI 10.1007/s00344-013-9328-6

  • Ali, B., Tao, Q.J., Zhou, Y.F., Gill, R.A., Ali, S., Rafiq, M.T., Xu, L., Zhou, W.J.: 5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. — Ecotoxicol. Environ. Safety 92: 271–280, 2013b.

    Article  CAS  PubMed  Google Scholar 

  • An, Y.N.: Assessment of comparative toxicities of lead and copper using plant assay. — Chemosphere 62: 1359–1365, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Bachir, M.L.D., Wu, F.B., Zhang, G.P., Wu, H.X.: Genotypic difference in effect of cadmium on the development and mineral concentrations of cotton. — Commun. Soil Sci. Plant Anal. 35: 285–299, 2004.

    Article  Google Scholar 

  • Banuelos, G.S., Meek, D.W.: Accumulation of selenium in plants grown on selenium treated soil. — J. environ. Qual. 19: 772–777, 1990.

    Article  CAS  Google Scholar 

  • Barcelo, J., Vasquez, M.D., Poschenrieder, C.: Structural and ultra-structural disorders in cadmium-treated bush bean plants (Phaseolus vulgaris L.). — New Phytol. 108: 37–49, 1988.

    Article  CAS  Google Scholar 

  • Bočová, B., Huttová, J., Liptaková, L., Mistrík, I., Olla, M., Tamas, L.: Impact of short-term cadmium treatment on catalase and ascorbate peroxidase activities in barley root tips. — Biol. Plant. 56: 724–728, 2012.

    Article  Google Scholar 

  • Bradford, M.M.: Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. — Anal Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Caasilit, M., Whitecross, M.I., Nayudu, M., Tanner, J.G.: UV-B irradiation induces differential leaf damage, ultrastructural changes and accumulation of specific phenolic compounds in rice cultivars. — Aust. J. Plant Physiol. 24: 261–274, 1997.

    Article  CAS  Google Scholar 

  • Chugh, L.K., Gupta, V.K., Sawhney, S.K.: Effect of cadmium on enzymes of nitrogen metabolism in pea seedlings. — Phytochemistry 3: 395–400, 1992.

    Article  Google Scholar 

  • Chugh, L.K., Sawhney, S.K.: Effect of cadmium on germination, amylases and rate of respiration of germinating pea seeds. — Environ. Pollut. 92: 1–5, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Daud, M.K., Yuqiang, S., Dawood, M., Hayat, Y., Variath, M.T., Wu, Y.X., Raziuddin, Mishkat, U., Salahuddin, Najeeb, U., Zhu, S.J.: Cadmium induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. — J. Hazard. Materials 161: 463–473, 2009a.

    Article  CAS  Google Scholar 

  • Daud, M.K., Variatha, M.T., Ali, S., Najeeb, U., Jamil, M., Hayat, Y., Dawood, M., Khand, M.I., Zaffar, M., Cheema, S.A., Tong, X.H., Zhu, S.: Cadmium-induced ultramorphological and physiological changes in leaves of two transgenic cotton cultivars and their wild relative. — J. Hazard. Materials 168: 614–625, 2009b.

    Article  CAS  Google Scholar 

  • Dietz, K.J., Baier, M., Kramer, U.: Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. — In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants: from Molecules to Ecosystems. Pp. 73–97. Springer-Verlag, Berlin 1999.

    Chapter  Google Scholar 

  • Fodor, A., Szabo-Nagy, A., Erdei, L.: The effects of cadmium on the fluidity and H+ ATPase activity of plasma membrane from sunflower and wheat roots. — J. Plant Physiol. 14: 787–792, 1995.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Garnier, L., Simon-Plas, F., Thuleau, P., Agnel, J.P., Blein, J.P., Ranjeva, R.: Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. — Plant Cell Environ. 29: 1956–1969, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Greger, M., Ogren, E.: Direct and indirect effects of Cd2+ on photosynthesis in sugar beet (Beta vulgaris). — Physiol. Plant. 83: 129–135, 1991.

    Article  CAS  Google Scholar 

  • Gong, H.J., Chen, K.M., Zhao, Z.G., Chen, G.C., Zhou, W.J.: Effects of silicon on defense of wheat against oxidative stress under drought at different developmental stages. — Biol. Plant. 52: 592–596, 2008.

    Article  CAS  Google Scholar 

  • Hassan, M.J., Shao, G., Zhang, G.P.: Influence of cadmium toxicity on antioxidant enzymes activity in rice cultivars with different grain Cd accumulation. — J. Plant Nutr. 28: 1259–1270, 2005a.

    Article  CAS  Google Scholar 

  • Hassan, M.J., Wang, F., Ali, S., Zhang, G.P.: Toxic effect of cadmium on rice as affected by nitrogen fertilizer form. — Plant Soil 277: 359–365, 2005b.

    Article  CAS  Google Scholar 

  • Jiang, M., Zhang, J.: Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. — Plant Cell Physiol. 42: 1265–1273, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, M., Zhang, J.: Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. — J. exp. Bot. 53: 2401–2410, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, H.M., Yang, J.C., Zhang, J.F.: Effects of external phosphorus on the cell ultra structure and the chlorophyll content of maize under cadmium and zinc stress. — Environ. Pollut. 147: 750–756, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Jin, X., Yang, X., Islam, E., Liu, D., Mahmood, Q.: Effects of cadmium on ultra-structure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredi Hance. — J. Hazard. Materials 156: 387–397, 2008.

    Article  CAS  Google Scholar 

  • Kupper, H., Lombi, E., Zhao, F.J., McGrath, S.P.: Cellular compartmentation of cadmium and zinc in relation to other elements in the hyper accumulator Arabidopsis halleri. — Planta 212: 75–84, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Labra, M., Gianazza, E., Waitt, R., Eberini, I., Sozzi, A., Regondi, S., Grassi, F., Agradi, E.: Zea mays L. protein changes in response to potassium dichromate treatments. — Chemosphere 60: 1234–1244, 2006.

    Article  Google Scholar 

  • Leul, M., Zhou, W.J.: Alleviation of waterlogging damage in winter rape by uniconazole application: effects on enzyme activity, lipid peroxidation and membrane integrity. — J. Plant Growth Regul. 18: 9–14, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Macnair, M.R.: The genetics of metal tolerance in vascular plants. — New Phytol. 124: 541–559, 1993.

    Article  CAS  Google Scholar 

  • MacRae, E.A., Ferguson, I.B.: Changes in catalase activity and H2O2 concentration in plants in response to low temperature. — Physiol. Plant. 65: 51–56, 1985.

    Article  CAS  Google Scholar 

  • Martin, S.R., Llugany, M., Barcelo, J., Poschenrieder, C.: Cadmium exclusion a key factor in differential Cdresistance in Thlaspi arvense ecotypes. — Biol. Plant. 56: 729–734, 2012.

    Article  CAS  Google Scholar 

  • Meng, H., Hua, S., Shamsi, I.H., Jilani, G., Li, Y., Jiang, L.: Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L. and its alleviation through exogenous plant growth regulators. — Plant Growth Regul. 58: 47–59, 2009.

    Article  CAS  Google Scholar 

  • Momoh, E.J.J., Zhou, W.J.: Growth and yield responses to plant density and stage of transplanting in winter oilseed rape (Brassica napus L.). — J. Agron. Crop Sci. 186: 253–259, 2001.

    Article  Google Scholar 

  • Najeeb, U., Jilani, G., Ali, S., Sarwar, M., Xu, L., Zhou, W.J.: Insight into cadmium induced physiological and ultrastructural disorders in Juncus effusus L. and its remediation through exogenous citric acid. — J. Hazard. Materials 186: 565–574, 2011.

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ouariti, O., Boussama, N., Zarrouk, M., Cherif, A., Ghorbal, M.H.: Cadmium and copper induced changes in tomato membrane lipids. — Phytochemistry 45: 1343–1350, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Ouzounidou, G., Moustakas, M., Eleftheriou, E.P.: Physiological and ultra-structural effects of cadmium on wheat (Triticum aestivum L.) leaves. — Arch. environ. Contam. Toxicol. 32: 154–160, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Papoyan, A., Pineros, M., Kochian, L.V.: Plant Cd2+ and Zn2+ status effects on root and shoot heavy metal accumulation in Thlaspi caerulescens. — New Phytol. 175: 51–58, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Pei, Z.F., Ming, D.F., Liu, D., Wan, G.L., Geng, X.X., Gong, H.J., Zhou, W.J.: Silicon improves the tolerance to waterdeficit stress induced by polyethylene glycol in wheat (Triticum aestivum L.) seedlings. — J. Plant Growth Regul. 29: 106–115, 2010.

    Article  CAS  Google Scholar 

  • Pinto, A.P., Mota, A.M., Devarennes, A., Pinto, F.: Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. — Sci. Total Environ. 326: 239–247, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Porra, R.J., Thompson, W.A., Kriedemann, P.E.: Determination of accurate extinction co-efficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. — Biochim. biophys. Acta 975: 384–394, 1989.

    Article  CAS  Google Scholar 

  • Quirino, B.F., Noh, Y.S., Himelbrau, E., Amasino, R.M.: Molecular aspects of leaf senescence. — Trends Plant Sci. 5: 278–282, 2001.

    Article  Google Scholar 

  • Rascio, N., Dalla, V.D., Ferretti, M., Merlo, L., Ghisi, R.: Some effects of cadmium on maize plants. — Arch. Environ. Contam. Toxicol. 25: 244–249, 1993.

    Article  CAS  Google Scholar 

  • Rodriguez-Serrano, M., Romero-Puertas, M., Pazmino, D.M., Testillano, P.S., Risueno, M.C., Delrio, L.A., Sandalio, L.M.: Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. — Plant Physiol. 150: 229–243, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sandalio, L.M., Dalurzo, H.C., Gomez, M., Romero-Puertas, M.C., Delrio, L.: Cadmium-induced changes in the growth and oxidative metabolism of pea plants. — J. exp. Bot. 52: 2115–2126, 2001.

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Schutzendubel, A., Nikolova, P., Rudolf, C., Polle, A.: Cadmium and H2O2-induced oxidative stress in Populus canescens roots. — Plant Physiol. Biochem. 40: 577–584, 2002.

    Article  CAS  Google Scholar 

  • Shamsi, I.H., Jilani, G., Zhang, G.P., Kang, W.: Cadmium stress tolerance through potassium nutrition in soybean. — Asian J. Chem. 20: 1099–1108, 2008.

    CAS  Google Scholar 

  • Singh, S., Sinha, S.: Accumulation of metals and its effects in Brassica juncea (L.) Czern. (cv. Rohini) grown on various amendments of tannery waste. — Ecotox. environ. Safety 62: 118–127, 2005.

    Article  CAS  Google Scholar 

  • Skorzynska, E., Baszynski, T.: Differences in sensitivity of the photosynthetic apparatus in Cd-stressed runner bean plants in relation to their age. — Plant Sci. 128: 11–21, 1997.

    Article  Google Scholar 

  • Somashekaraiah, B.V., Padmaja, K., Prassad, A.R.K.: Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. — Physiol. Plant. 85: 85–89, 1992.

    Article  CAS  Google Scholar 

  • Stobart, A.K., Griffiths, W.T., Ameen-Bukhari, I., Sherwood, R.P.: The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. — Physiol. Plant. 63: 293–298, 1985.

    Article  CAS  Google Scholar 

  • Tao, Y.M., Chen, Y.Z., Tan, T., Liu, X.C., Yang, D.L., Liang, S.C.: Comparison of antioxidant responses to cadmium and lead in Bruguiera gymnorrhiza seedlings. — Biol. Plant. 56: 149–152, 2012.

    Article  CAS  Google Scholar 

  • Tian, S.K., Lu, L.L., Yang, X.E., Huang, H.G., Wang, K., Brown, P.H.: Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyper accumulator Sedum alfredii. — Biol. Plant. 56: 344–350, 2012.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wong, M.K., Chuah, G.K., Koh, L.L., Ang, K.P., Hew, C.S.: The uptake of cadmium by Brassica chinensis and its effect on plant zinc and iron distribution. — Environ. exp. Bot. 24: 189–195, 1984.

    Article  CAS  Google Scholar 

  • Wu, F.B., Zhang, G.P.: Genotypic differences in effect of Cd on growth and mineral concentrations in barley seedlings. — Environ. Contam. Toxicol. 69: 219–227, 2002.

    Article  CAS  Google Scholar 

  • Zhang, X.Z.: The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. — In: Zhang, X.Z. (ed.): Research Methodology of Crop Physiology. Pp. 208–211. Agriculture Press, Beijing 1992.

    Google Scholar 

  • Zhang, W.F., Zhang, F., Raziuddin, R., Gong, H.J., Yang, Z.M., Lu, L., Ye, Q.F., Zhou, W.J.: Effects of 5-aminolevulinic acid on oilseed rape seedling growth under herbicide toxicity stress. — J. Plant Growth Regul. 27: 159–169, 2008.

    Article  Google Scholar 

  • Zhang, G.Q., Zhou, W.J., Gu, H.H., Song, W.J., Momoh, E.J.J.: Plant regeneration from the hybridization of Brassica juncea and B. napus through embryo culture. — J. Agron. Crop Sci. 189: 347–350, 2003.

    Article  Google Scholar 

  • Zhou, W.J., Leul, M.: Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. — Plant Growth Regul. 27: 99–104, 1999.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Crop Science and Zhejiang Key Laboratory of Crop Germplasm, Zhejiang University, Hangzhou, 310058, China

    B. Ali, P. Qian, M. Khan, T. Tian & W. Zhou

  2. Agricultural Experiment Station, Zhejiang University, Hangzhou, 310058, China

    R. Jin & W. Zhou

  3. College of Environment and Resource Science, Zhejiang University, Hangzhou, 310058, China

    R. Aziz

  4. Department of Environmental Sciences, Government College University, Faisalabad, 38000, Pakistan

    S. Ali

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  1. B. Ali
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  2. P. Qian
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Correspondence to W. Zhou.

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Acknowledgements: This work was supported by National High Technology Research and Development Program of China (2011AA10A206), National Key Science and Technology Supporting Program of China (2010BAD01B04), the Science and Technology Department of Zhejiang Province (2012C12902-1), and National Natural Science Foundation of China (31071698, 31170405).

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Ali, B., Qian, P., Jin, R. et al. Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biol Plant 58, 131–138 (2014). https://doi.org/10.1007/s10535-013-0358-5

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  • DOI: https://doi.org/10.1007/s10535-013-0358-5

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