biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 58:539-550, 2014 | DOI: 10.1007/s10535-014-0430-9

Genotypic variation of the responses to chromium toxicity in four oilseed rape cultivars

R. A. Gill1, X. Q. Hu2, B. Ali1, C. Yang1, J. Y. Shou3, Y. Y. Wu4,*, W. J. Zhou1,2,*
1 Institute of Crop Science and Zhejiang Key Laboratory of Crop Germplasm, Zhejiang University, Hangzhou, P.R. China
2 Agricultural Experiment Station, Zhejiang University, Hangzhou, P.R. China
3 Zhuji Municipal Agro-Tech Extension Center, Zhuji, P.R. China
4 College of Biology and Environment, Zhejiang Wanli University, Ningbo, P.R. China

Heavy metal toxicity in soils has been considered as major constraints for oilseed rape (Brassica napus L.) production. In the present study, toxic effects of chromium (Cr) were studied in 6-d-old seedlings of four different cultivars of B. napus (ZS 758, Zheda 619, ZY 50, and Zheda 622). The elevated content of Cr inhibited seedling growth, decreased the content of photosynthetic pigments, and activities of antioxidant enzymes, as well as increased the content of malondialdehyde and reactive oxygen species in all the cultivars. The Cr content in different parts of plants was higher in Zheda 622 than in other cultivars. The electron microscopic study showed changes in ultrastructure of leaf mesophyll and root tip cells at 400 μmol Cr, and these changes were more prominent in Zheda 622. An increased size and number of starch grains and number of plastoglobuli, damaged thylakoid membranes, and immature nucleoli and mitochondria were observed in leaves. In roots, enlarged vacuoles, disrupted cell walls and cell membranes, an increased number of mitochondria and a size of nucleolus, as well as plasmolysis (in Zheda 622) were observed. On the basis of these findings, it can be concluded that cv. Zheda 622 was more sensitive to Cr as compared to other three cultivars.

Keywords: antioxidants enzyme activities; cell ultrastructures; chlorophyll content; seedling growth; reactive oxygen species
Subjects: chromium; cell ultrastructure; chlorophyll content; reactive oxygen species; growth; carotenoids; ascorbate peroxidase; catalase; guaiacol peroxidase; superoxide dismutase; oilseed rape

Received: October 11, 2013; Revised: January 15, 2014; Accepted: January 17, 2014; Published: September 1, 2014  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Gill, R.A., Hu, X.Q., Ali, B., Yang, C., Shou, J.Y., Wu, Y.Y., & Zhou, W.J. (2014). Genotypic variation of the responses to chromium toxicity in four oilseed rape cultivars. Biologia plantarum, 58(3), 539-550. doi: 10.1007/s10535-014-0430-9
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aebi, H.: Catalase in vitro. - Methods Enzymol. 105: 121-126, 1984. Go to original source...
    2. Ali, B., Qian, P., Jin, R., Ali, S., Khan, M., Aziz, R., Tian, T., Zhou, W.: Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. - Biol. Plant. 58: 131-138, 2014. Go to original source...
    3. Ali, S., Farooq, M.A., Yasmeen, T., Hussain, S., Arif, M.S., Abbas, F., Bharwana, S.A., Guoping, Z.: The influence of silicon on barley growth, photosynthesis and ultra-structure under chromium stress. - Ecotox. environ. Safety 89: 66-72, 2013a. Go to original source...
    4. Ali, B., Huang, C.R., Qi, Z.Y., Ali, S., Daud, M.K., Geng, X.X., Liu, H.B., Zhou, W.J.: 5-Aminolevulinic acid ameliorates cadmium-induced morphological, biochemical and ultrastructural changes in seedlings of oilseed rape. - Environ. Sci. Pollution Res. 20: 7256-7267, 2013b. Go to original source...
    5. 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. - Ecotox. environ. Safety 92: 271-280, 2013c. Go to original source...
    6. 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. 32: 604-614, 2013d. Go to original source...
    7. Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
    8. Bera, A.K., Kanta-Bokaria, K.: Effect of tannery effluent on seed germination, seedling growth and chloroplast pigment content in mungbean (Vigna radiata L. Wilczek). - Environ. Ecol. 17: 958-961, 1999.
    9. Bočová, B., Huttová, J., Liptáková, Ą., Mistrík, I., Ollé, M., Tamás, L.: Impact of short-term cadmium treatment on catalase and ascorbate peroxidase activities in barley root tips. - Biol. Plant. 56: 724-728, 2012. Go to original source...
    10. Bradford, N.M.: Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    11. Caasilit, M., Whitecross, M.I., Nayudu, M., Tanner, G.J.: UV-B irradiation induces differential leaf damage, ultra-structural changes and accumulation of specific phenolic compounds in rice cultivars. - Aust. J. Plant Physiol. 24: 261-274, 1997. Go to original source...
    12. Choudhury, S., Panda, S.K.: Toxic effect, oxidative stress and ultrastructural changes in moss Taxitheelium nepalense (Schwaegr.) Broth. under lead and chromium toxicity. - Water Air Soil Pollut. 167: 73-90, 2005. Go to original source...
    13. Darko, E., Ambrus, H., Stefanovits, E., Anyais, B., Fodor, J., Bakos, F., Barnabas, B.: Aluminum toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. - Plant Sci. 166: 583-591, 2004. Go to original source...
    14. Delrio, L.A., Pastori, G.M., Palma, J.M., Sandalio, L.M., Sevilla, F., Corpas, F.J., Jimenez, A., Lopez-Huertas, E., Hernandez, J.A.: The activated oxygen role of peroxisomes in senescence. - Plant Physiol. 116: 1195-1200, 1998. Go to original source...
    15. Dey, S.K., Jena, P.P., Kundu, S.: Antioxidative efficiency of Triticum aestivum L. exposed to chromium stress. - J. environ. Biol. 30: 539-544, 2009.
    16. Dietz, K.J., Baier, M., Kramer, U.: Free radicals and reactive oxygen species as mediator of heavy metal toxicity in plants. - In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. From Molecules to Ecosystem. Pp. 73-89. Springer-Verlag, Berlin 1999. Go to original source...
    17. Dixit, V., Pandey, V., Shyam, R.: Chromium ions inactivate electron transport and enhance superoxide generation invivo in pea (Pisum sativum L. cv: Azad) root mitochondria. - Plant Cell Environ. 25: 687-693, 2002. Go to original source...
    18. Fernandez, R., Bertrand, A., Casares, A., Garcia, R., Gonzalez, A., Tames, R.S.: Cadmium accumulation and its effect on the in-vitro growth of woody fleabane and mycorrhized white birch. - Environ. Pollut. 152: 522-529, 2008. Go to original source...
    19. 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. Go to original source...
    20. Gallego, S.M., Benavides, M.P., Tomaro, M.L.: Involvement of an antioxidant defence system in the adaptive response to heavy metal ions in Helianthus annuus L. cells. - Plant Growth Regul. 36: 267-273, 2002. Go to original source...
    21. Ganesh, K.S., Baskaran, L., Rajasekaran, S., Sumathi, K., Chidambaram, A.L.A., Sundaramoorthy, P.: Chromium stress induced alterations in biochemical and enzyme metabolism in aquatic and terrestrial plants. - Colloid Surf. B 63: 159-163, 2008. Go to original source...
    22. Gomes, R.A., Jr., Moldes, C.A., Delite, F.S., Pompeu, G.B., Gratao, P.L., Mazzafera, P., Lea P.G., Azevedo, R.A.: Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. - Chemosphere 65: 1330-1337, 2006. Go to original source...
    23. Gunes, A., Inal, A., Bagci, E.G., Coban, S., Sahin, O.: Silicon increases boron tolerance and reduces oxidative damage of wheat grown in soil with excess boron. - Biol Plant. 51: 571-574, 2007. Go to original source...
    24. Halliwell, B., Gutteridge J.M.C., Aruoma, O.: The deoxyribose method: a simple' test tube' a ssay for determination of rate constants for reactions of hydroxyl radicals. - Anal. Biochem. 165: 215-219, 1987. Go to original source...
    25. Han, F.X., Sridhar, B.B.M., Monts, D.L., Su, Y.: Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. - New Phytol. 162: 489-499, 2004. Go to original source...
    26. Jiang, H.M., Yang, J.C., Zhang, J.F.: Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. - Environ. Pollut. 147: 750-756, 2007. Go to original source...
    27. 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. Go to original source...
    28. 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. Go to original source...
    29. 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 helleri. - Planta 212: 75-84, 2000. Go to original source...
    30. Martin, S.R., Llugany, M., Barceló, J., Poschenrieder, C.: Cadmium exclusion a key factor in differential Cd resistance in Thlaspi arvense ecotypes. - Biol. Plant. 56: 729-734, 2012. Go to original source...
    31. Nakano, Y., Asada, K.: Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
    32. Paiva, L.B., De Oliveira, J.G., Azevedo, R.A., Ribeiro, D.R., Da Silva M.G., Vitoria, A.P.: Ecophysiological responses of water hyacinth exposed to Cr3+ and Cr6+. - Environ. exp. Bot. 65: 403-409, 2009. Go to original source...
    33. Panda, S.K., Choudhury, S.: Chromium stress in plants. - Braz. J. Plant Physiol. 17: 95-102, 2005. Go to original source...
    34. Panda, S.K, Mahapatra, S., Patra, H.K.: Chromium toxicity and water stress simulation effects in intact senescing leaves of greengram (Vigna radiata L. var. Wilckzeck K851). - In: Panda, S.K. (ed.): Advances in Stress Physiology of Plants. Pp. 129-136. Scientific Publisher, Jodhpur 2002.
    35. Panda, S.K., Patra, H.K.: Does Cr (III) produce oxidative damage in excised wheat leaves? - J. Plant Biol. 27: 105-110, 2000. Go to original source...
    36. Pandey, V., Dixit, V., Shyam, R.: Antioxidative responses in relation to growth of mustard (Brassica juncea cv. Pusa Jaikisan) plants exposed to hexavalent chromium. - Chemosphere 61: 40-47, 2005. Go to original source...
    37. Pandey, V., Dixit, V., Shyam, R.: Chromium effect on ROS generation and detoxification in pea (Pisum sativum) leaf chloroplasts. - Protoplasma 236: 85-95, 2009. Go to original source...
    38. Porra, R.J., Thompson, W.A., Kriedemann, P.E.: Determination of accurate extinction coefficients 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. Go to original source...
    39. Purvis, A.C.: Role of the alternative oxidase in limiting superoxide production by plant mitochondria. - Physiol. Plant. 100: 165-170, 1997. Go to original source...
    40. Qiu, B., Zhou, W., Xue, D., Zeng, F., Ali, S., Zhang, G.: Identification of Cr-tolerant lines in a rice (Oryza sativa) DH population. - Euphytica 174: 199-207, 2010. Go to original source...
    41. Qureshi, M.I., Abdin, M.Z., Qadir, S., Iqbal, M.: Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. - Biol Plant. 51: 121-128, 2007. Go to original source...
    42. Reddy, A.M., Kumar, S.G., Jyothsnakumari, J., Thimmanaik, S., Sudhakar, C.: Lead induced changes in antioxidant metabolism of horse gram (Macrotyloma uniflorum (Lam.) Verdc.) and bengal gram (Cicer arietinum L.). - Chemosphere 60: 97-104, 2005. Go to original source...
    43. Rucinska-Sobkowiak, R., Pukacki, P.M.: Antioxidative defense system in lupin roots exposed to increasing concentrations of lead. - Acta Physiol. Plant. 28: 357-364, 2006. Go to original source...
    44. Shamsi, I.H., Wei, K., Zhang, G., Jilani, G., Hassan, M.J.: Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean. - Biol. Plant. 52: 165-169, 2008. Go to original source...
    45. Samantary, S.: Biochemical responses of Cr-tolerant and Crsensitive mungbean cultivars grown on varying levels of chromium. - Chemosphere 47: 1065-1072, 2002. Go to original source...
    46. Shahandeh, H., Hossner, L.R.: Plant screening for chromium phytoremediation. - Int. J. Phytorem. 2: 31-51, 2002. Go to original source...
    47. Shanker, A.K., Cervantes, T.C., Loza-Taverac, H., Avudainayagam, S.: Chromium toxicity in plants. - Environ. Int. 31: 739-753, 2005. Go to original source...
    48. Sinha, S., Basant, A., Malik, A., Singh, K.P.: Multivariate modeling of chromium-induced oxidative stress and biochemical changes in plants of Pistia stratiotes L. - Ecotoxicology 8: 555-566, 2009. Go to original source...
    49. Subrahmanyam, D.: Effects of chromium toxicity on leaf photosynthetic characteristics and oxidative changes in wheat (Triticuma estivum L.). - Photosynthetica 46: 339-345, 2008. Go to original source...
    50. Sundaramoorthy, P., Chidambaram, A., Ganesh, K.S., Unnikannan, P., Baskaran, L.: Chromium stress in paddy: (i) nutrient status of paddy under chromium stress; (ii) phytoremediation of chromium by aquatic and terrestrial weeds. - C. R. Biol. 8: 597-607, 2010. Go to original source...
    51. 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. Go to original source...
    52. Tiwari, K., Dwivedi, K., S. Singh, N. K., Rai, U. N., Tripathi, R. D.: Chromium (VI) induced phytotoxicity and oxidative stress in pea (Pisum sativum L.): biochemical changes and translocation of essential nutrients. - J. environ. Biol. 30: 389-394, 2009.
    53. Velikova, V., Yordanov, I., Edreva, A.: Oxidative stress and some antioxidant systems in acid rain-treated bean plants. - Plant Sci. 151: 59-66, 2000. Go to original source...
    54. 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. Go to original source...
    55. Zhen, Y., Miao, L., Su, J., Liu, S., Yin, Y., Wang, S., Pang, Y., Shen, H., Tian, D., Qi J., Yang, Y.: Differential responses of anti-oxidative enzymes to aluminum stress in tolerant and sensitive soybean genotypes. - J. Plant Nutr. 32: 1255-1270, 2009. Go to original source...
    56. 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. Go to original source...

    Return to the content