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Effects of Cadmium and Arsenic on Physiological Responses and Copper and Zinc Homeostasis of Rice

  • Jung, Ha-il (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA) ;
  • Chae, Mi-Jin (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA) ;
  • Kim, Sun-Joong (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA) ;
  • Kong, Myung-Suk (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA) ;
  • Kang, Seong-Soo (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA) ;
  • Lee, Deog-Bae (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA) ;
  • Ju, Ho-Jong (Department of Agricultural Biology, Chonbuk National University) ;
  • Kim, Yoo-Hak (Division of Soil and Fertilizer, National Academy of Agricultural Science, RDA)
  • Received : 2015.08.31
  • Accepted : 2015.10.25
  • Published : 2015.10.31

Abstract

Heavy metals reduce the photosynthetic efficiency and disrupt metabolic reactions in a concentration-dependent manner. Moreover, by replacing the metal ions in metalloproteins that use essential metal ions, such as Cu, Zn, Mn, and Fe, as co-factors, heavy metals ultimately lead to the formation of reactive oxygen species (ROS). These, in turn, cause destruction of the cell membrane through lipid peroxidation, and eventually cause the plant to necrosis. Given the aforementioned factors, this study was aimed to understand the physiological responses of rice to cadmium (Cd) and arsenic (As) toxicity and the effect of essential metal ions on homeostasis. In order to confirm the level of physiological inhibition caused by heavy metal toxicity, hydroponically grown rice (Oryza sativa L. cv. Dongjin) plants were exposed with $0-50{\mu}M$ cadmium (Cd, $CdCl_2$) and arsenic (As, $NaAsO_2$) at 3-leaf stage, and then investigated malondialdehyde (MDA) contents after 7 days of the treatment. With increasing concentrations of Cd and As, the MDA content in leaf blade and root increased with a consistent trend. At 14 days after treatment with $30{\mu}M$ Cd and As, plant height showed no significant difference between Cd and As, with an identical reduction. However, As caused a greater decline than Cd for shoot fresh weight, dry weight, and water content. The largest amounts of Cd and As were found in the roots and also observed a large amount of transport to the leaf sheath. Interestingly, in terms of Cd transfer to the shoot parts of the plant, it was only transported to upper leaf blades, and we did not detect any Cd in lower leaf blades. However, As was transferred to a greater level in lower leaf blades than in upper leaf blades. In the roots, Cd inhibited Zn absorption, while As inhibited Cu uptake. Furthermore, in the leaf sheath, while Cd and As treatments caused no change in Cu homeostasis, they had an antagonist effect on the absorption of Zn. Finally, in both upper and lower leaf blades, Cd and As toxicity was found to inhibit absorption of both Cu and Zn. Based on these results, it would be considered that heavy metal toxicity causes an increase in lipid peroxidation. This, in turn, leads to damage to the conductive tissue connecting the roots, leaf sheath, and leaf blades, which results in a reduction in water content and causes several physiological alterations. Furthermore, by disrupting homeostasis of the essential metal ions, Cu and Zn, this causes complete heavy metal toxicity.

Keywords

References

  1. Barcelo, J., M.D. Vazquez, and C. Poschenrieder. 1988.Structural and ultrastructural disorders in cadmium-treated bush bean plants (Phaseolus vulgaris L.). New Phytol. 108:37-49. https://doi.org/10.1111/j.1469-8137.1988.tb00202.x
  2. Buege, J.A. and S.D. Aust. 1978. Microsomal lipid peroxidation. Methods Enzymol. 52:302-310. https://doi.org/10.1016/S0076-6879(78)52032-6
  3. DalCorso, G., A. Manara, S. Piasentin, and A. Furini. 2014. Nutrient metal elements in plants. Metallomics. 6(10):1770-1788. https://doi.org/10.1039/C4MT00173G
  4. Fergusson, J.E. 1990. The heavy elements: Chemistry, environmental impact and health effects. Pergamon Press.
  5. Galiulin, R.V., V.N. Bashkin, R.R. Galiulina, and P. Birch. 2001. A critical review: Protection from pollution by heavy metals phytoremediation of industrial wastewater. Land Contam. Reclam. 9:349-358.
  6. Gayomba, S.R., H.I. Jung, J. Yan, J. Danku, M.A. Rutzke, M. Bernal, U. Kramer, L.V. Kochian, D.E. Salt, and O.K. Vatamaniuk. 2013. The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. Metallomics. 5(9):1262-1275. https://doi.org/10.1039/c3mt00111c
  7. Hall, J.L. 2002. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53:1-11. https://doi.org/10.1093/jexbot/53.366.1
  8. Hossain, Z. and S. Komatsu. 2013. Contribution of proteomic studies towards understanding plant heavy metal stress response. Front. Plant Sci. 3:310.
  9. Hossain, Z., M.Z. Nouri, and S. Komatsu. 2012. Plant cell organelle proteomics in response to abiotic stress. J. Proteome. Res. 11:37-48. https://doi.org/10.1021/pr200863r
  10. Kamachi, K., T. Yamaya, T. Mae, and K. Ojima. 1991. A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiol. 96(2):411-417. https://doi.org/10.1104/pp.96.2.411
  11. Lagriffoul, A., B. Mocquot, M. Mench, and J. Vangronsveld. 1998. Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil. 200: 241-250. https://doi.org/10.1023/A:1004346905592
  12. Lee, J.H., J.Y. Kim, W.R. Go, E.J. Jeong, A. Kunhikrishnan, G.B. Jung, D.H. Kim, and W.I. Kim. 2012. Current research trends for heavy metals of agricultural soils and crop uptake in Korea. Korean J. Environ. Agric. 31(1):75-95. https://doi.org/10.5338/KJEA.2012.31.1.75
  13. Mengel, K. and E.A. Kirby. 1978. Principles of plant nutrition. 5th ed. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  14. NAAS. 2011. Soil and Plant Analyses. National Academy of Agricultural Science, RDA, Suwon, Korea.
  15. Nagajyoti, P.C., K.D. Lee, and T.V.M. Sreekanth. 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8:199-216. https://doi.org/10.1007/s10311-010-0297-8
  16. Park, S.W., J.S. Yang, S.W. Ryu, D.Y. Kim, J.D. Shin, W.I. Kim, J.H. Choi, and S.L. Kim. 2009. Uptake and translocation of heavy metals to rice plant on paddy soils in "Top-rice" cultivation areas. Korean J. Environ. Agic. 28(2): 131-138. https://doi.org/10.5338/KJEA.2009.28.2.131
  17. Pasternak, T., V. Rudas, G. Potters, and M.A.K. Jansen. 2005. Morphogenic effects of abiotic stress: reorientation of growth in Arabidopsis thaliana seedlings. Environ. Exp. Bot. 53:299-314. https://doi.org/10.1016/j.envexpbot.2004.04.009
  18. Paulose, B., S. Chhikara, J. Coomey, H.I. Jung, O.K. Vatamaniuk, and O.P. Dhankher. 2013. A $\gamma$-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell. 25(11):4580-4595. https://doi.org/10.1105/tpc.113.111815
  19. Raven, K.P. and R.H. Loeppert. 1997. Heavy metals in the environment: Trace element composition of fertilizers and soil amendments. J. Environ. Qual. 26:551-557.
  20. Rodriguez-Serrano, M., M.C. Romero-Puertas, D.M. Pazmino, P.S. Testillano, M.C. Risueno, L.A. Del Rio, and L.M. Sandalio. 2009. Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150(1):229-243. https://doi.org/10.1104/pp.108.131524
  21. Salt, D.E., M. Blaylock, N.P.B.A. Kumar, V. Dushenkov, B.D. Ensley, I. Chet, and I. Raskin. 1995. Phytoremediation: A novel strategy for the removal of toxic metals from the environment using plants. Biotechnology. 13:468-474. https://doi.org/10.1038/nbt0595-468
  22. Shan, F.R., N. Ahmad, K.R. Masood, and D.M. Zahid. 2008. The influence of cadmium and chromium on the biomass production of shisham (Dalbergla sissoo Roxb.) seedlings. Pak. J. Bot. 40:1341-1348.
  23. Sharma, R.K. and M. Agrawal. 2005. Biological effects of heavy metals: an overview. J. Environ. Biol. 26:301-313.
  24. Singh, S., S. Eapen, and S.F. D'Souza. 2006. Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233-246. https://doi.org/10.1016/j.chemosphere.2005.05.017
  25. Vassilev, A. and I. Yordanov. 1997. Reductive analysis of factors limiting growth of cadmium-treated plants: A review. Bulg. J. Plant Physiol. 23:114-133.
  26. Vassilev, A., I. Yordanov, and T. Tsonev. 1997. Effects of $Cd^{2+}$ on the physiological state and photosynthetic activity of young barley plants. Photosynthetica. 34:293-302. https://doi.org/10.1023/A:1006805010560

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