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Effect of Phosphorus on the Cadmium Transfer and ROS-scavenging Capacity of Rice Seedlings

  • Jung, Ha-Il (Division of Soil and Fertilizer, National Institute of Agricultural Science, RDA) ;
  • Chae, Mi-Jin (Division of Soil and Fertilizer, National Institute of Agricultural Science, RDA) ;
  • Kong, Myung-Suk (Division of Soil and Fertilizer, National Institute of Agricultural Science, RDA) ;
  • Kim, Yoo-Hak (Division of Soil and Fertilizer, National Institute of Agricultural Science, RDA)
  • Received : 2017.08.07
  • Accepted : 2017.08.22
  • Published : 2017.08.31

Abstract

Environmental toxicity due to cadmium (Cd) pollution in croplands causes critical problems worldwide. Rice (Oryza sativa L.) is an important crop in Asia, including South Korea, and numerous studies have evaluated the relationship between Cd and antioxidants to alleviate Cd uptake from the soil into plants. However, information about the relationship between phosphorus (P) and antioxidants in rice seedlings is still limited with regard to Cd phytotoxicity. We therefore investigated the physiological responses of rice (Oryza sativa L. cv 'Dongjin') seedlings to Cd toxicity and the effect of P application on reactive oxygen species (ROS) and antioxidant changes. The exposure of rice seedlings to $30{\mu}M$ Cd inhibited plant growth; increased the contents of superoxide, hydrogen peroxide, and malondialdehyde; and induced Cd uptake by the roots and leaves. Application of P to Cd-exposed seedlings decreased Cd-induced oxidative stress by enhancing the capacity of ascorbate (AsA) production and ROS-scavenging, and decreased Cd transfer from the roots to the leaves. These results suggest that P application alleviated Cd-induced growth inhibition and oxidative damage by restricting Cd translocation from the roots to the leaves and maintaining sufficient levels of AsA.

Keywords

References

  1. Arshad, M., S. Ali, A. Noman, Q. Ali, M. Rizwan, M. Farid, and M.K. Irshad. 2016. Phosphorus amendment decreased cadmium (Cd) uptake and ameliorates chlorophyll contents, gas exchange attributes, antioxidants, and mineral nutrients in wheat (Triticum aestivum L.) under Cd stress. Arch. Agron. Soil Sci. 62:533-546. https://doi.org/10.1080/03650340.2015.1064903
  2. 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
  3. Brackhage, C., J.H. Huang, J. Schaller, E.J. Elzinga, and E.G. Dudel. 2014. Readily available phosphorous and nitrogen counteract for arsenic uptake and distribution in wheat (Triticum aestivum L.). Sci. Rep. 4:4944.
  4. Buege, J.A. and S.D. Aust. 1978. Microsomal lipid peroxidation. Methods Enzymol. 52:302-310.
  5. Elstner, E.F. and A. Heupel. 1976. Inhibition of nitrite formation from hydroxylammonium-chloride: a simple assay for superoxide dismutase. Anal. Biochem. 70:616-620. https://doi.org/10.1016/0003-2697(76)90488-7
  6. Fergusson, J.E. 1990. The heavy elements: chemistry, environmental impact and health effects. Pergamon Press.
  7. Gaitonde, M.K. 1967. A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem. J. 104:627-633. https://doi.org/10.1042/bj1040627
  8. 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.
  9. 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
  10. Gill, S.S. and N. Tuteja. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48:909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
  11. Gomes, M.P., A.M. Soares, and Q.S. Garcia. 2014. Phosphorous and sulfur nutrition modulate antioxidant defenses in Myracrodruom urundeuva plants exposed to arsenic. J. Hazard. Mater. 276:97-104. https://doi.org/10.1016/j.jhazmat.2014.05.020
  12. Harada, E., Y. Yamaguchi, N. Koizumi, and S. Hiroshi. 2002. Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J. Plant Physiol. 159: 445-448. https://doi.org/10.1078/0176-1617-00733
  13. Jalil, A., F. Selles, and J.M. Clarke. 1994. Effect of cadmium on growth and the uptake of cadmium and other elements by durum wheat. J. Plant Nutr. 17:1839-1858. https://doi.org/10.1080/01904169409364851
  14. Jan, A.T., M. Azam, K. Siddiqui, A. Ali, I. Choi, and Q.M. Haq. 2015. Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. Int. J. Mol. Sci. 16:29592-29630. https://doi.org/10.3390/ijms161226183
  15. Jana, S. and M.A. Choudhuri. 1982. Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat. Bot. 12:345-354. https://doi.org/10.1016/0304-3770(82)90026-2
  16. Jiang, H.M., J.C. Yang, and J.F. Zhang. 2007. Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ. Pollut. 147:750-756. https://doi.org/10.1016/j.envpol.2006.09.006
  17. Jung, H.I., M.J. Chae, M.S. Kong, S.S. Kang, and Y.H. Kim. 2016. Effect of rice straw compost on cadmium transfer and metal-ions distribution at different growth stages of soybean. Korean J. Soil Sci. Fert. 49(6):644-650. https://doi.org/10.7745/KJSSF.2016.49.6.644
  18. Jung, H.I., M.J. Chae, S.J. Kim, M.S. Kong, S.S. Kang, D.B. Lee, H.J. Ju, and Y.H. Kim. 2015. Effects of cadmium and arsenic on physiological responses and copper and zinc homeostasis of rice. Korean J. Soil Sci. Fert. 48(5): 397-403. https://doi.org/10.7745/KJSSF.2015.48.5.397
  19. 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
  20. Kerk, N.M. and L.J. Feldman. 1995. A biochemical model for the initiation and maintenance of the quiescent center: implications for organization of root meristems. Dev. 121:2825-2833.
  21. Kirkham, M.B. 2006. Cadmium in plants on polluted soils: effects of soil factors, hyperaccumulation and amendments. Geoderma 37:19-32.
  22. 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
  23. Law, M.Y., S.A. Charles, and B. Halliwell. 1983. Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts: the effect of hydrogen peroxide and of paraquat. Biochem. J. 210:899-903. https://doi.org/10.1042/bj2100899
  24. 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
  25. Luwe, M. 1996. Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and response to changing ozone concentrations in air. Plant Cell Environ. 19:321-328. https://doi.org/10.1111/j.1365-3040.1996.tb00254.x
  26. Meister, A. and M.E. Anderson. 1983. Glutathione. Annu. Rev. Biochem. 52:711-760. https://doi.org/10.1146/annurev.bi.52.070183.003431
  27. Mengel, K. and E.A. Kirby. 1978. Principles of plant nutrition. 5th ed. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  28. Meuwly, P. and W.E. Rauser. 1992. Alteration of thiol pools in roots and shoots of maize seedlings exposed to cadmium: adaptation and developmental cost. Plant Physiol. 99:8-15. https://doi.org/10.1104/pp.99.1.8
  29. Mishra, B., R.S. Sangwan, S. Mishra, J.S. Jadaun, F. Sabir, and N.S. Sangwan. 2014. Effect of cadmium stress on inductive enzymatic and nonenzymatic responses of ROS and sugar metabolism in multiple shoot cultures of Ashwagandha (Withania somnifera Dunal). Protoplasma 251(5):1031-1045. https://doi.org/10.1007/s00709-014-0613-4
  30. NAAS. 2011. Soil and Plant Analyses. National Academy of Agricultural Science, RDA, Suwon, Korea.
  31. 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
  32. 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. Agric. 28(2):131-138. https://doi.org/10.5338/KJEA.2009.28.2.131
  33. 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.
  34. Sajwan, K.S., S. Paramasivam, J.P. Richardson, and A.K. Alva. 2002. Phosphorus alleviation of cadmium phytotoxicity. J. Plant Nutr. 25:2027-2034. https://doi.org/10.1081/PLN-120013292
  35. 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. Biotechnol. 13:468-474.
  36. Siebers, N., M. Siangliw, and C. Tongcumpou. 2013. Cadmium uptake and subcellular distribution in rice plants as affected by phosphorus: soil and hydroponic experiments. J. Soil Sci. Plant Nutr. 3:833-844.
  37. Singh, R.P. and M. Agrawal. 2010. Biochemical and physiological responses of rice (Oryza sativa L.) grown on different sewage sludge amendments rates. Bull. Environ. Contam. Toxicol. 84:606-612. https://doi.org/10.1007/s00128-010-0007-z
  38. 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
  39. Talukdar, D. 2012. Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in medic. Seedlings through modulation of antioxidant enzyme activities. J. Crop Sci. Biotechnol. 15:325-334. https://doi.org/10.1007/s12892-012-0065-3
  40. 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.
  41. 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
  42. Xu, X., C. Liu, X. Zhao, R. Li, and W. Deng. 2014. Involvement of an antioxidant defense system in the adaptive response to cadmium in maize seedlings (Zea mays L.). Bull. Environ. Contam. Toxicol. 93:618-624. https://doi.org/10.1007/s00128-014-1361-z
  43. Yan, Y.F., D.H. Choi, D.S. Kim, and B.W. Lee. 2010a. Genotypic variation of cadmium accumulation and distribution in rice. J. Crop Sci. Biotechnol. 13:69-73. https://doi.org/10.1007/s12892-010-0036-5
  44. Yan, Y.F., D.H. Choi, D.S. Kim, and B.W. Lee. 2010b. Absorption, translocation, and remobilization of cadmium supplied at different growth stages of rice. J. Crop Sci. Biotechnol. 13:113-119. https://doi.org/10.1007/s12892-010-0045-4
  45. Zhang, B., S. Shang, H. Zhang, Z. Jabeen, and G. Zhang. 2013. Sodium chloride enhances cadmium tolerance through reducing cadmium accumulation and increasing anti-oxidative enzyme activity in tobacco. Environ. Toxicol. Chem. 32:1420-1425. https://doi.org/10.1002/etc.2183