Sulphur Supply Level Effects on the Assimilation of Nitrate and Sulphate into Amino Acids and Protein in Forage Rape (Brassica napus L.)

  • Lee, Bok-Rye (BK21 Research Team for the Control of Animal Hazards using Biotechnology, College of Agriculture & Life Science, Chonnam National University) ;
  • Kim, Tae-Hwan (BK21 Research Team for the Control of Animal Hazards using Biotechnology, College of Agriculture & Life Science, Chonnam National University)
  • Received : 2012.10.06
  • Accepted : 2012.11.14
  • Published : 2012.12.31


Sulphur deficiency has become widespread over the past several decades in most of the agricultural area. Oilseed rape (Brassica napus L.) is a very sensitive to S limitation which is becoming reduction of quality and productivity of forage. Few studies have assessed the sulphur mobilization in the source-sink relationship, very little is known about the regulatory mechanism in interaction between sulphur and nitrogen during the short-term sulphur deficiency. In this study, therefore, amount of sulphur and nitrogen incorporated into amino acids and proteins as affected by different S-supplied level (Control: 1 mM ${SO_4}^{2-}$, S-deficiency: 0.1 mM ${SO_4}^{2-}$, and S-deprivation: 0 mM ${SO_4}^{2-}$) were examined. The amount of sulphur in sulphate (S-sulphate) was significantly decreased by 25.8% in S-deprivation condition, compare to control, but not nitrogen in nitrate (N-nitrate). The markedly increase of sulphur and nitrogen incorporated amino acids (S-amino acids and N-amino acids) was observed in both S-deficiency and S-deprivation treatments. The amount of nitrogen incorporated proteins (N-protein) was strongly decreased as sulphur availability while the amount of sulphur incorporated into proteins (S-protein) was not affected. A highly significant ($p{\leq}0.001$) relationship between S-sulphate and S-amino acid was observed whereas the increase of N-amino acids is closely associated with decrease of N-proteins. These data indicate that increase of sulphur and nitrogen incorporated into amino acids was from different nitrogen and sulphur metabolites, respectively


Supported by : Korea Research Foundation


  1. Abdallah, M., Dubousset, L., Meuriot, F., Etienne, P., Avice, J.C. and Ourry, A. 2010. Effect of mineral sulphur availability on nitrogen and sulphur uptake and remobilization during the vegetative growth of Brassica napus L. Journal of Experiment Botany. 61:2335-2346.
  2. Anderson, J.W. 2005. Regulation of sulphur distribution and redistribution in grain plants. In: K. Saito, I. De KokStulen, M.J. Hwkesford, E. Schung, A. Sirko, H. Rennenberg (eds). Sulphur Transport and Assimilation in Plants in the Postgenomic Era. Backhys Publisher, Leiden, pp. 23-31.
  3. Bell, C.I., Clarkson, D.T. and Cram, W.J. 1995. Sulphate supply and its regulation of transport in roots of a tropical legume Macropitilium atropurpureum cv. Siratro. Journal of Experiment Botany. 46:65-71.
  4. Blake Klaff, M.M.A., Harrison, K.R., Hawkes- ford, M.J., Zhao F.J. and McGrath, S.P. 1998. Allocation of sulphur within oilseed rape (Brassica napus L.) leaves in response to sulphur deficiency. Plant Physioloy. 118:1337-1344.
  5. Clarkson, D.T. and Hawkesford, M.J. 1993. Molecular biological approaches to plant nutrition. Plant and Soil. 155/156:21-31.
  6. Dubousset, L., Abdallah, M., Desfeus, A.S., Etienne, P., Meuriot, F., Hawkesford, M.J., Gombert, J., Ségura, R., Bataillé, M.-P., Rezé, S., Bonnefoy, J., Ameline, A.F., Ourry, A., Le Dily F. and Avice, J.C. 2009. Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. Journal of Experimental Botany. 60: 3239-3253.
  7. Hawkesford, M.J. 2000. Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. Journal of Experimental Botany. 51: 131-138.
  8. Hawkesford, M.J. and De Kok, L.J. 2006. Managing sulphur metabolism in plants. Plant, Cell and Environment. 29:382-395.
  9. Kataoka, T., Watanabe-Takahashi, A., Hayashi, N., Ohnishi, M., Mimura, T., Buchner, P., Hawkesford, M.J., Yamaya, T. and Takahashi, H. 2004. Vacuolar sulphate transporters are essential determinants controlling internal distribution of sulphate in Arabidopsis. Plant Cell 16:2693-2704.
  10. Kim, H., Hirai, M.Y., Hayashi, H., Chino, M., Naito, S. and Fujiwara, T. 1999. Role of Oacetyl-L-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta. 209: 282-289.
  11. Kim, T.H., Lee, B.R., Jung, W.J., Kim, K.Y., Avice, J.C. and Ourry, A. 2004. De novo protein synthesis in relation to ammonia and proline accumulation in water stressed white clover. Functional Plant Biology. 31:847-855.
  12. Kopriva, S., Suter, M., von Ballmoos, P., Hesse, H., Krahenbühl, U., Rennenberg, H. and Brunold, C. 2002. Interaction of sulphate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiology. 130:1406-1413.
  13. Lappartient, A.G., Vidmar, J.J., Leustek, T., Glass, A.D.M. and Touraine, B. 1999. Inter-organ signaling in plants: regulation of ATP sulfurylase and sulphate transporter genes expression in roots mediated by phloem-translocated compound. Plant Journal. 18:89-95.
  14. Lee, B.R., Jung, W.J., Kim, K.Y., Avice, J.C., Ourry, A. and Kim, T.H. 2005. Transient increase of de novo amino acid synthesis and its physiological significance in water-stressed white clover (Trifolium repens). New Phytologist 182: 654-663.
  15. Li, Y., Gao, Y.X., Ding, L., Shenand, Q.R. and Guo, S.W. 2009. Ammonium enhances the tolerance of rice seedlings (Oryza sativa L.) to water stress. Agricultural Water Management. 96:1746-1750.
  16. Maruyama-Nakashita, A., Inoue, E., Watanabe- Takahashi, A., Yamaya, T. and Takahashi, H. 2003. Transcriptome profiling of sulphur responsive genes in Arabidopsis reveals global effects of sulphur nutrition on multiple metabolic pathways. Plant Physiology. 132:597-605.
  17. McGrath, S.P. and Zhao, F.J. 1996. Sulfur uptake, yield response and the interaction between nitrogen and sulfur in winter oilseed rape (Brassica napus). The Journal of Agricultural Science. 126:53-63.
  18. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H. and Höfgen, R. 2003. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant Journal. 33: 633-650.
  19. Prosser, I.M., Purves, J.V., Saker, L.R. and Clarkson, D.T. 2001. Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. Journal of Experimental Botany. 52:113-121.
  20. Rennenberg, H. 1984. The fate of excess sulphur in higher plants. Annual Review of Plant Physiology. 35:121-153.
  21. Reuveny, Z., Dougall, D.K. and Trintity, P.M. 1980. Regulatory coupling of nitrate and sulphate assimilation path ways in cultured Tobacco cells. Proceedings of the National Academy of Sciences 77:6670-6672.
  22. Rouhier, N., Lemaire, S.D. and Jacquot, J.P. 2008. The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annual Review of Plant Biology. 59:143-166.
  23. Sunarpi and Anderson, J.W. 1996. Distribution and redistribution of sulphur supplied as [$^{35}S$] sulphate to roots during vegetative growth of soybean. Plant Physiology. 110:1151-1157.
  24. Sunarpi and Anderson, J.W. 1997a. Effect of nitrogen nutrition on remobilization of protein sulfur in the leaves of vegetative soybean and associated changes in soluble sulfur metabolites. Plant Physiology. 115:1671-1680.
  25. Sunarpi and Anderson, J.W. 1997b. Effect of nitrogen nutrition on the export of sulfur from leaves in soybean. Plant and Soil 188:177-187.
  26. Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. 2011. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annual Review of Plant Biology. 62: 157-184.
  27. Yamaguchi, Y., Nakamura, T., Harada, E., Koizumi, N. and Sano, H. 1999. Differential accumulation of transcripts encoding sulfur assimilation enzymes upon sulfur and/or nitrogen deprivation in Arabidopsis thaliana. Bioscience, Biotechnology, and Biochemistry. 63:762-766.
  28. Zhao, F.J., Evans, E.J., Bilsborrow, P.E. and Syers, J.K. 1993. Influence of S and N on seed yield and quality of low glucosinolate oilseed rape (Brassica nepus L.). Journal of Science of Food and Agriculture. 63:29-37.
  29. Zhao, F.J., Hawkesford, M.J. and McGrath, S.P. 1999. Sulphur assimilation and effects on yield and quality of wheat. Journal of Cereal Science. 1:1-17.