, Volume 248, Issue 2, pp 299–311 | Cite as

Sulfur starvation and restoration affect nitrate uptake and assimilation in rapeseed

  • Gurjeet Kaur
  • Ruby Chandna
  • Renu Pandey
  • Yash Pal Abrol
  • Muhammad Iqbal
  • Altaf Ahmad
Original Article


We analyzed the effect of omission of sulfur (S) from the nutrient solution and then restoration of S-source on the uptake and assimilation of nitrate in rapeseed. Incubation in nutrient solution without S for 1–6 days led to decline in uptake of nitrate, activities, and expression levels of nitrate reductase (NR) and glutamine synthetase (GS). The nitrite reductase (NiR) and glutamate synthase (GOGAT) activities were not considerably affected. There was significant enhancement in nitrate content and decline in sulfate content. Evaluation of amino acid profile under S-starvation conditions showed two- to fourfold enhancement in the contents of arginine, asparagine and O-acetyl-l-serine (OAS), whereas the contents of cysteine and methionine were reduced heavily. When the S-starved plants were subjected to restoration of S for 1, 3, 5, and 7 days, activities and expression levels of NR and GS recovered within the fifth and seventh days of restoration, respectively. Exogenous supply of metabolites (arginine, asparagine, cysteine, glutamine, OAS, and methionine) also affected the uptake and assimilation of nitrate, with a maximum for OAS. These results corroborate the tight interconnection of S-nutrition with nitrate assimilation and that OAS plays a major role in this regulation. The study must be helpful in developing a nutrient-management technology for optimization of crop productivity.


Brassica rapa L. (rapeseed) Nitrate assimilation Nitrate uptake Sulfur restoration Sulfur starvation 


  1. Abrol YP, Raghuram N, Sachdev MS (2007) Agricultural nitrogen use and its environmental implications. IK International, New DelhiGoogle Scholar
  2. Ahmad A, Abdin MZ (1999) NADH: nitrate reductase and NAD(P)H: Nitrate reductase activities in mustard seedlings. Plant Sci 143:1–8CrossRefGoogle Scholar
  3. Ahmad A, Abdin MZ (2000) Photosynthesis and its related physiological variables in the leaves of Brassica genotypes as influenced by sulphur fertilization. Physiol Plant 110:144–149CrossRefGoogle Scholar
  4. Ahmad A, Khan I, Anjum NA, Abrol YP, Iqbal M (2005) Role of sulphate transporter systems in sulphate efficiency of mustard genotypes. Plant Sci 169:842–846CrossRefGoogle Scholar
  5. Amancio S, Clarkson DT, Diogo E, Lewis M, Santos H (1997) Assimilation of nitrate and ammonium by sulphur deficient Zea mays cells. Plant Physiol Biochem 35(1):41–48Google Scholar
  6. Bates B, Kundzewicz ZW, Wu S et al (2008) Climate change and water (Technical Paper of the Intergovernmental Panel on Climate change), IPCC Secretariat. (
  7. Batista K, Monteiro FA (2007) Nitrogen and sulphur in Marandu grass: relationship between supply and concentration in leaf tissues. Sci Agric 64:44–51CrossRefGoogle Scholar
  8. Brunold C (1993) Regulatory interactions between sulfate and nitrate assimilation. In: DeKok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WH (eds) Sulphur nutrition and sulphur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 61–75Google Scholar
  9. Buchner P, Stuiver CE, Westerman S et al (2004) Regulation of sulphate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulphate nutrition. Plant Physiol 136:3396–3408PubMedCrossRefGoogle Scholar
  10. Campbell WH, Samarrelli J (1978) Purification and kinetics of higher plant NADH: nitrate reductase. Plant Physiol 61:611–616PubMedCrossRefGoogle Scholar
  11. Chesnin L, Yien CH (1950) Turbidimetric determination of available sulphates. Soil Sci Soc Amer Proc 15:149–151CrossRefGoogle Scholar
  12. Chiaiese P, Ohkama-Ohtsu N, Molvig L et al (2004) Sulphur and nitrogen influence the response of chickpea seeds to an added, transgenic sink for organic sulphur. J Exp Bot 55(404):1889–1901PubMedCrossRefGoogle Scholar
  13. Droux M, Ruffet ML, Douce R, Job D (1998) Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants. Structural and kinetic properties of the free and bound enzymes. Eur J Biochem 255:235–245PubMedCrossRefGoogle Scholar
  14. FAO (2007) Current world fertilizer trends and outlook to 2010/11. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  15. Fowler MW, Jessup W, Sarkissian GS (1974) Glutamate synthetase type activity in higher plants. FEBS Lett 46:340–342PubMedCrossRefGoogle Scholar
  16. Fujiwara T, Matoh T (2009) Plant Nutrition- roots of life for fundamental biology and better crop production. Plant Cell Physiol 50(1):2–4PubMedCrossRefGoogle Scholar
  17. Grover HL, Nair TVR, Abrol YP (1978) Nitrogen metabolism of the upper three leaf blades of wheat at different soil nitrogen levels. I: Nitrate reductase activity and content of various nitrogenous constituents. Physiol Plant 42:287–292CrossRefGoogle Scholar
  18. Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296PubMedCrossRefGoogle Scholar
  19. Gupta SC, Beevers L (1984) Synthesis and degradation of nitrite reductase in pea leaves. Plant Physiol 75:251–252PubMedCrossRefGoogle Scholar
  20. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663PubMedCrossRefGoogle Scholar
  21. Hunt J, Seymour DJ (1985) Method for measuring nitrate-nitrogen in vegetables using anion-exchange high performance liquid chromatography. Analyst 110:131–133PubMedCrossRefGoogle Scholar
  22. Ida S, Morita Y (1973) Purification and general properties of spinach leaf nitrite reductase. Plant Cell Physiol 14:661–671Google Scholar
  23. Karmoker JL, Clarkson DT, Saker LR, Rooney JM, Purves JV (1991) Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L.) roots. Planta 185:269–278CrossRefGoogle Scholar
  24. Kim H, Hirai MY, Hayashi H, Chino M, Naito S, Fujiwara T (1999) Role of O-acetyl-L-serine in the co-ordinated regulation of the expression of a soybean seed storage-protein gene by sulphur and nitrogen nutrition. Planta 209:282–289PubMedCrossRefGoogle Scholar
  25. Koralewskaa A, Buchnerb P, Stuivera CEC et al (2009) Expression and activity of sulfate transporters and APS reductase in curly kale in response to sulfate deprivation and re-supply. J Plant Physiol 166:168–179CrossRefGoogle Scholar
  26. Lencioni L, Ranieri A, Fergola S, Soldatini GF (1997) Photosynthesis and metabolic changes in leaves of rapeseed grown under long-term sulphate deprivation. J Plant Nutr 20:405–415CrossRefGoogle Scholar
  27. Less H, Galili G (2008) Principle transcriptional programmes regulating plant amino acids metabolism in response to abiotic stresses. Plant Physiol 147:316–330PubMedCrossRefGoogle Scholar
  28. Macnicol PK (1983) Differential effect of sulphur deficiency on the composition of the aminoacyl-tRNA and free amino acid pools of the developing pea seed. FEBS Lett 156:55–57CrossRefGoogle Scholar
  29. Mcgrath SP, Zhao FJ (1996) Sulphur uptake, yield responses and the interactions between nitrogen and sulphur in winter oilseed rape (Brassica napus). J Agri Sci 126:53–62CrossRefGoogle Scholar
  30. McNally SF, Hirel B, Gadal P, Mann AF, Stewart GR (1983) Glutamine synthetases of higher plants-Evidence for a specific isoform content related to their possible physiological role and their compartmentation within the leaf. Plant Physiol 72:22–25PubMedCrossRefGoogle Scholar
  31. Migge A, Bork C, Hell R, Becker TW (2000) Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulphur-deprived tobacco. Planta 211:587–595PubMedCrossRefGoogle Scholar
  32. Millard P, Sharp GS, Scott NM (1985) The effect of sulphur deficiency on the uptake and incorporation of nitrogen in ryegrass. J Agri Sci 105:501–504CrossRefGoogle Scholar
  33. Mohanty B, Fletcher JS (1980) Ammonium influence on nitrogen assimilating enzymes and protein accumulation in suspension cultures of Paul’s scarlet rose. Physiol Plant 48:453–459CrossRefGoogle Scholar
  34. NAAS (2005) Policy options for efficient nitrogen use. National Academy of Agricultural Sciences, New DelhiGoogle Scholar
  35. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650PubMedCrossRefGoogle Scholar
  36. Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318PubMedCrossRefGoogle Scholar
  37. Olivares J, Martin E, Recalde-Martinez L (1983) Effect of nitrogen and sulphur application and seed inoculation with Rhizobium leguminosarum on the yield of beans (Vicia faba) in field trials. J Agri Sci 100:149–152CrossRefGoogle Scholar
  38. Prosser IM, Purves JV, Saker LR, Clarkson DT (2001) Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J Exp Bot 52:113–121PubMedCrossRefGoogle Scholar
  39. Redinbaugh MG, Campbell WH (1993) Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root primary response to nitrate. Plant Physiol 101:l249–l1255Google Scholar
  40. Rhodes D, Rendon GA, Stewart GR (1975) The control of glutamine synthetase level in Lemna minor L. Planta 125:201–211CrossRefGoogle Scholar
  41. Richardson D, Felgate H, Watmough N, Thomson A, Baggs E (2009) Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle - could enzymic regulation hold the key? Trends in Biotech 27(7):388–397CrossRefGoogle Scholar
  42. Ruffel S, Freixes S, Balzergue S et al (2008) Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146:2020–2035PubMedCrossRefGoogle Scholar
  43. Saito K (2000) Regulation of sulphate transport and synthesis of sulphur-containing amino acids. Curr Opin Plant Biol 3:188–195PubMedGoogle Scholar
  44. Scheible WR, Morcuende R, Czechowski T et al (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499PubMedCrossRefGoogle Scholar
  45. Tallec T, Diquelou S, Fauveau C, Bataille MP, Ourry A (2008a) Effects of nitrogen and sulphur gradients on plant competition, N and S use efficiencies and species abundance in a grassland plant mixture. Plant Soil 313:267–282CrossRefGoogle Scholar
  46. Tallec T, Diquelou S, Lemauviel S, Cliquet JB, Lesuffleur F, Ourry A (2008b) Nitrogen:sulphur ratio alters competition between Trifolium repens and Lolium perenne under cutting: Production and competitive abilities. Eur J Agron 29:94–101CrossRefGoogle Scholar
  47. Thomas SG, Bilsborrow PE, Hocking TJ, Bennett J (2000) Effect of sulphur deficiency on the growth and metabolism of sugar beet (Beta vulgaris cv Druid). J Sci Food Agric 80:2057–2062CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Gurjeet Kaur
    • 1
  • Ruby Chandna
    • 1
  • Renu Pandey
    • 2
  • Yash Pal Abrol
    • 1
  • Muhammad Iqbal
    • 1
  • Altaf Ahmad
    • 1
  1. 1.Molecular Ecology Laboratory, Department of Botany, Faculty of ScienceHamdard UniversityNew DelhiIndia
  2. 2.Division of Plant PhysiologyIndian Agricultural Research InstituteNew DelhiIndia

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