Plant Growth Regulation

, Volume 64, Issue 3, pp 251–261 | Cite as

Nickel and Al-excess inhibit nitrate reductase but upregulate activities of aminating glutamate dehydrogenase and aminotransferases in growing rice seedlings

Original paper


The present study was undertaken to examine the influence of toxic levels of Ni and Al, on the activities of key nitrogen assimilatory enzymes in roots and shoots of growing rice seedlings. When seedlings of two inbred rice (Oryza sativa L.) cvs. Malviya-36 and Pant-12, sensitive to both Ni and Al, were raised in sand cultures containing 200 and 400 μM NiSO4 or 80 and 160 μM Al2(SO4)3, a marked inhibition in the activities of NO3 assimilatory enzymes NR and GS was observed in roots as well as shoots during a 5–20 day growth period. Both Ni and Al treatments, in growth medium, stimulated the activity of aminating glutamate dehydrogenase (NADH-GDH) whereas the activity of deaminating GDH (NAD+-GDH) decreased under metal toxicities. The activities of the aminotransferases studied; alanine aminotransferase (AlaAT) and aspartate amino transferase (AspAT) increased due to Ni and Al treatments. Results suggest that both Ni and Al treatments impair N assimilation in rice seedlings by inhibiting the activities of NR and GS and that GDH appears to play a role in assimilation of NH4 + in metal stress conditions. Further, higher activity of aminotransferases in metal stressed seedlings might be helpful in meeting higher demand of amino acids under stressed conditions.


Nickel Aluminum Toxicity Nitrogen assimilation Oryza sativa L. 



PM is grateful to the Council of Scientific and Industrial Research (CSIR), New Delhi, for providing a Junior Research Fellowship.


  1. Astolfi S, Zuchi S, Passera C (2004) Role of sulphur availability on cadmium—induced changes of nitrogen and sulphur metabolism in maize (Zea mays L.) leaves. J Plant Physiol 161:795–802CrossRefPubMedGoogle Scholar
  2. Balestrasee KB, Gallego SM, Tomaro ML (2006a) Aluminium stress affects nitrogen fixation and assimilation in soybean (Glycine max L.). Plant Growth Regul 48:271–281Google Scholar
  3. Balestrasee KB, Gallego SM, Tomaro ML (2006b) Oxidation of the enzymes involved in nitrogen assimilation plays an important role in the cadmium induced toxicity in soybean plants. Plant Soil 284:187–194CrossRefGoogle Scholar
  4. Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64CrossRefGoogle Scholar
  5. Bernard SM, Habash Z (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620CrossRefPubMedGoogle Scholar
  6. Boyer PD, Mills RC, Fromm HJ (1959) Hypotheses for and some kinetic studies with glutamine synthetase and acetate thiokinase. Arch Biochem Biophys 81:249–263CrossRefPubMedGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  8. Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amimo acid storage strategy. Plant Cell Physiol 45:1681–1693CrossRefPubMedGoogle Scholar
  9. Chien H-F, Kao CH (2000) Accumulation of ammonium in rice leaves in response to excess cadmium. Plant Sci 156:111–115CrossRefPubMedGoogle Scholar
  10. de Sousa CAF, Sodek L (2003) Alanine metabolism and alanine aminotransferase activity in soyabean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environ Exp Bot 50:1–8CrossRefGoogle Scholar
  11. Dobermann A, Fairhurst T (2000) Rice: nutrient disorders and nutrient management. Potash and Phosphate Institute of Canada (PPIC) and International Rice Research Institute (IRRI), Philippines, pp 135–138Google Scholar
  12. Dubey RS, Pessarakli M (2002) Physiological mechanisms of nitrogen absorption and assimilating in plants under stressful conditions. In: Pessarakli M (ed) Handbook of crop physiology. Marcel Dekker, New York, pp 637–655Google Scholar
  13. Ferrario S, Valadier MH, Morat-Gaudry J-F, Foyer CH (1995) Effects of constitutive expression of nitrate reductase in transgenic Nicotiana plumbaginifolia L. in response to varying nitrogen supply. Planta 196:288–294CrossRefGoogle Scholar
  14. Fontaine JX, Saladino F, Agrimonti C, Bedu M, Terce-Laforgue T, Tetu T, Hirel B, Restivo FM, Dubois F (2006) Control of the synthesis and subcellular targeting of the two GDH genes products in leaves and stems of Nicotiana plumbaginifolia and Arabidopsis thaliana. Plant Cell Physiol 47:410–418CrossRefPubMedGoogle Scholar
  15. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358CrossRefPubMedGoogle Scholar
  16. Gajewska E, Sklodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–339CrossRefGoogle Scholar
  17. Gajewska E, Wielanek M, Bergier K, Sklodowska M (2009) Nickel- induced depression of nitrogen assimilation in wheat roots. Acta Physiol Plant 31:1291–1300CrossRefGoogle Scholar
  18. Hageman RH, Flesher D (1960) Nitrate reductase activity in corn seedlings as affected by light and nitrate content of nutrient media. Physiol Plant 35:700–708CrossRefGoogle Scholar
  19. Hassan MJ, Zhang G, Zhu Z (2008) Influence of cadmium toxicity on plant growth and nitrogen uptake in rice as affected by nitrogen form. J Plant Nutr 31:251–262CrossRefGoogle Scholar
  20. Jha AB, Dubey RS (2004) Arsenic exposure alters the activities of key nitrogen assimilatory enzymes in growing rice seedlings. Plant Growth Regul 43:259–268CrossRefGoogle Scholar
  21. Kevresan S, Petrovic N, Popovic M, Kandrac J (2001) Nitrogen and protein metabolism in young pea plants as affected by different concentrations of nickel, cadmium, lead, and molybdenum. J Plant Nutr 24:1633–1644CrossRefGoogle Scholar
  22. Kumar RG, Dubey RS (1999) Glutamine synthetase isoforms from rice seedlings: effects of stress on enzyme activity and the protective roles of osmolytes. J Plant Physiol 155:118–121Google Scholar
  23. Lam HM, Koschigano K, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Ann Rev Plant Physiol Plant Mol Biol 47:569–593CrossRefGoogle Scholar
  24. Lejay L, Quillere I, Roux Y, Tillard P, Cliquet JB, Meyer C, Morot Gaudry JF, Gojon A (1997) Abolition of post transcriptional regulation of nitrate reductase partially prevents, the decrease in leaf NO3 reduction when photosynthesis is inhibited by CO2 deprivation, but not in darkness. Plant Physiol 115:623–630PubMedGoogle Scholar
  25. Loulakakis KA, Roubelakis-Angelakis KA (1992) Ammonium-induced increase in NADH-glutamate dehydrogenase activity is caused by de novo synthesis of the α-subunit. Planta 187:322–327CrossRefGoogle Scholar
  26. Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49CrossRefGoogle Scholar
  27. Malik CP, Singh MB (1980) Plant enzymology and histoenzymology, text manual. Kalyani Publishers, New DelhiGoogle Scholar
  28. Matraszek R (2008) Nitrate reductase activity of two leafy vegetables as affected by nickel and different nitrogen forms. Acta Physiol Plant 30:361–370CrossRefGoogle Scholar
  29. Miyashita Y, Good AG (2008) Glutamate deamination by glutamate dehydrogenase plays a central role in amino acid catabolism in plants. Plant Signal Behav 3:842–843CrossRefPubMedGoogle Scholar
  30. Rana NK, Mohanpuria P, Yadav SK (2008) Expression of tea cytosolic glutamine synthetase is tissue specific and induced by cadmium and salt stress. Biol Plant 52:361–364CrossRefGoogle Scholar
  31. Restivo FM (2004) Molecular cloning of glutamate dehydrogenase genes of Nicotiana plumaginifolia: structure and regulation of their expression by physiological and stress conditions. Plant Sci 166:971–982CrossRefGoogle Scholar
  32. Roitto M, Rautio P, Julkunen-Tiito R, Kukkola E, Huttunen S (2005) Changes in the concentrations of phenolics and photosynthates in scots pine (Pinus sylvestris L.) seedlings exposed to nickel and copper. Environ Pollut 137:603–609CrossRefPubMedGoogle Scholar
  33. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277CrossRefGoogle Scholar
  34. Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864CrossRefPubMedGoogle Scholar
  35. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038CrossRefPubMedGoogle Scholar
  36. Sharma P, Dubey RS (2010) Metal toxicity in plants: uptake of metals, metabolic alterations and tolerance mechanisms. In: Hemantaranjan A (ed) Advances in plant physiology, vol 11. Scientific Publishers, Jodhpur, pp 53–106Google Scholar
  37. Sharma RK, Agrawal M, Marshall F (2007) Heavy metal contamination of soil and vegetables in suburban areas of Varanasi, India. Ecotox Environ Saf 66:258–266CrossRefGoogle Scholar
  38. Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781CrossRefPubMedGoogle Scholar
  39. Sukalovic VHT (1990) Properties of glutamate dehydrogenase from developing maize endosperm. Physiol Plant 80:238–242CrossRefGoogle Scholar
  40. Vajpayee P, Tripathi RD, Rai UN, Ali MB, Singh SN (2000) Chromium (VI) accumulation reduces chlorophyll biosynthesis, nitrate reductase activity and protein content in Nymphaea alba L. Chemosphere 41:1075–1082CrossRefPubMedGoogle Scholar
  41. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Biochemistry, Faculty of ScienceBanaras Hindu UniversityVaranasiIndia

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