Biologia Plantarum

, Volume 58, Issue 4, pp 733–742 | Cite as

Evaluation of amino acid profile in contrasting arsenic accumulating rice genotypes under arsenic stress

  • A. Kumar
  • S. Dwivedi
  • R. P. Singh
  • D. Chakrabarty
  • S. Mallick
  • P. K. Trivedi
  • B. Adhikari
  • R. D. Tripathi
Original Papers


Amino acids (AAs) play significant roles in metal binding, antioxidant defense, and signaling in plants during heavy metal stress. In the present study, the essential amino acids (EAAs), non-essential amino acids (NEAAs), as well as the enzymes of proline and cysteine biosynthetic pathways were studied in contrasting arsenic accumulating rice genotypes grown in hydroponic solutions with addition of arsenate (AsV) or arsenite (AsIII). Under a mild As stress, the total AAs content significantly increased in both the rice genotypes with a greater increase in a low As accumulating rice genotype (LAARG; IET-19226) than in a high As accumulating rice genotype (HAARG; BRG-12). At the equimolar concentration (10 μM), AsIII had a greater effect on EAAs than AsV. Conversely, AsV was more effective in inducing a proline accumulation than AsIII. Among NEAAs, As significantly induced the accumulation of histidine, aspartic acid, and serine. In contrast, a higher As concentration (50 μM) reduced the content of most AAs, the effect being more prominent during AsIII exposure. The inhibition of glutamate kinase activity was noticed in HAARG, conversely, serine acetyltransferase and cysteine synthase activities were increased which was positively correlated with the cysteine synthesis.

Additional key words

arsenate arsenite cysteine synthase glutamate kinase Oryza sativa proline serine acetyltransferase 



amino acid






aspartic acid


branched chain amino acids


cysteine synthase




essential amino acids


glutamate kinase


glutamic acid




high As accumulating rice genotype






low As accumulating rice genotype








non essential amino acids






recommended daily intake


serine acetyl transferase










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Supplementary material

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  1. Adams, E., Frank, L.: Metabolism of proline and the hydroxyprolines. — Annu. Rev. Biochem. 49: 1005–1061, 1980.PubMedCrossRefGoogle Scholar
  2. Ahsan, N., Lee, D.G., Alam, I., Kim, P J., Lee, J.J., Ahn, Y.O., Kwak, S.S., Lee, I.J., Bahk, J.D., Kang, K.Y., Renaut, J., Komatsu, S., Lee, B.H.: Comparative proteomic study of arsenic-induced differentially expressed proteins in rice roots reveals glutathione plays a central role during As stress. — Proteomics 8: 3561–3576, 2008.PubMedCrossRefGoogle Scholar
  3. Bidlingmeyer, B.A., Cohe, S.A., Tarvin, T.L.: Rapid analysis of amino acids using pre column derivatization. — J. Chromatogr. 336: 93–104, 1984.PubMedCrossRefGoogle Scholar
  4. Bradford, M.M.: A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254, 1976.PubMedCrossRefGoogle Scholar
  5. Chakrabarty, D., Trivedi, P.K., Misra, P., Tiwari, P., Shri, M., Shukla, D., Kumar, S., Rai, A., Pandey, A., Nigam, D., Tripathi, R.D., Tuli, R.: Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. — Chemosphere 74: 688–702, 2009.PubMedCrossRefGoogle Scholar
  6. Dave, R., Singh, P.K., Tripathi, P., Shri, M., Dixit, G., Dwivedi, S., Chakrabarty, D., Trivedi, P.K., Sharma, Y.K., Dhankher, O.P., Corpas, F.J., Barroso, J.B., Tripathi, R.D.: Arsenite tolerance is related to proportional thiolic metabolite synthesis in rice (Oryza sativa L.). — Arch. Environ. Contam. Toxicol. 64: 235–242, 2013.PubMedCrossRefGoogle Scholar
  7. Davies, K.J., Delsignore, M.E., Lin, S.W.: Protein damage and degradation by oxygen radicals II Modification of amino acids. — J. biol.Chem. 262: 9902–9907, 1987.PubMedGoogle Scholar
  8. Duan, M., Sun, S.S.M.: Profiling the expression of genes controlling rice grain quality. — Plant mol. Biol. 59: 165–178, 2005.PubMedCrossRefGoogle Scholar
  9. Dwivedi, S., Mishra, A., Tripathi, P., Dave, R., Kumar, A., Srivastava, S., Chakrabarty, D., Trivedi, P.K., Adhikari, B., Norton, G.J., Nautiyal, C.S., Tripathi, R.D.: Arsenic affects essential and non-essential amino acids differentially in rice grains: inadequacy of amino acids in rice based diet. — Environ. Int. 46: 16–22, 2012.PubMedCrossRefGoogle Scholar
  10. Dwivedi, S., Tripathi, R.D., Srivastava, S., Singh, R., Kumar, A., Tripathi, P., Dave, R., Rai, U.N., Chakrabarty, D., Trivedi, P.K., Tuli, R., Adhikari, B., Bag, M.K.: Arsenic affects mineral nutrients in grains of various Indian rice (Oryza sativa L.) genotypes grown under arseniccontaminated soils of West Bengal. — Protoplasma 245: 113–124, 2010a.PubMedCrossRefGoogle Scholar
  11. Dwivedi, S., Tripathi, R.D., Tripathi, P., Kumar. A., Dave, R., Mishra, S., Singh, R., Sharma, D., Rai, U.N., Chakrabarty, D., Trivedi, P.K., Adhikari, B., Bag, M.K., Dhankher, O. P., Tuli, R.: Arsenate exposure affects amino acids, mineral nutrient status and antioxidant in rice (Oryza sativa L.) genotypes. — Environ. Sci. Technol. 44: 9542–9549, 2010b.PubMedCrossRefGoogle Scholar
  12. Galili, G.: New insights into the regulation and functional significance of lysine metabolism in plants. — Annu. Rev. Plant Biol. 7: 153–156, 2002.Google Scholar
  13. Galili, G., Amir, R., Hoefgen, R., Hesse, H.: Improving the levels of essential amino acids and sulfur metabolites in plants. — Biol. Chem. 386: 817–831, 2005.PubMedCrossRefGoogle Scholar
  14. Hayzer, D.J., Leisinger, T.H.: The gene-enzyme relationships of proline biosynthesis in Escherichia coli. — J. gen. Microbiol. 11: 287–293, 1980.Google Scholar
  15. Herrera-Rodríguez, M.B., Pérez-Vicente, R., Maldonado, J.-M.: Expression of asparagine synthetase genes in sunflower (Helianthus annuus) under various environmental stresses. — Plant Physiol. Biochem. 45: 33–38, 2007.PubMedCrossRefGoogle Scholar
  16. Jaleel, C.A., Manivannan, P., Sankar, B., Kishorekumar, A., Panneerselvam, R.: Calcium chloride effects on salinityinduced oxidative stress, proline metabolism and indole alkaloid accumulation in Catharanthus roseus. — Compt. rend. Biol. 330: 674–683, 2007.CrossRefGoogle Scholar
  17. Kerkeb, L., Krämer, U.: The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. — Plant Physiol. 131: 716–724, 2003.PubMedCrossRefPubMedCentralGoogle Scholar
  18. Kishor, P.B.K., Sangam, S., Amrutha, R.N., Laxmi, P.S., Naidu, K.R., Rao, K.R.S.S., Sreenath, R., Reddy, K.J., Theriappan, T., Sreenivasulu, N.: Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. — Curr. Sci. 88: 424–438, 2005.Google Scholar
  19. Liu, W.J., Zhu, Y.G., Smith, F.A., Smith, S.E.: Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture? — Plant Physiol. 162: 481–488, 2004.Google Scholar
  20. Ma, J.F., Yamaji, N., Mitani, N., Xu, X.Y., Su, Y.H., McGrath, S.P., Zhao, F.J.: Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. — Proc. nat. Acad. Sci., USA 105: 9931–9935, 2008.CrossRefGoogle Scholar
  21. Maeda, H., Yoo, H., Dudareva, N.: Prephenate aminotransferase directs plant phenylalanine biosynthesis via arogenate. — Natur. Chem. Biol. 7: 19–21, 2011.CrossRefGoogle Scholar
  22. Miflin, B.J., Lea, P. (ed.): Biochemistry of Plants: a Comprehensive Treatise. — Academic Press, San Diego 1990.Google Scholar
  23. Mishra, S., Dubey, R.S.: Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. — J. Plant Physiol. 163: 927–936, 2006.PubMedCrossRefGoogle Scholar
  24. Mishra. S., Wellenreuther, G., Mattusch, J., Stärk, H.J., Küpper, H.: speciation and distribution of arsenic in the nonhyperaccumulator macrophyte Ceratophyllum demersum. — Plant Physiol. 163: 1396–408, 2013.PubMedCrossRefGoogle Scholar
  25. Naujokas, M.F., Anderson, B., Ahsan, H., Aposhian, H.V., Graziano, J.H., Thompson, C., Suk, W.A.: The broad scope of health effects from chronic arsenic exposure: update on a worldwide public health problem. — Environ. Health Perspect. 121: 295–302, 2013.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Nayyar, H., Walia, D.P.: Water stress-induced Pro accumulation in contrasting wheat genotypes as affected by calcium and abscisic acid. — Biol. Plant 46: 275–279, 2003.CrossRefGoogle Scholar
  27. Norton, G.J., Adomako, E.E., Deacon, C.M., Carey, A.M., Price, A.H., Meharg, A.A.: Effect of organic matter amendment, arsenic amendment and water management regime on rice grain arsenic species. — Environ. Pollut. 177: 38–47, 2013.PubMedCrossRefGoogle Scholar
  28. Norton, G.J., Duan, G.L., Dasgupta, T., Islam, M.R., Lei, M., Zhu, Y., Deacon, C.M., Moran, A.C., Islam, R., Zhao, F.-J., Stroud, J.L., Mcgrath, S.P., Feldmann, J., Price, A.H., Meharg, A.A.: Environmental and genetic control of arsenic accumulation and speciation in rice grain: comparing a range of common cultivars grown in contaminated sites across Bangladesh, China, and India. — Environ. Sci. Technol. 43: 8381–8386, 2009.PubMedCrossRefGoogle Scholar
  29. Paleg, L.G., Douglas, T.J., Daal, A.V., Keech, D.B.: Proline and betaine protect enzymes against heat inactivation. — Aust. J. Plant Physiol. 8: 107–114, 1981.Google Scholar
  30. Pavlík, M., Pavlíková, D., Staszková, L., Neuberg, M., Kaliszová, R., Száková, J., Tlustoš, P.: The effect of arsenic contamination on amino acids metabolism in Spinacia oleracea L. — Ecotox. Environ. Safety 73: 1309–1313, 2010.CrossRefGoogle Scholar
  31. Rai, V.K.: Role of amino acids in plant responses to stresses. — Biol. Plant. 45: 481–487, 2002.CrossRefGoogle Scholar
  32. Sharma, S.S., Dietz, K.J.: The significance of amino acids and amino acid derived molecules in plant responses and adaptation to heavy metal stress. — J. exp. Bot. 57: 711–726, 2006.PubMedCrossRefGoogle Scholar
  33. Simon-Sarkadi, L., Kocsy, G., Várhegyi, Á., Galiba, G., De Ronde, J.A.: Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. — Biol. Plant 50: 793–796, 2006.CrossRefGoogle Scholar
  34. Srivastava, S., Mishra, S., Tripathi, R.D., Dwivedi, S., Trivedi, P.K., Tandon, P.K.: Phytochelatins and antioxidants systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (L.f.) Royle. — Environ. Sci. Technol. 41: 2930–2936, 2007.PubMedCrossRefGoogle Scholar
  35. Srivastava, S., Srivastava, A., Suprasanna, P., D’souza, S.F.: Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. — J. exp. Bot. 60: 3419–3431, 2009.PubMedCrossRefGoogle Scholar
  36. Tripathi, P., Mishra, A., Dwivedi, S., Chakrabarty, D., Singh, R.P., Tripathi, R.D., Trivedi, P.K.: Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. — Ecotox. Environ. Safety 79: 189–98, 2012a.CrossRefGoogle Scholar
  37. Tripathi, P., Tripathi, R.D., Singh, R.P., Dwivedi, S., Chakrabarty, D., Trivedi, P.K., Adhikari, B.: Arsenite tolerance in rice (Oryza sativa L.) involves coordinated role of metabolic pathways of thiols and amino acids. — Environ. Sci. Pollut. Res. 20: 884–896, 2012b.CrossRefGoogle Scholar
  38. Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K., Mathuis, F.J.M.: Arsenic hazards; strategies for tolerance and remediation by plants. — Trends Biotechnol. 25: 158–165, 2007.PubMedCrossRefGoogle Scholar
  39. Vašáková, L., Štefl, M.: Glutamate kinases from winter wheat leaves and some properties of proline-inhibitable glutamate kinase. — Collect. Czech. Chem. Commun. 47: 349–359, 1982.CrossRefGoogle Scholar
  40. Williams, P.N., Villada, A., Deacon, C., Raab, A., Figuerola, J., Green, A.J., Feldmann, J., Meharg, A.A.: Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. — Environ. Sci. Technol. 41: 6854–6859, 2007.PubMedCrossRefGoogle Scholar
  41. Wirtz, M., Berkowitz, O., Droux, M., Hell, R.: The cysteine synthase complex from plants. Mitochondrial serine acetyltransferase from Arabidopsis thaliana carries a bifunctional domain for catalysis and protein-protein interaction. — Eur. J. Biochem. 268: 686–693, 2001.PubMedCrossRefGoogle Scholar
  42. Zagorchev, L., Seal, C.E., Kranner, I., Odjakova, M.: A central role for thiols in plant tolerance to abiotic stress. — Int. J. mol. Sci. 14: 7405–7432, 2013.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Zhao, F.J., Ago, Y., Mitani, N., Li, R.Y., Su, Y.H., Yamaji, N., McGrath, S.P., Ma, J.F.: The role of the rice aquaporin Lsi1 in arsenite efflux from roots. — New Phytol. 186: 392–399, 2010.PubMedCrossRefGoogle Scholar
  44. Zheng, M.Z., Cai, C., Hu, Y., Sun, G.X., Williams, P.N., Cui, H.J., Li, G., Zhao, F.J., Zhu, Y.G.: Spatial distribution of arsenic and temporal variation of its concentration in rice. — New Phytol. 189: 200–209, 2011.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • A. Kumar
    • 1
    • 2
  • S. Dwivedi
    • 1
  • R. P. Singh
    • 2
  • D. Chakrabarty
    • 1
  • S. Mallick
    • 1
  • P. K. Trivedi
    • 1
  • B. Adhikari
    • 3
  • R. D. Tripathi
    • 1
  1. 1.CSIR-National Botanical Research InstituteLucknowIndia
  2. 2.Department of Environmental ScienceB.B.A. UniversityLucknowIndia
  3. 3.Rice Research Station, Department of AgricultureGovernment of West BengalChinsurahIndia

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