Abstract
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.
Similar content being viewed by others
Abbreviations
- AA:
-
amino acid
- Ala:
-
alanine
- Arg:
-
arginine
- Asp:
-
aspartic acid
- BCAAs:
-
branched chain amino acids
- CS:
-
cysteine synthase
- Cys:
-
cysteine
- EEAs:
-
essential amino acids
- GK:
-
glutamate kinase
- Glu:
-
glutamic acid
- Gly:
-
glycine
- HAARG:
-
high As accumulating rice genotype
- His:
-
histidine
- Ile:
-
isoleucine
- LAARG:
-
low As accumulating rice genotype
- Leu:
-
leucine
- Lys:
-
lysine
- Met:
-
methionine
- NEEAs:
-
non essential amino acids
- Phe:
-
phenylalanine
- Pro:
-
proline
- RDI:
-
recommended daily intake
- SAT:
-
serine acetyl transferase
- Ser:
-
serine
- Thr:
-
threonine
- Tyr:
-
tyrosine
- Val:
-
valine
References
Adams, E., Frank, L.: Metabolism of proline and the hydroxyprolines. — Annu. Rev. Biochem. 49: 1005–1061, 1980.
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.
Bidlingmeyer, B.A., Cohe, S.A., Tarvin, T.L.: Rapid analysis of amino acids using pre column derivatization. — J. Chromatogr. 336: 93–104, 1984.
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.
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.
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.
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.
Duan, M., Sun, S.S.M.: Profiling the expression of genes controlling rice grain quality. — Plant mol. Biol. 59: 165–178, 2005.
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.
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.
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.
Galili, G.: New insights into the regulation and functional significance of lysine metabolism in plants. — Annu. Rev. Plant Biol. 7: 153–156, 2002.
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.
Hayzer, D.J., Leisinger, T.H.: The gene-enzyme relationships of proline biosynthesis in Escherichia coli. — J. gen. Microbiol. 11: 287–293, 1980.
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.
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.
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.
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.
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.
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.
Maeda, H., Yoo, H., Dudareva, N.: Prephenate aminotransferase directs plant phenylalanine biosynthesis via arogenate. — Natur. Chem. Biol. 7: 19–21, 2011.
Miflin, B.J., Lea, P. (ed.): Biochemistry of Plants: a Comprehensive Treatise. — Academic Press, San Diego 1990.
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.
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.
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.
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.
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.
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.
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.
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.
Rai, V.K.: Role of amino acids in plant responses to stresses. — Biol. Plant. 45: 481–487, 2002.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: The authors are thankful to the Director of the National Botanical Research Institute, CSIR, Lucknow for the facilities and for the financial support from the CSIR-network projects (INDEPTH). A. Kumar is thankful to the Council of Scientific and Industrial Research, New Delhi, India for the award of Senior Research Fellowship. The authors are thankful to Dr. S. Mishra, the Department of Biology, the University of Kontanz, Germany, for the linguistic improvement of the MS.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Kumar, A., Dwivedi, S., Singh, R.P. et al. Evaluation of amino acid profile in contrasting arsenic accumulating rice genotypes under arsenic stress. Biol Plant 58, 733–742 (2014). https://doi.org/10.1007/s10535-014-0435-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-014-0435-4