Abstract
Two wheat genotypes were grown in hydroponic culture, containing 4 mM KNO3, NH4Cl and NH4NO3. Activities of N metabolizing enzymes, aminotransferases, carbohydrate and TCA cycle enzymes were analyzed along with protein, amino acid, N, sugar content and growth parameters in shoot and root. After 12 days, the size of shoot and root system decreased significantly when plants were supplied with NH4Cl as exclusive N source. Under NH4NO3 growth parameters, N and carbon metabolism were elevated as compared to NH4Cl but less than KNO3 source indicating inhibition of NH4+ toxicity by NO3− uptake. Our results suggested that GDH, aminotransferases and PEPC play an important role in ammonium detoxification by its incorporation into amino acids. Thus, the morphologic differences among plants growing in NH4+ or NO3− nutrition confirm the hypothesis that N source determines the growth habit of plant in wheat by modulating the endogenous levels of protein and sugar content.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- 2-OG:
-
2-oxoglutarate
- GDH:
-
glutamate dehydrogenase
- GOGAT:
-
glutamate synthase
- GOT:
-
glutamate oxaloacetate transaminase
- GPT:
-
glutamate pyruvate transaminase
- GS:
-
glutamine synthetase
- ICDH:
-
isocitrate dehydrogenase
- MDH:
-
malate dehydrogenase
- NR:
-
nitrate reductase
- PEPC:
-
phosphoenolpyruvate carboxylase
References
Anjana, S.U., Iqbal, M., Abrol, Y.P. 2007. Are nitrate concentrations in leafy vegetables within safe limits? Current Sci. 92:355–360.
Anjana, S.U., Abrol, Y.P., Iqbal, M. 2011. Modulation of nitrogen utilization efficiency in wheat genotypes differing in nitrate reductase activity. J. Plant Nutr. 34:920–933.
Asthir, B., Bhatia, S. 2014. In vivo studies on artificial induction of thermotolerance to detached panicles of wheat (Triticum aestivum L.) cultivars under heat stress. J. Food Sci. and Technol. 51:118–123.
Bai, C.H., Liang, Y.L., Hawkesford, M.J. 2013. Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat. J. Exp. Bot. 64:1745–1753.
Balotf, S., Niazi, A., Kavoosi, G., Ramezani, A. 2012. Differential expression of nitrate reductase in response to potassium and sodium nitrate: realtime PCR analysis. Austr. J. Crop Sci. 6:130–134.
Below, F.E., Cazetta, J.O., Seebauer, J.R. 2000. Carbon/nitrogen interactions during ear and kernel development of maize, In: Westgate, M., Boote, K. (eds), Physiology and Modelling Kernel set in Maize. CSA Special Publication no. 29. CSSA-ASA. Madison, WI, USA. pp. 15–24.
Bijlsma, R.J., Lambers, H., Kooijman, S.A.L.M. 2000. A dynamic whole plant model of integrated metabolism of nitrogen and carbon. 1. Comparative ecological implications of ammonium-nitrate interactions. Plant Soil 220:49–69.
Britto, D.T., Kronzucker, H.J. 2002. Review NH4+ toxicity in higher plants: a critical review. J. Plant Physiol. 159:567–584.
Bulen, W.A. 1956. The isolation and characterization of glutamate dehydrogenase from corm leaves. Archives of Biochemistry and Biophysics 62:178–183.
Christeller, J.T., Laing, W.A., Sutton, W.D. 1977. Carbon dioxide fixation by lupin root nodules. I. Characterization, association with phosphoenolpyruvate carboxylase, and correlation with nitrogen fixation during nodule development. Plant Physiol. 60:47–50.
Cossey, D.A., Thomason, W.E., Mullen, R.W., Wynn, K.J., Woolfolk, C.W., Johnson, G.V., Raun, W.R. 2002. Relationship between ammonium and nitrate in wheat plant tissue and estimated nitrogen loss. J. Plant Nutrition 25:1429–1442.
Cruz, C., Bio, A.F.M., Dominguez-Valdivia, M.D., Aparicio-Tejo, P.M., Lamsfus, C., Martins-Loucao, M.A. 2006. How does glutamine synthetase activity determine plant tolerance to ammonium? Planta 223:1068–1080.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350–356.
Fathi, G. 2008. Effect of genotype variability on nitrate uptake and assimilation of wheat cultivars. J. of Agric. Sci. and Technol. 10:11–22.
Gietl, C. 1992. MDH isoenzymes: Cellular localization and role in the flow of metabolites between the cytoplasm and cell organelles. Biochimica et Biophysica Acta 1100:217–234.
Hawkesford, M.J. 2014. Reducing the reliance on nitrogen fertilizer for wheat production. J. Cereal Sci. 59:276–283.
Hoagland, D.R., Arnon, D.I. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station Publication 347:1–32.
Hodges, M. 2002. Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53:905–916.
Huppe, H., Turpin. D.H. 1994. Integration of carbon and nitrogen metabolism in plant and alga cells. Annu. Rev. Plant Physiol. and Plant Mol. Biol. 45:577–607.
Ikram, S., Bedu, M., Daniel-Vedele, F., Chaillou, S., Chardon, F. 2012. Natural variation of Arabidopsis response to nitrogen availability. J. Exp. Bot. 63:91–105.
Jain, V., Khetarpal, S., Das, R., Abrol, Y.P. 2011. Nitrate assimilation in contrasting wheat genotypes. Physiol. and Mol. Biol. of Plants 17:137–144.
Jaworski, E.G. 1971. Nitrate reductase in intact plant tissue. Biochem. and Biophysic. Res. Commun. 43:1274–1279.
Jiang, D., Cao, W.X., Dai, T.B., Jing, Q. 2003. Activities of key enzymes for starch synthesis in relation to growth of superior and inferior grains on winter wheat (Triticum aestivum L.) spike. Plant Growth Regul. 41:247–257.
Kanamori, T., Matsumoto, H. 1974. Asparagine synthesis by Oryza sativa seedlings. Phytochem. 13:1407–1412.
Lancien, M., Gadal, P., Hodges, M. 2000. Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiol. 123:817–824.
Lancien, M., Martin, M., Hsieh, M-H., Leustek, T., Goodman, H., Coruzzi, G.M. 2002. Arabidopsis glt1-T mutant defines a role for NADH-GOGAT in the non-photorespiratory ammonium assimilatory pathway. The Plant J. 29:347–358.
Lasa, B., Frechilla, S., Aparicio-Tejo, P.M., Lamsfus, C. 2002. Role of glutamate dehydrogenase and phosphoenolpyruvate carboxylase activity in ammonium nutrition tolerance in roots. Plant Physiol. and Biochem. 40:969–976.
Lea, D.J., Robinson, S.A., Steward, G.R. 1990. The enzymology and metabolism of glutamine, glutamate and asparagines. In: Miflin, B.J., Lea, P.J. (eds), The Biochemistry of Plants, Vol. 16. Academics Press. New York, USA. pp. 121–159.
Lee, Y.P., Takahashi, T. 1966. An improved colorimetric determination of amino acid with the use of ninhydrin. Anal. Biochem. 14:71–77.
Lewis, O.A.M., Fulton, B., von Zelewski, A.A.A. 1987. The differential distribution of carbon in response to nitrate, ammonium and nitrate-ammonium nutrition in wheat. In: Ullrich, W.R., Aparcio, P.J., Syrett, P.J., Castillo, F. (eds), Inorganic Nitrogen Metabolism. Springer Verlag. Berlin, Germany. pp. 240–246.
Lin, C.C., Kao, C.H. 2001. Regulation of ammonium-induced proline accumulation in detached rice leaves. Plant Growth Regul. 35:69–74.
Lowry, O.H., Rosenbrough, N.J., Farr, A.L., Randall, R.J. 1951. Protein measurement with folin phenol reagent. J. Biol. Chem. 193:265–275.
Luo, J., Sun, S., Jia, L., Chen, W., Shen, Q. 2006. The mechanism of nitrate accumulation in pakchoi [Brassica campestris L. ssp. Chinensis (L.)]. Plant Soil 282:291–300.
Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., Suzuki, A. 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105:1141–1157.
Masclaux-Daubresse, C., Reisdorf-Cren, M., Pageau, K., Lelandais, M.A., Grandjean, O., Kronenberger, J., Valadier, M.-H., Feraud, M., Jouglet, T., Suzuki, A. 2006. Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol. 140:444–456.
McKenzie, H.A., Wallace, H.S. 1954. The Kjeldahl determination of nitrogen. Austr. J. Chem. 17:55–59.
Miflin, B.J., Lea, P.J. 1976. The pathway of nitrogen assimilation in plants. Phytochem. 15:873–885.
Miyao, M., Fukayama, H. 2003. Metabolic consequences of overproduction of phosphoenolpyruvate carboxylase in C3 plants. Archives of Biochemistry and Biophysics 414:197–203.
Mohanty, B., Fletcher, J.S. 1980. Ammonium influence on nitrogen assimilatory enzymes and protein accumulation in suspension cultures of pearl scarlet rose. Physiologia Plantarum 48:453–459.
Morell, M., Copeland, L. 1985. Sucrose synthase of soybean nodules. Plant Physiol. 78:149–154.
Morozkina, E.V., Zvyagilskaya, R.A. 2007. Nitrate reductases: Structure, functions and effect of stress factors. Biochem. 72:1151–1160.
Nasholm, T., Kielland, K., Ganeteg, U. 2009. Uptake of organic nitrogen by plants. New Phytologist 182:31–48.
Nunes-Nesi, A., Fernie, A.R., Stitt, M. 2010. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol. Plant 3:973–996.
Osuji, G.O., Brown, T.K., South, S.M. 2009. Nucleotide-dependent reprogramming of mRNAs encoding acetyl coenzyme A carboxylase and lipoxygenase in relation to the fat contents of peanut. J. Bot. 10:1–8.
Pasqualini, S., Ederli, L., Piccioni, C., Batini, P., Bellucci, M., Arcioni, S., Antonielli, M. 2001. Metabolic regulation and gene expression of root phosphoenolpyruvate carboxylase by different nitrogen sources. Plant Cell Environ. 24:439–447.
Patterson, K., Cakmak, T., Cooper, A., Lager, I., Rasmusson, A.G., Escobar, M.A. 2010. Distinct signaling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ. 33:1486–1501.
Raab, T.K., Terry, N. 1994. Nitrogen source regulation of growth and photosynthesis in Beta vulgaris L. Plant Physiol. 105:1159–1166.
Rad, J.S., Rad, M.S., Miri, A. 2013. Regulation of the expression of nitrate reductase genes in leaves of medical plant, Foeniculum vulgare by different nitrate sources. Int. J. of Agric. and Crop Sci. 5:2911–2916.
Roosta, H.R., Sajjadinia, A., Rahimi, A., Schrjoerring, J.K. 2009. Responses of cucumber plant to NH4+ and NO3− nutrition: the relative addition rate technique vs. cultivation at constant nitrogen concentration. Scientia Horticulturae 121:397–403.
Sadras, V.O., Lawson, C. 2013. Nitrogen and water-use efficiency of Australian wheat varieties released between 1958 and 2007. Eur. J. Agron. 46:34–41.
Schluter, U., Mascher, M., Colmsee, C., Scholz, U., Brautigam, A., Fahnenstich, H., Sonnewald, U. 2012. Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol. 160:1384–1406.
Singh, R., Perez, C.M., Pascual, C.G., Juliano, B.O. 1978. Grain size, sucrose level and starch accumulation in developing rice grain. Phytochem. 17:1869–1874.
Singh, R., Asthir, B.1988. Import of sucrose and its transformation to starch in the developing sorghum caryopsis. Physiologica Plantarum 74:58–65.
Stommel, J.R. 1992. Enzymic components of sucrose accumulation in the wild tomato species Lycopersicon peruvianum. Plant Physiol. 99:324–328.
Tercé-Laforgue, T., Dubois, F., Ferrario-Mery, S., Pou de Crecenzo, M.A., Sangwan, R., Hirel, B. 2004. Glutamate dehydrogenase of tobacco (Nicotiana tabacum L.) is mainly induced in the cytosol of phloem companion cells when ammonia is provided either externally or released during photorespiration. Plant Physiol. 136:4308–4317.
Tezuka, T., Yamamoto, Y., Kondo, N. 1990. Activation of O2 uptake and NAD-specific isocitrate dehydrogenase in mitochondria isolated from cotyledons of castor bean by cis,trans-abscisic acid. Plant Physiol. 92:147–150.
Tonhazy, N.E. 1960a. Glutamate-oxaloacetate-transaminase. In: Bergmeyer, H.U. (ed.), Methods of Enzyme Analysis. Akademie-Verlag, Berlin, Germany. pp. 665–698.
Tonhazy, N.E. 1960b. Glutamate-pyruvate-transaminase. In: Bergmeyer, H.U. (ed.), Methods of Enzyme Analysis. Akademie-Verlag, Berlin, Germany. pp. 727–731.
Vance, C.P., Stade, S. 1984. Alfalfa root nodule carbon dioxide fixation. II. Partial purification and characterization of root nodule phosphoenolpyruvate carboxylase. Plant Physiol. 75:261–264.
Wojciechowski, T., Gooding, M.J., Ramsay, L., Gregory, P.J. 2009. The effects of dwarfing genes on seedling root growth of wheat. J. Exp. Bot. 60:2565–2573.
Author information
Authors and Affiliations
Corresponding author
Additional information
Conflict of Interest
The authors declare that they have no conflict of interest.
Communicated by J. Zhang
Electronic Supplementary Material (ESM)
42976_2016_4403381_MOESM1_ESM.pdf
Hydroponic Culturing Upregulates Sucrose and Glutamine Metabolism by Enhancing Their Utilization via Intermediates of Aerobic Pathway in Wheat
Rights and permissions
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Kaur, B., Asthir, B. Hydroponic Culturing Upregulates Sucrose and Glutamine Metabolism by Enhancing Their Utilization via Intermediates of Aerobic Pathway in Wheat. CEREAL RESEARCH COMMUNICATIONS 44, 381–392 (2016). https://doi.org/10.1556/0806.44.2016.003
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1556/0806.44.2016.003