Advertisement

Cereal Research Communications

, Volume 44, Issue 3, pp 381–392 | Cite as

Hydroponic Culturing Upregulates Sucrose and Glutamine Metabolism by Enhancing Their Utilization via Intermediates of Aerobic Pathway in Wheat

  • B. Kaur
  • B. AsthirEmail author
Physiology

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.

Keywords

nitrogen carbon hydroponics wheat genotypes 

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Supplementary material

42976_2016_4403381_MOESM1_ESM.pdf (1.6 mb)
Hydroponic Culturing Upregulates Sucrose and Glutamine Metabolism by Enhancing Their Utilization via Intermediates of Aerobic Pathway in Wheat

References

  1. Anjana, S.U., Iqbal, M., Abrol, Y.P. 2007. Are nitrate concentrations in leafy vegetables within safe limits? Current Sci. 92:355–360.Google Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 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.Google Scholar
  6. 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.Google Scholar
  7. 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.Google Scholar
  8. Britto, D.T., Kronzucker, H.J. 2002. Review NH4+ toxicity in higher plants: a critical review. J. Plant Physiol. 159:567–584.CrossRefGoogle Scholar
  9. Bulen, W.A. 1956. The isolation and characterization of glutamate dehydrogenase from corm leaves. Archives of Biochemistry and Biophysics 62:178–183.CrossRefGoogle Scholar
  10. 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.PubMedPubMedCentralGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.Google Scholar
  13. 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.CrossRefGoogle Scholar
  14. Fathi, G. 2008. Effect of genotype variability on nitrate uptake and assimilation of wheat cultivars. J. of Agric. Sci. and Technol. 10:11–22.Google Scholar
  15. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Hawkesford, M.J. 2014. Reducing the reliance on nitrogen fertilizer for wheat production. J. Cereal Sci. 59:276–283.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Hoagland, D.R., Arnon, D.I. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station Publication 347:1–32.Google Scholar
  18. Hodges, M. 2002. Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53:905–916.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Jaworski, E.G. 1971. Nitrate reductase in intact plant tissue. Biochem. and Biophysic. Res. Commun. 43:1274–1279.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. Kanamori, T., Matsumoto, H. 1974. Asparagine synthesis by Oryza sativa seedlings. Phytochem. 13:1407–1412.CrossRefGoogle Scholar
  25. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.Google Scholar
  29. Lee, Y.P., Takahashi, T. 1966. An improved colorimetric determination of amino acid with the use of ninhydrin. Anal. Biochem. 14:71–77.CrossRefGoogle Scholar
  30. 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.Google Scholar
  31. Lin, C.C., Kao, C.H. 2001. Regulation of ammonium-induced proline accumulation in detached rice leaves. Plant Growth Regul. 35:69–74.CrossRefGoogle Scholar
  32. 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.PubMedPubMedCentralGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  36. McKenzie, H.A., Wallace, H.S. 1954. The Kjeldahl determination of nitrogen. Austr. J. Chem. 17:55–59.CrossRefGoogle Scholar
  37. Miflin, B.J., Lea, P.J. 1976. The pathway of nitrogen assimilation in plants. Phytochem. 15:873–885.CrossRefGoogle Scholar
  38. Miyao, M., Fukayama, H. 2003. Metabolic consequences of overproduction of phosphoenolpyruvate carboxylase in C3 plants. Archives of Biochemistry and Biophysics 414:197–203.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Morell, M., Copeland, L. 1985. Sucrose synthase of soybean nodules. Plant Physiol. 78:149–154.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Morozkina, E.V., Zvyagilskaya, R.A. 2007. Nitrate reductases: Structure, functions and effect of stress factors. Biochem. 72:1151–1160.Google Scholar
  42. Nasholm, T., Kielland, K., Ganeteg, U. 2009. Uptake of organic nitrogen by plants. New Phytologist 182:31–48.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 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.Google Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.PubMedPubMedCentralGoogle Scholar
  47. Raab, T.K., Terry, N. 1994. Nitrogen source regulation of growth and photosynthesis in Beta vulgaris L. Plant Physiol. 105:1159–1166.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 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.Google Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Singh, R., Asthir, B.1988. Import of sucrose and its transformation to starch in the developing sorghum caryopsis. Physiologica Plantarum 74:58–65.Google Scholar
  54. Stommel, J.R. 1992. Enzymic components of sucrose accumulation in the wild tomato species Lycopersicon peruvianum. Plant Physiol. 99:324–328.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Tonhazy, N.E. 1960a. Glutamate-oxaloacetate-transaminase. In: Bergmeyer, H.U. (ed.), Methods of Enzyme Analysis. Akademie-Verlag, Berlin, Germany. pp. 665–698.Google Scholar
  58. Tonhazy, N.E. 1960b. Glutamate-pyruvate-transaminase. In: Bergmeyer, H.U. (ed.), Methods of Enzyme Analysis. Akademie-Verlag, Berlin, Germany. pp. 727–731.Google Scholar
  59. 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.PubMedPubMedCentralGoogle Scholar
  60. 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.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2016

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.

Authors and Affiliations

  1. 1.Department of BiochemistryPunjab Agricultural UniversityLudhiana, PunjabIndia

Personalised recommendations