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An Overview of Important Enzymes Involved in Nitrogen Assimilation of Plants

  • Reddy Kishorekumar
  • Mallesham Bulle
  • Aakanksha Wany
  • Kapuganti Jagadis GuptaEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 2057)

Abstract

Nitrogen (N) is a macro-nutrient that is essential for growth development and resistance against biotic and abiotic stresses of plants. Nitrogen is a constituent of amino acids, proteins, nucleic acids, chlorophyll, and various primary and secondary metabolites. The atmosphere contains huge amounts of nitrogen but it cannot be taken up directly by plants. Plants can take up nitrogen in the form of nitrate, ammonium, urea, nitrite, or a combination of all these forms. In addition, in various leguminous rhizobia, bacteria can convert atmospheric nitrogen to ammonia and supply it to the plants. The form of nitrogen nutrition is also important in plant growth and resistance against pathogens. Nitrogen content has an important function in crop yield. Nitrogen deficiency can cause reduced root growth, change in root architecture, reduced plant biomass, and reduced photosynthesis. Hence, understanding the function and regulation of N metabolism is important. Several enzymes and intermediates are involved in nitrogen assimilation. Here we provide an overview of the important enzymes such as nitrate reductase, nitrite reductase, glutamine synthase, GOGAT, glutamate dehydrogenase, and alanine aminotransferase that are involved in nitrogen metabolism.

Key words

Nitrogen Nitrate Ammonium Glutamate Glutamine Alanine 

References

  1. 1.
    Krapp A (2005) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25:115–122CrossRefGoogle Scholar
  2. 2.
    Temple SJ, Vance CP, Gantt JS (1998) Glutamate synthase and nitrogen assimilation. Trends Plant Sci 3:51–56CrossRefGoogle Scholar
  3. 3.
    Crawford NM, Glass AD (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395CrossRefGoogle Scholar
  4. 4.
    O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutiérrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856CrossRefPubMedGoogle Scholar
  5. 5.
    Oaks A (1994) Primary nitrogen assimilation in higher plants and its regulation. Can J Bot 72:739–750CrossRefGoogle Scholar
  6. 6.
    Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239:289–297PubMedPubMedCentralGoogle Scholar
  7. 7.
    Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168CrossRefPubMedGoogle Scholar
  8. 8.
    Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110CrossRefPubMedGoogle Scholar
  9. 9.
    Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411CrossRefPubMedGoogle Scholar
  10. 10.
    Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5Google Scholar
  11. 11.
    Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M (2008) Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. J Integr Plant Biol 50:231–243CrossRefPubMedGoogle Scholar
  12. 12.
    Wany A, Gupta AK, Kumari A, Mishra S, Singh N, Pandey S, Vanvari R, Igamberdiev AU, Fernie AR, Gupta KJ (2018) Nitrate nutrition influences multiple factors in order to increase energy efficiency under hypoxia in Arabidopsis. Ann Bot 123(4):691–705.  https://doi.org/10.1093/aob/mcy202 CrossRefGoogle Scholar
  13. 13.
    Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318CrossRefPubMedGoogle Scholar
  14. 14.
    Hao F, Zhao S, Dong H, Zhang H, Sun L, Miao C (2010) Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis. J Integr Plant Biol 52:298–307CrossRefPubMedGoogle Scholar
  15. 15.
    Seligman K, Saviani EE, Oliveira HC, Pinto-Maglio CAF, Salgado I (2008) Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol 49:1112–1121CrossRefPubMedGoogle Scholar
  16. 16.
    Kolbert Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975CrossRefPubMedGoogle Scholar
  17. 17.
    Lombardo MC, Lamattina L (2012) Nitric oxide is essential for vesicle formation and trafficking in Arabidopsis root hair growth. J Exp Bot 63:4875–4885CrossRefPubMedGoogle Scholar
  18. 18.
    Kolbert Z, Ortega L, Erdei L (2010) Involvement of nitrate reductase (NR) in osmotic stress-induced NO generation of Arabidopsis thaliana L. roots. J Plant Physiol 167:77–80CrossRefPubMedGoogle Scholar
  19. 19.
    Royo B, Moran JF, Ratcliffe RG, Gupta KJ (2015) Nitric oxide induces the alternative oxidase pathway in Arabidopsis seedlings deprived of inorganic phosphate. J Exp Bot 66:6273–6280CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Solomonson LP, Barber MJ (1990) Assimilatory nitrate reductase: functional properties and regulation. Annu Rev Plant Physiol Plant Mol Biol 41:225–253CrossRefGoogle Scholar
  22. 22.
    Crawford NM, Smith M, Bellissimo D, Davis RW (1988) Sequence and nitrate regulation of the Arabidopsis thaliana mRNA encoding nitrate reductase, a metalloflavoprotein with three functional domains. Proc Natl Acad Sci USA 85:5006–5010CrossRefPubMedGoogle Scholar
  23. 23.
    Neame PJ, Barber MJ (1989) Conserved domains in molybdenum hydroxylases. The amino acid sequence of chicken hepatic sulfite oxidase. J Biol Chem 264:20894–20901PubMedPubMedCentralGoogle Scholar
  24. 24.
    Campbell WH (2001) Structure and function of eukaryotic NAD(P)H:nitrate reductase. Cell Mol Life Sci 58:194–204CrossRefPubMedGoogle Scholar
  25. 25.
    Kleinhofs A, Warner RL (1990) Advances in nitrate assimilation. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants, Intermediary nitrogen metabolism, vol 16. Academic Press, San Diego, pp 89–120Google Scholar
  26. 26.
    Kaiser WM, Brendle-Behnisch E (1991) Rapid modulation of spinach leaf nitrate reductase activity by photosynthesis: I. Modulation in vivo by CO2 availability. Plant Physiol 96:363–367CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Bowsher CG, Long DM, Oaks A, Rothstein SJ (1991) Effect of light/dark cycles on expression of nitrate assimilatory genes in maize shoots and roots. Plant Physiol 95:281–285CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868PubMedPubMedCentralGoogle Scholar
  29. 29.
    Baki GAE, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ 23:515–521CrossRefGoogle Scholar
  30. 30.
    Campbell WH (1996) Nitrate reductase biochemistry comes of age. Plant Physiol 111:355–361CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Planchet E, Jagadis Gupta K, Sonoda M, Kaiser WM (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743CrossRefPubMedGoogle Scholar
  32. 32.
    Neyra CA, Hageman RH (1975) Nitrate uptake and induction of nitrate reductase in excised corn roots. Plant Physiol 56:692–695CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Meyer C (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435CrossRefPubMedGoogle Scholar
  34. 34.
    Vincentz M, Caboche M (1991) Constitutive expression of nitrate reductase allows normal growth and development of Nicotiana plumbaginifolia plants. EMBO J 10:1027–1035CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Gupta KJ, Stoimenova M, Kaiser WM (2005) In higher plants, only root mitochondria, but not leaf mitochondria, reduce nitrite to NO, in vitro and in situ. J Exp Bot 56:2601–2609CrossRefPubMedGoogle Scholar
  36. 36.
    Botrel A, Kaiser WM (1997) Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta (Berl) 201:496–501CrossRefGoogle Scholar
  37. 37.
    Hoff T, Truong HN, Caboche M (1994) The use of mutants and transgenic plants to study nitrate assimilation. Plant Cell Environ 17:489–506CrossRefGoogle Scholar
  38. 38.
    Gigli-Bisceglia N, Engelsdorf T, Strnad M, Vaahtera L, Khan GA, Jamoune A, Hamann T (2018) Cell wall integrity modulates Arabidopsis thaliana cell cycle gene expression in a cytokinin- and nitrate reductase-dependent manner. Development (Camb) 145:145(19). dev166678.  https://doi.org/10.1242/dev.166678 CrossRefGoogle Scholar
  39. 39.
    Sestili F, Rouphael Y, Cardarelli M, Pucci A, Bonini P, Canaguier R, Colla G (2018) Protein hydrolysate stimulates growth in tomato coupled with N-dependent gene expression involved in N assimilation. Front Plant Sci 9:1233CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Bachmann M, Shiraishi N, Campbell WH, Yoo BC, Harmon AC, Huber SC (1996) Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell 8:505–517PubMedPubMedCentralGoogle Scholar
  41. 41.
    Kaiser WM, Spill D (1991) Rapid modulation of spinach leaf nitrate reductase by photosynthesis: II. In vitro modulation by ATP and AMP. Plant Physiol 96:368–375CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Douglas P, Moorhead G, Hong Y, Morrice N, MacKintosh C (1998) Purification of a nitrate reductase kinase from Spinacea oleracea leaves, and its identification as a calmodulin-domain protein kinase. Planta (Berl) 206:435–442CrossRefGoogle Scholar
  43. 43.
    Elliott WH (1953) Isolation of glutamine synthetase and glutamotransferase from green peas. J Biol Chem 201:661–672PubMedPubMedCentralGoogle Scholar
  44. 44.
    Hirel B, Andrieu B, Valadier MH, Renard S, Quillere I, Chelle M, Pommel B, Fournier C, Drouet JL (2005) Physiology of maize II: identification of physiological markers representative of the nitrogen status of maize (Zea mays) leaves during grain filling. Physiol Plant 124:178–188CrossRefGoogle Scholar
  45. 45.
    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 105:1141–1157CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Brugière N, Dubois F, Limami AM, Lelandais M, Roux Y, Sangwan RS, Hirel B (1999) Glutamine synthetase in the phloem plays a major role in controlling proline production. Plant Cell 11:1995–2011CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Lea PJ, Miflin BJ (2003) Glutamate synthase and the synthesis of glutamate in plants. Plant Physiol Biochem 41:555–564CrossRefGoogle Scholar
  48. 48.
    Moison M, Marmagne A, Dinant S, Soulay F, Azzopardi M, Lothier J, Avice JC (2018) Three cytosolic glutamine synthetase isoforms located in different order veins work together for N remobilization and seed filling in Arabidopsis. J Exp Bot 69:4379–4393CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Tercé-Laforgue T (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Lebedev VG, Korobova AV, Shendel GV, Kudoyarova GR, Shestibratov KA (2018) Effect of glutamine synthetase gene overexpression in birch (Betula pubescens) plants on auxin content and rooting in vitro. Dokl Biochem Biophys 48:143–145CrossRefGoogle Scholar
  51. 51.
    Hirel B, Lea PJ (2001) Ammonia assimilation. In: Lea PJ, Morot-Gaudry JF (eds) Plant nitrogen. Springer, Berlin, HeidelbergGoogle Scholar
  52. 52.
    Bernard SM, Møller AL, Dionisio G, Kichey T, Jahn TP, Dubois F, Baudo M, Lopes MS, Tercé-Laforgue T, Foyer CH, Parry MA (2008) Gene expression, cellular localization and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol Biol 67:89–105CrossRefPubMedGoogle Scholar
  53. 53.
    Ishiyama K, Inoue E, Tabuchi M, Yamaya T, Takahashi H (2004) Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol 45:1640–1647CrossRefPubMedGoogle Scholar
  54. 54.
    Guan M, Møller IS, Schjørring JK (2014) Two cytosolic glutamine synthetase isoforms play specific roles for seed germination and seed yield structure in Arabidopsis. J Exp Bot 66:203–212CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Zhang Z, Xiong S, Wei Y, Meng X, Wang X, Ma X (2017) The role of glutamine synthetase isozymes in enhancing nitrogen use efficiency of N-efficient winter wheat. Sci Rep 7:1000CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Sakakibara H, Shimizu H, Hase T, Yamazaki Y, Takao T, Shimonishi Y, Sugiyama T (1996) Molecular identification and characterization of cytosolic isoforms of glutamine synthetase in maize roots. J Biol Chem 271:29561–29568CrossRefPubMedGoogle Scholar
  57. 57.
    Li MG, Villemur R, Hussey PJ, Silflow CD, Gantt JS, Snustad DP (1993) Differential expression of six glutamine synthetase genes in Zea mays. Plant Mol Biol 23:401–440CrossRefPubMedGoogle Scholar
  58. 58.
    Guiz C, Hirel B, Shedlofsky G, Gadal P (1979) Occurrence and influence of light on the relative proportions of two glutamine sythetases in rice leaves. Plant Sci Lett 15:271–277CrossRefGoogle Scholar
  59. 59.
    Taira M, Valtersson U, Burkhardt B, Ludwig RA (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16:2048–2058CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Mann AF, Fentem PA, Stewart GR (1979) Identification of two forms of glutamine synthetase in barley (Hordeum vulgare). Biochem Biophys Res Commun 88:515–521CrossRefPubMedGoogle Scholar
  61. 61.
    Kumagai E, Araki T, Hamaoka N, Ueno O (2011) Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Ann Bot 108:1381–1386CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549CrossRefGoogle Scholar
  63. 63.
    Wang X, Wei Y, Shi L, Ma X, Theg SM (2015) New isoforms and assembly of glutamine synthetase in the leaf of wheat (Triticum aestivum L.). J Exp Bot 66:6827–6834CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Gregerson RG, Miller SS, Twary SN, Gantt JS, Vance CP (1993) Molecular characterization of NADH-dependent glutamate synthase from alfalfa nodules. Plant Cell 5:215–226PubMedPubMedCentralGoogle Scholar
  65. 65.
    Sakakibara H, Watanabe M, Hase T, Sugiyama T (1991) Molecular cloning and characterization of complementary DNA encoding for ferredoxin-dependent glutamate synthase in maize leaf. J Biol Chem 266:2028–2035PubMedPubMedCentralGoogle Scholar
  66. 66.
    Suzuki A, Rothstein S (1997) Structure and regulation of ferredoxin-dependent glutamase synthase from Arabidopsis thaliana: cloning of cDNA, expression in different tissues of wild-type and gltS mutant strains, and light induction. Eur J Biochem 243:708–718CrossRefPubMedGoogle Scholar
  67. 67.
    Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Biol 47:569–593CrossRefGoogle Scholar
  68. 68.
    Oliveira IC, Lam HM, Coschigano K, Melo-Oliveira R, Coruzzi G (1997) Molecular-genetic dissection of ammonium assimilation in Arabidopsis thaliana. Plant Physiol Biochem 35:185–198Google Scholar
  69. 69.
    Fox GG, Ratcliffe RG, Robinson SA, Stewart GR (1995) Evidence for deamination by glutamate dehydrogenase in higher plants: commentary. Can J Bot 73:1112–1115CrossRefGoogle Scholar
  70. 70.
    Purnell MP, Botella JR (2007) Tobacco isoenzyme 1 of NAD (H)-dependent glutamate dehydrogenase catabolizes glutamate in vivo. Plant Physiol 143:530–539CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Miyashita Y, Good AG (2008) NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation. J Exp Bot 59:667–680CrossRefPubMedGoogle Scholar
  72. 72.
    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 18:2767–2781CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Limami AM, Glévarec G, Ricoult C, Cliquet JB, Planchet E (2008) Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. J Exp Bot 59:2325–2335CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Melo-Oliveira R, Oliveira IC, Coruzzi GM (1996) Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation. Proc Natl Acad Sci USA 93:4718–4723CrossRefPubMedGoogle Scholar
  75. 75.
    Loulakakis KA, Roubelakis-Angelakis KA (1996) The seven NAD (H)-glutamate dehydrogenase isoenzymes exhibit similar anabolic and catabolic activities. Physiol Planta 96:29–35CrossRefGoogle Scholar
  76. 76.
    Marchi L, Degola F, Polverini E, Tercé-Laforgue T, Dubois F, Hirel B, Restivo FM (2013) Glutamate dehydrogenase isoenzyme 3 (GDH3) of Arabidopsis thaliana is regulated by a combined effect of nitrogen and cytokinin. Plant Physiol Biochem 73:368–374CrossRefPubMedGoogle Scholar
  77. 77.
    Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M, Pham P (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302:842–846CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Fontaine JX, Tercé-Laforgue T, Bouton S, Pageau K, Lea PJ, Dubois F, Hirel B (2013) Further insights into the isoenzyme composition and activity of glutamate dehydrogenase in Arabidopsis thaliana. Plant Signal Behav 8:e23329CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Dubois F, Tercé-Laforgue T, Gonzalez-Moro MB, Estavillo JM, Sangwan R, Gallais A, Hirel B (2003) Glutamate dehydrogenase in plants: is there a new story for an old enzyme? Plant Physiol Biochem 41:565–576CrossRefGoogle Scholar
  80. 80.
    Tercé-Laforgue T, Dubois F, Ferrario-Méry S, de Crecenzo MAP, Sangwan R, Hirel B (2004) Glutamate dehydrogenase of tobacco is mainly induced in the cytosol of phloem companion cells when ammonia is provided either externally or released during photorespiration. Plant Physiol 136:4308–4317CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Tercé-Laforgue T, Clément G, Marchi L, Restivo FM, Lea PJ, Hirel B (2015) Resolving the role of plant NAD-glutamate dehydrogenase: III. Overexpressing individually or simultaneously the two enzyme subunits under salt stress induces changes in the leaf metabolic profile and increases plant biomass production. Plant Cell Physiol 56:1918–1929CrossRefPubMedGoogle Scholar
  82. 82.
    Ameziane R, Bernhard K, Lightfoot D (2000) Expression of the bacterial gdhA gene encoding a NADPH glutamate dehydrogenase in tobacco affects plant growth and development. Plant Soil 221:47–57CrossRefGoogle Scholar
  83. 83.
    Nolte SA, Young BG, Mungur R, Lightfoot DA (2004) The glutamate dehydrogenase gene gdhA increased the resistance of tobacco to glufosinate. Weed Res 44:335–339CrossRefGoogle Scholar
  84. 84.
    Lightfoot DA, Mungur R, Ameziane R, Nolte S, Long L, Bernhard K, Young B (2007) Improved drought tolerance of transgenic Zea mays plants that express the glutamate dehydrogenase gene (gdhA) of E. coli. Euphytica 156:103–116CrossRefGoogle Scholar
  85. 85.
    Kazachkova Y, Batushansky A, Cisneros A, Tel-Zur N, Fait A, Barak S (2013) Growth platform-dependent and independent phenotypic and metabolic responses of Arabidopsis thaliana and its halophytic relative Eutrema salsugineum, to salt stress. Plant Physiol 162:1583–1598CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Gechev TS, Hille J, Woerdenbag HJ, Benina M, Mehterov N, Toneva V, Mueller-Roeber B (2014) Natural products from resurrection plants: potential for medical applications. Biotechnol Adv 32:1091–1101CrossRefPubMedGoogle Scholar
  87. 87.
    Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Tsai KJ, Lin CY, Ting CY, Shih MC (2016) Ethylene-regulated glutamate dehydrogenase fine-tunes metabolism during anoxia-reoxygenation. Plant Physiol 172:1548–1562CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Fontaine JX, Tercé-Laforgue T, Armengaud P, Clément G, Renou JP, Pelletier S, Hirel B (2012) Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell 24:4044–4065CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Rocha M, Sodek L, Licausi F, Hameed MW, Dornelas MC, Van Dongen JT (2010) Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids 39:1043–1053CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Miyashita Y, Dolferus R, Ismond KP, Good AG (2007) Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana. Plant J 49:1108–1121CrossRefPubMedGoogle Scholar
  92. 92.
    Kikuchi H, Hirose S, Toki S, Akama K, Takaiwa F (1999) Molecular characterization of a gene for alanine aminotransferase from rice (Oryza sativa). Plant Mol Biol 39:149–159CrossRefPubMedGoogle Scholar
  93. 93.
    Igarashi D, Miwa T, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Ohsumi C (2003) Identification of photorespiratory glutamate: glyoxylate aminotransferase (GGAT) gene in Arabidopsis. Plant J 33:975–987CrossRefPubMedGoogle Scholar
  94. 94.
    De Sousa CA, Sodek L (2003) Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environ Exp Bot 50:1–8CrossRefGoogle Scholar
  95. 95.
    Ricoult C, Echeverria LO, Cliquet JB, Limami AM (2006) Characterization of alanine aminotransferase (AlaAT) multi gene family and hypoxic response in young seedlings of the model legume Medicago truncatula. J Exp Bot 57:3079–3089CrossRefPubMedGoogle Scholar
  96. 96.
    Good AG, Johnson SJ, De Pauw M, Carroll RT, Savidov N, Vidmar J, Lu Z, Taylor G, Stroeher V (2007) Engineering nitrogen use efficiency with alanine amino transferase. Botany 85:252–262Google Scholar
  97. 97.
    Beatty PH, Shrawat AK, Carroll RT, Zhu T, Good AG (2009) Transcriptome analysis of nitrogen-efficient rice over-expressing alanine aminotransferase. Plant Biotechnol J 7:562–576CrossRefPubMedGoogle Scholar
  98. 98.
    Liepman AH, Olsen LJ (2003) Alanine aminotransferase homologs catalyze the glutamate: glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiol 131:215–227CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Son D, Kobe A, Sugiyama T (1992) Nitrogen-dependent regulation of the gene for alanine aminotransferase which is involved in the C4 pathway of Panicum miliaceum. Plant Cell Physiol 33:507–509Google Scholar
  100. 100.
    Muench DG, Christopher ME, Good AG (1998) Cloning and expression of a hypoxic and nitrogen inducible maize alanine aminotransferase gene. Physiol Plant 103:503–512CrossRefGoogle Scholar
  101. 101.
    Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732CrossRefPubMedGoogle Scholar
  102. 102.
    Snyman SJ, Hajari E, Watt MP, Lu Y, Kridl JC (2015) Improved nitrogen use efficiency in transgenic sugarcane: phenotypic assessment in a pot trial under low nitrogen conditions. Plant Cell Rep 34:667–669CrossRefPubMedGoogle Scholar
  103. 103.
    Rocha M, Licausi F, Araujo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  • Reddy Kishorekumar
    • 1
  • Mallesham Bulle
    • 1
  • Aakanksha Wany
    • 1
  • Kapuganti Jagadis Gupta
    • 1
    Email author
  1. 1.National Institute of Plant Genome ResearchNew DelhiIndia

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