Transgenic Manipulation of Glutamine Synthetase: A Target with Untapped Potential in Various Aspects of Crop Improvement

  • Donald James
  • Bhabesh Borphukan
  • Dhirendra Fartyal
  • V. M. M. Achary
  • M. K. ReddyEmail author


Glutamine synthetase (GS) plays a key role in the nitrogen (N) metabolism in higher plants. N is a major limiting nutrient in crop production, and most of it is lost due to volatilization or leaching which has deleterious effects on the environment. Hence, GS is considered a prime target for transgenic approaches to increase nitrogen use efficiency (NUE) which is paramount for sustainable agriculture. The current status of such attempts at increasing NUE utilizing GS, their outcomes, constraints, and future prospects have been discussed in detail. GS is also modulated by various abiotic stresses including salt and drought which have adverse effects on crop production. Modulation of GS by various abiotic stresses and transgenic approaches utilizing GS for tolerance, their results, limitations, and possibilities of further advancement have been reviewed. GS is also the target of the commonly used herbicide glufosinate (Basta). Herbicide-tolerant transgenic crops have become a necessity for modern agriculture, given the labor and expenditure involved in traditional weed control practices. In the light of public resentment and biosafety concerns of utilizing bacterial genes for herbicide tolerance in food crops, the overexpression of mutant GS enzymes as an alternative strategy for developing glufosinate-resistant crops has been discussed. This chapter also examines the inconsistent results of overexpression of GS genes for various applications in view of intricate regulation of GS due to its critical role in metabolism.


Glutamine synthetase Nitrogen use efficiency Abiotic stress Herbicide tolerance Glufosinate Transgenic overexpression Regulation 


  1. Almassy RJ, Janson CA, Hamlin R et al (1986) Novel subunit–subunit interactions in the structure of glutamine synthetase. Nature 323:304–309CrossRefPubMedGoogle Scholar
  2. Amaya KR, Kocherginskaya SA, Mackie RI et al (2005) Biochemical and mutational analysis of glutamine synthetase type III from the rumen anaerobe Ruminococcus albus. J Bacteriol 187:7481–7491. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Atkins CA (1987) Metabolism and translocation of fixed nitrogen in the nodulated legume. In: van Diest A (ed) Plant and soil interfaces and interactions. Springer Netherlands, Dordrecht, pp 157–169CrossRefGoogle Scholar
  4. Avila-Ospina L, Marmagne A, Talbotec J et al (2015) The identification of new cytosolic glutamine synthetase and asparagine synthetase genes in barley (Hordeum vulgare L.), and their expression during leaf senescence. J Exp Bot 66:2013–2026. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Baima S, Haegi A, Stroman P et al (1989) Characterization of a cDNA clone for barley leaf glutamine synthetase. Carlsb Res Commun 54:1–9CrossRefGoogle Scholar
  6. Bao A, Zhao Z, Ding G et al (2014) Accumulated expression level of cytosolic glutamine synthetase gene (OsGS1;1 or OsGS1;2) alter plant development and the carbon-nitrogen metabolic status in rice. PLoS One 9:e95581. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bauer D, Biehler K, Fock H et al (1997) A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato. Physiol Plant 99:241–248. CrossRefGoogle Scholar
  8. Bayer E, Gugel KH, Hagele K et al (1972) Phosphinothricin und Phosphinothricylalanyl-alanin. Helv Chim Acta 55:224–239. (In German)CrossRefPubMedGoogle Scholar
  9. Bernard SM, Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620CrossRefPubMedGoogle Scholar
  10. Bernard SM, Møller ALB, Dionisio G et al (2008) Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol Biol 67:89–105. CrossRefPubMedGoogle Scholar
  11. Biesiadka J, Legocki AB (1997) Evolution of the glutamine synthetase gene in plants. Plant Sci 128:51–58. CrossRefGoogle Scholar
  12. Bouwman AF, Boumans LJM, Batjes NH (2002) Emissions of N2O and NO from fertilised fields: summary of available measurement data. Global Biogeochem Cycles 16:1058Google Scholar
  13. Brauer EK, Shelp BJ (2010) Nitrogen use efficiency: re-consideration of the bioengineering approach. Botany 88:103–109CrossRefGoogle Scholar
  14. Brauer EK, Rochon A, Bi YM et al (2011) Reappraisal of nitrogen use efficiency in rice overexpressing glutamine synthetase. Physiol Plant 141:361–372. CrossRefPubMedGoogle Scholar
  15. Brestic M, Zivcak M, Olsovska K et al (2014) Reduced glutamine synthetase activity plays a role in control of photosynthetic responses to high light in barley leaves. Plant Physiol Biochem 81:74–83CrossRefGoogle Scholar
  16. Brugière N, Dubois F, Limami A et al (1999) Glutamine synthetase in the phloem plays a major role in controlling proline production. Plant Cell 11:1995–2012. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cai H, Zhou Y, Xiao J et al (2009) Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Rep 28:527–537. CrossRefPubMedGoogle Scholar
  18. Canas RA, Quilleré I, Lea PJ et al (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol J 8:966–978CrossRefPubMedGoogle Scholar
  19. Carvalho HG, Lopes-Cardoso IA, Lima LM et al (2003) Nodule-specific modulation of glutamine synthetase in transgenic Medicago truncatula leads to inverse alterations in asparagine synthetase expression. Plant Physiol 133:243–252. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Castaings L, Camargo A, Pocholle D et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435. CrossRefPubMedGoogle Scholar
  21. Castro-Rodríguez V, García-Gutiérrez A, Canales J et al (2011) The glutamine synthetase gene family in Populus. BMC Plant Biol 11:119. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chaffei C, Pageau K, Suzuki A et al (2004) Cadmium toxicity induced changes in nitrogen Management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45:1681–1693. CrossRefPubMedGoogle Scholar
  23. Cheng L, Wang Y, He Q et al (2016) Comparative proteomics illustrates the complexity of drought resistance mechanisms in two wheat (Triticum aestivum L.) cultivars under dehydration and rehydration. BMC Plant Biol 16:188. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Chompoo J, Pornprom T (2008) RT-PCR based detection of resistance conferred by an insensitive GS in glufosinate-resistant maize cell lines. Pestic Biochem Physiol 90:189–195. CrossRefGoogle Scholar
  25. Clemente MT, Márquez AJ (1999) Site-directed mutagenesis of Glu-297 from the α-polypeptide of Phaseolus vulgaris glutamine synthetase alters kinetic and structural properties and confers resistance to L-methionine sulfoximine. Plant Mol Biol 40:835–845. CrossRefPubMedGoogle Scholar
  26. Cren M, Hirel B (1999) Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol 40:1187–1193. CrossRefGoogle Scholar
  27. DasSarma S, Tisher E, Goodman HM (1986) Plant glutamine synthetase complements Glu a mutation in Escherichia coli. Science 232:1242–1244CrossRefPubMedGoogle Scholar
  28. De Block M, Botterman J, Vandewiele M et al (1987) Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J 6:2513–2518. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Debouba M, Gouia H, Suzuki A et al (2006) NaCl stress effects on enzymes involved in nitrogen assimilation pathway in tomato “Lycopersicon esculentum” seedlings. J Plant Physiol 163:1247–1258. CrossRefPubMedGoogle Scholar
  30. Díaz P, Betti M, Sánchez DH et al (2010) Deficiency in plastidic glutamine synthetase alters proline metabolism and transcriptomic response in Lotus japonicus under drought stress. New Phytol 188:1001–1013. CrossRefPubMedGoogle Scholar
  31. Donn G, Köcher H (2002) Inhibitors of glutamine Synthetase. In: Böger P et al (eds) Herbicide Classes in Development. Springer, Berlin/Heidelberg, pp 87–101CrossRefGoogle Scholar
  32. Donn G, Tischer E, Smith JA et al (1984) Herbicide-resistant alfalfa cells: an example of gene amplification in plants. J Mol Appl Genet 2:621–635PubMedGoogle Scholar
  33. Doskočilová A, Plíhal O, Volc J et al (2011) A nodulin/glutamine synthetase-like fusion protein is implicated in the regulation of root morphogenesis and in signalling triggered by flagellin. Planta 234:459–476. CrossRefPubMedGoogle Scholar
  34. Doyle JJ (1991) Evolution of higher plant glutamine synthetase genes tissue specificity as a criterion for predicting orthology. Mol Biol Evol 8:366–377Google Scholar
  35. Eckes P, Schmitt P, Daub W et al (1989) Overproduction of alfalfa glutamine synthetase in transgenic tobacco plants. Mol Gen Genet 217:263–268CrossRefPubMedGoogle Scholar
  36. Eisenberg D, Gill HS, Pfluegl GMU et al (2000) Structure–function relationships of glutamine synthetases. Biochim Biophys Acta Protein Struct Mol Enzymol 1477:122–145. CrossRefGoogle Scholar
  37. El-Khatib RT, Hamerlynck EP, Gallardo F et al (2004) Transgenic poplar characterized by ectopic expression of a pine cytosolic glutamine synthetase gene exhibits enhanced tolerance to water stress. Tree Physiol 24:729–736. CrossRefPubMedGoogle Scholar
  38. Fan X, Tang Z, Tan Y et al (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci U S A 113:7118–7123. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Fei H, Chaillou S, Hirel B et al (2003) Overexpression of a soybean cytosolic glutamine synthetase gene linked to organ-specific promoters in pea plants grown in different concentrations of nitrate. Planta 216:467–474. CrossRefPubMedGoogle Scholar
  40. Fei H, Chaillou S, Hirel B et al (2006) Effects of the overexpression of a soybean cytosolic glutamine synthetase gene (GS15) linked to organ-specific promoters on growth and nitrogen accumulation of pea plants supplied with ammonium. Plant Physiol Biochem 44:543–550. CrossRefPubMedGoogle Scholar
  41. Ferrante A, Savin R, Slafer GA (2010) Floret development of durum wheat in response to nitrogen availability. J Exp Bot 61:4351–4359. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Finnemann J, Schjoerring JK (2000) Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. Plant J 24:171–181. CrossRefPubMedGoogle Scholar
  43. Fischer JJ, Beatty PH, Good AG et al (2013) Manipulation of MicroRNA expression to improve nitrogen use efficiency. Plant Sci 210:70–81CrossRefPubMedGoogle Scholar
  44. Fontaine JX, Ravel C, Pageau K et al (2009) A quantitative genetic study for elucidating the contribution of glutamine synthetase, glutamate dehydrogenase and other nitrogen-related physiological traits to the agronomic performance of common wheat. Theor Appl Genet 119:645–662. CrossRefPubMedGoogle Scholar
  45. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358CrossRefPubMedGoogle Scholar
  46. Forde BG, Day HM, Turton JF et al (1989) Two glutamine Synthetase genes from Phaseolus vulgaris L. display contrasting developmental and spatial patterns of expression in transgenic Lotus corniculatus plants. Plant Cell 1:391–401CrossRefPubMedPubMedCentralGoogle Scholar
  47. Freney JR (2013) Management practices to increase efficiency of fertilizer and animal nitrogen and minimize nitrogen loss to the atmosphere and groundwater, CSIRO Plant Industry, Australia, Accessed 19 Mar 2017
  48. Fu J, Sampalo R, Gallardo F et al (2003) Assembly of a cytosolic pine glutamine synthetase holoenzyme in leaves of transgenic poplar leads to enhanced vegetative growth in young plants. Plant Cell Environ 26:411–418. CrossRefGoogle Scholar
  49. Fuentes SI, Allen DJ, Ortiz-Lopez A et al (2001) Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52:1071–1081. CrossRefPubMedGoogle Scholar
  50. Funayama K, Kojima S, Tabuchi M et al (2013) Cytosolic glutamine Synthetase1 ; 2 is responsible for the primary assimilation of ammonium in Rice roots. 54:934–943.
  51. Gadaleta A, Nigro D, Giancaspro A et al (2011) The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Funct Integr Genomics 11:665–670. CrossRefPubMedGoogle Scholar
  52. Gallais A, Hirel B (2004) An approach to the genetics of nitrogen use efficiency in maize. J Exp Bot 55:295–306CrossRefPubMedGoogle Scholar
  53. Gallardo F, Fu J, Cantón FR et al (1999) Expression of a conifer glutamine synthetase gene in transgenic poplar. Planta 210:19–26CrossRefPubMedGoogle Scholar
  54. Ghoshroy S, Binder M, Tartar A et al (2010) Molecular evolution of glutamine synthetase II: phylogenetic evidence of a non-endosymbiotic gene transfer event early in plant evolution. BMC Evol Biol 10:198. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Gill HS, Eisenberg D (2001) The crystal structure of phosphinothricin in the active site of glutamine synthetase illuminates the mechanism of enzymatic inhibition. Biochemistry 40:1903–1912. CrossRefPubMedGoogle Scholar
  56. Gill SS, Gill R, Tuteja R et al (2014) Genetic engineering of crops: a ray of hope for enhanced food security. Plant Signal Behav 9:e28545. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Goel P, Singh AK (2015) Abiotic stresses downregulate key genes involved in nitrogen uptake and assimilation in Brassica juncea l. PLoS One 10:e0143645. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9:597–605CrossRefGoogle Scholar
  59. Goodall AJ, Kumar P, Tobin AK (2013) Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). Plant Cell Physiol 54:492–505. CrossRefPubMedGoogle Scholar
  60. Goodman HJK, Woods DR (1993) Cloning and nucleotide sequence of the Butyrivibrio fibrisolvens gene encoding a type III glutamine synthetase. J Gen Microbiol 139:1487–1493. CrossRefPubMedGoogle Scholar
  61. Goodman H, DasSarma S, Tischer E et al (1990) Expression of wild type and mutant glutamine synthetase in foreign hosts. US Patent US4975374 A, 4 Dec 1990Google Scholar
  62. Guan M, Moller IS, Schjoerring JK (2015) Two cytosolic glutamine synthetase isoforms play specific roles for seed germination and seed yield structure in Arabidopsis. J Exp Bot 66:203–212. CrossRefPubMedGoogle Scholar
  63. Guan M, de Bang TC, Pedersen C et al (2016) Cytosolic glutamine Synthetase Gln1;2 is the main Isozyme contributing to GS1 activity and can be up-regulated to relieve ammonium toxicity. Plant Physiol 171:1921–1933. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Gutiérrez RA (2012) Systems biology for enhanced plant nitrogen nutrition. Science (80- ) 336:1673–1675. CrossRefPubMedGoogle Scholar
  65. Gutiérrez RA, Stokes TL, Thum K et al (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci U S A 105:4939–4944. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Habash DZ, Massiah AJ, Rong HL et al (2001) The role of cytosolic glutamine synthetase in wheat. Ann Appl Biol 138:83–89. CrossRefGoogle Scholar
  67. Habash DZ, Bernard S, Schondelmaier J et al (2007) The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theor Appl Genet 114:403–419. CrossRefPubMedGoogle Scholar
  68. Harper CJ, Hayward D, Kidd M, Wiid I, van Helden P (2010) Glutamate dehydrogenase and glutamine synthetase are regulated in response to nitrogen availability in Myocbacterium smegmatis. BMC Microbiol 10:138CrossRefPubMedPubMedCentralGoogle Scholar
  69. Harrison J, Pou de Crescenzo MA, Sene O et al (2003) Does lowering glutamine synthetase activity in nodules modify nitrogen metabolism and growth of Lotus japonicus? Plant Physiol 133:253–262. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Häusler RE, Lea PJ, Leegood RC (1994) Control of photosynthesis in barley leaves with reduced activities of glutamine synthetase or glutamate synthase - II. Control of electron transport and CO2 assimilation. Planta 194:418–435 CrossRefGoogle Scholar
  71. He YX, Gui L, Liu YZ et al (2009) Crystal structure of Saccharomyces cerevisiae glutamine synthetase Gln1 suggests a nanotube-like supramolecular assembly. Proteins Struct Funct Bioinf 76:249–254. CrossRefGoogle Scholar
  72. He C, Liu C, Liu Q et al (2014) Over-expression of glutamine synthetase genes Gln1-3/Gln1-4 improved nitrogen assimilation and maize yields. Maydica 59:50–256. Google Scholar
  73. Hemon P, Robbins MP, Cullimore JV (1990) Targeting of glutamine synthetase to the mitochondria of transgenic tobacco. Plant Mol Biol 15:895–904. CrossRefPubMedGoogle Scholar
  74. Hirel B, Lea PJ (2001) Ammonia Assimilation. In: Lea PJ et al (eds) Plant Nitrogen. Springer, Berlin/Heidelberg, pp 79–99. (ISBN 978–3–662-04064-5)CrossRefGoogle Scholar
  75. Hirel B, Marsolier MC, Hoarau J et al (1992) Forcing expression of a soybean root glutamine synthetase gene in tobacco leaves induces a native gene encoding cytosolic enzyme. Plant Mol Biol 20:207–218CrossRefPubMedGoogle Scholar
  76. Hirel B, Phillipson B, Murchie E et al (1997) Manipulating the pathway of ammonia assimilation in transgenic non-legumes and legumes. Z Pflanzenernähr Bodenk 160:283–290CrossRefGoogle Scholar
  77. Hirel B, Bertin P, Quilleré I et al (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125:1258–1270. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Hirel B, Le Gouis J, Ney B et al (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387CrossRefPubMedGoogle Scholar
  79. Hoshida H, Tanaka Y, Hibino T et al (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43:103–111CrossRefPubMedGoogle Scholar
  80. Hossain MA, Uddin MK, Ismail MR et al (2012) Responses of glutamine Synthetase-glutamate synthase cycle enzymes in tomato leaves under salinity stress. Int J Agric Biol 14:509–515Google Scholar
  81. Huang QM, Liu WH, Sun H et al (2005) Agrobacterium tumefaciens mediated transgenic wheat plants with glutamine synthetases confer tolerance to herbicide. J Plant Ecol 29:338–344. (in Chinese)CrossRefGoogle Scholar
  82. Ishida Y, Hiyoshi T, Sano M et al (1989) Selection and characterization of a herbicide-tolerant cell line of tobacco (Nicotiana tabacum L.). Plant Sci 63:227–235. CrossRefGoogle Scholar
  83. Ishida H, Anzawa D, Kokubun N et al (2002) Direct evidence for non-enzymatic fragmentation of chloroplastic glutamine synthetase by a reactive oxygen species. Plant Cell Environ 25:625–631. CrossRefGoogle Scholar
  84. Ishiyama K, Inoue E, Watanabe-Takahashi A et al (2004a) Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. J Biol Chem 279:16598–16605CrossRefPubMedGoogle Scholar
  85. Ishiyama K, Inoue E, Tabuchi M et al (2004b) Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol 45:1640–1647CrossRefPubMedGoogle Scholar
  86. Jalaludin A, Ngim J, Bakar BHJ et al (2010) Preliminary findings of potentially resistant goosegrass (Eleusine indica) to glufosinate-ammonium in Malaysia. Weed Biol Manag 10:256–260. CrossRefGoogle Scholar
  87. Ji Y (2011) The role of cytosolic glutamine synthetases in abiotic stress and development in Arabidopsis thaliana. Dissertation, University of SaskatchewanGoogle Scholar
  88. Jing ZP, Gallardo F, Pascual MB et al (2004) Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytol 164:137–145CrossRefGoogle Scholar
  89. Kamachi K, Yamaya T, Mae T et al (1991) A role for glutamine Synthetase in the remobilization of leaf nitrogen during natural senescence in Rice leaves. Plant Physiol 96:411–417. CrossRefPubMedPubMedCentralGoogle Scholar
  90. Kamachi K, Yamaya T, Hayakawa T et al (1992) Changes in cytosolic glutamine Synthetase polypeptide and its mRNA in a leaf blade of Rice plants during natural senescence. Plant Physiol 98:1323–1329. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Kaminski KP, Kørup K, Andersen MN et al (2015) Cytosolic glutamine synthetase is important for photosynthetic efficiency and water use efficiency in potato as revealed by high-throughput sequencing QTL analysis. Theor Appl Genet 128:2143–2153. CrossRefPubMedPubMedCentralGoogle Scholar
  92. Kant S, Bi YM, Weretilnyk E et al (2008) The Arabidopsis halophytic relative Thellungiella halophila tolerates nitrogen-limiting conditions by maintaining growth, nitrogen uptake, and assimilation. Plant Physiol 147:1168–1180CrossRefPubMedPubMedCentralGoogle Scholar
  93. Keys AJ, Bird IF, Cornelius MJ et al (1978) Photorespiratory nitrogen cycle. Nature 275:741–743CrossRefGoogle Scholar
  94. Kichey T, Heumez E, Pocholle D et al (2006) Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytol 169:265–278. CrossRefPubMedGoogle Scholar
  95. Kondo Y, Shomura T, Ogawa Y et al (1973) Isolation and physicochemical and biological characterization of SF-1293 substances. Sci Rep Meiji Seika Kaisha 13:34–43Google Scholar
  96. Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun 4:1617. CrossRefPubMedGoogle Scholar
  97. Konishi N, Ishiyama K, Beier MP et al (2016) Contributions of two cytosolic glutamine synthetase isozymes to ammonium assimilation in Arabidopsis roots. J Exp Bot 19:erw454. CrossRefGoogle Scholar
  98. Kozaki A, Takeba G (1996) Photorespiration protects C 3 plants from photooxidation. Nature 384:557–560. CrossRefGoogle Scholar
  99. Krajewski WW, Jones TA, Mowbray SL (2005) Structure of mycobacterium tuberculosis glutamine synthetase in complex with a transition-state mimic provides functional insights. Proc Natl Acad Sci U S A 102:10499–10504. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Krajewski WW, Collins R, Holmberg-Schiavone L et al (2008) Crystal structures of mammalian glutamine Synthetases illustrate substrate-induced conformational changes and provide opportunities for drug and herbicide design. J Mol Biol 375:217–228. CrossRefPubMedGoogle Scholar
  101. Kumada Y, Benson DR, Hillemann D et al (1993) Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes. Proc Natl Acad Sci U S A 90:3009–3013CrossRefPubMedPubMedCentralGoogle Scholar
  102. Kusano M, Tabuchi M, Fukushima A, Funayama K, Diaz C, Kobayashi M, Hayashi N, Tsuchiya YN, Takahashi H, Kamata A, et al (2011) Metabolomics data reveal a crucial role of cytosolic glutamine synthetase 1;1 in coordinating metabolic balance in rice. Plant J 66: 456–466CrossRefPubMedGoogle Scholar
  103. Kwinta J, Cal K (2005) Effects of salinity stress on the activity of glutamine synthetase and glutamate dehydrogenase in triticale seedlings. Pol J Environ Stud 14:125–130Google Scholar
  104. Kwon SJ, Kwon SI, Bae MS et al (2007) Role of the methionine sulfoxide reductase MsrB3 in cold acclimation in Arabidopsis. Plant Cell Physiol 48:1713–1723. CrossRefPubMedGoogle Scholar
  105. Lam HM, Coschigano K, Schultz C et al (1995) Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. Plant Cell 7:887. CrossRefPubMedPubMedCentralGoogle Scholar
  106. Lancien M, Gadal P, Hodges M (2000) Update on biochemistry enzyme redundancy and the importance of 2-Oxoglutarate in higher plant ammonium assimilation. Plant Physiol 123:817–824. CrossRefPubMedPubMedCentralGoogle Scholar
  107. Larher F, Aziz A, Deleu C et al (1998) Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines. Physiol Plant 102:139–147. CrossRefGoogle Scholar
  108. Lee HJ, Abdula SE, Jang DW et al (2013) Overexpression of the glutamine synthetase gene modulates oxidative stress response in rice after exposure to cadmium stress. Plant Cell Rep 32:1521–1529. CrossRefPubMedGoogle Scholar
  109. Leegood RC, Lea PJ, Adcock MD et al (1995) The regulation and control of photorespiration. J Exp Bot 46:1397–1414CrossRefGoogle Scholar
  110. Li M, Villemur R, Hussey PJ et al (1993) Differential expression of six glutamine synthetase genes in Zea mays. Plant Mol Biol 23:401–407. CrossRefPubMedGoogle Scholar
  111. Li RJ, Hua W, Lu YT (2006) Arabidopsis cytosolic glutamine synthetase AtGLN1;1 is a potential substrate of AtCRK3 involved in leaf senescence. Biochem Biophys Res Commun 342:119–126. CrossRefPubMedGoogle Scholar
  112. Lima L, Seabra A, Melo P et al (2006a) Phosphorylation and subsequent interaction with 14-3-3 proteins regulate plastid glutamine synthetase in Medicago truncatula. Planta 223:558–567. CrossRefPubMedGoogle Scholar
  113. Lima L, Seabra A, Melo P et al (2006b) Post-translational regulation of cytosolic glutamine synthetase of Medicago truncatula. J Exp Bot 57:2751–2761. CrossRefPubMedGoogle Scholar
  114. Limami A, Phillipson B, Ameziane R et al (1999) Does root glutamine synthetase control plant biomass production in Lotus japonicus L.? Planta 209:495–502. CrossRefPubMedGoogle Scholar
  115. Lothier J, Gaufichon L, Sormani R et al (2011) The cytosolic glutamine synthetase GLN1;2 plays a role in the control of plant growth and ammonium homeostasis in Arabidopsis rosettes when nitrate supply is not limiting. J Exp Bot 62:1375–1390. CrossRefPubMedGoogle Scholar
  116. Loudet O, Chaillou S, Merigout P et al (2003) Quantitative trait loci analysis of nitrogen use efficiency in Arabidopsis. Plant Physiol 131:345–358. CrossRefPubMedPubMedCentralGoogle Scholar
  117. Lu B, Yuan Y, Zhang C et al (2005) Modulation of key enzymes involved in ammonium assimilation and carbon metabolism by low temperature in rice (Oryza sativa L.) roots. Plant Sci 169:295–302. CrossRefGoogle Scholar
  118. Lutts S, Majerus V, Kinet J-M (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105:450–458. CrossRefGoogle Scholar
  119. Man HM, Boriel R, El-Khatib R et al (2005) Characterization of transgenic poplar with ectopic expression of pine cytosolic glutamine synthetase under conditions of varying nitrogen availability. New Phytol 167:31–39. CrossRefPubMedGoogle Scholar
  120. Manderscheid R, Wild A (1986) Studies on the mechanism of inhibition of phosphinothricin of glutamine synthetase isolated from Triticum aestivum L. J Plant Physiol 123:135–142. CrossRefGoogle Scholar
  121. Mann AF, Femten PA, Stewart GR (1979) Identification of two forms of glutamine synthetase in barley (Hordeum vulgare L.). Biochem Biophys Res Comm 88:515–521CrossRefPubMedGoogle Scholar
  122. Marchive C, Roudier F, Castaings L et al (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4:1713. CrossRefPubMedGoogle Scholar
  123. Martin A, Lee J, Kichey T et al (2006) Two cytosolic glutamine Synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274. CrossRefPubMedPubMedCentralGoogle Scholar
  124. Martinelli T, Whittaker A, Bochicchio A et al (2007) Amino acid pattern and glutamate metabolism during dehydration stress in the “resurrection” plant Sporobolus stapfianus: a comparison between desiccation-sensitive and desiccation-tolerant leaves. J Exp Bot 58:3037–3046. CrossRefPubMedGoogle Scholar
  125. Masclaux-Daubresse C, Carrayol E, Valadier MH (2005) The two nitrogen mobilisation- and senescence-associated GS1 and GDH genes are controlled by C and N metabolites. Planta 221:580–588. CrossRefPubMedGoogle Scholar
  126. Masumoto C, Miyazawa S-I, Ohkawa H et al (2010) Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc Natl Acad Sci U S A 107:5226–5231. CrossRefPubMedPubMedCentralGoogle Scholar
  127. Mathis R, Gamas P, Meyer Y, Cullimore JV (2000) The presence of GSI-like genes in higher plants: support for the paralogous evolution of GSI and GSII genes. J Mol Evol 50:116–122CrossRefPubMedGoogle Scholar
  128. McNally SF, Hirel B, Gadal P et al (1983) Evidence for a specific isoform content related to their possible physiological role and their compartmentation within the leaf. Plant Physiol 72:22–25CrossRefPubMedPubMedCentralGoogle Scholar
  129. McParland RH, Guevara JG, Becker RR et al (1976) The purification and properties of the glutamine synthetase from the cytosol of Soyabean root nodules. Biochem J 153:597–606CrossRefPubMedPubMedCentralGoogle Scholar
  130. Miflin BJ, Habash DZ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53:979–987CrossRefPubMedGoogle Scholar
  131. Migge A, Carrayol E, Hirel B, Becker TW (2000) Leaf-specific overexpression of plastidic glutamine synthetase stimulates the growth of transgenic tobacco seedlings. Planta 210:252–260. CrossRefPubMedGoogle Scholar
  132. Miki B, Abdeen A, Manabe Y, MacDonald P (2009) Selectable marker genes and unintended changes to the plant transcriptome. Plant Biotechnol J 7:211–218. CrossRefPubMedGoogle Scholar
  133. Molina-Rueda JJ, Kirby EG (2015) Transgenic poplar expressing the pine GS1a show alterations in nitrogen homeostasis during drought. Plant Physiol Biochem 94:181–190CrossRefPubMedGoogle Scholar
  134. Molina-Rueda JJ, Tsai CJ, Kirby EG (2013) The Populus superoxide dismutase gene family and its responses to drought stress in transgenic poplar overexpressing a pine cytosolic glutamine Synthetase (GS1a). PLoS One 8:e56421CrossRefPubMedPubMedCentralGoogle Scholar
  135. Moorhead G, Douglas P, Cotelle V et al (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J 18:1–12. CrossRefPubMedGoogle Scholar
  136. Mulvaney RL, Khan SA, Ellsworth TR (2009) Synthetic nitrogen fertilizers deplete soil nitrogen: a global dilemma for sustainable cereal production. J Environ Qual 38:2295–2314CrossRefPubMedGoogle Scholar
  137. Nagy Z, Nemeth E, Guoth A et al (2013) Metabolic indicators of drought stress tolerance in wheat: glutamine synthetase isoenzymes and Rubisco. Plant Physiol Biochem 67:48–54. CrossRefPubMedGoogle Scholar
  138. Nigro D, Fortunato S, Giove SL, Paradiso A, Gu YQ, Blanco A, de Pinto MC, Gadaleta A (2016) Glutamine synthetase in Durum Wheat: Genotypic Variation and Relationship with Grain Protein Content. Front Plant Sci 7: 971Google Scholar
  139. Nogueira EM, Olivares FL, Japiassu JC et al (2005) Characterization of glutamine synthetase genes in sugarcane genotypes with different rates of biological nitrogen fixation. Plant Sci 169:14CrossRefGoogle Scholar
  140. O’Neal TD, Joy KW (1973) Glutamine synthetase of pea leaves: purification, stabilization and pH optima. Arch Biochem Biophys 159:113–122CrossRefPubMedGoogle Scholar
  141. Obara M, Kajiura M, Fukuta Y et al (2001) Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). J Exp Bot 52:1209–1217PubMedGoogle Scholar
  142. Obara M, Sato T, Sasaki S et al (2004) Identification and characterization of a QTL on chromosome2 for cytosolic glutamine synthetase content and panicle number in rice. Theor Appl Genet 110:1–11. CrossRefPubMedGoogle Scholar
  143. Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35:415–442. CrossRefGoogle Scholar
  144. Ohashi M, Ishiyama K, Kusano M et al (2015) Lack of cytosolic glutamine synthetase1;2 in vascular tissues of axillary buds causes severe reduction in their outgrowth and disorder of metabolic balance in rice seedlings. Plant J 81:347–356. CrossRefPubMedGoogle Scholar
  145. Oliveira IC, Brears T, Knight TJ et al (2002) Overexpression of cytosolic glutamine synthetase: relation to nitrogen, light, and photorespiration. Plant Physiol 129:1170–1180. CrossRefPubMedPubMedCentralGoogle Scholar
  146. Orsel M, Moison M, Clouet V et al (2014) Sixteen cytosolic glutamine synthetase genes identified in the Brassica napus L. genome are differentially regulated depending on nitrogen regimes and leaf senescence. J Exp Bot 65:3927–3947. CrossRefPubMedPubMedCentralGoogle Scholar
  147. Ortega JL, Roche D, Sengupta-Gopalan C (1999) Oxidative turnover of soybean root glutamine synthetase. In vitro and in vivo studies. Plant Physiol 119:1483–1496. CrossRefPubMedPubMedCentralGoogle Scholar
  148. Ortega JL, Temple SJ, Sengupta-Gopalan C (2001) Constitutive overexpression of cytosolic glutamine synthetase (GS1) gene in transgenic alfalfa demonstrates that GS1 may be regulated at the level of RNA stability and protein turnover. Plant Physiol 126:109–121. CrossRefPubMedPubMedCentralGoogle Scholar
  149. Ortega JL, Moguel-Esponda S, Potenza C et al (2006) The 3′ untranslated region of a soybean cytosolic glutamine synthetase (GS1) affects transcript stability and protein accumulation in transgenic alfalfa. Plant J 45:832–846. CrossRefPubMedGoogle Scholar
  150. Ortega JL, Wilson OL, Sengupta-Gopalan C (2012) The 5′ untranslated region of the soybean cytosolic glutamine synthetase β1 gene contains prokaryotic translation initiation signals and acts as a translational enhancer in plants. Mol Gen Genomics 287:881–893. CrossRefGoogle Scholar
  151. Osanai T, Kuwahara A, Otsuki H et al (2017) ACR11 is an activator of plastid-type glutamine Synthetase GS2 in Arabidopsis thaliana. Plant Cell Physiol 6:29668. CrossRefGoogle Scholar
  152. Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46:1351–1362. CrossRefGoogle Scholar
  153. Ouyang B, Yang T, Li H et al (2007) Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J Exp Bot 58:507–520. CrossRefPubMedGoogle Scholar
  154. Palatnik JF, Carrillo N, Valle EM (1999) The role of photosynthetic electron transport in the oxidative degradation of Chloroplastic glutamine Synthetase. Plant Physiol 121:471–478CrossRefPubMedPubMedCentralGoogle Scholar
  155. Pascual MB, Jing ZP, Kirby EG et al (2008) Response of transgenic poplar overexpressing cytosolic glutamine synthetase to phosphinothricin. Phytochemistry 69:382–389. CrossRefPubMedGoogle Scholar
  156. Pesole G, Bozzettit MP, Lanave C et al (1991) Glutamine synthetase gene evolution: a good molecular clock. Proc Natl Acad Sci U S A 88:522–526CrossRefPubMedPubMedCentralGoogle Scholar
  157. Pornprom T, Pengnual A, Udomprasert N et al (2008) The role of altered glutamine Synthetase in conferring resistance to Glufosinate in Mungbean cell selections. Thai J Agric Sci 41:3–4Google Scholar
  158. Pornprom T, Prodmatee N, Chatchawankanphanich O (2009) Glutamine synthetase mutation conferring target-site-based resistance to glufosinate in soybean cell selections. Pest Manag Sci 65:216–222. CrossRefPubMedGoogle Scholar
  159. Que Q, Chilton M-DM, de Fontes CM et al (2010) Trait stacking in transgenic crops: challenges and opportunities. GM Crops 1:220–229. CrossRefPubMedGoogle Scholar
  160. Quraishi UM, Abrouk M, Murat F et al (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J 65:745–756. CrossRefPubMedGoogle Scholar
  161. Ramanjulu S, Veeranjaneyulu K, Sudhakar C (1994) Short-term shifts in nitrogen metabolism in mulberry Morus alba under salt shock. Phytochemistry 37:991–995. CrossRefGoogle Scholar
  162. Rana NK, Mohanpuria P, Yadav SK (2008) Cloning and characterization of a cytosolic glutamine synthetase from Camellia sinensis (L.) O. Kuntze that is upregulated by ABA, SA, and H2O2. Mol Biotechnol 39:49–56. CrossRefPubMedGoogle Scholar
  163. Reyes JC, Florencio FJ (1994) A new type of glutamine synthetase in cyanobacteria: the protein encoded by the glnN gene supports nitrogen assimilation in Synechocystis sp. strain PCC 6803. J Bacteriol 176:1260–1267. CrossRefPubMedPubMedCentralGoogle Scholar
  164. Riedel J, Tischner R, Mäck G (2001) The chloroplastic glutamine synthetase (GS-2) of tobacco is phosphorylated and associated with 14-3-3 proteins inside the chloroplast. Planta 213:396–401. CrossRefPubMedGoogle Scholar
  165. Ronzio RA, Meister A (1968) Phosphorylation of methionine sulfoximine by glutamine synthetase. Proc Natl Acad Sci USA 59:164–170CrossRefPubMedGoogle Scholar
  166. Rueda-López M, Crespillo R, Cánovas FM et al (2008) Differential regulation of two glutamine synthetase genes by a single Dof transcription factor. Plant J 56:73–85. CrossRefPubMedGoogle Scholar
  167. Sahu AC, Sahoo SK, Sahoo N (2001) NaCl-stress induced alteration in glutamine synthetase activity in excised senescing leaves of a salt-sensitive and a salt-tolerant rice cultivar in light and darkness. Plant Growth Regul 34:287–292. CrossRefGoogle Scholar
  168. Santos C, Pereira A, Pereira S et al (2004) Regulation of glutamine synthetase expression in sunflower cells exposed to salt and osmotic stress. Sci Hortic (Amsterdam) 103:101–111. CrossRefGoogle Scholar
  169. Schjoerring JK (2005) EU Research Project SUSTAIN: Developing Wheat with Enhanced Nitrogen Use Efficiency Towards a Sustainable System of Production, QLK5-CT-2001-01461, CORDIS
  170. Seabra AR, Carvalho HG (2015) Glutamine synthetase in Medicago truncatula, unveiling new secrets of a very old enzyme. Front Plant Sci 6:578. CrossRefPubMedPubMedCentralGoogle Scholar
  171. Seabra AR, Carvalho H, Pereira PJB (2009) Crystallization and preliminary crystallographic characterization of glutamine synthetase from Medicago truncatula. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:1309–1312. CrossRefPubMedPubMedCentralGoogle Scholar
  172. Seabra AR, Vieira CP, Cullimore JV, Carvalho HG (2010) Medicago truncatula contains a second gene encoding a plastid located glutamine synthetase exclusively expressed in developing seeds. BMC Plant Biol 10:183. CrossRefPubMedPubMedCentralGoogle Scholar
  173. See D, Kanazin V, Kephart K, Blake T (2002) Mapping genes controlling variation in barley grain protein concentration. Crop Sci 42:680–685. CrossRefGoogle Scholar
  174. Seger M, Ortega JL, Bagga S et al (2009) Repercussion of mesophyll-specific overexpression of a soybean cytosolic glutamine synthetase gene in alfalfa (Medicago sativa L.) and tobacco (Nicotiana tabacum L.). Plant Sci 176:119–129. CrossRefPubMedPubMedCentralGoogle Scholar
  175. Seger M, Gebril S, Tabilona J et al (2014) Impact of concurrent overexpression of cytosolic glutamine synthetase (GS1) and sucrose phosphate synthase (SPS) on growth and development in transgenic tobacco. Planta 241:69–81. CrossRefPubMedGoogle Scholar
  176. Shrawat AK, Carroll RT, DePauw M et al (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732. CrossRefPubMedGoogle Scholar
  177. Silva LS, Seabra AR, Leitão JN, Carvalho HG (2015) Possible role of glutamine synthetase of the prokaryotic type (GSI-like) in nitrogen signaling in Medicago truncatula. Plant Sci 240:98–108. CrossRefPubMedGoogle Scholar
  178. Silveira JAG, Melo AR, Viégas R, Oliveira JT (2001) Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. Environ Exp Bot 46:171–179. CrossRefGoogle Scholar
  179. Silveira JAG, Viégas R, da Rocha IMA et al (2003) Proline accumulation and glutamine synthetase activity are increased by salt-induced proteolysis in cashew leaves. J Plant Physiol 160:115–123. CrossRefPubMedGoogle Scholar
  180. Simon B, Sengupta-Gopalan C (2010) The 3′ untranslated region of the two cytosolic glutamine synthetase (GS1) genes in alfalfa (Medicago sativa) regulates transcript stability in response to glutamine. Planta 232:1151–1162. CrossRefPubMedGoogle Scholar
  181. Simons M, Saha R, Amiour N et al (2014) Assessing the metabolic impact of nitrogen availability using a compartmentalized maize leaf genome-scale model. Plant Physiol 166:1659–1674. CrossRefPubMedPubMedCentralGoogle Scholar
  182. Singh KK, Ghosh S (2013) Regulation of glutamine synthetase isoforms in two differentially drought-tolerant rice (Oryza sativa L.) cultivars under water deficit conditions. Plant Cell Rep 32:183–193. CrossRefPubMedGoogle Scholar
  183. Socolow R (1999) Nitrogen management and the future of food: lessons from the management of energy and carbon. Proc Natl Acad Sci U S A 96:6001–6008CrossRefPubMedPubMedCentralGoogle Scholar
  184. Strauch E, Wohlleben W, Pühler A et al (1988) Cloning of a phosphinothricin N-acetyltransferase gene from Streptomyces viridochromogenes Tü494 and its expression in Streptomyces lividans and Escherichia coli. Gene 63:65–74CrossRefPubMedGoogle Scholar
  185. Su J, Zhang X, Yan Q et al (1995) Construction of plant expression vectors carrying glnA gene encoding glutamine synthetase and regeneration of transgenic rice plants. Sci China B 38:963–970Google Scholar
  186. Suárez R, Márquez J, Shishkova S et al (2003) Overexpression of alfalfa cytosolic glutamine synthetase in nodules and flowers of transgenic Lotus japonicus plants. Physiol Plant 117:326–336. CrossRefPubMedGoogle Scholar
  187. Sun H, Huang Q-M, Su J (2005a) Highly effective expression of glutamine synthetase genes GS1 and GS2 in transgenic rice plants increases nitrogen-deficiency tolerance. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 31:492–498. (in Chinese)PubMedGoogle Scholar
  188. Sun H, Huang QM, Su J (2005b) Overexpression of glutamine synthetases confers transgenic rice herbicide resistance. High Technol Lett 11:75–79. (in Chinese)Google Scholar
  189. Sun H, Qian Q, Wu K et al (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656. CrossRefPubMedGoogle Scholar
  190. Sun Y, Zhang X, Wu C et al (2016) Engineering herbicide-resistant Rice plants through CRISPR/Cas9-mediated homologous recombination of Acetolactate synthase. Mol Plant 9:628–631CrossRefPubMedGoogle Scholar
  191. Suzuki N, Rivero RM, Shulaev V et al (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43. CrossRefPubMedPubMedCentralGoogle Scholar
  192. Swarbreck SM, Defoin-Platel M, Hindle M et al (2011) New perspectives on glutamine synthetase in grasses. J Exp Bot 62:1511–1522. CrossRefPubMedGoogle Scholar
  193. Tabuchi M, Sugiyama K, Ishiyama K et al (2005) Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant J 42:641–651CrossRefPubMedGoogle Scholar
  194. Tabuchi M, Abiko T, Yamaya T (2007) Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). J Exp Bot 58:2319–2327CrossRefPubMedGoogle Scholar
  195. Tachibana K, Watanabe T, Sekizawa Y, Takematsu T (1986) Accumulation of ammonia in plants treated with bialaphos. J Pestic Sci 11:33–37. CrossRefGoogle Scholar
  196. Taira M et al (2004) Arabidopsis thaliana GLN2-encoded glutamine Synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16:2048–2058. CrossRefPubMedPubMedCentralGoogle Scholar
  197. Teixeira J, Fidalgo F (2009) Salt stress affects glutamine synthetase activity and mRNA accumulation on potato plants in an organ-dependent manner. Plant Physiol Biochem 47:807–813. CrossRefPubMedGoogle Scholar
  198. Teixeira J, Pereira S (2007) High salinity and drought act on an organ-dependent manner on potato glutamine synthetase expression and accumulation. Environ Exp Bot 60:121–126. CrossRefGoogle Scholar
  199. Temple SJ, Knight TJ, Unkefer PJ et al (1993) Modulation of glutamine synthetase gene expression in tobacco by the introduction of an alfalfa glutamine synthetase gene in sense and antisense orientation: molecular and biochemical analysis. Mol Gen Genet 236:315–325CrossRefPubMedGoogle Scholar
  200. Temple SJ, Bagga S, Sengupta-Gopalan C (1994) Can glutamine synthetase activity be modulated in transgenic plants by the use of recombinant DNA technology? Biochem Soc Trans 22:915–920CrossRefPubMedGoogle Scholar
  201. Temple SJ, Bagga S, Sengupta-Gopalan C (1998) Down regulation of specific members of the glutamine synthetase gene family in alfalfa by antisense RNA technology. Plant Mol Biol 37:535–547CrossRefPubMedGoogle Scholar
  202. Thompson CJ, Moval NR, Tizard R et al (1987) Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J 6:2519–2523. CrossRefPubMedPubMedCentralGoogle Scholar
  203. Thomsen HC, Eriksson D, Møller IS et al (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19:656–663. CrossRefPubMedGoogle Scholar
  204. Tian Y-S, Xu J, Zhao W et al (2015) Identification of a phosphinothricin-resistant mutant of rice glutamine synthetase using DNA shuffling. Sci Rep 5:15495. CrossRefPubMedPubMedCentralGoogle Scholar
  205. Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium assimilation in rice and barley. J Exp Bot 52:591–604. CrossRefPubMedGoogle Scholar
  206. Torreira E, Seabra AR, Marriott H et al (2014) The structures of cytosolic and plastid-located glutamine synthetases from Medicago truncatula reveal a common and dynamic architecture. Acta Crystallogr Sect D Biol Crystallogr 70:981–993. CrossRefGoogle Scholar
  207. Uhrig RG, Ng KKS, Moorhead GBG (2009) PII in higher plants: a modern role for an ancient protein. Trends Plant Sci 14:505–511CrossRefPubMedGoogle Scholar
  208. Unno H, Uchida T, Sugawara H et al (2006) Atomic structure of plant glutamine Synthetase: a key enzyme for plant productivity. J Biol Chem 281:287–296. CrossRefGoogle Scholar
  209. Urriola J, Rathore KS (2015) Overexpression of a glutamine synthetase gene affects growth and development in sorghum. Transgenic Res 24:397–407. CrossRefPubMedGoogle Scholar
  210. Van Rooyen JM, Abratt VR, Belrhali H et al (2011) Crystal structure of type III glutamine Synthetase: surprising reversal of the inter-ring Interface. Structure 19:471–483. CrossRefPubMedGoogle Scholar
  211. Veeranagamallaiah G, Chandraobulreddy P, Jyothsnakumari G et al (2007) Glutamine synthetase expression and pyrroline-5-carboxylate reductase activity influence proline accumulation in two cultivars of foxtail millet (Setaria italica L.) with differential salt sensitivity. Environ Exp Bot 60:239–244. CrossRefGoogle Scholar
  212. Vincent R, Fraisier V, Chaillou S et al (1997) Overexpression of a soybean gene encoding glutamine synthetase in shoots of transgenic Lotus corniculatus L. plants triggers changes in ammonium assimilation and plant development. Planta 201:424–433CrossRefPubMedGoogle Scholar
  213. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132CrossRefPubMedGoogle Scholar
  214. Wallsgrove RM, Turner JC, Hall NP et al (1987) Barley mutants lacking chloroplast glutamine synthetase - biochemical and genetic analysis. Plant Physiol 83:155–158CrossRefPubMedPubMedCentralGoogle Scholar
  215. Wang ZQ, Yuan YZ, Ou JQ et al (2007) Glutamine synthetase and glutamate dehydrogenase contribute differentially to proline accumulation in leaves of wheat (Triticum aestivum) seedlings exposed to different salinity. J Plant Physiol 164:695–701. CrossRefPubMedGoogle Scholar
  216. Wang H, Zhang M, Guo R et al (2012) Effects of salt stress on ion balance and nitrogen metabolism of old and young leaves in rice (Oryza sativa L.). BMC Plant Biol 12:194. CrossRefPubMedPubMedCentralGoogle Scholar
  217. Wang Y, Fu B, Pan L et al (2013) Overexpression of Arabidopsis Dof1, GS1 and GS2 enhanced nitrogen assimilation in transgenic tobacco grown under low-nitrogen conditions. Plant Mol Biol Report 31:886–900. CrossRefGoogle Scholar
  218. Wang X, Wei Y, Shi L et al (2015) New isoforms and assembly of glutamine synthetase in the leaf of wheat (Triticum aestivum L.). J Exp Bot 66:6827–6834. CrossRefPubMedPubMedCentralGoogle Scholar
  219. Watanabe A, Takagi N, Hayashi H et al (1997) Internal Gln/Glu ratio as a potential regulatory parameter for the expression of a cytosolic glutamine Synthetase gene of radish in cultured cells. Plant Cell Physiol 38:1000–1026. CrossRefGoogle Scholar
  220. Wild A, Manderscheid R (1984) The effect of phosphinothricin on the assimilation of ammonia in plants. Z Naturforsch Sect C Biosci 39:500–504. CrossRefGoogle Scholar
  221. Willekens H, Chamnongpol S, Davey M et al (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816. CrossRefPubMedPubMedCentralGoogle Scholar
  222. Wingler A, Quick WP, Bungard RA et al (1999) The role of photorespiration during drought stress: an analysis utilizing barley mutants with reduced activities of photorespiratory enzymes. Plant Cell Environ 22:361–373. CrossRefGoogle Scholar
  223. Wingler A, Lea PJ, Quick WP et al (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond Ser B Biol Sci 355:1517–1529. CrossRefGoogle Scholar
  224. Woods DR, Reid SJ (1993) Recent developments on the regulation and structure of glutamine synthetase enzymes from selected bacterial groups. FEMS Microbiol Rev 11: 273–283CrossRefPubMedGoogle Scholar
  225. Wray LV, Fisher SH (2010) Functional roles of the conserved Glu304 loop of Bacillus subtilis glutamine synthetase. J Bacteriol 192:5018–5025. CrossRefPubMedPubMedCentralGoogle Scholar
  226. Yamaya T, Obara M, Nakajima H et al (2002) Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. J Exp Bot 53:917–925. CrossRefPubMedGoogle Scholar
  227. Yan S, Tang Z, Su W et al (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244. CrossRefPubMedGoogle Scholar
  228. Yanagisawa S, Akiyama A, Kisaka H et al (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci U S A 101:7833–7838. CrossRefPubMedPubMedCentralGoogle Scholar
  229. Yousfi S, Márquez AJ, Betti M et al (2015) Gene expression and physiological responses to salinity and water stress of contrasting durum wheat genotypes. J Integr Plant Biol 58:48–66CrossRefPubMedGoogle Scholar
  230. Yu LH, Wu J, Tang H et al (2016) Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation. Sci Rep 6:27795. CrossRefPubMedPubMedCentralGoogle Scholar
  231. Zhu C, Fan Q, Wang W et al (2014) Characterization of a glutamine synthetase gene DvGS2 from Dunaliella viridis and biochemical identification of DvGS2-transgenic Arabidopsis thaliana. Gene 536:407–415. CrossRefPubMedGoogle Scholar
  232. Zhu C, Zhang G, Shen C et al (2015) Expression of bacterial glutamine synthetase gene in Arabidopsis thaliana increases the plant biomass and level of nitrogen utilization. Biologia 70:1586–1596. CrossRefGoogle Scholar
  233. Zozaya-Hinchliffe M, Potenza C, Ortega JL et al (2005) Nitrogen and metabolic regulation of the expression of plastidic glutamine synthetase in alfalfa (Medicago sativa). Plant Sci 168:1041–1052. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Donald James
    • 1
  • Bhabesh Borphukan
    • 1
  • Dhirendra Fartyal
    • 1
  • V. M. M. Achary
    • 1
  • M. K. Reddy
    • 1
    Email author
  1. 1.International Centre for Genetic Engineering and BiotechnologyNew DelhiIndia

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