Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency?

Robertson, 2009, Nitrogen in agriculture: balancing the cost of an essential resource, Annu. Rev. Environ. Resour., 34, 97, 10.1146/annurev.environ.032108.105046 McAllister, 2012, Engineering nitrogen use efficient crop plants: the current status, Plant Biotechnol. J., 10, 1011, 10.1111/j.1467-7652.2012.00700.x Good, 2004, Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production?, Trends Plant Sci., 9, 597, 10.1016/j.tplants.2004.10.008 McNally, 1983, Glutamine synthetases of higher-plants – evidence for a specific isoform content related to their possible physiological role and their compartmentation within the leaf, Plant Physiol., 72, 22, 10.1104/pp.72.1.22 Tobin, 1985, Changes in the activities of chloroplast and cytosolic isoenzymes of glutamine-synthetase during normal leaf growth and plastid development in wheat, Planta, 163, 544, 10.1007/BF00392711 Edwards, 1990, Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetase, Proc. Natl. Acad. Sci. U.S.A., 87, 3459, 10.1073/pnas.87.9.3459 Swarbreck, 2011, New perspectives on glutamine synthetase in grasses, J. Exp. Bot., 62, 1511, 10.1093/jxb/erq356 Wallsgrove, 1987, Barley mutants lacking chloroplast glutamine synthetase – biochemical and genetic analysis, Plant Physiol., 83, 155, 10.1104/pp.83.1.155 Bernard, 2008, Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.), Plant Mol. Biol., 67, 89, 10.1007/s11103-008-9303-y Ishiyama, 2004, Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis, J. Biol. Chem., 279, 16598, 10.1074/jbc.M313710200 Lothier, 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, 10.1093/jxb/erq299 Ishiyama, 2004, Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots, Plant Cell Physiol., 45, 1640, 10.1093/pcp/pch190 Plett, 2010, Dichotomy in the NRT gene families of dicots and grass species, PLoS ONE, 5, e15289, 10.1371/journal.pone.0015289 Gallais, 2004, An approach to the genetics of nitrogen use efficiency in maize, J. Exp. Bot., 55, 295, 10.1093/jxb/erh006 Obara, 2001, Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.), J. Exp. Bot., 52, 1209 Habash, 2007, The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield, Theor. Appl. Genet., 114, 403, 10.1007/s00122-006-0429-5 Gadaleta, 2014, Isolation and characterisation of cytosolic glutamine synthetase (GSe) genes and association with grain protein content in durum wheat, Crop Pasture Sci., 65, 38, 10.1071/CP13140 Christiansen, 2014, Members of the barley NAC transcription factor gene family show differential co-regulation with senescence-associated genes during senescence of flag leaves, J. Exp. Bot., 10.1093/jxb/eru046 Orsel, 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., 10.1093/jxb/eru041 Kichey, 2005, Changes in the cellular and subcellular localization of glutamine synthetase and glutamate dehydrogenase during flag leaf senescence in wheat (Triticum aestivum L.), Plant Cell Physiol., 46, 964, 10.1093/pcp/pci105 Brugiere, 2000, Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol, Planta, 211, 519, 10.1007/s004250000309 Kamachi, 1992, Changes in cytosolic glutamine-synthetase polypeptide and its messenger-RNA in a leaf blade of rice plants during natural senescence, Plant Physiol., 98, 1323, 10.1104/pp.98.4.1323 Canas, 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, 10.1111/j.1467-7652.2010.00524.x Martin, 2006, Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production, Plant Cell, 18, 3252, 10.1105/tpc.106.042689 Tabuchi, 2005, Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1, Plant J., 42, 641, 10.1111/j.1365-313X.2005.02406.x Kusano, 2011, Metabolomics data reveal a crucial role of cytosolic glutamine synthetase 1;1 in coordinating metabolic balance in rice, Plant J., 66, 456, 10.1111/j.1365-313X.2011.04506.x Funayama, 2013, Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots, Plant Cell Physiol., 54, 934, 10.1093/pcp/pct046 Yamaya, 2014, Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice, J. Exp. Bot., 10.1093/jxb/eru103 Habash, 2001, The role of cytosolic glutamine synthetase in wheat, Ann. Appl. Biol., 138, 83, 10.1111/j.1744-7348.2001.tb00087.x Fuentes, 2001, Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations, J. Exp. Bot., 52, 1071, 10.1093/jexbot/52.358.1071 Oliveira, 2002, Overexpression of cytosolic glutamine synthetase Relation to nitrogen, light, and photorespiration, Plant Physiol., 129, 1170, 10.1104/pp.020013 Ortega, 2004, Biochemical and molecular characterization of transgenic Lotus japonicus plants constitutively over-expressing a cytosolic glutamine synthetase gene, Planta, 219, 807, 10.1007/s00425-004-1292-8 Fei, 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, 10.1016/j.plaphy.2006.09.007 Fei, 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, 10.1007/s00425-002-0873-7 Vincent, 1997, Overexpression of a soybean gene encoding cytosolic glutamine synthetase in shoots of transgenic Lotus corniculatus L plants triggers changes in ammonium assimilation and plant development, Planta, 201, 424, 10.1007/s004250050085 Man, 2011, Increased glutamine in leaves of poplar transgenic with pine GS1a caused greater anthranilate synthetase alpha-subunit (ASA1) transcript and protein abundances: an auxin-related mechanism for enhanced growth in GS transgenics?, J. Exp. Bot., 62, 4423, 10.1093/jxb/err026 Cai, 2009, Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice, Plant Cell Rep., 28, 527, 10.1007/s00299-008-0665-z Gallardo, 1999, Expression of a conifer glutamine synthetase gene in transgenic poplar, Planta, 210, 19, 10.1007/s004250050649 Brauer, 2011, Reappraisal of nitrogen use efficiency in rice overexpressing glutamine synthetase 1, Physiol. Plant., 141, 361, 10.1111/j.1399-3054.2011.01443.x Stitt, 1999, The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background, Plant Cell Environ., 22, 583, 10.1046/j.1365-3040.1999.00386.x Lawlor, 2002, Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems, J. Exp. Bot., 53, 773, 10.1093/jexbot/53.370.773 Coruzzi, 2001, Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’, Curr. Opin. Plant Biol., 4, 247, 10.1016/S1369-5266(00)00168-0 Schjoerring, 2005 Harper, 2010, Glutamate dehydrogenase and glutamine synthetase are regulated in response to nitrogen availability in Myocbacterium smegmatis, BMC Microbiol., 10, 138, 10.1186/1471-2180-10-138 Ortega, 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, 10.1104/pp.126.1.109 Seger, 2009, Repercussion of mesophyll-specific overexpression of a soybean cytosolic glutamine synthetase gene in alfalfa (Medicago sativa L.) and tobacco (Nicotiana tabaccum L.), Plant Sci., 176, 119, 10.1016/j.plantsci.2008.10.006 Oliveira, 1999, Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis, Plant Physiol., 121, 301, 10.1104/pp.121.1.301 Caputo, 2009, Regulation of glutamine synthetase 1 and amino acids transport in the phloem of young wheat plants, Plant Physiol. Biochem., 47, 335, 10.1016/j.plaphy.2009.01.003 Goodall, 2013, Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.), Plant Cell Physiol., 54, 494, 10.1093/pcp/pct006 El Omari, 2010, Ammonium tolerance and the regulation of two cytosolic glutamine synthetases in the roots of sorghum, Funct. Plant Biol., 37, 55, 10.1071/FP09162 Masclaux-Daubresse, 2005, The two nitrogen mobilisation- and senescence-associated GS1 and GDH genes are controlled by C and N metabolites, Planta, 221, 580, 10.1007/s00425-004-1468-2 Watanabe, 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, 10.1093/oxfordjournals.pcp.a029263 Castro-Rodriguez, 2011, The glutamine synthetase gene family in Populus, BMC Plant Biol., 11, 119, 10.1186/1471-2229-11-119 Gutierez, 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, 10.1073/pnas.0800211105 Gutierrez, 2012, Systems biology for enhanced plant nitrogen nutrition, Science, 336, 1673, 10.1126/science.1217620 El-Kereamy, 2012, The rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism, PLoS ONE, 7, e52030, 10.1371/journal.pone.0052030 Yanagisawa, 2002, The Dof family of plant transcription factors, Trends Plant Sci., 7, 555, 10.1016/S1360-1385(02)02362-2 Kurai, 2011, Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions, Plant Biotechnol. J., 9, 826, 10.1111/j.1467-7652.2011.00592.x Yanagisawa, 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, 10.1073/pnas.0402267101 Marchive, 2013, Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants, Nat. Commun., 4, 1713, 10.1038/ncomms2650 Ortega, 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, 10.1111/j.1365-313X.2005.02644.x Simon, 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, 10.1007/s00425-010-1247-1 Ortega, 2012, The 5′ untranslated region of the soybean cytosolic glutamine synthetase 1 gene contains prokaryotic translation initiation signals and acts as a translational enhancer in plants, Mol. Genet. Genomics, 287, 881, 10.1007/s00438-012-0724-6 Finnemann, 2000, Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction, Plant J., 24, 171, 10.1046/j.1365-313x.2000.00863.x Lima, 2006, Post-translational regulation of cytosolic glutamine synthetase of Medicago truncatula, J. Exp. Bot., 57, 2751, 10.1093/jxb/erl036 Lima, 2006, Phosphorylation and subsequent interaction with 14-3-3 proteins regulate plastid glutamine synthetase in Medicago truncatula, Planta, 223, 558, 10.1007/s00425-005-0097-8 Riedel, 2001, The chloroplastic glutamine synthetase (GS-2) of tobacco is phosphorylated and associated with 14-3-3 proteins inside the chloroplast, Planta, 213, 396, 10.1007/s004250000509 Jiang, 1998, The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state, Biochemistry, 37, 12802, 10.1021/bi980666u Uhrig, 2009, PII in higher plants: a modern role for an ancient protein, Trends Plant Sci., 14, 505, 10.1016/j.tplants.2009.07.003 Ortega, 1997, Constitutive over expression of cytosolic glutamine synthetase gene in alfalfa is not accompanied by an increase in GS(1) protein and activity, Plant Physiol., 114, 210 Ortega, 1999, Oxidative turnover of soybean root glutamine synthetase In vitro and in vivo studies, Plant Physiol., 119, 1483, 10.1104/pp.119.4.1483 Melo, 2011, Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration, Plant Physiol., 157, 1505, 10.1104/pp.111.186056 Lea, 2003, Glutamate synthase and the synthesis of glutamate in plants, Plant Physiol. Biochem., 41, 555, 10.1016/S0981-9428(03)00060-3 Wang, 2013, Overexpression of Arabidopsis Dof1 GS1 and GS2 enhanced nitrogen assimilation in transgenic tobacco grown under low-nitrogen conditions, Plant Mol. Biol. Rep., 31, 886, 10.1007/s11105-013-0561-8 Kumar, 2009, Influence of nitrogen on the expression of TaDof1 transcription factor in wheat and its relationship with photo synthetic and ammonium assimilating efficiency, Mol. Biol. Rep., 36, 2209, 10.1007/s11033-008-9436-8 Xia, 2013, Physiological and metabolic enzymes activity changes in transgenic rice plants with increased phosphoenolpyruvate carboxylase activity during the flowering stage, Acta Physiol. Plant, 35, 1503, 10.1007/s11738-012-1191-8 Fischer, 2013, Manipulation of microRNA expression to improve nitrogen use efficiency, Plant Sci., 210, 70, 10.1016/j.plantsci.2013.05.009 Fu, 2012, Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production, Plant Biotechnol. J., 10, 443, 10.1111/j.1467-7652.2011.00677.x Good, 2007, Engineering nitrogen use efficiency with alanine aminotransferase, Can. J. Bot., 85, 252, 10.1139/B07-019 Shrawat, 2008, Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase, Plant Biotechnol. J., 6, 722, 10.1111/j.1467-7652.2008.00351.x Gaufichon, 2013, Arabidopsis thaliana ASN2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth, Plant Cell Environ., 36, 328, 10.1111/j.1365-3040.2012.02576.x Tegeder, 2012, Transporters for amino acids in plant cells: some functions and many unknowns, Curr. Opin. Plant Biol., 15, 315, 10.1016/j.pbi.2012.02.001 Hensel, 2011, Transgene expression systems in the Triticeae cereals, J. Plant Physiol., 168, 30, 10.1016/j.jplph.2010.07.007 Reynolds, 2009, Raising yield potential in wheat, J. Exp. Bot., 60, 1899, 10.1093/jxb/erp016 Ferrante, 2010, Floret development of durum wheat in response to nitrogen availability, J. Exp. Bot., 61, 4351, 10.1093/jxb/erq236