Advances in Study of Ammonium Assimilation and its Regulatory Mechanism in Plants

doi:10.11983/CBB15077

Abstract

Abstract: Nitrogen is one of the most important mineral nutrient elements for plant growth and development, playing an essential role in the whole process of plant life. Nitrogen assimilation is a central link for plants to utilize nitrogen and also a factor in low nitrogen use efficiency in plants. It includes two types: assimilation of nitrate (NO₃^-) and ammonium (NH₄⁺); the latter is the critical step in the process of nitrogen assimilation. The source of NH₄⁺ during ammonium assimilation can be divided into 2 types—primary assimilation and secondary assimilation—but both proceed in the glutamine/glutamate (GS/GOGAT) pathway. Ammonium assimilation requires much energy resources but also consumes abundant carbon skeletons, so it is strictly regulated at different levels including transcription, post-transcription, and post-translation. We review the current progress in study of ammonium assimilation and its regulatory mechanism in plants.

null

Key words: ammonium, primary assimilation, secondary assimilation, GS/GOGAT, regulatory mechanism

Xiaopeng Xu, Xiangdong Fu, Hong Liao. Advances in Study of Ammonium Assimilation and its Regulatory Mechanism in Plants[J]. Chinese Bulletin of Botany, 2016, 51(2): 152-166.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.11983/CBB15077

https://www.chinbullbotany.com/EN/Y2016/V51/I2/152

Figures/Tables 4

References 116

[1]	巨晓棠, 谷保静 (2014). 我国农田氮肥施用现状、问题及趋势. 植物营养与肥料学报 20, 783-795.
[2]	李俊良, 陈新平, 李晓林, 张福锁 (2003). 大白菜氮肥施用的产量效应、品质效应和环境效应. 土壤学报 40, 261-266.
[3]	李新鹏, 童依平 (2007). 植物吸收转运无机氮的生理及分子机制. 植物学通报 24, 714-725.
[4]	祁通, 刘易, 冯耀祖, 孙九胜, 王新勇 (2014). 氮肥施用方式对耐盐冬小麦干物质积累和氮素吸收利用的影响. 植物营养与肥料学报 20, 1288-1293.
[5]	Abiko T, Obara M, Ushioda A, Hayakawa T, Hodges M, Yamaya T (2005). Localization of NAD-isocitrate dehydrogenase and glutamate dehydrogenase in rice roots: candidates for providing carbon skeletons to NADH- glutamate synthase. Plant Cell Physiol 46, 1724-1734.
[6]	Almassy RJ, Janson CA, Hamlin R, Xuong NH, Eisen- berg D (1986). Novel subunit-subunit interactions in the structure of glutamine synthetase. Nature 323, 304-309.
[7]	Arcondeguy T, Jack R, Merrick M (2001). PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65, 80-105.
[8]	Bao A, Zhao Z, Ding G, Shi L, Xu F, Cai H (2014). Accu- mulated expression level of cytosolic glutamine synthetase 1 gene (OsGS1;1 or OsGS1;2) alter plant deve- lopment and the carbon-nitrogen metabolic status in rice. PLoS One 9, e95581.
[9]	Baud S, Boutin JP, Miquel M, Lepiniec L, Rochat C (2002). An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Bioch 40, 151-160.
[10]	Bernard SM, Habash DZ (2009). The importance of cytoso- lic glutamine synthetase in nitrogen assimilation and re- cycling. New Phytol 182, 608-620.
[11]	Bernard SM, Moller ALB, Dionisio G, Kichey T, Jahn TP, Dubois F, Baudo M, Lopes MS, Terce-Laforgue T, Foyer CH, Parry MAJ, Forde BG, Araus JL, Hirel B, Schjoerring JK, Habash DZ (2008). Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol Biol 67, 89-105.
[12]	Bindu Simon CS (2010). The 3' untranslated region of the two cytosolic glutamine synthetase (GS1) genes in alfalfa (Medicago sativa) regulates transcript stability in respon- se to glutamine. Planta 232, 1151-1162. DOI PMID
[13]	Bloom AJ (2015). Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen. Photosynth Res 123, 117-128.
[14]	Bodirsky BL, Popp A, Lotze-Campen H, Dietrich JP, Rolinski S, Weindl I, Schmitz C, Müller C, Bonsch M, Humpenöder F, Biewald A, Stevanovic M (2014). Reactive nitrogen requirements to feed the world in 2050 and potential to mitigate nitrogen pollution. Nat Commun 5, 3858. DOI PMID
[15]	Britto DT, Kronzucker HJ (2002). NH₄⁺ toxicity in higher plants: a critical review. J Plant Physiol 159, 567-584.
[16]	Cai H, Zhou Y, Xiao J, Li X, Zhang Q, Lian X (2009). Overexpressed glutamine synthetase gene modifies ni- trogen metabolism and abiotic stress responses in rice. Plant Cell Rep 28, 527-537.
[17]	Camargo JA, Alonso A, Salamanca A (2005). Nitrate toxi- city to aquatic animals: a review with new data for freshwater invertebrates. Chemosphere 58, 1255-1267. PMID
[18]	Cañas RA, Quilleré I, Lea PJ, Hirel B (2010). Analysis of amino acid metabolism in the ear of maize mutants defi- cient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol J 8, 966-978.
[19]	Caputo C, Criado MV, Roberts IN, Gelso MA, Barneix AJ (2009). Regulation of glutamine synthetase 1 and amino acids transport in the phloem of young wheat plants. Plant Physiol Bioch 47, 335-342.
[20]	Carvalho H, Lescure N, de Billy F, Chabaud M, Lima L, Salema R, Cullimore J (2000a). Cellular expression and regulation of the Medicago truncatula cytosolic glutamine synthetase genes in root nodules. Plant Mol Biol 42, 741-756.
[21]	Carvalho H, Lima L, Lescure N, Camut S, Salema R, Cullimore J (2000b). Differential expression of the two cytosolic glutamine synthetase genes in various organs of Medicago truncatula. Plant Sci 159, 301-312.
[22]	Coruzzi GM, Zhou L (2001). Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4, 247-253. DOI PMID
[23]	Coskun D, Britto DT, Li M, Becker A, Kronzucker HJ (2013). Rapid ammonia gas transport accounts for futile transmembrane cycling under NH₃/NH₄⁺ toxicity in plant roots. Plant Physiol 163, 1859-1867.
[24]	Dechorgnat J, Nguyen CT, Armengaud P, Jossier M, Diatloff E, Filleur S, Daniel-Vedele F (2011). From the soil to the seeds: the long journey of nitrate in plants. J Exp Bot 62, 1349-1359. DOI PMID
[25]	Diaz RJ, Rosenberg R (2008). Spreading dead zones and consequences for marine ecosystems. Science 321, 926-929. DOI PMID
[26]	Dragićević M, Todorović S, Bogdanović M, Filipović B, Mišić D, Simonović A (2014). Knockout mutants as a tool to identify the subunit composition of Arabidopsis glutamine synthetase isoforms. Plant Physiol Bioch 79, 1-9.
[27]	El-Kereamy A, Bi YM, Ranathunge K, Beatty PH, Good AG, Rothstein SJ (2012). The rice R2R3-MYB transcrip- tion factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism. PLoS One 7, e52030.
[28]	Fei H, Chaillou S, Hirel B, Mahon JD, Vessey JK (2003). Overexpression of a soybean cytosolic glutamine syn- thetase gene linked to organ-specific promoters in pea plants grown in different concentrations of nitrate. Planta 216, 467-474.
[29]	Ferrario-Mery S, Besin E, Pichon O, Meyer C, Hodges M (2006). The regulatory PII protein controls arginine bio- synthesis in Arabidopsis. FEBS Lett 580, 2015-2020. DOI PMID
[30]	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. PMID
[31]	Forde BG, Day HM, Turton JF, Shen WJ, Cullimore JV, Oliver JE (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, 391-401. PMID
[32]	Fuentes SI, Allen DJ, Ortiz-Lopez A, Hernandez G (2001). Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52, 1071-1081. DOI PMID
[33]	Fukumorita T, Chino M (1982). Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol 23, 273-283.
[34]	Funayama K, Kojima S, Tabuchi-Kobayashi M, Sawa Y, Nakayama Y, Hayakawa T, Yamaya T (2013). Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant Cell Phy- siol 54, 934-943.
[35]	Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N (1999). Three functional transporters for constitutive, diurnally regulated, and starvation-indu- ced uptake of ammonium into Arabidopsis roots. Plant Cell 11, 937-947. DOI PMID
[36]	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. DOI PMID
[37]	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. DOI PMID
[38]	Gutiérrez RA (2012). Systems biology for enhanced plant nitrogen nutrition. Science 336, 1673-1675. DOI PMID
[39]	Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, Mcclung CR, Coruzzi GM (2008). Systems approach identifies an organic nitrogen-responsive gene network that is regu- lated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105, 4939-4944. DOI PMID
[40]	Hayakawa T, Kudo T, Ito T, Takahashi N, Yamaya T (2006). ACT domain repeat protein 7, ACR7, interacts with a chaperone HSP18.0-CII in rice nuclei. Plant Cell Physiol 47, 891-904. PMID
[41]	Hayashi H, Chino M (1990). Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31, 247-251.
[42]	Ho CH, Tsay YF (2010). Nitrate, ammonium, and potassium sensing and signaling. Curr Opin Plant Biol 13, 604-610.
[43]	Hong YF, Ho THD, Wu CF, Ho SL, Yeh RH, Lu CA, Chen PW, Yu LC, Chao A, Yu SM (2012). Convergent starva- tion signals and hormone crosstalk in regulating nutrient mobilization upon germination in cereals. Plant Cell 24, 2857-2873.
[44]	Hsieh MH, Goodman HM (2002). Molecular characteriza- tion of a novel gene family encoding ACT domain repeat proteins in Arabidopsis. Plant Physiol 130, 1797-1806.
[45]	Hsieh MH, Lam HM, van de Loo FJ, Coruzzi G (1998). A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc Natl Acad Sci USA 95, 13965-13970. DOI PMID
[46]	Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000). A critical experimental evaluation of methods for determination of NH₄⁺ in plant tissue, xylem sap and apo- plastic fluid. Physiol Plant 109, 167-179.
[47]	Husted S, Mattsson M, Mollers C, Wallbraun M, Schjoer- ring JK (2002). Photorespiratory NH₄⁺ production in leaves of wild-type and glutamine synthetase 2 antisense oilseed rape. Plant Physiol 130, 989-998. PMID
[48]	Ireland RJ, Lea PJ (1999). The enzymes of glutamine, glutamate, asparagine and aspartate metabolisms. In: Singh BK, ed. Plant Amino Acids: Biochemistry and Biotechnology. New York: Marcel Dekker Inc. pp. 49-109.
[49]	Ishiyama K, Inoue E, Tabuchi M, Yamaya T, Takahashi H (2004a). Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol 45, 1640-1647.
[50]	Ishiyama K, Inoue E, Watanabe-Takahashi A, Obara M, Yamaya T, Takahashi H (2004b). Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. J Biol Chem 279, 16598-16605.
[51]	Jukanti AK, Fischer AM (2008). A high-grain protein content locus on barley (Hordeum vulgare) chromosome 6 is associated with increased flag leaf proteolysis and nitrogen remobilization. Physiol Plant 132, 426-439. DOI PMID
[52]	Kiyomiya S, Nakanishi H, Uchida H, Tsuji A, Nishiyama S, Futatsubashi M, Tsukada H, Ishioka NS, Watanabe S, Ito T, Mizuniwa C, Osa A, Matsuhashi S, Hashimoto S, Sekine T, Mori S (2001). Real time visualization of 13N-translocation in rice under different environmental conditions using positron emitting tracer imaging system. Plant Physiol 125, 1743-1753. DOI PMID
[53]	Konishi N, Ishiyama K, Matsuoka K, Maru I, Hayakawa T, Yamaya T, Kojima S (2014). NADH-dependent gluta- mate synthase plays a crucial role in assimilating ammo- nium in the Arabidopsis root. Physiol Plant 152, 138-151.
[54]	Kumagai E, Araki T, Hamaoka N, Ueno O (2011a). Am- monia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthe- tase activity. Ann Bot-London 108, 1381-1386.
[55]	Kumagai E, Araki T, Ueno O (2011b). Ammonia emission from leaves of different rice (Oryza sativa L.) cultivars. Plant Prod Sci 14, 249-253.
[56]	Kumar R, Taware R, Gaur VS, Guru SK, Kumar A (2009). Influence of nitrogen on the expression of TaDof1 tran- scription factor in wheat and its relationship with photo- synthetic and ammonium assimilating efficiency. Mol Biol Rep 36, 2209-2220.
[57]	Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R (2011). Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low- nitrogen conditions. Plant Biotechnol J 9, 826-837.
[58]	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 Physiol Plant Mol Biol 47, 569-593.
[59]	Lancien M, Ferrario-M RS, Roux Y, Bismuth E, Masclaux C, Hirel B, Gadal P, Hodges M (1999). Simultaneous expression of NAD-dependent isocitrate dehydrogenase and other krebs cycle genes after nitrate resupply to short- term nitrogen-starved tobacco. Plant Physiol 120, 717-726. PMID
[60]	Lea PJ, Miflin BJ (2003). Glutamate synthase and the synthesis of glutamate in plants. Plant Physiol Bioch 41, 555-564.
[61]	Lea PJ, Miflin BJ (1974). Alternative route for nitrogen assimilation in higher plants. Nature 251, 614-616.
[62]	Lewis OAM, James DM, Hewitt EJ (1982). Nitrogen as- similation in barley (Hordeum vulgare L. cv. 'Mazurka') in response to nitrate and ammonium nutrition. Ann Bot- London 49, 39-49.
[63]	Liberles JS, Thórólfsson M, Martinez A (2005). Allosteric mechanisms in ACT domain containing enzymes involved in amino acid metabolism. Amino Acids 28, 1-12. PMID
[64]	Lima L, Seabra A, Melo P, Cullimore J, Carvalho H (2006a). Phosphorylation and subsequent interaction with 14-3-3 proteins regulate plastid glutamine synthetase in Medicago truncatula. Planta 223, 558-567.
[65]	Lima L, Seabra A, Melo P, Cullimore J, Carvalho H (2006b). Post-translational regulation of cytosolic gluta- mine synthetase of Medicago truncatula. J Exp Bot 57, 2751-2761.
[66]	Limami AM, Rouillon C, Glevarec G, Gallais A, Hirel B (2002). Genetic and physiological analysis of germination efficiency in maize in relation to nitrogen metabolism reveals the importance of cytosolic glutamine synthetase. Plant Physiol 130, 1860-1870. DOI PMID
[67]	Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013). Enhanced nitrogen deposition over China. Nature 494, 459-462.
[68]	Lothier J, Gaufichon L, Sormani R, Lemaitre T, Azzo- pardi M, Morin H, Chardon F, Reisdorf-Cren M, Avice JC, Masclaux-Daubresse C (2011). The cytosolic glu- tamine 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. DOI PMID
[69]	Mae T, Ohira K (1981). The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22, 1067-1074.
[70]	Maeda S, Konishi M, Yanagisawa S, Omata T (2014). Nitrite transport activity of a novel HPP family protein conserved in cyanobacteria and chloroplasts. Plant Cell Physiol 55, 1311-1324.
[71]	Man H, Pollmann S, Weiler EW, Kirby EG (2011). In- creased glutamine in leaves of poplar transgenic with pine GS1a caused greater anthranilate synthetase alpha-sub- unit (ASA1) transcript and protein abundances: an auxin- related mechanism for enhanced growth in GS transgenics? J Exp Bot 62, 4423-4431.
[72]	Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Terce- Laforgue T, Quillere I, Coque M, Gallais A, Gonzalez- Moro M, Bethencourt L, Habash DZ, Lea PJ, Char- cosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B (2006). Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18, 3252-3274. DOI PMID
[73]	Masalkar PD, Roberts DM (2015). Glutamine synthetase isoforms in nitrogen-fixing soybean nodules: distinct oligomeric structures and thiol-based regulation. FEBS Lett 589, 215-221. DOI PMID
[74]	Masclaux C, Quillere I, Gallais A, Hirel B (2001). The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Ann Appl Biol 138, 69-81.
[75]	Melo PM, Silva LS, Ribeiro I, Seabra AR, Carvalho HG (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, 1505-1517.
[76]	Miller AJ, Fan X, Shen Q, Smith SJ (2008). Amino acids and nitrate as signals for the regulation of nitrogen acqui- sition. J Exp Bot 59, 111-119.
[77]	Miyazawa SI, Hayashi K, Nakamura H, Hasegawa T, Miyao M (2014). Elevated CO₂ decreases the photorespiratory NH₃ production but does not decrease the NH₃ compensation point in rice leaves. Plant Cell Physiol 55, 1582-1591.
[78]	Morey KJ, Ortega JL, Sengupta-Gopalan C (2002). Cyto- solic glutamine synthetase in soybean is encoded by a multigene family, and the members are regulated in an organ-specific and developmental manner. Plant Physiol 128, 182-193.
[79]	Ohashi M, Ishiyama K, Kojima S, Konishi N, Nakano K, Kanno K, Hayakawa T, Yamaya T (2015). Asparagine synthetase1, but not asparagine synthetase2, is respon- sible for the biosynthesis of asparagine following the supply of ammonium to rice roots. Plant Cell Physiol 56, 769-778. DOI PMID
[80]	Oliveira IC, Brears T, Knight TJ, Clark A, Coruzzi GM (2002). Overexpression of cytosolic glutamine synthetase. Relation to nitrogen, light, and photorespiration. Plant Phy- siol 129, 1170-1180.
[81]	Oliveira IC, Coruzzi GM (1999). Carbon and amino acids reciprocally modulate the expression of glutamine syn- thetase in Arabidopsis. Plant Physiol 121, 301-310. DOI PMID
[82]	Orsel M, Moison M, Clouet V, Thomas J, Leprince F, Canoy A, Just J, Chalhoub B, Masclaux-Daubresse C (2014). Sixteen cytosolic glutamine synthetase genes identified in the Brassica napus L. genome are differen- tially regulated depending on nitrogen regimes and leaf senescence. J Exp Bot 65, 3927-3947.
[83]	Ortega JL, Moguel-Esponda S, Potenza C, Conklin CF, Quintana A, Sengupta-Gopalan C (2006). The 3' un- translated region of a soybean cytosolic glutamine synthetase (GS1) affects transcript stability and protein accumulation in transgenic alfalfa. Plant J 45, 832-846. DOI PMID
[84]	Ortega JL, Temple SJ, Bagga S, Ghoshroy S, Sen- gupta-Gopalan C (2004). Biochemical and molecular characterization of transgenic Lotus japonicus plants constitutively over-expressing a cytosolic glutamine syn- thetase gene. Planta 219, 807-818. PMID
[85]	Ortega JL, Wilson OL, Sengupta-Gopalan C (2012). The 5' untranslated region of the soybean cytosolic glutamine synthetase beta (1) gene contains prokaryotic translation initiation signals and acts as a translational enhancer in plants. Mol Genet Genomics 287, 881-893. DOI PMID
[86]	Rachmilevitch S, Cousins AB, Bloom AJ (2004). Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci USA 101, 11506-11510. DOI PMID
[87]	Rahn CR, Bending GD, Lillywhite RD, Turner MK (2009). Co-incorporation of biodegradable wastes with crop residues to reduce nitrate pollution of groundwater and decrease waste disposal to landfill. Soil Use Manage 25, 113-123.
[88]	Rentsch D, Schmidt S, Tegeder M (2007). Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581, 2281-2289. DOI PMID
[89]	Riedel J, Tischner R, Mack 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. DOI PMID
[90]	Sakurai N, Katayama Y, Yamaya T (2001). Overlapping expression of cytosolic glutamine synthetase and pheny- lalanine ammoni-lyase in immature leaf blades of rice. Physiol Plant 113, 400-408. PMID
[91]	Seabra AR, Carvalho H, Pereira PJ (2009). Crystallization and preliminary crystallographic characterization of glu- tamine synthetase from Medicago truncatula. Acta Crystallogr Sect F Struct Biol Cryst Commun 65, 1309-1312. DOI PMID
[92]	Seabra AR, Silva LS, Carvalho HG (2013). Novel aspects of glutamine synthetase (GS) regulation revealed by a detailed expression analysis of the entire GS gene family of Medicago truncatula under different physiological conditions. BMC Plant Biol 13, 137. DOI PMID
[93]	Seabra AR, Vieira CP, Cullimore JV, Carvalho HG (2010). Medicago truncatula contains a second gene encoding a plastid located glutamine synthetase exclusively expres- sed in developing seeds. BMC Plant Biol 10, 183. DOI PMID
[94]	Shewry PR, Halford NG (2002). Cereal seed storage pro- teins: structures, properties and role in grain utilization. J Exp Bot 53, 947-958. DOI PMID
[95]	Silva LS, Carvalho HG (2013). Possible role of glutamine synthetase in the NO signaling response in root nodules by contributing to the antioxidant defenses. Front Plant Sci 4: 372. DOI PMID
[96]	Smith CS, Weljie AM, Moorhead BG (2003). Molecular properties of the putative nitrogen sensor PII from Arabi- dopsis thaliana. Plant J 33, 353-360.
[97]	Sugiyama K, Hayakawa T, Kudo T, Ito T, Yamaya T (2004). Interaction of N-acetylglutamate kinase with a PII-like protein in rice. Plant Cell Physiol 45, 1768-1778. DOI PMID
[98]	Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H, Fu X (2014). Hete- rotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46, 652-656.
[99]	Sung TY, Chung TY, Hsu CP, Hsieh MH (2011). The ACR11 encodes a novel type of chloroplastic ACT domain repeat protein that is coordinately expressed with GLN2 in Arabidopsis. BMC Plant Biol 11, 118.
[100]	Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y (2014). Perception of root-derived pep- tides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346, 343-346. DOI PMID
[101]	Tabuchi M, Abiko T, Yamaya T (2007). Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). J Exp Bot 58, 2319-2327. DOI PMID
[102]	Tabuchi M, Sugiyama K, Ishiyama K, Inoue E, Sato T, Takahashi H, Yamaya T (2005). Severe reduction in growth rate and grain filling of rice mutants lacking Os- GS1;1, a cytosolic glutamine synthetase1;1. Plant J 42, 641-651. DOI PMID
[103]	Tamura W, Hidaka Y, Tabuchi M, Kojima S, Hayakawa T, Sato T, Obara M, Kojima M, Sakakibara H, Yamaya T (2010). Reverse genetics approach to characterize a function of NADH-glutamate synthase1 in rice plants. Amino Acids 39, 1003-1012. DOI PMID
[104]	Tamura W, Kojima S, Toyokawa A, Watanabe H, Tabu- chi-Kobayashi M, Hayakawa T, Yamaya T, (2011). Disruption of a novel NADH-glutamate synthase2 gene caused marked reduction in spikelet number of rice. Front Plant Sci 2: 57. DOI PMID
[105]	Thomsen HC, Eriksson D, Moller IS, Schjoerring JK (2014). Cytosolic glutamine synthetase: a target for im- provement of crop nitrogen use efficiency? Trends Plant Sci 19, 656-663. DOI PMID
[106]	Tobin AK, Yamaya T (2001). Cellular compartmentation of ammonium assimilation in rice and barley. J Exp Bot 52, 591-604. PMID
[107]	Ueno O, Yoshimura Y, Sentoku N (2005). Variation in the activity of some enzymes of photorespiratory metabolism in C4 grasses. Ann Bot-London 96, 863-869. DOI PMID
[108]	Unno H, Uchida T, Sugawara H, Kurisu G, Sugiyama T, Yamaya T, Sakakibara H, Hase T, Kusunoki M (2006). Atomic structure of plant glutamine synthetase: a key enzyme for plant productivity. J Biol Chem 281, 29287-29296. DOI PMID
[109]	Vincent R, Fraisier V, Chaillou S, Limami MA, Deleens E, Phillipson B, Douat C, Boutin JP, Hirel B (1997). Ov- erexpression of a soybean gene encoding cytosolic glutamine synthetase in shoots of transgenic Lotus cor- niculatus L. plants triggers changes in ammonium assimilation and plant development. Planta 201, 424-433. DOI PMID
[110]	Wang L, Pedas P, Eriksson D, Schjoerring JK (2013). Elevated atmospheric CO₂ decreases the ammonia com- pensation point of barley plants. J Exp Bot 64, 2713-2724.
[111]	Yamaya T, Kusano M (2014). Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. J Exp Bot 65, 5519-5525. DOI PMID
[112]	Yanagisawa S (2000). Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21, 281-288. DOI PMID
[113]	Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004). Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and grow- th under low-nitrogen conditions. Proc Natl Acad Sci USA 101, 7833-7838. DOI PMID
[114]	Yuan L, Loque D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wiren N (2007). The organization of high-affinity ammonium uptake in Arabidopsis roots de- pends on the spatial arrangement and biochemical pro- perties of AMT1-type transporters. Plant Cell 19, 2636-2652.
[115]	Zhang F, Chen X, Vitousek P (2013). Chinese agriculture: an experiment for the world. Nature 497, 33-35.
[116]	Zheng ZL (2009). Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav 4, 584-591.

物种	基因名称	表达部位	基因主要功能
水稻 (Oryza sativa)	OsGS1;1	维管束特异定位(根部、茎和叶片)	参与水稻衰老过程中氮再利用过程, 为籽粒发育提供氮源^b
	OsGS1;2	根系表皮、皮层细胞, 茎, 叶鞘	水稻根部同化NH₄⁺的一个关键基因^a
	OsGS1;3	种子	可能主要参与种子发育时氮的供应或种子萌发时氮的再利用过程^b
	OsNADH-GOGAT1	根系表皮、皮层细胞, 幼嫩叶片维管束	与OsGS1;2一起参与水稻根部NH₄⁺的同化^a
	OsNADH-GOGAT2	成熟叶片维管束	为OsGS1;1反应提供底物Glu, 参与水稻氮的再利用过程^b
拟南芥 (Arabidopsis thaliana)	AtGln1;1	根(表皮和根尖)	同化根部吸收的NH₄⁺; 对根构型具有显著影响, 突变体主根生长受抑制^a
拟南芥 (Arabidopsis thaliana)	AtGln1;2	维管组织中(根、叶片、萼片、花瓣和雄蕊)	参与根系和叶片缓解氨毒^a; 参与地上部同化由NO₃^-还原产生的NH₄⁺(供应高浓度NO₃^-时)^a; 参与为种子萌发和种子发育提供氮源的过程^b
	AtGln1;3	根部维管组织	未知
	AtGln1;4	侧根形成区的中柱鞘细胞	可能在缺氮条件下参与同化根部吸收的NH₄⁺或由NO₃^-还原产生的NH₄^+a
	AtNADH-GOGAT	根、花粉、柱头和顶端分生组织	负责拟南芥根部NH₄⁺的同化^a
玉米	ZmGln1;1	根表皮、皮层细胞	参与同化根系中由NO₃^-还原产生的NH₄^+a
(Zea mays)	ZmGln1;2	根系和叶片韧皮部	参与玉米体内氮的再利用及转运^b
	ZmGln1;3	叶肉细胞	同化叶肉细胞中由NO₃^-还原产生的NH₄⁺, 对玉米籽粒数目有显著影响^a
	ZmGln1;4	叶片维管束鞘细胞	参与重新同化叶片产生的NH₄⁺, 对玉米籽粒大小有显著影响^b
大麦 (Hordeum	HvGS1;1	维管束特异定位(根部、茎和叶片)	可能与OsGS1;1具有类似的功能, 在氮再利用方面起重要作用^b
vulgare)	HvGS1;2	叶肉细胞, 根部的皮层和中柱鞘细胞	可能主要参与同化叶肉细胞中由NO₃^-还原产生的NH₄^+a
	HvGS1;3	谷粒, 根部	可能参与谷粒发育中氮源的供应^b; 参与根系缓解NH₄⁺的毒害^a
苜蓿 (Medicago truncatula)	MtGS1a	维管束定位(根瘤、根、茎和叶)	同化侵染细胞中类菌体释放到细胞质中的NH₄⁺(来源于固氮酶固定的氮)^a; 提供体内氮运转的来源^b
苜蓿 (Medicago truncatula)	MtGS1b	根瘤、根、茎和叶	可能参与同化根系吸收的氮^a
	MtGS2b	籽粒	可能为籽粒发育提供氮源, 表达量随着籽粒的发育而升高^b
大豆 (Glycine max)	GmGlnα	子叶、新根、发育中的根瘤和花	未知
	GmGlnβ(β1和β2)	组成型表达, 根瘤中较高	可能参与同化根瘤固氮产生的NH₄^+a
	GmGlnγ1	根瘤特异	未知
	GmGlnγ2	根瘤增强, 子叶和花	未知

物种	基因名称	表达部位	基因主要功能
水稻 (Oryza sativa)	OsGS1;1	维管束特异定位(根部、茎和叶片)	参与水稻衰老过程中氮再利用过程, 为籽粒发育提供氮源^b
	OsGS1;2	根系表皮、皮层细胞, 茎, 叶鞘	水稻根部同化NH₄⁺的一个关键基因^a
	OsGS1;3	种子	可能主要参与种子发育时氮的供应或种子萌发时氮的再利用过程^b
	OsNADH-GOGAT1	根系表皮、皮层细胞, 幼嫩叶片维管束	与OsGS1;2一起参与水稻根部NH₄⁺的同化^a
	OsNADH-GOGAT2	成熟叶片维管束	为OsGS1;1反应提供底物Glu, 参与水稻氮的再利用过程^b
拟南芥 (Arabidopsis thaliana)	AtGln1;1	根(表皮和根尖)	同化根部吸收的NH₄⁺; 对根构型具有显著影响, 突变体主根生长受抑制^a
拟南芥 (Arabidopsis thaliana)	AtGln1;2	维管组织中(根、叶片、萼片、花瓣和雄蕊)	参与根系和叶片缓解氨毒^a; 参与地上部同化由NO₃^-还原产生的NH₄⁺(供应高浓度NO₃^-时)^a; 参与为种子萌发和种子发育提供氮源的过程^b
	AtGln1;3	根部维管组织	未知
	AtGln1;4	侧根形成区的中柱鞘细胞	可能在缺氮条件下参与同化根部吸收的NH₄⁺或由NO₃^-还原产生的NH₄^+a
	AtNADH-GOGAT	根、花粉、柱头和顶端分生组织	负责拟南芥根部NH₄⁺的同化^a
玉米	ZmGln1;1	根表皮、皮层细胞	参与同化根系中由NO₃^-还原产生的NH₄^+a
(Zea mays)	ZmGln1;2	根系和叶片韧皮部	参与玉米体内氮的再利用及转运^b
	ZmGln1;3	叶肉细胞	同化叶肉细胞中由NO₃^-还原产生的NH₄⁺, 对玉米籽粒数目有显著影响^a
	ZmGln1;4	叶片维管束鞘细胞	参与重新同化叶片产生的NH₄⁺, 对玉米籽粒大小有显著影响^b
大麦 (Hordeum	HvGS1;1	维管束特异定位(根部、茎和叶片)	可能与OsGS1;1具有类似的功能, 在氮再利用方面起重要作用^b
vulgare)	HvGS1;2	叶肉细胞, 根部的皮层和中柱鞘细胞	可能主要参与同化叶肉细胞中由NO₃^-还原产生的NH₄^+a
	HvGS1;3	谷粒, 根部	可能参与谷粒发育中氮源的供应^b; 参与根系缓解NH₄⁺的毒害^a
苜蓿 (Medicago truncatula)	MtGS1a	维管束定位(根瘤、根、茎和叶)	同化侵染细胞中类菌体释放到细胞质中的NH₄⁺(来源于固氮酶固定的氮)^a; 提供体内氮运转的来源^b
苜蓿 (Medicago truncatula)	MtGS1b	根瘤、根、茎和叶	可能参与同化根系吸收的氮^a
	MtGS2b	籽粒	可能为籽粒发育提供氮源, 表达量随着籽粒的发育而升高^b
大豆 (Glycine max)	GmGlnα	子叶、新根、发育中的根瘤和花	未知
	GmGlnβ(β1和β2)	组成型表达, 根瘤中较高	可能参与同化根瘤固氮产生的NH₄^+a
	GmGlnγ1	根瘤特异	未知
	GmGlnγ2	根瘤增强, 子叶和花	未知