Asparagine: an amide of particular distinction in the regulation of symbiotic nitrogen fixation of legumes

References

• Abd-Alla MH, Koyro HW, Yan F, Schubert S, Peiter E. 2000. Functional structure of the indeterminate Vicia faba L. root nodule: Implications for metabolite transport. J Plant Physiol 157: 335–343.
   Google Scholar
• Almeida JP, Hartwig UA, Frehner M, Nösberger J, Lüscher A. 2000. Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). J Exp Bot 51: 1289–1297.
   PubMed Web of Science ®Google Scholar
• Antunes F, Aguilar M, Pineda M, Sodek L. 2008. Nitrogen stress and the expression of asparagine synthetase in roots and nodules of soybean (Glycine max). Physiol Plant 133: 736–743.
   PubMed Web of Science ®Google Scholar
• Arrese-Igor C, González EM, Marino D, Ladrera R, Larrainzar E, Gil-Quintana E. 2011. Physiological responses of legume nodules to drought. Plant Stress 5: 24–31.
   Google Scholar
• Atkins CA. 1999. Spontaneous phloem exudation accompanying abscission in Lupinus mutabilis (Sweet). J Exp Bot 50: 805–812.
   Google Scholar
• Atkins CA, Minchin FR. 1995. Oxygen as the major regulating factor in symbiotic nitrogen fixation. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE. eds. Nitrogen Fixation: Fundamentals and Applications. Dordrecht, The Netherlands: Kluwer, 801–803.
   Google Scholar
• Atkins CA, Smith PM. 2007. Translocation in legumes: assimilates, nutrients, and signaling molecules. Plant Physiol 144: 550–561.
   PubMed Web of Science ®Google Scholar
• Atkins CA, Storer PJ, Pate JS. 1988. Pathways of nitrogen assimilation in cowpea nodules studied using 15N2 and allopurinol. Plant Physiol 86: 204–207.
   PubMedGoogle Scholar
• Atkins CA, Dakora FD, Storer PJ. 1990. Effect of oxygen pressure on synthesis and export of nitrogenous solutes by nodules of cowpea. Planta 182: 565–571.
   PubMedGoogle Scholar
• Atkinson DE. 1968. The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7: 4030–4034.
   PubMed Web of Science ®Google Scholar
• Bacanamwo M, Harper JE. 1997. The feedback mechanism of nitrate inhibition of nitrogenase activity in soybean may involve asparagine and/or products of its metabolism. Physiol Plant 100: 371–377.
   Web of Science ®Google Scholar
• Battaglia M, Solórzano RM, Hernández M, Cuéllar-Ortiz S, García-Gómez B, Márquez J, Covarrubias AA. 2007. Proline-rich cell wall proteins accumulate in growing regions and phloem tissue in response to water deficit in common bean seedlings. Planta 225: 1121–1133.
   PubMedGoogle Scholar
• Berry AM, Mendoza-Herrera A, Guo Y-Y, Hayashi J, Persson T, Barabote R, Demchenko K, Zhang S, Pawlowski K. 2011. New perspectives on nodule nitrogen assimilation in actinorhizal symbioses. Funct Plant Biol 38: 645–652.
   Google Scholar
• Bertrand A, Prévost D, Juge C, Chalifour F-P. 2011. Impact of elevated CO2 on carbohydrate and ureide concentrations in soybean inoculated with different strains of Bradyrhizobium japonicum. Botany 89: 481–490.
   Google Scholar
• Beuve N, Rispail N, Laine P, Cliquet J-B, Ourry A, Le Deunff E. 2004. Putative role of γ-aminobutyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ 27: 1035–1046.
   Web of Science ®Google Scholar
• Bhattacharya J, Singh AK, Rai AN. 2002. Nitrogen nutrition in cyanobacterium Nostoc ANTH, a symbiotic isolate from Anthoceros: uptake and assimilation of inorganic-N and amino acids. Indian J Biochem Biophys 39: 163–169.
   PubMedGoogle Scholar
• Blum A. 2011. Drought resistance and its improvement. In: Blum A, ed. Plant Breeding for Water-limited Environments. Dordrecht, The Netherlands: Springer, 53–152.
   Google Scholar
• Brouquisse R, Rolin D, Cortès S, Gaudillère M, Evrard A, Roby C. 2007. A metabolic study of the regulation of proteolysis by sugars in maize root tips: effects of glycerol and dihydroxyacetone. Planta 225: 693–709.
   PubMedGoogle Scholar
• Choudhary PS, Kanwar M, Bhardwaj R, Yu J-Q, Tran LS. 2012. Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ON, 7: e33210.
   Google Scholar
• Coruzzi G, Bush DR. 2001. Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125: 61–64.
   PubMed Web of Science ®Google Scholar
• Curtis J, Shearer G, Kohl DH. 2004. Bacteroid proline catabolism affects N2 fixation rate of drought-stressed soybeans. Plant Physiol 136: 3313–3318.
   PubMedGoogle Scholar
• Day DA, Poole PS, Tyerman SD, Rosendahl L. 2001. Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell Mol Life Sci 58: 61–71.
   PubMed Web of Science ®Google Scholar
• Díaz P, Borsani O, Márquez A, Monza J. 2005. Nitrogen metabolism in relation to drought stress responses in cultivated and model Lotus species. Lotus Newsletter 7: 83–92.
   Google Scholar
• Fan X, Gordon-Weeks R, Shen Q, Miller AJ. 2006. Glutamine transport and feedback regulation of nitrate reductase activity in barley roots leads to changes in cytosolic nitrate pools. J Exp Bot 57: 1333–1340.
   PubMed Web of Science ®Google Scholar
• Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM. 2010. Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52: 61–76.
   PubMed Web of Science ®Google Scholar
• Fischinger SA, Drevon JJ, Claassen N, Schulze J. 2006. Nitrogen from senescing lower leaves of common bean is re-translocated to nodules and might be involved in a N-feedback regulation of nitrogen fixation. J Plant Physiol 163: 987–995.
   PubMed Web of Science ®Google Scholar
• Forde BG, Lea PJ. 2007. Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58: 2339–2358.
   PubMed Web of Science ®Google Scholar
• Fotelli MN, Tsikou D, Kolliopoulou A, Aivalakis G, Katinakis P, Udvardi MK, Rennenberg H, Flemetakis E. 2011. Nodulation enhances dark CO2 fixation and recycling in the model legume Lotus japonicus. J Exp Bot 62: 2959–2971.
   PubMedGoogle Scholar
• Fougère F, Le Rudulier D, Streeter JG. 1991. Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of Alfalfa (Medicago sativa L.). Plant Physiol 96: 1228–1236.
   PubMed Web of Science ®Google Scholar
• Gaufichon L, Reisdorf-Cren M, Rothstein SJ, Chardon F, Suzuki A. 2010. Biological functions of asparagine synthetase in plants. Plant Sci 179: 141–153.
   Web of Science ®Google Scholar
• Gessler A, Schultze M, Schrempp S, Rennenberg H. 1998. Interaction of phloem-translocated amino compounds with nitrate net uptake by roots of beech (Fagus sylvatica) seedlings. J Exp Bot 49: 1529–1537.
   Web of Science ®Google Scholar
• Giannino D, Nicolodi C, Testone G, Frugis G, Pace E, Santamaria P, Guardasole M, Mariotti D. 2008. The overexpression of asparagine synthetase A from E. coli affects the nitrogen status in leaves of lettuce (Lactuca sativa L.) and enhances vegetative growth. Euphytica 162: 11–22.
   Google Scholar
• Girousse C, Bonnemain J-L, Delrot S, Bournoville R. 1991. Sugar and amino acid composition of phloem sap of Medicago sativa: a comparative study of two collecting methods. Plant Physiol Bioch 29: 41–48.
   Web of Science ®Google Scholar
• Girousse C, Bournoville R, Bonnemain JL. 1996. Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111: 109–113.
   PubMed Web of Science ®Google Scholar
• González EM, Gálvez L, Royuela M, Aparicio-Tejo PM, Arrese-Igor C. 2001. Insights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agronomie 21: 607–613.
   Google Scholar
• Gordon AJ, Skøt L, James CL, Minchin FR. 2002. Short-term metabolic responses of soybean root nodules to nitrate. J Exp Bot 53: 423–428.
   PubMed Web of Science ®Google Scholar
• Gustafson AM, Allen E, Givan S, Smith D, Carrington JC, Kasschau KD. 2005. ASRP: the Arabidopsis Small RNA Project Database. Nucleic Acids Res 33: D637–D640.
   PubMed Web of Science ®Google Scholar
• Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. 2012. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17: 172–179.
   PubMed Web of Science ®Google Scholar
• Hadiarto T, Tran LS. 2011. Progress studies of drought-responsive genes in rice. Plant Cell Rep 30: 297–310.
   PubMed Web of Science ®Google Scholar
• Hartmann K, Peiter E, Koch K, Schubert S, Schreiber L. 2002. Chemical composition and ultrastructure of broad bean (Vicia faba L.) nodule endodermis in comparison to the root endodermis. Planta 215: 14–25.
   PubMed Web of Science ®Google Scholar
• Hartwig UA, Trommler J. 2001. Increase in the concentrations of amino acids in the vascular tissue of white clover and white lupin after defoliation: an indication of a N feedback regulation of symbiotic N2 fixation. Agronomie 21: 615–620.
   Google Scholar
• Hartwig UA, Trommler J, Weisbach C, Walther P, Curioni P, Schuller KA, Nösberger J. 1997. Is the variable oxygen permeability in nodules a physical or a physiological phenomenon? In: Legocki A, Bothe H, Pühler A. eds. Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Berlin, Heidelberg: Springer-Verlag, 241–244.
   Google Scholar
• Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK, Vance CP. 2009. Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol 151: 1221–1238.
   PubMed Web of Science ®Google Scholar
• Hosie AH, Allaway D, Galloway CS, Dunsby HA, Poole PS. 2002. Rhizobium leguminosarum has a second general amino acid permease with unusually broad substrate specificity and high similarity to branched-chain amino acid transporters (Bra/LIV) of the ABC family. J Bacteriol 184: 4071–4080.
   PubMed Web of Science ®Google Scholar
• Huerta-Zepeda A, Durán S, Du Pont G, Calderón J. 1996. Asparagine degradation in Rhizobium etli. Microbiol 142: 1071–1076.
   PubMed Web of Science ®Google Scholar
• Høgh-Jensen H, Schjoerring J, Soussana JF. 2002. The influence of phosphorus deficiency on growth and nitrogen fixation of white clover plants. Ann Bot 90: 745–753.
   PubMed Web of Science ®Google Scholar
• Jebara M, Harzalli-Jebara S, Payré H, Aouani ME, Drevon JJ. 2006. Influence of salinity and abscisic acid on the O2 uptake by N2-fixing nodules of common bean. Biol Plant 50: 717–721.
   Google Scholar
• Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni AL, Morel S, Journet EP, Duc G, Gojon A, Lepetit M, Salon C. 2010. Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses. New Phytol 185: 817–828.
   PubMed Web of Science ®Google Scholar
• Jogaiah S, Govind SR, Tran LS. 2012. Systems biology-based approaches toward understanding drought tolerance in food crops. Crit Rev Biotechnol. doi: 10.3109/07388551.2012.659174.
   PubMedGoogle Scholar
• Joy KW, Ireland RJ, Lea PJ. 1983. Asparagine synthesis in pea leaves, and the occurrence of an asparagine synthetase inhibitor. Plant Physiol 73: 165–168.
   PubMedGoogle Scholar
• Kahn ML, Kraus J, Somerville JE. 1985. A model of nutrient exchange in the Rhizobium-legume symbiosis. In: Evans HJ, Bottomley PJ, Newton WE. eds. Nitrogen Fixation Research Progress. Dordrecht, The Netherlands: Martinus Nijhoff, 193–199.
   Google Scholar
• Kawachi T, Sunaga Y, Ebato M, Hatanaka T, Harada H. 2006. Repression of nitrate uptake by replacement of Asp105 by asparagine in AtNRT3.1 in Arabidopsis thaliana L. Plant Cell Physiol 47: 1437–1441.
   PubMedGoogle Scholar
• Keller SY. 2003. The Influence of P Nutrition on the Root Metabolism in Lotus japonicus (Regel) K. Larsen: An Approach at Transcriptional Level. Ph.D. thesis, Swiss Federal Institute of Technology, ZürichM.
   Google Scholar
• Keller S, Colebatch G, Udvardi M, Sautter C, Hartwig UA. 2002. Nitrogen feedback regulation in phosphorus deficient Lotus japonicus plants. In: Finan TM, O’Brian MR, Layzell DB, Vessey JK, Newton W. eds. Nitrogen Fixation: global Perspectives. UK: CABI International, 433.
   Google Scholar
• King CA, Purcell LC. 2005. Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol 137: 1389–1396.
   PubMed Web of Science ®Google Scholar
• King GA, Woollard DC, Irving DE, Borst WM. 1990. Physiological changes in asparagus spear tips after harvest. Physiol Plant 80: 393–400.
   Web of Science ®Google Scholar
• Kohl DH, Kennelly EJ, Zhu Y-X, Schubert KR, Shearer G. 1991. Proline accumulation, nitrogenase (C2H2 reducing) activity, and activities of enzymes related to proline metabolism in drought stressed soybean nodules. J Exp Bot 42: 831–837.
   Web of Science ®Google Scholar
• Küster H, Albus U, Frühling M, Tchetkova SA, Tikhonovitch IA, Pühler A, Perlick AM. 1997. The asparagine synthetase gene VfASl is strongly expressed in the nitrogen-fixing zone of broad bean (Vicia faba L.) root nodules. Plant Sci 124: 89–95.
   Google Scholar
• Ladrera R, Marino D, Larrainzar E, González EM, Arrese-Igor C. 2007. Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiol 145: 539–546.
   PubMed Web of Science ®Google Scholar
• Lam HM, Hsieh MH, Coruzzi G. 1998. Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J 16: 345–353.
   PubMed Web of Science ®Google Scholar
• Larrainzar E, Wienkoop S, Weckwerth W, Ladrera R, Arrese-Igor C, González EM. 2007. Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiol 144: 1495–1507.
   PubMed Web of Science ®Google Scholar
• Larrainzar E, Wienkoop S, Scherling C, Kempa S, Ladrera R, Arrese-Igor C, Weckwerth W, González EM. 2009. Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Mol Plant Microbe Interact 22: 1565–1576.
   PubMed Web of Science ®Google Scholar
• Layzell DB. 2000. Oxygen regulation and adenylates in legume nodules. In: Pedrosa FO, Hungria M, Yates MG, Newton WE. eds. Nitrogen Fixation: From Molecules to Crop Productivity. Dordrecht, The Netherlands: Kluwer, 367–368.
   Google Scholar
• Layzell DB, Larue TA. 1982. Modeling C and N transport to developing soybean fruits. Plant Physiol 70: 1290–1298.
   PubMedGoogle Scholar
• Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG. 2007. Asparagine in plants. Ann Appl Biol 150: 1–26.
   Web of Science ®Google Scholar
• Li Y, Parsons R, Day DA, Bergersen FJ. 2002. Reassessment of major products of N2 fixation by bacteroids from soybean root nodules. Microbiology (Reading, Engl) 148: 1959–1966.
   PubMed Web of Science ®Google Scholar
• Lim CW, Lee YW, Hwang CH. 2011. Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression. Plant Cell Physiol 52: 1613–1627.
   PubMed Web of Science ®Google Scholar
• Lima JD, Sodek L. 2003. N-stress alters aspartate and asparagine levels of xylem sap in soybean. Plant Sci 165: 49–56.
   Google Scholar
• Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP. 2005. Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41: 257–268.
   PubMed Web of Science ®Google Scholar
• Lodwig EM, Hosie AH, Bourdès A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS. 2003. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422: 722–726.
   PubMed Web of Science ®Google Scholar
• Louahlia S, Laine P, MacDuff JH, Ourry A, Humphreys M, Boucaud J. 2008. Interaction between reserve mobilization and regulation of nitrate uptake during regrowth of Lolium perenne L.: putative roles of amino acids and carbohydrates. Botany 86: 1101–1110.
   Google Scholar
• Luciñski R, Polcyn W, Ratajczak L. 2002. Nitrate reduction and nitrogen fixation in symbiotic association Rhizobium-legumes. Acta Biochim Pol 49: 537–546.
   PubMed Web of Science ®Google Scholar
• Maclean AM, White CE, Fowler JE, Finan TM. 2009. Identification of a hydroxyproline transport system in the legume endosymbiont Sinorhizobium meliloti. Mol Plant Microbe Interact 22: 1116–1127.
   PubMed Web of Science ®Google Scholar
• Manavalan LP, Guttikonda SK, Tran LS, Nguyen HT. 2009. Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50: 1260–1276.
   PubMed Web of Science ®Google Scholar
• Mane AV, Deshpande TV, Wagh VB, Karadge BA, Samant JS. 2011. A critical review on physiological changes associated with reference to salinity. Int J Environ Sci 1: 1192–1216.
   Google Scholar
• Marino D, González EM, Arrese-Igor C. 2006. Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by paraquat: evidence for the occurrence of two regulation pathways under oxidative stresses. J Exp Bot 57: 665–673.
   PubMedGoogle Scholar
• Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, González EM. 2007. Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143: 1968–1974.
   PubMed Web of Science ®Google Scholar
• Miller G, Stein H, Honig A, Kapulnik Y, Zilberstein A. 2005. Responsive modes of Medicago sativa proline dehydrogenase genes during salt stress and recovery dictate free proline accumulation. Planta 222: 70–79.
   PubMedGoogle Scholar
• Miller AJ, Fan X, Shen Q, Smith SJ. 2008. Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J Exp Bot 59: 111–119.
   PubMed Web of Science ®Google Scholar
• Minchin FR, Witty JF. 2005. Respiratory/carbon costs of symbiotic nitrogen fixation in legumes. In: Lambers H, Ribas-Carbo M. eds. Plant Respiration: from Cell to Ecosystem. Dordrecht, The Netherlands: Springer, 195–205.
   Google Scholar
• Minchin FR, James EK, Becana M. 2008. Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE. eds. Nitrogen-fixing Leguminous Symbioses. Dordrecht, The Netherlands: Springer, 321–362.
   Google Scholar
• Mizukoshi K, Nishiwaki T, Ohtake N, Minagawa R, Ikarashi T, Ohyama T. 1995. Nitrate transport pathway into soybean nodules traced by Tungstate and 15NO3-1. Soil Sci Plant Nutr 41: 75–88.
   Web of Science ®Google Scholar
• Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S. 2012. Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70: 367–376.
   PubMedGoogle Scholar
• Neo HH, Layzell DB. 1997. Phloem glutamine and the regulation of O2 diffusion in legume nodules. Plant Physiol 113: 259–267.
   PubMed Web of Science ®Google Scholar
• Nishiyama R, Le DT, Watanabe Y, Matsui A, Tanaka M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. 2012. Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS ONE 7: e32124.
   PubMed Web of Science ®Google Scholar
• Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran LS. 2011. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23: 2169–2183.
   PubMed Web of Science ®Google Scholar
• Ohyama T, Kumazawa K. 1978. Incorporation of 15N into various nitrogenous compounds in intact soybean nodules after exposure to 15N2 gas. Soil Sci Plant Nutr 24: 525–533.
   Web of Science ®Google Scholar
• Ohyama T, Ohtake N, Sueyoshi K, Tewari K, Takahashi Y, Ito S, Nishiwaki T, Nagumo Y, Ishii S, Sato T. 2009. Nitrogen Fixation and Metabolism in Soybean Plants. Hauppauge NY, USA. Nova Science Publishers Inc.
   Google Scholar
• Okumoto S, Pilot G. 2011. Amino acid export in plants: a missing link in nitrogen cycling. Mol Plant 4: 453–463.
   PubMed Web of Science ®Google Scholar
• Oldroyd GE, Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45: 119–144.
   PubMed Web of Science ®Google Scholar
• Omrane S, Ferrarini A, D’Apuzzo E, Rogato A, Delledonne M, Chiurazzi M. 2009. Symbiotic competence in Lotus japonicus is affected by plant nitrogen status: transcriptomic identification of genes affected by a new signalling pathway. New Phytol 183: 380–394.
   PubMed Web of Science ®Google Scholar
• Oti-Boateng C. 2000. Effect of debudding of faba bean on the soluble nitrogen and ammonia concentration of the root nodules and associated nitrogenase activity. W Afr J Appl Ecol 1: 73–79.
   Google Scholar
• Oti-Boateng C, Silsbury JH. 1993. The effects of exogenous amino acid on acetylene reduction activity of Vicia faba L. cv. Fiord. Ann Bot 71: 71–74.
   Google Scholar
• Osipova MA, Mortier V, Demchenko KN, Tsyganov VE, Tikhonovich IA, Lutova LA, Dolgikh EA, Goormachtig S. 2012. Wuschel-related homeobox5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiol 158: 1329–1341.
   PubMedGoogle Scholar
• Parsons R, Baker A. 1996. Cycling of amino compounds in symbiotic lupin. J Exp Bot 47: 421–429.
   Google Scholar
• Parsons R, Sunley RJ. 2001. Nitrogen nutrition and the role of root-shoot nitrogen signalling particularly in symbiotic systems. J Exp Bot 52: 435–443.
   PubMedGoogle Scholar
• Parsons R, Stanforth A, Raven AJ, Sprent JI. 1993. Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen. Plant Cell Environ 16: 125–136.
   Web of Science ®Google Scholar
• Parsons R, Morris RN, Baker A. 1995. Whole plant regulation of N2 fixation in soybean: The role of C/N ratio and nitrogen translocation. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE. eds. Nitrogen Fixation: Fundamentals and Applications. Dordrecht, The Netherlands: Kluwer, 588.
   Google Scholar
• Pate JS, Gunning BES, Briarty LG. 1969. Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta 85: 11–34.
   PubMed Web of Science ®Google Scholar
• Pate JS, Atkins CA, Herridge DF, Layzell DB. 1981. Synthesis, storage, and utilization of amino compounds in white lupin (Lupinus albus L.). Plant Physiol 67: 37–42.
   PubMedGoogle Scholar
• Pate JS, Peoples MB, Atkins CA. 1984. Spontaneous phloem bleeding from cryopunctured fruits of a ureide-producing legume. Plant Physiol 74: 499–505.
   PubMedGoogle Scholar
• Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Hérouart D, Frendo P, Puppo A. 2006. Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J Exp Bot 57: 1769–1776.
   PubMed Web of Science ®Google Scholar
• Pedersen AL, Feldner HC, Rosendahl L. 1996. Effect of proline on nitrogenase activity in symbiosomes from root nodules of soybean (Glycine max L.) subjected to drought stress. J Exp Bot 47: 1533–1539.
   Web of Science ®Google Scholar
• Poole PS, Allaway D, Lodwig E, Wheeler T. 2000. Ammonium and alanine are the primary nitrogen secretion products of pea bacteroids. In: Pedrosa FO, Hungria M, Yates MG, Newton WE, eds. Nitrogen Fixation: from Molecules to Crop Productivity. Dordrecht, The Netherlands: Kluwer, 371–372.
   Google Scholar
• Prell J, Poole P. 2006. Metabolic changes of rhizobia in legume nodules. Trends Microbiol 14: 161–168.
   PubMed Web of Science ®Google Scholar
• Prell J, Bourdès A, Karunakaran R, Lopez-Gomez M, Poole P. 2009a. Pathway of γ-aminobutyrate metabolism in Rhizobium leguminosarum 3841 and its role in symbiosis. J Bacteriol 191: 2177–2186.
   PubMed Web of Science ®Google Scholar
• Prell J, White JP, Bourdes A, Bunnewell S, Bongaerts RJ, Poole PS. 2009b. Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci USA 106: 12477–12482.
   PubMed Web of Science ®Google Scholar
• Prell J, Bourdès A, Kumar S, Lodwig E, Hosie A, Kinghorn S, White J, Poole P. 2010. Role of symbiotic auxotrophy in the Rhizobium-legume symbioses. PLoS ONE 5: e13933.
   PubMedGoogle Scholar
• Prell J, Mulley G, Haufe F, White JP, Williams A, Karunakaran R, Downie JA, Poole PS. 2012. The PTS(Ntr) system globally regulates ATP-dependent transporters in Rhizobium leguminosarum. Mol Microbiol 84: 117–129.
   PubMed Web of Science ®Google Scholar
• Purcell LC. 2009. Physiological responses of N2 fixation to drought and selecting genotypes for improved N2 fixation. In: Emerich DW, Krishnan HB (eds). Nitrogen Fixation in Crop Production. Agron. Monogr. 52. ASA, CSSA, and SSSA, Madison, USA, 211–38.
   Google Scholar
• Raggi V. 1994. Changes in free amino acids and osmotic adjustment in leaves of water-stressed bean. Physiol Plant 91: 427–434.
   Web of Science ®Google Scholar
• Ramos MLG, Parsons R, Sprent JI. 2005. Differences in ureide and amino acid content of water stressed soybean inoculated with Bradyrhizobium japonicum and B. elkanii. Pesq Agropec Bras 40: 453–458.
   Google Scholar
• Reid DE, Ferguson BJ, Hayashi S, Lin YH, Gresshoff PM. 2011a. Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108: 789–795.
   PubMed Web of Science ®Google Scholar
• Reid DE, Ferguson BJ, Gresshoff PM. 2011b. Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 24: 606–618.
   PubMedGoogle Scholar
• Rosendahl L, Vance CP, Pedersen WB. 1990. Products of dark CO2 fixation in pea root nodules support bacteroid metabolism. Plant Physiol 93: 12–19.
   PubMedGoogle Scholar
• Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, van der Merwe MJ, Kakar K, Gouzy J, Fernie AR, Udvardi M, Salon C, Gojon A, Lepetit M. 2008. Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146: 2020–2035.
   PubMedGoogle Scholar
• Saleem M, Lamkemeyer T, Schützenmeister A, Madlung J, Sakai H, Piepho HP, Nordheim A, Hochholdinger F. 2010. Specification of cortical parenchyma and stele of maize primary roots by asymmetric levels of auxin, cytokinin, and cytokinin-regulated proteins. Plant Physiol 152: 4–18.
   PubMedGoogle Scholar
• Sato S, Isobe S, Tabata S. 2010. Structural analyses of the genomes in legumes. Curr Opin Plant Biol 13:146–152.
   PubMedGoogle Scholar
• Schubert S. 2007. The apoplast of indeterminate legume nodules: compartment for transport of amino acids, amides and sugars? In: Sattelmacher B, Horst WJ. eds. The Apoplast of Higher Plants: Compartment of Storage, Transport and Reactions. Dordrecht, The Netherlands: Springer, 445–454.
   Google Scholar
• Schulze J. 2003. Source-sink manipulations suggest an N-feedback mechanism for the drop in N2 fixation during pod-filling in pea and broad bean. J Plant Physiol 160: 531–537.
   PubMedGoogle Scholar
• Schulze J. 2004. How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167: 125–137.
   Web of Science ®Google Scholar
• Schulze J, Adgo E, Schilling G. 1994. The influence of N2-fixation on the carbon balance of leguminous plants. Experientia 50: 906–912.
   Google Scholar
• Schulze J, Adgo E, Merbach W. 1999. Carbon costs associated with N2 fixation in Vicia faba L. and Pisum sativum L. over a 14-day period. Plant Biol 1: 625–631.
   Google Scholar
• Schulze J, Tesfaye M, Litjens RHMG, Bucciarelli B, Trepp G, Miller S, Samac D, Allan D, Vance CP. 2002. Malate plays a central role in plant nutrition. Plant Soil 247: 133–139.
   Web of Science ®Google Scholar
• Serraj R, Frangne N, Maeshima M, Fleurat-Lessard P, Drevon JJ. 1998. A α−TIP cross-reacting protein is abundant in the cortex of soybean N2-fixing nodules. Planta 206: 681–684.
   Google Scholar
• Serraj R, Vadez V V, Denison RF, Sinclair TR. 1999. Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiol 119: 289–296.
   PubMedGoogle Scholar
• Serraj R, Vadez V, Sinclair TR. 2001. Feedback regulation of symbiotic N2 fixation under drought stress. Agronomie 21: 621–626.
   Google Scholar
• Serventi F, Ramazzina I, Lamberto I, Puggioni V, Gatti R, Percudani R. 2010. Chemical basis of nitrogen recovery through the ureide pathway: formation and hydrolysis of S-ureidoglycine in plants and bacteria. ACS Chem Biol 5: 203–214.
   PubMedGoogle Scholar
• Sinclair TR, Vadez V, Chenu K. 2003. Ureide accumulation in response to Mn nutrition by eight soybean genotypes with N2 fixation tolerance to soil drying. Crop Sci 43: 592–597.
   Google Scholar
• Soussana J-F, Tallec T. 2010. Can we understand and predict the regulation of biological N2 fixation in grassland ecosystems? Nutr Cycl Agroecosyst 88, 197–213.
   Google Scholar
• Soussana JF, Minchin FR, Macduff JH, Raistrick N, Abberton MT, Michaelson-Yeates TP. 2002. A simple model of feedback regulation for nitrate uptake and N2 fixation in contrasting phenotypes of white clover. Ann Bot 90: 139–147.
   PubMed Web of Science ®Google Scholar
• Sprent JI, James EK. 2007. Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144: 575–581.
   PubMed Web of Science ®Google Scholar
• Sprent JI. 2009. Legume Nodulation: A Global Perspective. First Edition. UK: Wiley-Blackwell.
   Google Scholar
• Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A. 2002. Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53: 959–970.
   PubMed Web of Science ®Google Scholar
• Streeter JG. 1977. Asparaginase and asparagine transaminase in soybean leaves and root nodules. Plant Physiol 60: 235–239.
   PubMed Web of Science ®Google Scholar
• Streeter JG. 1987. Effect of nitrate on the organic acid and amino Acid composition of legume nodules. Plant Physiol 85: 774–779.
   PubMedGoogle Scholar
• Sulieman S. 2009. Physiological Regulation of Symbiotic N₂ fixation in the Model Legume Medicago truncatula. Ph.D. thesis, Germany: Georg-August-University Göttingen. Cuvillier Verlag. ISBN: 978-3-86955-043-5.
   Google Scholar
• Sulieman S. 2011. Does GABA increase the efficiency of symbiotic N2 fixation in legumes? Plant Signal Behav 6: 32–36.
   PubMedGoogle Scholar
• Sulieman S, Schulze J. 2010a. The efficiency of nitrogen fixation of the model legume Medicago truncatula (Jemalong A17) is low compared to Medicago sativa. J Plant Physiol 167: 683–692.
   PubMed Web of Science ®Google Scholar
• Sulieman S, Schulze J. 2010b. Phloem-derived γ-aminobutyric acid (GABA) is involved in upregulating nodule N2 fixation efficiency in the model legume Medicago truncatula. Plant Cell Environ 33: 2162–2172.
   PubMed Web of Science ®Google Scholar
• Sulieman S, Fischinger S, Schulze J. 2008. N-feedback regulation of N2 fixation in Medicago truncatula under P-deficiency. Gen Appl Plant Physiol 34: 33–54.
   Google Scholar
• Sulieman S, Fischinger SA, Gresshoff PM, Schulze J. 2010. Asparagine as a major factor in the N-feedback regulation of N2 fixation in Medicago truncatula. Physiol Plant 140: 21–31.
   PubMed Web of Science ®Google Scholar
• Sunley RJ, Parsons R. 2002. Alteration of glutamine synthetase and arginase activities in Lotus japonicus and the concomitant effects on nitrogen metabolism. In: Finan TM, O’Brian MR, Layzell DB, Vessey JK, Newton W. eds. Nitrogen Fixation: Global Perspectives. UK: CABI International, 8.
   Google Scholar
• Ta TC, Faris MA, Macdowall FD. 1986. Pathways of nitrogen metabolism in nodules of alfalfa (Medicago sativa L.). Plant Physiol 80: 1002–1005.
   PubMed Web of Science ®Google Scholar
• Tajima S, Takane K, Nomura M, Kouchi H. 2000. Symbiotic nitrogen fixation at the late stage of nodule formation in Lotus japonicus and other legume plants. J Plant Res 113: 467–473.
   Google Scholar
• Thao NP, Tran LS. 2011. Potentials toward genetic engineering of drought-tolerant soybean. Crit Rev Biotechnol. doi: 10.3109/07388551.2011.643463.
   PubMedGoogle Scholar
• Todd CD, Tipton PA, Blevins DG, Piedras P, Pineda M, Polacco JC. 2006. Update on ureide degradation in legumes. J Exp Bot 57: 5–12.
   PubMedGoogle Scholar
• Touraine B. 2004. Nitrate uptake by roots – transporters and root development. In: Amâncio S, Stulen I, eds. Nitrogen Acquisition and Assimilation in Higher Plants. Dordrecht, The Netherlands: Kluwer, 1–34.
   Google Scholar
• Tran LS, Mochida K. 2010. Functional genomics of soybean for improvement of productivity in adverse conditions. Funct Integr Genomics 10: 447–462.
   PubMed Web of Science ®Google Scholar
• Trinchant J-C, Yang Y-S, Rigaud J. 1998. Proline accumulation inside symbiosome of faba bean nodules under salt stress. Physiol Plant 104: 38–49.
   Google Scholar
• Trinchant JC, Boscari A, Spennato G, Van de Sype G, Le Rudulier D. 2004. Proline betaine accumulation and metabolism in alfalfa plants under sodium chloride stress. Exploring its compartmentalization in nodules. Plant Physiol 135: 1583–1594.
   PubMedGoogle Scholar
• Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL. 2003. Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248: 99–116.
   Web of Science ®Google Scholar
• Vadez V, Sinclair TR, Serraj R. 2000a. Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean. Physiol Plant 110: 215–223.
   Web of Science ®Google Scholar
• Vadez V, Sinclair TR, Serraj R, Purcell LC. 2000b. Manganese application alleviates the water deficit-induced decline of N2 fixation. Plant Cell Environ 23: 497–499.
   Web of Science ®Google Scholar
• Valentine AJ, Benedito VA, Kang Y. 2011. Legume nitrogen fixation and soil abiotic stress: from physiology to genome and beyond. Annu Plant Rev 42: 207–248.
   Google Scholar
• Valverde C, Huss-Danell K. 2008. Carbon and nitrogen metabolism in actinorhizal nodules. In: Pawlowski K, Newton WE, eds. Nitrogen-fixing Actinorhizal Symbioses. Dordrecht, The Netherlands: Springer, 167–198.
   Google Scholar
• Vance CP. 2008. Carbon and nitrogen metabolism in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE, eds. Nitrogen-fixing Leguminous Symbioses. Dordrecht, The Netherlands: Springer, 293–320.
   Google Scholar
• Venkateshwaran M, Ané J-M. 2011. Legumes and nitrogen fixation: physiological, molecular, evolutionary perspectives, and applications. In: Hawkesford MJ, Barraclough P. eds. The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops. Chichester, West Sussex; Ames, Iowa: Wiley-Blackwell, 457–490.
   Google Scholar
• Verdoy D, Coba De La Peña T, Redondo FJ, Lucas MM, Pueyo JJ. 2006. Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant Cell Environ 29: 1913–1923.
   PubMed Web of Science ®Google Scholar
• van Heerden PD, Kiddle G, Pellny TK, Mokwala PW, Jordaan A, Strauss AJ, de Beer M, Schlüter U, Kunert KJ, Foyer CH. 2008. Regulation of respiration and the oxygen diffusion barrier in soybean protect symbiotic nitrogen fixation from chilling-induced inhibition and shoots from premature senescence. Plant Physiol 148: 316–327.
   PubMedGoogle Scholar
• Wang G, Fiers M. 2010. CLE peptide signaling during plant development. Protoplasma 240: 33–43.
   PubMed Web of Science ®Google Scholar
• Waters JK, Hughes BL 2nd, Purcell LC, Gerhardt KO, Mawhinney TP, Emerich DW. 1998. Alanine, not ammonia, is excreted from N2-fixing soybean nodule bacteroids. Proc Natl Acad Sci USA 95: 12038–12042.
   PubMed Web of Science ®Google Scholar
• Werner AK, Sparkes IA, Romeis T, Witte CP. 2008. Identification, biochemical characterization, and subcellular localization of allantoate amidohydrolases from Arabidopsis and soybean. Plant Physiol 146: 418–430.
   PubMed Web of Science ®Google Scholar
• White J, Prell J, James EK, Poole P. 2007. Nutrient sharing between symbionts. Plant Physiol 144: 604–614.
   PubMed Web of Science ®Google Scholar
• White JP, Prell J, Ramachandran VK, Poole PS. 2009. Characterization of a γ-aminobutyric acid transport system of Rhizobium leguminosarum bv. viciae 3841. J Bacteriol 191: 1547–1555.
   PubMed Web of Science ®Google Scholar
• Whitehead LF, Tyerman SD, Day DA. 2001. Polyamines as potential regulators of nutrient exchange across the peribacteroid membrane in soybean root nodules. Aust J Plant Physiol 28: 675–681.
   Google Scholar
• Widiez T, El Kafafi el S, Girin T, Berr A, Ruffel S, Krouk G, Vayssières A, Shen WH, Coruzzi GM, Gojon A, Lepetit M. 2011. High nitrogen insensitive 9 (HNI9)-mediated systemic repression of root NO3-1 uptake is associated with changes in histone methylation. Proc Natl Acad Sci USA 108: 13329–13334.
   PubMed Web of Science ®Google Scholar
• Wong HK, Chan HK, Coruzzi GM, Lam HM. 2004. Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis. Plant Physiol 134: 332–338.
   PubMed Web of Science ®Google Scholar
• Yang X, Wang X, Wei M, Hikosaka SH, Goto E. 2011. Changes of glutamine and asparagine content in cucumber seedlings in response to nitrate stress. Int J Plant Prod 5: 1–8.
   Google Scholar
• Yuan L, Loqué D, Ye F, Frommer WB, von Wirén N. 2007. Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol 143: 732–744.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Shearer G, Kohl DH. 1992. Proline fed to intact soybean plants influences acetylene reducing activity and content and metabolism of proline in bacteroids. Plant Physiol 98: 1020–1028.
   PubMed Web of Science ®Google Scholar