Abstract
Nitrogen (N2) is a very unreactive molecule. The reason for its chemical stability lies in the electronic structure of the molecule, but nitrogen is not totally inert. The industrial reduction of nitrogen to ammonia (principally by the Haber-Bosch process) is very important commercially.
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References
Albrecht C, Geurts R, Lapeyrie F, Bisseling T (1998) Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J 15: 605–614
Albrecht C, Geurts R, Bisseling T (1999) Legume nodulation and mycorrhizae formation; two extremes in host specificity meet. EMBO J 18: 281–288
Ardourel M, Demont N, Debellé F, Maillet F, De Billy F, Promé JC, Dénarié J, Truchet G (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6: 1357–1374
Arredondo-Peter R, Hargrove MS, Moran JF, Sarath G, Klucas RV (1998) Plant hemoglobins. Plant Physiol 18: 1121–1125
Atkins CA, Smith PMC, Storer PJ (1997) Re-examination of the intracellular localization of de novo purine synthesis in cowpea nodules. Plant Physiol 113: 127–135
Awonaike KO, Lea PJ, Miflin BJ (1981) The localisation of the enzymes of ammonia assimilation in root nodules of Phaseolus vulgaris. Plant Sci Lett 23: 189–195
Bakkers J, Semino CE, Stroband H, Kijne JW, Robbins PW, Spaink HP (1997) An important developmental role for oligosaccharides during early embryogenesis of cyprinid fish. Proc Natl Acad Sci USA 94: 7982–7986
Barker DG, Bianchi S, Blondon F, Dattee Y, Duc G, Essad S, Flament P, Gallusci P, Génier G, Guy P, Muel X, Tourneur J, Dénarié J, Huguet T (1990) Medicago truncatula, a model plant for studying the molecular genetics of the rhizobium-legume symbiosis. Plant Mol Biol Rep 8: 40–49
Batut J, Boistard P (1994) Oxygen control of rhizobium. Antonie van Leeuwenhoek Journal: Antonie varr Leeuwenhoek 66: 129
Bauer P, Ratet P, Crespi MD, Schultze M, Kondorosi A (1996) Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsEnodl2A expression patterns in alfalfa roots. Plant J 10: 91–105
Bergersen FJ, Turner GL (1975a) Leghaemoglobin and the supply of O2 to nitrogen fixing root nodule bacteroids: studies of an experimental system with no gas phase. J Gen Microbiol 89: 31–47
Bergersen FJ, Turner GL (1975b) Leghaemoglobin and the supply of O2 to nitrogen fixing root nodule bacteroids: presence of two oxidase systems and ATP production at low free O2 concentration. J Gen Microbiol 91: 345–354
Bergersen FJ, Turner GL (1980) Properties of terminal oxidase systems of bacteroids from root nodules of soybean and cowpea and of N2-fixing bacteria grown in continuous culture. J Gen Microbiol 118: 235–252
Bohme H (1998) Regulation of nitrogen fixation in heterocyst-forming bacteria. Trends Plant Sci 3: 346–351
Bono J-J, Riond J, Nicolaou KC, Bockovich NJ, Estevez VA, Cullimore JV, Ranjeva R (1995) Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J 7: 253–260
Brears T, Walker EL, Coruzzi GM (1991) A promoter sequence involved in cell-specific expression of the pea glutamine synthetase GS3A gene in organs of transgenic tobacco and alfalfa. Plant J 1: 235–244
Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7: 191–226
Brown SM, O’Parka KJ, Sprent JI, Walsh KB (1995) Symplastic transport in soybean nodules. Soil Biol Biochem 27: 387–399
Bryce JH, Day DA (1990) Tricarboxylic acid cycle activity in mitochondria from soybean nodules and cotyledons. J Exp Bot 41: 961–967
Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96: 2983–3011
Capone DG, Zehr JP. Paerl HW, Bergman B, Carpenter EJ (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221–1229
Carlson RW, Price NPJ, Stacey G (1994) The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Mol Plant-Microbe Interact 7: 684–695
Charon C, Johansson C, Kondorosi E, Kondorosi A, Crespi M (1997) ENOD40 induces dedifferentiation and division of root cortical cells in legumes. Proc Natl Acad Sci USA 94: 8901–8906
Chen R, Siver DL, de Bruijn FJ (1998) Nodule parenchyma-specific expression of the Sesbania rostrata early nodulin gene SrEnod2 is mediated by its 3 untranslated region. Plant Cell 10: 1585–1602
Cohn J, Day RB, Stacey G (1998) Legume nodule organogenesis. Trends Plant Sci 3: 105–110
Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6: 215–225
Craig J, Barratt P, Tatge H, Dejardin A, Handley L, Gardner CD, Barber L, Wang T, Hedley C, Martin C, Smith AM (1999) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J 17: 353–362
Csanadi G, Szecsi J, Kalo P, Kiss P, Endre G, Kondorosi A, Kondorosi E, Kiss GB (1994) ENOD 12, an early nodulin gene, is not required for nodule formation and efficient nitrogen fixation in alfalfa. Plant Cell 6: 201–213
Cullimore JV, Cock JM, Daniell TJ, Swarup R, Bennett MJ (1992) Inducibility of the glutamine synthetase gene family of Phaseolus vulgaris L. Inducible plant proteins. J.L. Wray Cambridge University Press, pp 79–95
Day DA, Copeland L (1991) Carbon metabolism and compartmentation in nitrogen-fixing legume nodules. Plant Physiol Biochem 29: 185–201
Day DA, Mannix M (1988) Malate oxidation by soybean nodule mitochondria and the possible consequences for nitrogen fixation. Plant Physiol Biochem 26: 567–273
Dean RM, Rivers, RL, Zeidel, ML, Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38: 347–353
deBilly F, Barker G, Gallusci P, Truchet G (1991) Leghaemoglobion gene transcrtiption is triggered in a single layer in the indeterminate nitrogen-fixing root nodule of alfalfa. Plant J 1: 27–35
de Carvalho-Niebel F, Lescure N, Cullimore JV, Gamas P (1998) The Medicago truncatula MtAnnl gene encoding an annexin is induced by Nod factors and during the symbiotic interaction with Rhizobium meliloti. Mol Plant-Microbe Interact 11: 504–513
de Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, Schiavo FL, Terzi M, Bisseling T, Van Kammen A, de Vries SC (1993) Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5: 615–620
Dénarié J, Debellé F, Rosenberg C (1992) Signaling and host range variation in nodulation. Annu Rev Microbiol 46: 497–531
Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503–535
Dixon R, Cheng Q, Shen G-F, Day A, Dowson-Day M (1997) Nif gene transfer and expression in chloroplasts: prospects and problems. Plant Soil 194: 193–203
Downie JA (1994) Signalling strategies for nodulation of legumes by rhizobia. Trends Microbiol 2: 318–324
Downie JA (1998) Functions of rhizobial nodulation genes. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae, Molecular biology of model Plant-associated bacteria. Kluwer, Dordrecht, pp 387–402
Driscoll BT, Finan TM (1996) NADP-dependent malic enzyme of Rhizobium meliloti. J Bacteriol 178: 2224–2231
Driscoll BT, Finan TM (1997) Properties of NAD- and NADP-dependent malic enzymes of Rhizobium (Sinorhizobium meliloti) and differential expression of their genes in nitrogen-fixing bacteroids. Microbiology 143: 489–498
Dubrovo PN, Krylova W, Livanova GI, Zhiznevskaya GY, Izmailov SF (1992) Properties of ATPases of the peribacteroid membrane in root nodules of yellow lupine. Sov Plant Physiol 39: 318–324
Duc G, Messager A (1989) Mutagenesis of Pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Sci 60: 207–213
Eady RR (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96: 3013–3030
Ehrhardt DW, Atkinson EM, Long SR (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256: 998–1000
Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673–681
Elmerich C, Kondorosi A, Newton WE (eds) (1998) Biological nitrogen fixation for the 21st century. 11th Int Congr on Nitrogen Fixation. Kluwer, Dordrecht
Etzler ME, Kalsi G, Ewing NN, Roberts NJ, Day RB, Murphy JB (1999) A Nod factor binding lectin with apyrase activity from legume roots. Proc Natl Acad Sci USA 96: 5856–5861
Fang YW, Hirsch AM (1998) Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol 116: 53–68
Felle HH, Kondorosi E, Kondorosi A, Schultze M (1995) Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant J 7: 939–947
Felle HH, Kondorosi E, Kondorosi A, Schultze M (1998) The role of ion fluxes in Nod factor signalling in Medicago sativa. Plant J 13: 455–463
Firmin JL, Wilson KE, Carlson RW, Davies AE, Downie JA (1993) Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an Oacetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol Microbiol 10: 351–360
Fischer H-M (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58: 352–386
Fischer H-M (1996) Environmental regulation of rhizobial symbiotic nitrogen fixing genes.Trends Microbiol 4: 317–319
Fischer H-M, Schneider K, Babst M, Hennecke H (1999) GRoE1 chaperon are required for the formation of functional nitrogenase in Bradyrhizobium japonicum. Arch Microbiol 171: 279–289
Fisher RF, Long SR (1992) Rhizobium-plant signal exchange. Nature 357: 655–660
Fisher RF, Egelhoff TT, Mulligan JT, Long SR (1988) Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev 2: 282–293
Forde BG, Day HM, Turton JF, Shen W-J, Cullimore JV, Oliver JE (1989) Two glutamine synthetase genes from Phaseolus vulgaris display contrasting developmental and spatial patterns of expression in transgenic Lotus corniculatus plants. Plant Cell 1: 391–401
Fuller F, Minster PW, Nguyen T, Verma DPS (1983) Soybean nodule genes: analysis of cDNA clones reveals several major tissue specific sequences nitrogen-fixing root nodules. Proc Natl Acad Sci USA 80: 2594–2598
Gallon JR, Chaplin AE (1987) An introduction to nitrogen fixation. Cassell, London
Gamas P, Niebel FDC, Lescure N, Cullimore JV (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol Plant-Microbe Interact 9: 233–242
Gantt JS, Larson RJ, Farnham MW, Parthirana SM, Miller S, Vance C (1992) Aspartate aminotransferase in effective and ineffective root nodules. Plant Physiol 98: 868–878
Gogorcena Y, Gordon AJ, Escuredo PR, Minchin FR, Witty JF, Moran JF, Becana M (1998) N2 fixation, carbon metabolism and oxidative damage in nodules of dark-stressed common bean plants. Plant Physiol 113: 1193–1201
Gonzalez EM, Gordon AJ, James CL, Arrese-Igor C (1995) The role of sucrose syn- thase in the response of soybean nodules to drought. J Exp Bot 46: 1515–1523
Gonzalez JE, York GM, Walker GC (1996) Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene 179: 141–146
Gordon AJ (1992) Carbon metabolism in the legume nodule. In: Pollock CJ, Farrar JF, Gordon AJ (eds) Carbon partitioning within and between organisms. Bios, Oxford, pp 33–162
Gordon AJ, James CL (1997) Enzymes of carbohydrate and amino acid metabolism in developing and mature nodules of white clover. J Exp Bot 48: 895–903
Gordon AJ, Ryle GJA, Mitchell DF, Powell CE (1985) The flux of 14C-labelled photosynthate through soyabean root nodules during N2 fixation. J Exp Bot 36: 756–769
Gordon AJ, Ryle GJA, Mitchell DF, Lowry KH, Powell CE (1986) The effect of defoliation on carbohydrate, protein and leghaemoglobin content of white clover nodules. Ann Bot 58: 141–154
Gordon AJ, Mitchell DF, Ryle, GJA, Powell CE (1987) Diurnal production and utilization of photosynthate in nodulated white clover. J Exp Bot 38: 84–98
Gordon AJ, Thomas BJ, Reynolds PHS(1992) Localisation of sucrose synthase in soybean root nodules. New Phytol 122: 35–44
Gordon AJ, Minchin FR, Skot L, James CL (1997) Stress induced declines in soybean nitrogen fixation are related to nodule sucrose synthase activity. Plant Physiol 114: 937–946
Gordon AJ, Minchin FR, James CL, Komina O (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol 120: 867–877
Gunning BES, Pate JS, Minchin FR, Marks I (1974) Quantitative aspects of transfer cell structure in relation to vein loading in leaves and solute transport in legume nodules. In: Transport at the cellular level. SEB Symposium, vol 28. Cambridge University Press, Cambridge, pp 87–126
Hadri AE, Bisseling T (1998) Responses of the plant to Nod factors. In:Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae, molecular biology of model plant-associated bacteria. Kluwer, Dordrecht, pp 403–416
Hanning I, Baumgarten K, Schott K, Heldt HW (1999) Oxaloacetate transport into plant mitochondria. Plant Physiol 119: 1025–1031
Henikoff S, Haughn GW, Calvo JM, Wallace JC (1988) A large family of bacterial activator proteins. Proc Natl Acad Sci USA 85: 6602–6606
Hernandez LE, Cooke DT (1996) Lipid composition of symbiosomes from pea root nodules. Phytochemistry 42: 341–346
Herrada G, Puppo A, Rigaud J (1989) Uptake of metabolites by bacteroid-containing vesicles and by free bacteroids from french bean nodules. J Gen Microbiol 135: 3165–3171
Hirsch AM, Fang YW (1994) Plant hormones and nodulation: what’s the connection? Plant Mol Biol 26: 5–9
Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the rhizobium legume symbiosis. Fungal Genet Biol 23: 205–212
Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86: 1244–1248
Hohnjec N, Becker JD, Puhler A, Perlick AM, Kuster H (1999) Genomic organisation and expression of the MtSucS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula. Mol Gen Genet 261: 524–522
Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96: 2965–2982
Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44: 483–511
Huss-Danell K (1997) Tansley review no 93: actinorhizal symbioses and their N2 fixation. New Phytol 136: 375–405
Jiang QY, Gresshoff PM (1997) Classical and molecular genetics of the model legume Lotus japonicus. Mol Plant-Microbe Interact 10: 59–68
Journet EP, Pichon M, Dedieu A, deBilly F, Truchet G, Barker DG (1994) Rhizobium meliloti Nod factors elicit cell specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J 6: 241–249
Kamst E, Bakkers J, Quaedvlieg NE, Pilling J, Kijne JW, Lugtenberg BJ, Spaink HP (1999) Chitin oligosaccharide synthesis by rhizobia and zebrafish embryos starts by glycosyl transfer to 04 of the reducing-terminal residue. Biochemistry 38: 4045–4052
Kannenberg EL, Brewin NJ (1994) Host-plant invasion by Rhizobium: the role of cell-surface components. Trends Microbiol 2: 277–283
Karl D, Letelier R, Tupas L, Dore J, Christian J, Hebel D (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature, 388: 533–538
Kondorosi A (1992) Regulation of nodulation genes in rhizobia. In: Verma DPS (ed), Molecular signals in plant-microbe communications. CRC Press, Boca Raton, pp 325–340
Kozik A, Heidstra R, Horvath B, Kulikova O, Tikhonovich I, Ellis THN, Vankammen A, Lie TA, Bisseling T (1995) Pea lines carrying syml or sym2 can be modulated by Rhizobium strains containing nodX; syml and sym2 are allelic. Plant Sci 108: 41–49
Kurkdjian AC (1995) Role of the differentiation of root epidermal cells in Nod factor (from Rhizobium meliloti)-induced root hair depolarization of Medicago sativa. Plant Physiol 107: 783–790
Kuzma MM, Winter H, Storer P, Oresnik I, Atkins CA, Layzell DB (1999) The site of oxygen limitation in soybean nodules. Plant Physiol 119: 399–407
Leigh JA, Walker GC (1994) Exopolysaccharides of Rhizobium — synthesis, regulation and symbiotic function. Trends Genet 10: 63–67
Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J (1990) Symbiotic host specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781–784
Le Vier K, Day DA, Guerinot ML (1996) Iron uptake by symbiosomes from soybean root nodules. Plant Physiol 111: 613–618
Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8: 1885–1898
Lorquin J, Lortet G, Ferro M, Mear N, Dreyfus B, Prome JC, Boivin C (1997) Nod factors from Sinorhizobium saheli and S teranga by. sesbaniae are both arabinosylated and fucosylated, a structural feature specific to Sesbania rostrata symbionts. Mol Plant-Microbe Interact 10: 879–890
Madsen O, Sandal L, Sandal N, Marcker KA (1993) A soybean copropopyrinogen oxidase gene is highly expressed in root nodules. Plant Mol Biol 23: 35–43
Marcker K, Lund M, Jensen EO, Marcker KA (1984) Transcription of soybean leghemoglobin gene during nodule development. EMBO J 3: 1691–1695
Mellor RB, Werner D (1986) The fractionation of Glycine max root nodule cells — a methodological overview. Endocytobios Cell Res 3: 317–336
Mellor RB, Christensen TMIE, Bassarab S, Werner D (1985) Phospholipid transfer from ER to the peribacteroid membrane in soybean nodules. Z Naturforsch 40c: 73–79
Mergaert P, Ferro M, D’Haeze W, van Montagu M, Holsters M, Promé JC (1997) Nod factors of Azorhizobium caulinodans strain ORS571 can be glycosylated with an arabinosyl group, a fucosyl group, or both. Mol Plant-Microbe Interact 10: 683–687
Millar AH, Day DA, Bergersen FJ (1995) Microaerobic respiration and oxidative phosphorylation by soybean mitochondria: implications for nitrogen fixation. Plant Cell Environ 18: 715–726
Miller DD, de Ruijter NCA, Bisseling T, Emons AM (I 999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin-perturbing drug. Plant J 17: 141–154
Miller SS, Driscoll BT, Gregerson RG, Gantt JS, Vance CP (1998) Alfalfa malate dehydrogenase (MDH): molecular cloning and characterisation of five different forms reveals a unique nodule-enhanced MDH. Plant J 15: 173–184
Minami E, Kouchi H, Carlson RW, Cohn JR, Kolli VK, Day RB, Ogawa T, Stacey G (1996) Cooperative action of lipo-chitin nodulation signals on the induction of the early nodulin, ENOD2, in soybean roots. Mol Plant-Microbe Interact 7: 574–583
Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29: 881–888
Moreau S, Meyer JM, Puppo A (1995) Uptake of iron by symbiosomes and bacteroids from soybean nodules. FEBS Lett 361: 225–228
Morrell M, Copeland L (1984) Enzymes of sucrose breakdown in soybean nodules. Plant Physiol 74: 1030–1034
Morrell M, Copeland L (1985) Sucrose synthase of soybean nodules. Plant Physiol 78: 149–154
Mouritzen P, Rosendahl L (1997) Identification of a transport mechanism for NH4+ in the symbiosome membrane of pea root nodules. Plant Physiol 115: 519–526
Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7: 869–885
Nap JP, Bisseling T (1990) Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science 250: 948–954
Nicolaou KC, Bockovich NJ, Carcanague DR, Hummel CW, Even LF (1992) Total synthesis of the NodRm-IV factors, the Rhizobium nodulation signals. J Am Chem Soc 114: 8701–8702
Niebel A, Bono JJ, Ranjeva R, Cullimore JV (1997) Identification of a high-affinity binding site for lipo-oligosaccharidic NodRm factors in the microsomal fraction of Medicago cell suspension cultures. Mol Plant-Microbe Interact 10: 132–134
O’Brian MR (1996) Herne synthesis in the Rhizobium-legume symbiosis: a palette for bacterial and eukaryotic pigments. J Bacteriol 178; 2471–2478
Ou Yang L-J, Day DA (1992) Transport properties of sybiosomes isolated from sir-atro nodules. Plant Physiol Biochem 30: 613–623
Palacios R, Mora J, Newton WE (1993) (eds) New horizons in nitrogen fixation. 9th International Congress on Nitrogen Fixation. Kluwer, Dordrecht
Pate JS, Gunning BES, Briarty LG (1969) Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta 85: 11–34
Pathirana MS, Samac DA, Roeven R, Yoshioka H, Vance CP (1997) Analysis phosphoenolpyruvate carboxylase gene structure and expression in alfalfa nodules. Plant J 12: 293–304
Pawlowski K (1997) Nodule-specific gene expression. Physiol Plant 99: 617–631
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 303: 1533–1539
Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527–530
Perotto S, Vandenbosch KA, Butcher GW, Brewin NJ (1991) Molecular composition and development of the plant glycocalyx associated with the peribacteroid membrane of pea nodules. Development 112: 763–773
Peters NK (1997) Nodulation: finding the lost common denominator. Curr Biol 7: R223 - R226
Pingret JL, Journet EP, Barker DG (1998) Rhizobium Nod factor signaling. Evidence for a G protein-mediated transduction mechanism. Plant Cell 10: 659672
Postgate J (1987) Nitrogen fixation, 2nd edn. Arnold, London
Preisig O, Anthamatten D, Hennecke H (1993) Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for nitrogen-fixing endosymbiosis. Proc Natl Acad Sci USA 90: 3309–3313
Preisig O, Zufferey R, Hennecke H (1996) The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high affinity cbb 3 type cytochrome oxidase. Arch Microbiol 165: 297–305
Price GD, Day DA, Gresshoff PM (1987) Rapid isolation of intact peribacteroid envelopes from soybean nodules and demonstration of selective permeability to metabolites. J Plant Physiol 130: 157–164
Price NPJ, Relic B, Talmont E, Lewin A, Prome D, Pueppke SG, Maillet F, Dénarié J, Promé JC, Broughton WJ (1992) Broad host range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are 0-acetylated or sulphated. Mol Microbiol 6: 3575–3584
Radyukina NL, Bruskova RK, Izmailov SF (1992) Transport of 14C substrate through peribacteroidal membrane of yellow-lupin nodules. Dokl Bot Sci 323: 603–606
Rai AN (ed) (1990) A handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, Florida
Rawsthorne S, La Rue TA (1986) Metabolism under microaerobic conditions of mitochondria from cowpea nodules. Plant Physiol 81: 1097–1102
Ribbe M, Gadkari D, Meyer O (1997) N2 fixation by Steptomyces thermoautotrophicus involves a molybdenum-dinitrogenase and a manganese superoxide oxidoreductase that couple N2 reduction to the oxidation of superoxide produced from O2 by a molybdenum-Co dehydrogenase. J Biol Chem 272: 26627–26633
Robertson JG, Taylor MP (1973) Acid and alkaline invertases in roots and nodules of Lupinus augustifolius infected with Rhizobium lupini. Planta 112: 1–6
Robertson JG, Lyttleton P (1984) Division of peribacteroid membranes in root nodules of white clover. J Cell Sci 69: 147–157
Robertson JG, Warburton MP, Lyttleton P, Fordyce AM, Bullivan S (1978) Membranes in lupin root nodules. II. Preparation and properties of peribacteroid membranes and bacteroid envelope inner membranes from developing lupin nodules. J Cell Sci 30: 151–174
Robinson DL, Pathirana SM, Gantt JS, Vance CP (1996) Immunogold localisation of nodule-enhanced phosphoenolpyruvate carboxylase in alfalfa. Plant Cell Environ 19: 602–608
Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, Truchet G, Dénarié J, Promé JC (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulphation of lipo-oligosaccharide signals. Cell 67: 1131–1143
Roche P, Maillet F, Plazanet C, Debellé F, Ferro M, Truchet G, Promé JC, Dénarié J (1996) The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc Natl Acad Sci USA 93: 15305–15310
Rosendahl L, Dilworth MJ, Glenn AR (1992) Exchange of metabolites across the peribacteroid membrane in pea root nodules. J Plant Physiol 139: 635–638
Roth EJK, Stacey G (1988) Homology in endosymbiotic systems: the term “symbiosome”. In: Palacios R, Verma DPS (eds) Molecular genetics of plant-microbe interactions. American Phytopathology Society, St Paul, pp 220–225
Sadowsky MJ, Graham PH (1998) Soil biology of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae, molecular biology of model plant-associated bacteria. Kluwer, Dordrecht, pp 155–172
Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula ( Gaertn) after gamma-ray mutagenesis. Plant Sci 111: 63–71
Santana MA, Pihakaski-Maunsbach K, Sandal N, Marker KA, Smith AG (1998) Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiol 116: 1259–1269
Schauser L, Handberg K, Sandal N, Stiller J, Thykjaer T, Pajuelo E, Nielsen A, Stougaard J (1998) Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol Gen Genet 259: 414–423
Scheres B, Van De Wiel C, Zalensky A, Horvath B, Spaink HP, van Eck H, Zwartkruis F, Wolters AM, Gloudemans T, Van Kammen A, Bisseling T (1990) The ENOD12 gene product is involved in the infection process during pea-Rhizobium interaction. Cell 60: 281–294
Schlaman HRM, Okker RJH, Lugtenberg BJJ (1992) Regulation of nodulation gene expression by nodD in Rhizobia. J Bacteriol 174: 5177–5182
Schlaman HRM, Phillips DA, Kondorosi E (1998) Genetic organization and transcriptional regulation of rhizobial nodulation genes. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae, molecular biology of model plant-associated bacteria. Kluwer, Dordrecht, pp 361–386
Schmidt J, Rohrig H, John M, Wieneke U, Stacey G, Koncz C, Schell J (1993) Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J 4: 651–658
Schubert KR, Boland MJ (1990) The ureides. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants, vol 16. Academic Press, San Diego, pp 197–282
Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32: 33–57
Schultze M, Kondorosi E, Ratet P, Buire M, Kondorosi A (1994) Cell and molecular biology of Rhizobium-plant interactions. Int Rev Cytol 156: 1–75
Selker JML (1988) Three-dimensional organization of uninfected tissue in soybean root nodules and its relation to cell specialization in the central region. Protoplasma 147: 178–190
Selker JML, Newcomb EH (1985) Spatial relationships between uninfected and infected cells in root nodules of soybean. Planta 156: 446–454
Semino CE, Robbins PW (1995) Synthesis of “Nod”-like chitin oligosaccharides by the Xenopus developmental protein DG42. Proc Natl Acad Sci USA 92: 3498–3501
She Q, Lauridsen P, Stougaard J, Marcker KA (1993) Minimal enhancer elements of the leghaemoglobin lba and lbc3 gene promoters from Glycine max have different properties. Plant Mol Biol 22: 945–956
Shi LF, Twary SN, Yoshioka H, Gregerson RG, Miller SS, Samac DA, Gantt, Unkefer PJ, Vance CP (1997) Nitrogen assimilation in alfalfa: isolation and characterisation of an asparagine synthetase gene showing enhanced expression in root nodules and dark adapted leaves. Plant Cell 9: 1339–1356
Smit G, de Koster CC, Schripsema J, Spaink HP, van Brussel AAN, Kijne JW (1995) Uridine, a cell division factor in pea roots. Plant Mol Biol 29: 869–873
Soupene E, Foussard M, Boistard P, Truchet G, Batut J (1995) Oxygen as a key developmental regulator of Rhizobium meliloti N2 fixation gene-expression within the alfalfa root-nodule. Proc Natl Acad Sci USA 92: 3759–3763
Spaink H P (1995) The molecular basis of infection and nodulation by rhizobia — the ins and outs of sympathogenesis. Annu Rev Phytopathol 33: 345–368
Spaink HP (1996) Regulation of plant morphogenesis by lipo-chitin oligosaccharides. Crit Rev Plant Sci 15: 559–582
Sprent JI, Sprent P (1990) Nitrogen-fixing organisms: pure and applied aspects. Chapman and Hall, London
Streeter JG (1991) Transport and metabolism of carbon and nitrogen in legume nodules. Adv Bot Res 18: 129–187
Streeter JG (1992) Analysis of apoplastic solutes in the cortex of soybean nodules. Physiol Plant 84: 584–592
Streeter JG (1995) Recent developments in carbon transport and metabolism in symbiotic systems. Symbiosis 19: 175–196
Sutton JM, Lea EJA, Downie JA (1994) The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci USA 91: 9990–9994
Szafran MM, Haaker H (1995) Properties of the peribacteroid membrane ATPase of pea root nodules and its effect on the nitrogenase activity. Plant Physiol 108: 1227–1232
Szczyglowski K, Hamburger D, Kapranov P, deBruijn FJ (1997) Construction of a Lotus japonicus late nodulin expressed sequence tag library and identification of novel nodule specific genes. Plant Physiol 114: 1335–1346
Szczyglowski K, Kapranov P, Hamburger D, deBruijn FJ (1998a) The Lotus japonicus NOD70 nodulin gene encodes a protein with similarities to transporters. Plant Mol Biol 37: 651–661
Szczyglowski K, Shaw RS, Wopereis J, Copeland S, Hamburger D, Kasiborski B, Dazzo FB, De Bruijn FJ (1998b) Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol Plant-Microbe Interact 11: 684–697
Takane K, Tajimas, Kouchi H (1997) Two distinct uricase (nodulin 35) genes are differentially expressed in soybean plants. Mol Plant-Microbe Interactions 10: 735–741
Temple SJ, Heard J, Ganter J, Dunn G, Sengupta-Gopalan C (1995) Characterisation of a nodule-enhanced glutamine synthetase from alfalfa. Mol Plant-Microbe Interact 8: 218–227
Temple SJ, Kunjibettu S, Roche D, Sengupta-Gopalan S (1996) Total glutamine synthetase activity during soybean nodule development is controlled at the level of transcription and holoprotein turnover. Plant Physiol 112: 1723–1733
Temple SJ, Vance CP, Gantt JS (1998) Glutamate synthase and nitrogen assimilation. Trends Plant Sci 3: 51–56
Tercé-Laforgue T, Carrayol E, Cren M, Desbrosses G, Hecht V, Hirel B (1999) A strong constitutive positive element is essential for the ammonium-regulated expression of a soybean gene encoding cytosolic glutamine synthetase. Plant Mol Biol 39: 551–564
Thummler F, Verma DPS (1987) Nodulin-100 of soybean is the subunit of sucrose synthase regulated by the availability of free heme in nodules. J Biol Chem 262: 14730–14736
Tikonovich IA, Provoro NA, Romanov VI, Newton WE (1995) Nitrogen fixation: fundamentals and applications. 10th International Congress of Nitrogen Fixation. Kluwer, Dordrecht
Timmers ACJ, Auriac MC, Debilly F, Truchet G (1998) Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125: 339–349
Trepp GB, van de Mortel M, Yoshioka H, Miller SS, Samac DA, Gantt JS, Vance CP (1999a) NADH-glutamate synthase in alfalfa roots. Genetic regulation and cellular expression. Plant Physiol 119: 817–828
Trepp GB, Plank DW, Gantt, Vance CP (1999b) NADH-glutamate synthase in alfalfa root nodules. Immunocytochemical localisation. Plant Physiol 119: 829837
Trepp GB, Temple SJ, Bucciarelli B, Shi LF, Vance CP (1999c) Expresssion map for genes involved in nitrogen and carbon metabolism in alfalfa root nodules. Mol Plant-Microbe Interact 12: 526–535
Trinchant J-C, Birot AM, Rigaud J (1981) Oxygen supply and energy-yielding substrates for nitrogen fixation (acetylene reduction) by bacteroid preparations. J Gen Microbiol 125: 159–165
Trinchant J-C, Guérin V, Rigaud J (1994) Acetylene reduction by symbiosomes and free bacteroids from faba-bean (Vicia faba L.) nodules. Plant Physiol 105: 555–561
Trinchant J-C, Yang Y.S., Rigaud J (1998) Proline accumulation inside symbiosomes of faba bean nodules under salt stress. Physiol Plant 104: 38–49
Truchet G, Roche P, Lerouge P, Vasse J, Camut S, De Billy F, Promé JC, Dénarié J (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670–673
Tyerman SD, Whitehead LF, Day DA (1995) A channel-like transporter for NH4+ on the symbiotic surface of N2 fixing plants. Nature 378: 629–632
Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett 231: 36–40
Udvardi MK, Day DA (1989) Electrogenic ATPase activity on the peribacteroid membrane of soybean (Glycine max L.) root nodules. Plant Physiol 90: 982–987
Udvardi MK, Day DA (1990) Ammonia (14C-methylamine) transport across the bacteroid and peribacteroid membranes of soybean (Glycine max L.) root nodules. Plant Physiol 94: 71–76
Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 42: 373–392
Udvardi MK, Lister DL, Day DA (1991) ATPase activity and anion transport across the peribacteroid membrane of isolated soybean symbiosomes. Arch Microbiol 156: 362–366
van Brussel AAN, Zaat SAJ, Canter-Cremers HCJ, Wijffelman CA, Pees E, Tak T, Lugtenberg BJJ (1986) Role of plant root exudate and Sym plasmid-localized nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor, which causes thick and short roots on common vetch. J Bacteriol 165: 517–522
van Brussel AAN, Bakhuizen R, Van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJJ, Kijne JW (1992) Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257: 70–72
Vanden Bosch KA, Newcomb EH (1988) The occurrence of leghaemoglobin protein in the uninfected instertitial cells of soybean root nodules. Planta 175: 442–451
van der Sande K, Pawlowski K, Czaja I, Wieneke U, Schmidt J, Walden R, Matvienko M, Wellink J, van Kammen A, Franssen H, Bisseling T (1996) Modification of phytohormone response by a peptide encoded by ENOD40 of legume and a nonlegume. Science 273: 370–373
van der Weil C, Scheres B, Franssen H, van Lierop MJ, van Lammeren A, van Kammen A, Bisseling T (1990) The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J 9: 1–7
Vance CP, Gantt JS (1992) Control of nitrogen and carbon metabolism in root nodules. Physiol Plant 85: 266–274
Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaption. Annu Rev Plant Physiol Plant Mol Biol 42: 373–392
Vance CP, Gregerson RG, Robinson SL, Miller SS, Gantt JS (1994) Primary assimilation of nitrogen in alfalfa nodules: molecular features of the enzymes involved. Plant Sci 101: 51–64
Vance CP, Miller SS, Gregerson RG, Samac DA, Robinson DL, Gantt JS (1995) Alfalfa NADH-dependent glutamate synthase: structure of the gene and importance in symbiotic nitrogen fixation. Plant J 8: 345–358
Verma DPS, Hong ZL (1996) Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol 4: 364–368
Walsh (1995) Physiology of the legume nodule and its response to stress. Soil Biol Biochem 27: 637–655
Walsh KB, Vessey JK, Layzell DB (1987) Carbohydrate supply and N2 fixation in soybean. The effect of varied daylength and stem girdling. Plant Physiol 85: 137–144
Walsh KB, Canny MJ, Layzell DB (1989) Vascular transport and soybean nodule function: II, a role for phloem supply in product export. Plant Cell Environ 12: 713–723
Wang TL, Hedley CL (1993) Seed mutants in Pisum. Pisum Genet 25: 64–70
Waters JK, Hughes BL, Purcell LC, Gerhardt KO, Mawhinney TP, Emerich DW (1998) Alanine, not ammonia, is excreted from nitrogen-fixing soybean nodule bacteroids. Proc Natl Acad Sci USA 95: 12038–12042
Weaver CD, Shomer NH, Louis CF, Roberts DM (1994) Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem 269: 1858–1862
Wittenberg JB, Wittenberg BA, Day DA, Udvardi MK, Appelby CA (1996) Siderophore-bound iron in the peribacteroid space of soybean root nodules. Plant Soil 178: 161–169
Wycoff KL, Hunt S, Gonzales MB, VandenBosch KA, Layzell DB, Hirsch AM (1998) Effects of oxygen on nodule physiology and expression of nodulins in alfalfa. Plant Physiol 117: 385–395
Yang GP, Debellé F, Savagnac A, Ferro M, Schiltz O, Maillet F, Promé D, Trilhou M, Vialas C, Lindstrom K, Dénarié J, Promé JC (1999) Structure of the Mesorhizobium huakuii and Rhizobium gaelgae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with a,(3-unsaturated N-acyl substitutions. Mol Microbiol 34: 227–237
Yoshioka H, Gregerson RG, Samac DA, Hoevens KCM, Trepp G, Gantt JS, Vance CP (1999) Aspartate aminotransferase in alfalfa nodules. Mol Plant-Microbe Interact 12: 263–274
Young JPW (1992) Phylogenetic classification of nitrogen-fixing organisms. In: Biological nitrogen fixation. Stacey G, Burris RH, Evans HJ (eds) Chapman and Hall, New York pp. 43–86
Zammit A, Copeland L (1993) Immunocytochemical localisation of nodule-specific sucrose synthase in soybean nodules. Aust J Plant Physiol 20: 25–32
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Gordon, A.J., Lea, P.J., Rosenberg, C., Trinchant, JC. (2001). Nodule Formation and Function. In: Lea, P.J., Morot-Gaudry, JF. (eds) Plant Nitrogen. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-04064-5_5
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