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Plant and Soil

, Volume 321, Issue 1–2, pp 35–59 | Cite as

Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants

  • Claudine Franche
  • Kristina Lindström
  • Claudine Elmerich
Review Article

Abstract

Nitrogen is generally considered one of the major limiting nutrients in plant growth. The biological process responsible for reduction of molecular nitrogen into ammonia is referred to as nitrogen fixation. A wide diversity of nitrogen-fixing bacterial species belonging to most phyla of the Bacteria domain have the capacity to colonize the rhizosphere and to interact with plants. Leguminous and actinorhizal plants can obtain their nitrogen by association with rhizobia or Frankia via differentiation on their respective host plants of a specialized organ, the root nodule. Other symbiotic associations involve heterocystous cyanobacteria, while increasing numbers of nitrogen-fixing species have been identified as colonizing the root surface and, in some cases, the root interior of a variety of cereal crops and pasture grasses. Basic and advanced aspects of these associations are covered in this review.

Keywords

Nitrogen fixation Symbiosis Rhizobia Frankia Cyanobacteria Azospirillum 

Notes

Acknowledgments

The authors are indebted to Dr. German Jurgens, Department of Applied Chemistry and Microbiology, Helsinki University, Finland, for drawing a phylogenetic tree of nitrogen fixers, and to Ms. Jerri Bram for improving the language.

References

  1. Aßmus B, Hutzler P, Kirchhof G, Amann R, Lawrence JR, Hartmann A (1995) In situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled, rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl Environ Microbiol 61:1013–1019PubMedGoogle Scholar
  2. Adams DG (2002) Symbioses with hornworts and liverworts. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic, Dordrecht, pp 117–136Google Scholar
  3. Arnold W, Rump A, Klipp W, Priefer UB, Pühler A (1988) Nucleotide sequence of a 24,206-base-pair DNA fragment carrying the entire nitrogen fixation gene cluster of Klebsiella pneumoniae. J Mol Biol 203:715–738 doi: 10.1016/0022-2836(88)90205-7 PubMedCrossRefGoogle Scholar
  4. Arsène F, Katupitiya S, Kennedy IR, Elmerich C (1994) Use of lacZ fusions to study the expression of nif genes of Azospirillum brasilense in association with plants. Mol Plant Microbe Interact 7:748–757Google Scholar
  5. Ausmees N, Kobayashi H, Deakin WJ, Marie C, Krishnan HB, Broughton WJ, Perret X (2004) Characterization of NopP, a type III secreted effector of Rhizobium sp. strain NGR234. J Bacteriol 18:4774–4780 doi: 10.1128/JB.186.14.4774-4780.2004 CrossRefGoogle Scholar
  6. Baca BE, Elmerich C (2007) Microbial production of plant hormones. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 113–143CrossRefGoogle Scholar
  7. Balandreau J (1983) Microbiology of the association. Can J Microbiol 29:851–859Google Scholar
  8. Baldani JI, Baldani VLD (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Cienc 77:549–579 doi: 10.1590/S0001-37652005000300014 PubMedGoogle Scholar
  9. Benson DR, Clawson ML (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330 doi: 10.1111/j.1399-3054.2007.00934.x CrossRefGoogle Scholar
  10. Benson DR, Clawson ML (2000) Evolution of the actinorhizal plant symbioses. In: Triplett EW (ed) Prokaryotic nitrogen fixation: A model system for analysis of biological process. Horizon Scientific Press, Wymondham, UK, pp 207–224Google Scholar
  11. Berg RH (1990) Cellulose and xylans in the interface capsule in symbiotic cells of actinorhizae. Protoplasma 159:35–43 doi: 10.1007/BF01326633 CrossRefGoogle Scholar
  12. Berg RH (1999) Frankia forms infection threads. Can J Bot 77:1327–1333 doi: 10.1139/cjb-77-9-1327 CrossRefGoogle Scholar
  13. Bergersen F (1980) Methods for evaluating biological nitrogen fixation. Willey and Sons, ChichesterGoogle Scholar
  14. Bergman B (2002) Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic, Dordrecht, pp 207–232Google Scholar
  15. Bergman B, Matveyev A, Rasmussen U (1996) Chemical signalling in cyanobacterial-plant symbioses. Trends Plant Sci 1:191–197 doi: 10.1016/1360-1385(96)10021-2 CrossRefGoogle Scholar
  16. Berry MA, Sunell AL (1990) The infection process and nodule development. In: Schwintzer RC, Tjepkema JD (eds) The Biological of Frankia and actinorhizal plants. Academic press Inc, San Diego, pp 61–88Google Scholar
  17. Bock JV, Battershell T, Wiggington J, John TR, Johnson JD (2001) Frankia sequences exhibiting RNA polymerase promoter activity. Microbiology 147:499–506PubMedGoogle Scholar
  18. Boddey RM, Döbereiner J (1982) Association of Azospirillum and other diazotrophs with tropical gramineae. In: Non symbiotic nitrogen fixation and organic matter in the tropics. Indian Society of Soil Science, New Delhi, pp 28–47Google Scholar
  19. Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) The use of 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosyst 57:235–270 doi: 10.1023/A:1009890514844 CrossRefGoogle Scholar
  20. Boddey RM, Polidoro JC, Resende AS, Alves BJR, Urquiaga S (2001) Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses. Aust J Plant Physiol 28:889–895Google Scholar
  21. Borthakur PB, Orozco CC, Young-Robbins SS, Haselkorn R, Callahan SM (2005) Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp PCC 7120. Mol Microbiol 57:111–113 doi: 10.1111/j.1365-2958.2005.04678.x PubMedCrossRefGoogle Scholar
  22. Boyer M, Bally R, Perrotto S, Chaintreuil C, Wisniewski-Dyé F (2008) A quorum quenching approach to identify quorum-sensing-regulated functions in Azospirillum lipoferum. Res Microbiol ▪▪▪:159 doi: 10.1016/j.resmic.2008.08.003
  23. Buikema WJ, Haselkorn R (1991) Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena sp PCC 7120. Genes Dev 5:321–330 doi: 10.1101/gad.5.2.321 PubMedCrossRefGoogle Scholar
  24. Buikema WJ, Haselkorn R (1993) Molecular genetics of cyanobacterial development. Annu Rev Plant Physiol 44:33–52 doi: 10.1146/annurev.pp.44.060193.000341 CrossRefGoogle Scholar
  25. Burdman S, Dulguerova G, Okon Y, Jurkevitch E (2001) Purification of the major outer membrane protein of Azospirillum brasilense, its affinity to plant roots and its involvement in cell aggregation. Mol Plant Microbe Interact 14:555–561 doi: 10.1094/MPMI.2001.14.4.555 PubMedCrossRefGoogle Scholar
  26. Burris RH, Miller CE (1941) Application of 15N to the study of biological nitrogen fixation. Science 93:114–115 doi: 10.1126/science.93.2405.114 PubMedCrossRefGoogle Scholar
  27. Caballero-Mellado J, Martínez-Aguilar L, Paredes-Valdez G, Estrada-de los Santos P (2004) Burkholderia unamae sp nov, an N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 5:1165–1172 doi: 10.1099/ijs.0.02951-0 CrossRefGoogle Scholar
  28. Callaham D, DelTredici P, Torrey JG (1978) Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199:899–902 doi: 10.1126/science.199.4331.899 PubMedCrossRefGoogle Scholar
  29. Callahan SM, Buikema WJ (2001) The role of HetN in maintenance of the heterocyst pattern in Anabaena sp PCC 7120. Mol Microbiol 40:941–950 doi: 10.1046/j.1365-2958.2001.02437.x PubMedCrossRefGoogle Scholar
  30. Campbell EL, Meeks JC (1989) Characteristics of hormogonia formation by symbiotic Nostoc spp in response to the presence of Anthoceros punctatus or its extracellular products. Appl Environ Microbiol 55:125–131PubMedGoogle Scholar
  31. Carreño-Lopez R, Campos-Reales NB, Elmerich C, Baca BE (2000) Physiological evidence for differently regulated tryptophan-dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilense. Mol Gen Genet 264:521–530 doi: 10.1007/s004380000340 PubMedCrossRefGoogle Scholar
  32. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647–1666PubMedCrossRefGoogle Scholar
  33. Cérémonie H, Cournoyer B, Maillet F, Normand P, Fernandez MP (1998) Genetic complementation of rhizobial nod mutants with Frankia DNA: artefact or realty? Mol Gen Genet 260:115–119 doi: 10.1007/s004380050877 PubMedCrossRefGoogle Scholar
  34. Cérémonie H, Debellé F, Fernandez MP (1999) Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can J Bot 77:1293–1301 doi: 10.1139/cjb-77-9-1293 CrossRefGoogle Scholar
  35. Chelius MK, Triplett EW (2000) Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl Environ Microbiol 66:783–787 doi: 10.1128/AEM.66.2.783-787.2000 PubMedCrossRefGoogle Scholar
  36. Chen WM, James EK, Chou JH, Sheu SY, Yang SZ, Sprent JI (2005) Beta-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol 168:661–675 doi: 10.1111/j.1469-8137.2005.01533.x PubMedCrossRefGoogle Scholar
  37. Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legumes symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272 doi: 10.1128/JB.185.24.7266-7272.2003 PubMedCrossRefGoogle Scholar
  38. Clawson ML, Bourret A, Benson DR (2004) Assessing the phylogeny of Frankia-related plant nitrogen-fixing root nodule symbioses with Frankia 16SRNA and glutamine synthetase gene sequences. Mol Phylogenet Evol 31:131–138 doi: 10.1016/j.ympev.2003.08.001 PubMedCrossRefGoogle Scholar
  39. Cohen MF, Meeks JC (1997) A hormogonium regulating locus, hrmUA, of the cyanobacterium Nostoc punctiforme strain ATCC29133 and its response to an extract of a symbiotic plant partner Anthoceros punctatus. Mol Plant Microbe Interact 10:280–289 doi: 10.1094/MPMI.1997.10.2.280 PubMedCrossRefGoogle Scholar
  40. Cohen MF, Sakihama Y, Takagi YC, Ichiba T, Yamasaki H (2002) Synergistic effect of deoxyanthocyanins from symbiotic fern Azolla spp on hrmA gene induction in the cyanobacterium Nostoc punctiforme. Mol Plant Microbe Interact 9:875–882 doi: 10.1094/MPMI.2002.15.9.875 CrossRefGoogle Scholar
  41. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365 doi: 10.1111/j.1365-2672.2007.03366.x PubMedCrossRefGoogle Scholar
  42. Costa JL, Lindblad P (2002) Cyanobacteria in symbiosis in cycads. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic, Dordrecht, pp 195–206Google Scholar
  43. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18 doi: 10.3109/10408419509113531 PubMedCrossRefGoogle Scholar
  44. Cournoyer B, Normand P (1994) Gene expression in Frankia: characterization of promoters. Microbiology 78:229–236Google Scholar
  45. Dawson JO (1983) Dinitrogen fixation in forest ecosystems. Can J Microbiol 29:979–992Google Scholar
  46. Dawson JO (1990) Interaction among actinorhizal and associated plant species. In: Schwintzer RC, Tjepkema JD (eds) The Biological of Frankia and actinorhizal plants. Academic press Inc, San Diego, pp 299–316Google Scholar
  47. De Oliveira Pinheiro R, Boddey LH, James EK, Sprent JI, Boddey RM (2002) Adsorption and anchoring of Azospirillum strains to roots of wheat. Plant Soil 246:151–166 doi: 10.1023/A:1020645203084 CrossRefGoogle Scholar
  48. Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signalling moleculaes mediating regcognition and morphogenosis. Annu Rev Biochem 65:503–535 doi: 10.1146/annurev.bi.65.070196.002443 PubMedCrossRefGoogle Scholar
  49. Dénarié J, Debellé F, Truchet G, Promé JC (1993) Rhizobium and legume nodulation: A molecular dialogue. In: Palacios R, Mora J, Newton WE (eds) New horizons in nitrogen fixation. Kluwer, Dordrecht, pp 19–30Google Scholar
  50. Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631 doi: 10.1038/nrmicro954 PubMedCrossRefGoogle Scholar
  51. Dobbelaere S, Okon Y (2007) The plant growth promoting effect and plant response. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 145–170CrossRefGoogle Scholar
  52. Döbereiner J, Day JM, Dart PJ (1972) Nitrogenase activity and oxygen sensitivity of the Paspalum notatum-Azotobacter paspali association. J Gen Microbiol 71:103–116Google Scholar
  53. Döbereiner J, Pedrosa FO (1987) Nitrogen-fixing bacteria in non-leguminous crop plants. Science Tech, Madison and Springer Verlag, BerlinGoogle Scholar
  54. Döbereiner J (1992) History and new perspectives of diazotrophs in association with non-leguminous plants. Symbiosis 13:1–13Google Scholar
  55. Dörr J, Hurek T, Reinhold-Hurek B (1998) Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol Microbiol 30:7–17 doi: 10.1046/j.1365-2958.1998.01010.x PubMedCrossRefGoogle Scholar
  56. Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 1331:900–910 doi: 10.1104/pp.102.018150 Google Scholar
  57. Dresler-Nurmi A, Fewer D, Räsänen LA, Lindström K (2007) The diversity and evolution of rhizobia. In: Pawlowski K (ed) Prokaryotic endosymbionts in plants. Springer Verlag doi: 101007/7171
  58. Duhoux E, Diouf D, Gherbi H, Franche C, Ahée J, Bogusz D (1996) Le nodule actinorhizien. Acta Bot Gallica 143:593–608Google Scholar
  59. Ehira S, Ohmori M, Sato N (2003) Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp strain PCC 7120. DNA Res 10:97–113 doi: 10.1093/dnares/10.3.97 PubMedCrossRefGoogle Scholar
  60. Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp isolated from wild rice species. Appl Environ Microbiol 67:5285–5293 doi: 10.1128/AEM.67.11.5285-5293.2001 PubMedCrossRefGoogle Scholar
  61. Elmerich C, Newton WE (2007) Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations. Springer, The NetherlandsCrossRefGoogle Scholar
  62. Elmerich C, Zimmer W, Vieille C (1992) Associative nitrogen-fixing bacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall Inc, New York, pp 212–258Google Scholar
  63. Fallik E, Okon Y, Epstein E, Goldman A, Fischer M (1989) Identification and quantification of IAA and IBA in Azospirillum brasilense-inoculated maize roots. Soil Biol Biochem 21:147–153 doi: 10.1016/0038-0717(89)90024-2 CrossRefGoogle Scholar
  64. FAO (2008) Current world fertilizer trends and outlook 2011/2012. Food and agricultural organization of the United Nations, RomeGoogle Scholar
  65. Fischer HM (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386PubMedGoogle Scholar
  66. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401 doi: 10.1038/387394a0 PubMedCrossRefGoogle Scholar
  67. Foucher C, Kondorosi E (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43:773–786 doi: 10.1023/A:1006405029600 PubMedCrossRefGoogle Scholar
  68. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300 doi: 10.1128/MMBR.68.2.280-300.2004 PubMedCrossRefGoogle Scholar
  69. Geurts R, Bisseling T (2002) Rhizobium nod factor perception and signalling. Plant Cell 14(Suppl):S239–S249PubMedGoogle Scholar
  70. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008a) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria. Proc Natl Acad Sci USA 105:4928–4932 doi: 10.1073/pnas.0710618105 PubMedCrossRefGoogle Scholar
  71. Gherbi H, Nambiar-Veetil M, Zhong C, Félix J, Autran D, Girardin R, Auguy F, Bogusz D, Franche C (2008b) Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Mol Plant Microbe Interact 21:518–524 doi: 10.1094/MPMI-21-5-0518 PubMedCrossRefGoogle Scholar
  72. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Verméglio A, Médigue C, Sadowsky M (2007) Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312 doi: 10.1126/science.1139548 PubMedCrossRefGoogle Scholar
  73. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7 doi: 10.1016/j.femsle.2005.07.030 PubMedCrossRefGoogle Scholar
  74. Golden JW, Yoon HS (2003) Heterocyst development in Anabaena. Curr Opin Microbiol 6:557–563 doi: 10.1016/j.mib.2003.10.004 PubMedCrossRefGoogle Scholar
  75. Goormachtig S, Capoen W, Holsters M (2004) Rhizobium infection : lessons from the versatile nodulation behaviours of water tolerant legumes. Trends Plant Sci 9:518–522 doi: 10.1016/j.tplants.2004.09.005 PubMedCrossRefGoogle Scholar
  76. Hamelin J, Fromin N, Tarnawski S, Teyssier-Cuvelle S, Aragno M (2002) nifH gene diversity in the bacterial community associated with the rhizosphere of Molinia coerulea, an oligonitrophilic perennial grass. Environ Microbiol 4:477–481 doi: 10.1046/j.1462-2920.2002.00319.x PubMedCrossRefGoogle Scholar
  77. Hardy RWF, Burns RC, Holsten RD (1973) Application of the acetylene-ethylene reduction assay for measurement of nitrogen fixation. Soil Biol Biochem 5:47–81 doi: 10.1016/0038-0717(73)90093-X CrossRefGoogle Scholar
  78. Hauwaerts D, Alexandre G, Das SK, Vanderleyden J, Zhulin IB (2002) A major chemotaxis gene cluster in Azospirillum brasilense and relationships between chemotaxis operons in α-proteobacteria. FEMS Microbiol Lett 208:61–67PubMedGoogle Scholar
  79. Henson BJ, Watson LE, Barnum SR (2004) The evolutionary history of nitrogen fixation, as assessed by nifD. J Mol Evol 58:390–399 doi: 10.1007/s00239-003-2560-0 PubMedCrossRefGoogle Scholar
  80. Hocher V, Auguy F, Argout X, Laplaze L, Franche C, Bogusz D (2006) Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytol 169:681–688 doi: 10.1111/j.1469-8137.2006.01644.x PubMedCrossRefGoogle Scholar
  81. Holguin G, Glick BR (2001) Expression of the ACC deaminase gene from Enterobacter cloacae UW4 in Azospirillum brasilense. Microb Ecol 41:281–288PubMedGoogle Scholar
  82. Hu Y, Fay AW, Lee CC, Ribbe MW (2007) P-cluster maturation on nitrogenase MoFe protein. Proc Natl Acad Sci USA 104:10424–10429 doi: 10.1073/pnas.0704297104 PubMedCrossRefGoogle Scholar
  83. Huang X, Dong Y, Zhao J (2004) HetR homodimer is a DNA binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. Proc Natl Acad Sci USA 101:4848–4853 doi: 10.1073/pnas.0400429101 PubMedCrossRefGoogle Scholar
  84. Hurd TM, Raynal DJ, Schwintzer CR (2001) Symbiotic N2 fixation of Alnus incana spp rugosa in shrub wetlands of the Adirondack mountains, New York, USA. Oecologia 126:94–103 doi: 10.1007/s004420000500 CrossRefGoogle Scholar
  85. Hurek T, Reinhold-Hurek B (2003) Azoarcus sp strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178 doi: 10.1016/j.jbiotec.2003.07.010 PubMedCrossRefGoogle Scholar
  86. Hurek T, Handlley LL, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant Microbe Interact 15:233–242 doi: 10.1094/MPMI.2002.15.3.233 PubMedCrossRefGoogle Scholar
  87. Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405 doi: 10.1046/j.1469-8137.1997.00755.x CrossRefGoogle Scholar
  88. James EK, Olivares FL (1998) Infection and colonisation of sugarcane and other graminaceous plants by endophytic diazotrophs. Crit Rev Plant Sci 17:77–119 doi: 10.1016/S0735-2689(98)00357-8 CrossRefGoogle Scholar
  89. John TR, Rice JM, Johnson JD (2001) Analysis of pFQ12, a 224-kb Frankia plasmid. Can J Microbiol 47:608–617 doi: 10.1139/cjm-47-7-608 PubMedCrossRefGoogle Scholar
  90. Johnston AWB, Beynon JL, Buchanan-Wollaston AV, Setchell SM, Hirsch PR, Beringer JE (1978) High frequency transfer of nodulating ability between strains and species of Rhizobium. Nature 276:634–636 doi: 10.1038/276634a0 CrossRefGoogle Scholar
  91. Kaijalainen S, Lindström K (1989) Restriction fragment length polymorphism analysis of Rhizobium galegae strains. J Bacteriol 171:5561–5566PubMedGoogle Scholar
  92. Kinkema M, Scott PT, Gresshoff PM (2006) Legume nodulation: successful symbiosis through short and long-distance signalling. Funct Plant Biol 33:1–15 doi: 10.1071/FP06056 CrossRefGoogle Scholar
  93. Koga J, Adachi T, Hidaka H (1991) Molecular cloning of the gene for indolepyruvate decarboxylase from Enterobacter cloacae. Mol Gen Genet 226:10–16 doi: 10.1007/BF00273581 PubMedCrossRefGoogle Scholar
  94. Krause A, Ramakumar A, Bartels D, Battistoni F, Bekel T, Boch J, Böhm M, Friedrich F, Hurek T, Krause L, Linke B, McHardy AC, Sarkar A, Schneiker S, Syed AA, Thauer R, Vorhölter FJ, Weidner S, Pühler A, Reinhold-Hurek B, Kaiser O, Goesmann A (2006) Complete genome of the mutualistic, N(2)-fixing grass endophyte Azoarcus sp. strain BH72. Nat Biotechnol 24:1385–1391 doi: 10.1038/nbt1243 PubMedCrossRefGoogle Scholar
  95. Laguerre G, Géniaux E, Mazurier SI, Rodriguez Casartelli R, Amarger N (1992) Conformity and diversity among field isolates of Rhizobium leguminosarum bv. viciae, bv. trifolii, and bv. phaseoli revealed by DNA hybridization using chromosome and plasmid probes. Can J Microbiol 39:412–419CrossRefGoogle Scholar
  96. Laguerre G, Mavingui P, Allard MR, Charnay MP, Louvrier P, Mazurier SI, Rigottier-Gois L, Amarger N (1996) Typing of rhizobia by PCR DNA fingerprinting and PCR restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rizobium leguminosarum and its different biovars. Appl Environ Microbiol 62:2029–2036PubMedGoogle Scholar
  97. Lamm RB, Neyra CA (1981) Characterization and cyst production of Azospirilla isolated from selected grasses growing in New Jersey and New York. Can J Microbiol 27:1320–1325Google Scholar
  98. Laplaze L, Duhoux E, Franche C, Frutz T, Svistoonoff S, Bogusz D (2000) Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells. Mol Plant Microbe Interact 13:107–112 doi: 10.1094/MPMI.2000.13.1.107 PubMedCrossRefGoogle Scholar
  99. Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix J-J, Auguy F, Bogusz D, Duhoux E (1999) Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules. Plant Physiol 121:113–122 doi: 10.1104/pp.121.1.113 PubMedCrossRefGoogle Scholar
  100. Laplaze L, Svistoonoff S, Santi C, Auguy F, Franche C, Bogusz D (2008) Molecular biology of actinorhizal symbioses. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 235–259CrossRefGoogle Scholar
  101. Lavire C, Cournoyer B (2003) Progress on the genetics of the N2-fixing actinorhizal symbiont Frankia. Plant Soil 254:125–137 doi: 10.1023/A:1024915300030 CrossRefGoogle Scholar
  102. Lavire C, Louis D, Perriere G, Briolay J, Normand P, Cournoyer B (2001) Analysis of pFQ31, a 8551-bp cryptic plasmid from three symbiotic nitrogen-fixing actinomycete. Frankia. FEMS Microbiol Lett 197:111–116 doi: 10.1111/j.1574-6968.2001.tb10591.x PubMedCrossRefGoogle Scholar
  103. Lechevalier MP (1994) Taxonomy of the genus Frankia (Actinomycetales). Int J Syst Bacteriol 44:1–8Google Scholar
  104. Lechno-Yossef S, Nierzwicki-Bauer SA (2002) Azolla-Anabaena azollae symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic publishers, Dordrecht, pp 153–178Google Scholar
  105. Lery LMS, von Krüger WMA, Viana FC, Teixeira KRS, Bisch PM (2008) a comparative proteomic analysis of Gluconacetobacter diazotrophicus PAL5 at exponential and stationary phases of cultures in the presence of high and low levels of inorganic nitrogen compound. Biochim Biophys ActaGoogle Scholar
  106. Limpens E, Bisseling T (2003) Signaling in symbiosis. Curr Opin Plant Biol 6:343–350 doi: 10.1016/S1369-5266(03)00068-2 PubMedCrossRefGoogle Scholar
  107. Lindström K, Martínez-Romero E (2007) International committee on systematics of prokaryotes subcommittee on the taxonomy of Agrobacterium and Rhizobium: minutes of the meeting, 23-24 July 2006, Århus, Denmark. Int J Syst Evol Microbiol 57:1365–1366 doi: 10.1099/ijs.0.65255-0 CrossRefGoogle Scholar
  108. Lindström K, Kokko-Gonzales P, Terefework Z, Räsänen LA (2006) Differentiation of nitrogen-fixing legume root nodule bacteria. In: Cooper JE, Rao JR (eds) Molecular techniques for soil and rhizosphere microorganisms. CABI Publishing, Wallingford, pp 236–258Google Scholar
  109. Lipsanen P, Lindström K (1988) Infection and root nodule structure in the Rhizobium galegae sp nov—Galega sp symbiosis. Symbiosis 6:81–96Google Scholar
  110. Liu CC, Zheng WW (1992) Nitrogen fixation of Azolla and its utilization in agriculture in China. In: Hong GF (ed) Nitrogen fixation and its research in China. Springer-Verlag, Berlin, pp 526–537Google Scholar
  111. Liu Q, Berry AM (1991) The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis. Protoplasma 163:82–92 doi: 10.1007/BF01323332 CrossRefGoogle Scholar
  112. Long SR (2001) Gene and signals in the Rhizobium-legume symbiosis. Plant Physiol 125:69–72 doi: 10.1104/pp.125.1.69 PubMedCrossRefGoogle Scholar
  113. Lumpkin TA, Plucknett DL (1980) Azolla: botany, physiology, and use as a green manure. Econ Bot 34:111–153Google Scholar
  114. Lumpkin TA, Plucknett DL (1982) Azolla as a green manure: use and management in crop production. Westview, Boulder, ColoradoGoogle Scholar
  115. MacLean AM, Finan TM, Sadowsky MJ (2007) Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 144:615–622 doi: 10.1104/pp.107.101634 PubMedCrossRefGoogle Scholar
  116. Macura J (1966) Rapport général. Ann Inst Pasteur (Paris) 111(suppl 3):9–38Google Scholar
  117. Marie C, Broughton WJ, Deakin WJ (2001) Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol 4:336–342 doi: 10.1016/S1369-5266(00)00182-5 PubMedCrossRefGoogle Scholar
  118. McEwan NR, Gatherer D (1999) Codon indices as a predictor of gene functionality in a Frankia operon. Can J Bot 77:1287–1292 doi: 10.1139/cjb-77-9-1287 CrossRefGoogle Scholar
  119. Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66:94–121 doi: 10.1128/MMBR.66.1.94-121.2002 PubMedCrossRefGoogle Scholar
  120. Mergaert P, Van Montagu M, Promé JC, Holsters M (1993) Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc Natl Acad Sci USA 90:1551–1555 doi: 10.1073/pnas.90.4.1551 PubMedCrossRefGoogle Scholar
  121. Merrick MJ, Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59:604–622PubMedGoogle Scholar
  122. Miché L, Bouillant ML, Rohr R, Salle G, Bally R (2000) Physiological and cytological studies on the inhibition of Striga seed germination by the plant growth-promoting bacterium Azospirillum brasilense. Eur J Plant Pathol 106:347–351 doi: 10.1023/A:1008734609069 CrossRefGoogle Scholar
  123. Miller IM, Baker DD (1985) The initiation, development and structure of root nodules in Eleagnus angustifolia L (Eleagnaceae). Protoplasma 128:107–119 doi: 10.1007/BF01276333 CrossRefGoogle Scholar
  124. Mosier AR (2002) Environmental challenges associated with needed increases in global nitrogen fixation. Nutr Cycl Agroecosyst 63:101–116 doi: 10.1023/A:1021101423341 CrossRefGoogle Scholar
  125. Mutch LA, Young JPW (2004) Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol Ecol 13:2435–2444 doi: 10.1111/j.1365-294X.2004.02259.x PubMedCrossRefGoogle Scholar
  126. Myrold DD, Huss-Danell K (2003) Alder and lupine enhance nitrogen cycling in a degraded forest soil in Northern Sweden. Plant Soil 254:47–56 doi: 10.1023/A:1024951115548 CrossRefGoogle Scholar
  127. Newton WE (2007) Physiology, biochemistry and molecular biology of nitrogen fixation. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 109–130CrossRefGoogle Scholar
  128. Nierzwicki-Bauer SA (1990) Azolla-Anabaena symbiosis. In: Rai AN (ed) Handbook of symbiotic cyanobacteria. CRC, Boca Raton, pp 119–136Google Scholar
  129. Normand P, Mullin BC (2008) Prospects for the study of a ubiquitous actinomycete, Frankia, and its host plants. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 289–303CrossRefGoogle Scholar
  130. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Martinez M, Mastronunzio JE, Mullin BC, Nieman J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tvares F, Tomkins JP, Vallenet D, Valverde C, Wall L, Wang Y, Médigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp strains reflect host range and host plant biogeography. Genome Res 17:7–15 doi: 10.1101/gr.5798407 PubMedCrossRefGoogle Scholar
  131. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of family Frankiaceae. Int J Syst Bacteriol 46:1–9PubMedCrossRefGoogle Scholar
  132. Okon Y (1985) Azospirillum as a potential inoculant for agriculture. Trends Biotechnol 3:223–228 doi: 10.1016/0167-7799(85)90012-5 CrossRefGoogle Scholar
  133. Okon Y, Labandera-Gonzales CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years world-wide field inoculation. Soil Biol Biochem 26:1591–1601 doi: 10.1016/0038-0717(94)90311-5 CrossRefGoogle Scholar
  134. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in Legumes. Annu Rev Plant Biol 59:519–546 doi: 10.1146/annurev.arplant.59.032607.092839 PubMedCrossRefGoogle Scholar
  135. Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 6:1899–1913CrossRefGoogle Scholar
  136. Pawlowski K, Sprent JI (2008) Comparison between actinorhizal symbiosis and legume symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 261–288CrossRefGoogle Scholar
  137. Pedrosa FO, Elmerich C (2007) Regulation of nitrogen fixation and ammonium assimilatiuon in associated and endophytic nitrogen fixing bacteria. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, The Netherlands, pp 41–71CrossRefGoogle Scholar
  138. Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:2–28Google Scholar
  139. Pereg-Gerk L, Paquelin A, Gounon A, Kennedy IR, Elmerich C (1998) A transcriptional regulator of the LuxR-UhpA family, FlcA, controls flocculation and wheat root surface colonization by Azospirillum brasilense Sp7. Mol Plant Microbe Interact 11:177–187 doi: 10.1094/MPMI.1998.11.3.177 PubMedCrossRefGoogle Scholar
  140. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201 doi: 10.1128/MMBR.64.1.180-201.2000 PubMedCrossRefGoogle Scholar
  141. Peters GA, Meeks JC (1989) The Azolla-Anabaena symbiosis: basic biology. Annu Rev Plant Physiol Plant Mol Biol 40:193–210 doi: 10.1146/annurev.pp.40.060189.001205 CrossRefGoogle Scholar
  142. Postgate J (1981) Microbiology of the free-living nitrogen-fixing bacteria, excluding cyanobacteria. In: Gibson AH, Newton WE (eds) Current perspectives in nitrogen fixation. Elsevier/North-Holland Biomedical, Amsterdam, pp 217–228Google Scholar
  143. Pothier JF, Wisniewski-Dyé F, Weiss-Gayet M, Moënne-Loccoz Y, Prigent-Combaret C (2007) Promoter-trap identification of wheat seed extract-induced genes in the plant-growth-promoting rhizobacterium Azospirillum brasilense Sp245. Microbiology 153:3608–3622 doi: 10.1099/mic.0.2007/009381-0 PubMedCrossRefGoogle Scholar
  144. Prell J, Poole P (2006) Metabolic changes of rhizobia in legume nodules. Trends Microbiol 14:161–168 doi: 10.1016/j.tim.2006.02.005 PubMedCrossRefGoogle Scholar
  145. Prigent-Combaret C, Blaha D, Pothier F, Vial L, Poirier M-A, Wisniewski-Dyé F, Moënne-Loccoz Y (2008) FEMS Microbiol Ecol 65:220-219 doi: 10.1111/j.1574-6941.2008.00545.x Google Scholar
  146. Prin Y, Rougier M (1987) Preinfection events in the establishment of Alnus-Frankia symbiosis: study of the root hair deformation step. Plant Physiol 6:99–106Google Scholar
  147. Pueppke SG, Broughton WJ (1999) Rhizobium sp strain NGR234 and R fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant Microbe Interact 12:293–318 doi: 10.1094/MPMI.1999.12.4.293 PubMedCrossRefGoogle Scholar
  148. Radeva G, Jurgens G, Niemi M, Nick G, Suominen L, Lindström K (2001) Description of two biovars in the Rhizobium galegae species: biovar orientalis and biovar officinalis. Syst Appl Microbiol 24:195–205 doi: 10.1078/0723-2020-00029 CrossRefGoogle Scholar
  149. Rai AN (1990) Handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, Florida, USAGoogle Scholar
  150. Rai AN, Bergman B, Rasmussen U (2002) Cyanobacteria in symbiosis. Kluwer Academic, DordrechtGoogle Scholar
  151. Rai AN, Söderbäck E, Bergman B (2000) Cyanobacterium-plant symbiosis. New Phytol 147:449–481 doi: 10.1046/j.1469-8137.2000.00720.x CrossRefGoogle Scholar
  152. Räsänen LA, Heikkilä-Kallio U, Suominen L, Lipsanen P, Lindström K (1991) Expression of common nodulation genes of Rhizobium galegae in various backgrounds. Mol Plant Microbe Interact 4:535–544PubMedGoogle Scholar
  153. Rasmussen U, Svenning MM (2001) Characterization of genotypic methods of symbiotic Nostoc strains isolated from five species of Gunnera. Arch Microbiol 176:204–210 doi: 10.1007/s002030100313 PubMedCrossRefGoogle Scholar
  154. Rasmussen U, Johansson C, Bergman B (1994) Early communication in the Gunnera-Nostoc symbiosis: plant-induced cell differentiation and protein synthesis in the cyanobacterium. Mol Plant Microbe Interact 6:696–702Google Scholar
  155. Rasmussen U, Johansson C, Renglin A, Petersson C, Bergman B (1996) A molecular characterization of the Gunnera-Nostoc symbiosis: comparison with Rhizobium- and Agrobacterium-plant interactions. New Phytol 133:391–398 doi: 10.1111/j.1469-8137.1996.tb01906.x CrossRefGoogle Scholar
  156. Reinhold-Hurek B, Hurek T (1998) Life in grasses, diazotrophic endophytes. Trends Microbiol 6:139–144 doi: 10.1016/S0966-842X(98)01229-3 PubMedCrossRefGoogle Scholar
  157. Rennie RJ (1980) Dinitrogen-fixing bacteria: computer-assisted identification of soil isolates. Can J Microbiol 26:1275–1283PubMedGoogle Scholar
  158. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Genetic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  159. Rodrigues EP, Rodrigues LS, Martinez de Oliveira AL, Baldani VLD, dos Santos Teixeira KR, Urquiaga S, Reis VM (2008) Azospirillum amazonense inoculation: effect on growth yield and N2 fixation of rice (Oryza sativa L.). Plant Soil doi: 10.1007/s11104-00079476-1
  160. Roesch LFW, Camargo FAO, Bento FM, Triplett EW (2008) Biodiversity of diazotrophs within the soil, root and stem of field grown maize. Plant Soil 302:91–104 doi: 10.1007/s11104-007-9458-3 CrossRefGoogle Scholar
  161. Rothballer M, Eckert B, Schmid M, Fekete A, Scholter M, Lehner A, Pollmann S, Hartmann A (2008) Endophytic root colonization of gramineous plants by Herbaspirillum frisingense. FEMS Microbiol Ecol 66:85–95 doi: 10.1111/j.1574-6941.2008.00582.x PubMedCrossRefGoogle Scholar
  162. Rothballer M, Schmid M, Hartmann A (2003) In situ localization and PGPR-effect of Azospirillum brasilense colonizing roots of different wheat varieties. Symbiosis 34:261–279Google Scholar
  163. Rovira AD (1991) Rhizosphere research, 85 years of progress and frustration. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic, The Netherlands, pp 3–13Google Scholar
  164. Rubio LM, Ludden PW (2005) Maturation of nitrogenase: a biochemical puzzle. J Bacteriol 187:405–414 doi: 10.1128/JB.187.2.405-414.2005 PubMedCrossRefGoogle Scholar
  165. Rubio LM, Ludden PW (2008) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu Rev Microbiol 62:93–111 doi: 10.1146/annurev.micro.62.081307.162737 PubMedCrossRefGoogle Scholar
  166. Schank SC, Smith RL, Weiser GC, Zuberer DA, Bouton JH, Quesenberry KH, Tyler ME, Milam JR, Littel RC (1979) Fluorescent antibody technique to identify Azospirillum brasilense associated with roots of grasses. Soil Biol Biochem 11:287–295 doi: 10.1016/0038-0717(79)90074-9 CrossRefGoogle Scholar
  167. Schmid M, Hartmann A (2007) Molecular phylogeny and ecology of root associated diazotrophic α and β Proteobacteria. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 41–71Google Scholar
  168. Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57 doi: 10.1146/annurev.genet.32.1.33 PubMedCrossRefGoogle Scholar
  169. Sevilla M, Burris RH, Gunapala N, Kennedy C (2001) Comparison of benefit to sugar cane plant growth and 15N2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and Nif -mutant strains. Mol Plant Microbe Interact 14:359–366 doi: 10.1094/MPMI.2001.14.3.358 CrossRefGoogle Scholar
  170. Shi Y, Zhao W, Zhang W, Ye Z, Zhao J (2006) Regulation of intracellular free calcium concentration during heterocyst differentiation by HetR and NtcA in Anabaena sp Pcc7120. Proc Natl Acad Sci USA 103:11334–11339 doi: 10.1073/pnas.0602839103 PubMedCrossRefGoogle Scholar
  171. Simonet P, Normand P, Hirch M, Akkermans ADL (1990) The genetics of the Frankia-actinorhizal symbiosis. In: Gresshoff PM (ed) Molecular biology of symbiotic nitrogen fixation. CRC, Bocaraton, USA, pp 77–109Google Scholar
  172. Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol 54:257–288 doi: 10.1146/annurev.micro.54.1.257 PubMedCrossRefGoogle Scholar
  173. Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, UKGoogle Scholar
  174. Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581 doi: 10.1104/pp.107.096156 PubMedCrossRefGoogle Scholar
  175. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506 doi: 10.1111/j.1574-6976.2000.tb00552.x PubMedCrossRefGoogle Scholar
  176. Stephens BB, Loar SN, Alexandre G (2006) Role of CheB and CheR in the complex chemotactic and aerotactic pathway of Azospirillum brasilense. J Bacteriol 188:4759–4768 doi: 10.1128/JB.00267-06 PubMedCrossRefGoogle Scholar
  177. Stewart WDP (1969) Biological and ecological aspects of nitrogen fixation by free-living microorganisms. Proc Roy Soc B (London) 172:367–388CrossRefGoogle Scholar
  178. Stoffels M, Castellanos T, Hartmann A (2001) Design and application of new 16S-rRNA-targeted oligonucleotide probes for the Azospirillum-Skermanella-Rhodocista-cluster. Syst Appl Microbiol 24:83–97 doi: 10.1078/0723-2020-00011 PubMedCrossRefGoogle Scholar
  179. Suominen L, Lortet G, Roos C, Paulin L, Lindström K (2001) Identification and structure of the Rhizobium galegae common nodulation genes: evidence for horizontal gene transfer. Mol Biol Evol 18:906–916Google Scholar
  180. Suominen L, Luukkainen R, Lindström K (2003) Activation of the nodA promoter by the nodD genes of Rhizobium galegae induced by synthetic flavonoids or Galega orientalis root exudates. FEMS Microbiol Lett 19:225–232 doi: 10.1016/S0378-1097(02)01206-5 CrossRefGoogle Scholar
  181. Svistoonoff S, Laplaze L, Auguy F, Runions J, Duponnois R, Haseloff J, Franche C, Bogusz D (2003) cg12 expression is specifically linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development. Mol Plant Microbe Interact 16:600–607 doi: 10.1094/MPMI.2003.16.7.600 PubMedCrossRefGoogle Scholar
  182. Tapia-Hernández A, Mascarúa-Esperza MA, Caballero-Mellado J (1990) Production of bacteriocins and siderophore-like activity by Azospirillum brasilense. Microbios 64:73–83PubMedGoogle Scholar
  183. Tarrand JJ, Krieg NR, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group with description a new genus, Azospirillum gen nov and two species, Azospirillum lipoferum (Beijerinck) comb nov and Azospirillum brasilense sp nov. Can J Microbiol 24:967–980PubMedGoogle Scholar
  184. Tas E, Leinonen P, Saano A, Piippola S, Kaijalainen S, Räsänen LA, Hakola S, Lindström K (1996) Assessment of the competitiveness of rhizobia infecting Galega orientalis using plant yield, nodulation, and strain identification by PCR and antibiotic resistance. Appl Environ Microbiol 62:529–535PubMedGoogle Scholar
  185. Torrey JG, Tjepkema JD (1979) Symbiotic nitrogen fixation in actinomycete-nodulated plants. Bot Gaz 140(Suppl):i–ii doi: 10.1086/337026 CrossRefGoogle Scholar
  186. Turner SL, Young JPW (2000) The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319PubMedGoogle Scholar
  187. Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995) Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J Bacteriol 177:1414–1417PubMedGoogle Scholar
  188. van Berkum P, Bohlool BB (1980) Evaluation of nitrogen fixation by bacteria in association with roots of tropical grasses. Microbiol Rev 44:491–517PubMedGoogle Scholar
  189. van Ghelue M, Lovaas E, Ringo E, Solheim B (1997) Early interaction between Alnus glutinosa and Frankia strain Arl3. Production and specificity of root hair deformation factors. Physiol Plant 9:579–587 doi: 10.1111/j.1399-3054.1997.tb05360.x Google Scholar
  190. Van Hove C, Lejeune A (2002) Applied aspects of Azolla-Anabaena symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic, Dordrecht, pp 179–194Google Scholar
  191. Vanbleu E, Marchal K, Lambrecht M, Mathys J, Vanderleyden J (2004) Annotation of the pRhico plasmid of Azospirillum brasilense reveals its role in determining the outer surface composition. FEMS Microbiol Lett 232:165–172 doi: 10.1016/S0378-1097(04)00046-1 PubMedCrossRefGoogle Scholar
  192. Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606PubMedCrossRefGoogle Scholar
  193. Vande Broek A, Michiels J, Van Gool AP, Vanderleyden J (1993) Spatial-temporal colonization patterns of Azospirillum brasilense on the wheat root surface and expression of the bacterial nifH gene during association. Mol Plant Microbe Interact 6:592–600Google Scholar
  194. Vessey JK, Pawlowski K, Bergman B (2004) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia and cycads. Plant Soil 266:205–230 doi: 10.1007/s11104-005-0871-1 CrossRefGoogle Scholar
  195. Vlek PLG, Diakite MY, Mueller H (1995) The role of Azolla in curbing ammonia volatilization from flooded rice systems. Fert Res 42:165–174 doi: 10.1007/BF00750511 CrossRefGoogle Scholar
  196. Von Bülow JFW, Döbereiner J (1975) Potential for nitrogen fixation in maize genotypes in Brazil. Proc Natl Acad Sci USA 72:2389–2393 doi: 10.1073/pnas.72.6.2389 CrossRefGoogle Scholar
  197. Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182PubMedGoogle Scholar
  198. Wall LG, Berry AM (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 147–166CrossRefGoogle Scholar
  199. Wang CM, Ekman M, Bergman B (2004) Expression of cyanobacterial genes involved in heterocyst differentiation and dinitrogen fixation along a plant symbiosis development profile. Mol Plant Microbe Interact 17:436–443 doi: 10.1094/MPMI.2004.17.4.436 PubMedCrossRefGoogle Scholar
  200. Wei TF, Ramasubramanian TS, Golden JW (1994) Anabaena sp strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176:4473–4482PubMedGoogle Scholar
  201. Wheeler CT, Miller IM (1990) Current potential uses of actinorhizal plants in Europe. In: Schwintzer RC, Tjepkema JD (eds) The biological of Frankia and actinorhizal plants. Academic press Inc, San Diego, pp 365–389Google Scholar
  202. White J, Prell J, James EK, Poole P (2007) Nutrient sharing between symbionts. Plant Physiol 144:604–614 doi: 10.1104/pp.107.097741 PubMedCrossRefGoogle Scholar
  203. Wong FCY, Meeks JC (2001) The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J Bacteriol 183:2654–2661 doi: 10.1128/JB.183.8.2654-2661.2001 PubMedCrossRefGoogle Scholar
  204. Wong FCY, Meeks JC (2002) Establishment of a functional symbiosis between the cyanobacterium Nostoc punctiforme and the bryophyte Anthoceros punctatus requires genes involved in nitrogen control and initiation of heterocyst differentiation. Microbiology 148:315–323PubMedGoogle Scholar
  205. Xu X, Elhai J, Wolk CP (2008) Transcriptional and developmental responses by Anabaena to deprivation of fixed nitrogen. In: Herrero A, Flores E (eds) Cyanobacteria: Molecular biology, genomics and evolution. Horizon Scientific, Norwich, pp 383–422Google Scholar
  206. Xu XD, Kong RQ, de Bruijn FJ, He SY, Murry MA, Newman T, Wolk P (2002) DNA sequence and genetic characterization of plasmid pFQ11 from Frankia alni strain CpI1. FEMS Microbiol Lett 207:103–107 doi: 10.1111/j.1574-6968.2002.tb11036.x PubMedCrossRefGoogle Scholar
  207. Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, Lu W, Zhang W, Yao Z, Li H, Liu W, He S, Geng L, Zhang X, Yang F, Yu H, Zhan Y, Li D, Lin Z, Wang Y, Elmerich C, Lin M, Jin Q (2008) Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci USA 105:7564–7569 doi: 10.1073/pnas.0801093105 PubMedCrossRefGoogle Scholar
  208. Yang GP, Debellé F, Savagnac A, Ferro M, Schiltz O, Maillet F, Promé D, Treilhou M, Vialas C, Lindström K, Dénarié J, Promé JC (1999) Structure of the Mesorhizobium huakuii and Rhizobium galegae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with alpha,beta-unsaturated N-acyl substitutions. Mol Microbiol 34:227–237 doi: 10.1046/j.1365-2958.1999.01582.x PubMedCrossRefGoogle Scholar
  209. Yoon HS, Golden JW (1998) Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935–938 doi: 10.1126/science.282.5390.935 PubMedCrossRefGoogle Scholar
  210. Young P (1992) Phylogenetic classification of nitrogen-fixing organisms. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall Inc, New York, pp 43–86Google Scholar
  211. Young JPW, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson ARJ, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34 doi: 10.1186/gb-2006-7-4-r34 PubMedCrossRefGoogle Scholar
  212. Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium spp. Appl Environ Microbiol 55:2522–2526PubMedGoogle Scholar
  213. Zhang CC, Laurent S, Sakr S, Peng L, Bedu S (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59:367–375 doi: 10.1111/j.1365-2958.2005.04979.x PubMedCrossRefGoogle Scholar
  214. Zheng L, Cash DL, Flint DH, Dean DR (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273:13264–1327272 doi: 10.1074/jbc.273.21.13264 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Claudine Franche
    • 1
  • Kristina Lindström
    • 2
  • Claudine Elmerich
    • 3
  1. 1.Equipe Rhizogénèse, UMR DIAPCInstitut de Recherche pour le DéveloppementMontpellier Cedex 5France
  2. 2.Department of Applied Chemistry and Microbiology, Viikki BiocenterUniversity of HelsinkiHelsinkiFinland
  3. 3.Biologie Moléculaire du Gène chez les Extrêmophiles, Département de MicrobiologieInstitut PasteurParis Cedex 15France

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