Skip to main content
SpringerLink
Log in

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

  • Review Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • 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 61:1013–1019

    PubMed  Google Scholar 

  • Adams DG (2002) Symbioses with hornworts and liverworts. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic, Dordrecht, pp 117–136

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 7:748–757

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 113–143

    Chapter  Google Scholar 

  • Balandreau J (1983) Microbiology of the association. Can J Microbiol 29:851–859

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 207–224

    Google Scholar 

  • Berg RH (1990) Cellulose and xylans in the interface capsule in symbiotic cells of actinorhizae. Protoplasma 159:35–43 doi:10.1007/BF01326633

    Article  CAS  Google Scholar 

  • Berg RH (1999) Frankia forms infection threads. Can J Bot 77:1327–1333 doi:10.1139/cjb-77-9-1327

    Article  Google Scholar 

  • Bergersen F (1980) Methods for evaluating biological nitrogen fixation. Willey and Sons, Chichester

    Google Scholar 

  • Bergman B (2002) Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer academic, Dordrecht, pp 207–232

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 61–88

    Google Scholar 

  • Bock JV, Battershell T, Wiggington J, John TR, Johnson JD (2001) Frankia sequences exhibiting RNA polymerase promoter activity. Microbiology 147:499–506

    PubMed  CAS  Google Scholar 

  • 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 28–47

  • 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

    Article  Google Scholar 

  • 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 28:889–895

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 55:125–131

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 12:1647–1666

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 195–206

    Google Scholar 

  • Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18 doi:10.3109/10408419509113531

    Article  PubMed  Google Scholar 

  • Cournoyer B, Normand P (1994) Gene expression in Frankia: characterization of promoters. Microbiology 78:229–236

    CAS  Google Scholar 

  • Dawson JO (1983) Dinitrogen fixation in forest ecosystems. Can J Microbiol 29:979–992

    CAS  Google Scholar 

  • 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 299–316

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 19–30

    Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631 doi:10.1038/nrmicro954

    Article  PubMed  CAS  Google Scholar 

  • 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 145–170

    Chapter  Google Scholar 

  • Döbereiner J, Day JM, Dart PJ (1972) Nitrogenase activity and oxygen sensitivity of the Paspalum notatum-Azotobacter paspali association. J Gen Microbiol 71:103–116

    Google Scholar 

  • Döbereiner J, Pedrosa FO (1987) Nitrogen-fixing bacteria in non-leguminous crop plants. Science Tech, Madison and Springer Verlag, Berlin

    Google Scholar 

  • Döbereiner J (1992) History and new perspectives of diazotrophs in association with non-leguminous plants. Symbiosis 13:1–13

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 

  • 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

  • Duhoux E, Diouf D, Gherbi H, Franche C, Ahée J, Bogusz D (1996) Le nodule actinorhizien. Acta Bot Gallica 143:593–608

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Elmerich C, Newton WE (2007) Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations. Springer, The Netherlands

    Book  Google Scholar 

  • 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 212–258

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • FAO (2008) Current world fertilizer trends and outlook 2011/2012. Food and agricultural organization of the United Nations, Rome

    Google Scholar 

  • Fischer HM (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Geurts R, Bisseling T (2002) Rhizobium nod factor perception and signalling. Plant Cell 14(Suppl):S239–S249

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Golden JW, Yoon HS (2003) Heterocyst development in Anabaena. Curr Opin Microbiol 6:557–563 doi:10.1016/j.mib.2003.10.004

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 208:61–67

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Holguin G, Glick BR (2001) Expression of the ACC deaminase gene from Enterobacter cloacae UW4 in Azospirillum brasilense. Microb Ecol 41:281–288

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405 doi:10.1046/j.1469-8137.1997.00755.x

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kaijalainen S, Lindström K (1989) Restriction fragment length polymorphism analysis of Rhizobium galegae strains. J Bacteriol 171:5561–5566

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 39:412–419

    Article  Google Scholar 

  • 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 62:2029–2036

    PubMed  CAS  Google Scholar 

  • 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 27:1320–1325

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 235–259

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lechevalier MP (1994) Taxonomy of the genus Frankia (Actinomycetales). Int J Syst Bacteriol 44:1–8

    Google Scholar 

  • 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 153–178

    Google Scholar 

  • 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 Acta

  • Limpens E, Bisseling T (2003) Signaling in symbiosis. Curr Opin Plant Biol 6:343–350 doi:10.1016/S1369-5266(03)00068-2

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 236–258

    Google Scholar 

  • Lipsanen P, Lindström K (1988) Infection and root nodule structure in the Rhizobium galegae sp nov—Galega sp symbiosis. Symbiosis 6:81–96

    Google Scholar 

  • 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 526–537

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Long SR (2001) Gene and signals in the Rhizobium-legume symbiosis. Plant Physiol 125:69–72 doi:10.1104/pp.125.1.69

    Article  PubMed  CAS  Google Scholar 

  • Lumpkin TA, Plucknett DL (1980) Azolla: botany, physiology, and use as a green manure. Econ Bot 34:111–153

    CAS  Google Scholar 

  • Lumpkin TA, Plucknett DL (1982) Azolla as a green manure: use and management in crop production. Westview, Boulder, Colorado

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Macura J (1966) Rapport général. Ann Inst Pasteur (Paris) 111(suppl 3):9–38

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Merrick MJ, Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59:604–622

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mosier AR (2002) Environmental challenges associated with needed increases in global nitrogen fixation. Nutr Cycl Agroecosyst 63:101–116 doi:10.1023/A:1021101423341

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 109–130

    Chapter  Google Scholar 

  • Nierzwicki-Bauer SA (1990) Azolla-Anabaena symbiosis. In: Rai AN (ed) Handbook of symbiotic cyanobacteria. CRC, Boca Raton, pp 119–136

    Google Scholar 

  • 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 289–303

    Chapter  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 46:1–9

    Article  PubMed  CAS  Google Scholar 

  • Okon Y (1985) Azospirillum as a potential inoculant for agriculture. Trends Biotechnol 3:223–228 doi:10.1016/0167-7799(85)90012-5

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 6:1899–1913

    Article  Google Scholar 

  • 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 261–288

    Chapter  Google Scholar 

  • 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 41–71

    Chapter  Google Scholar 

  • Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:2–28

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 217–228

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Prin Y, Rougier M (1987) Preinfection events in the establishment of Alnus-Frankia symbiosis: study of the root hair deformation step. Plant Physiol 6:99–106

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rai AN (1990) Handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, Florida, USA

    Google Scholar 

  • Rai AN, Bergman B, Rasmussen U (2002) Cyanobacteria in symbiosis. Kluwer Academic, Dordrecht

    Google Scholar 

  • Rai AN, Söderbäck E, Bergman B (2000) Cyanobacterium-plant symbiosis. New Phytol 147:449–481 doi:10.1046/j.1469-8137.2000.00720.x

    Article  CAS  Google Scholar 

  • 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 4:535–544

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 6:696–702

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Reinhold-Hurek B, Hurek T (1998) Life in grasses, diazotrophic endophytes. Trends Microbiol 6:139–144 doi:10.1016/S0966-842X(98)01229-3

    Article  PubMed  CAS  Google Scholar 

  • Rennie RJ (1980) Dinitrogen-fixing bacteria: computer-assisted identification of soil isolates. Can J Microbiol 26:1275–1283

    PubMed  CAS  Google Scholar 

  • 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 111:1–61

    Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rothballer M, Schmid M, Hartmann A (2003) In situ localization and PGPR-effect of Azospirillum brasilense colonizing roots of different wheat varieties. Symbiosis 34:261–279

    Google Scholar 

  • 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 3–13

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 41–71

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 77–109

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, UK

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stewart WDP (1969) Biological and ecological aspects of nitrogen fixation by free-living microorganisms. Proc Roy Soc B (London) 172:367–388

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 18:906–916

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tapia-Hernández A, Mascarúa-Esperza MA, Caballero-Mellado J (1990) Production of bacteriocins and siderophore-like activity by Azospirillum brasilense. Microbios 64:73–83

    PubMed  Google Scholar 

  • 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 24:967–980

    PubMed  CAS  Google Scholar 

  • 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 62:529–535

    PubMed  CAS  Google Scholar 

  • Torrey JG, Tjepkema JD (1979) Symbiotic nitrogen fixation in actinomycete-nodulated plants. Bot Gaz 140(Suppl):i–ii doi:10.1086/337026

    Article  Google Scholar 

  • Turner SL, Young JPW (2000) The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319

    PubMed  CAS  Google Scholar 

  • 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 177:1414–1417

    PubMed  CAS  Google Scholar 

  • van Berkum P, Bohlool BB (1980) Evaluation of nitrogen fixation by bacteria in association with roots of tropical grasses. Microbiol Rev 44:491–517

    PubMed  Google Scholar 

  • 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 

  • 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 179–194

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606

    Article  PubMed  CAS  Google Scholar 

  • 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 6:592–600

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182

    PubMed  CAS  Google Scholar 

  • 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 147–166

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wei TF, Ramasubramanian TS, Golden JW (1994) Anabaena sp strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176:4473–4482

    PubMed  CAS  Google Scholar 

  • 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 365–389

    Google Scholar 

  • White J, Prell J, James EK, Poole P (2007) Nutrient sharing between symbionts. Plant Physiol 144:604–614 doi:10.1104/pp.107.097741

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 148:315–323

    PubMed  CAS  Google Scholar 

  • 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 383–422

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Golden JW (1998) Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935–938 doi:10.1126/science.282.5390.935

    Article  PubMed  CAS  Google Scholar 

  • 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 43–86

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium spp. Appl Environ Microbiol 55:2522–2526

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Equipe Rhizogénèse, UMR DIAPC, Institut de Recherche pour le Développement, B. P. 64501, 34394, Montpellier Cedex 5, France

    Claudine Franche

  2. Department of Applied Chemistry and Microbiology, Viikki Biocenter, University of Helsinki, P. O. Box 56, 00014, Helsinki, Finland

    Kristina Lindström

  3. Biologie Moléculaire du Gène chez les Extrêmophiles, Département de Microbiologie, Institut Pasteur, 25 rue du Dr. Roux, 75724, Paris Cedex 15, France

    Claudine Elmerich

Authors
  1. Claudine Franche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristina Lindström
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudine Elmerich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudine Elmerich.

Additional information

Responsible Editor: Robert Reid.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Franche, C., Lindström, K. & Elmerich, C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321, 35–59 (2009). https://doi.org/10.1007/s11104-008-9833-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-008-9833-8

Keywords

Search

Navigation