Skip to main content
SpringerLink
Log in

The Diversity and Evolution of Rhizobia

  • Chapter
  • First Online:
Prokaryotic Symbionts in Plants

Part of the book series: Microbiology Monographs ((MICROMONO,volume 8))

Abstract

Rhizobia are soil bacteria that are able to fix nitrogen in symbiosis with plants from the family Leguminosae. Rhizobia populate both soil and nodule niches. The rhizobial genome can be divided into a core of housekeeping genes and an accessory pool of non-essential genes. The accessory genome, together with factors acting within plants, confers symbiotic interaction between rhizobia and plant hosts. Rhizobia are distributed within the α- and β subdivisions of the Proteobacteria and intermingled with non-symbiotic photosynthetic and pathogenic relatives in the following genera: Allorhizobium, Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium, Sinorhizobium and Methylobacterium (α-rhizobia), as well as Burkholderia and Cupriavidus (β-rhizobia). Recently α-proteobacterial nitrogen-fixing isolates have been identified in the genera Ochrobactrum, Devosia and Blastobacter. Lateral gene transfer of the mobile accessory genome is the most likely explanation for the occurrence of rhizobial symbiotic loci in distantly related genera of proteobacteria. Consequently, similar symbiotic types can be found in different chromosomal backgrounds, and the same chromosomal background can harbour different symbiotic genotypes. Thus, comparisons of genes from core loci and the accessory gene pool reflect their separate evolutionary histories. Similarly, phylogenies from ribosomal sequences of rhizobia do not show parallel divergence with plant taxonomy. Phylogenies of closely evolving organisms might develop in parallel. In the case of rhizobia, only phylogenetic trees based on symbiotic genes show some correlation with host plant range, indicating that evolution of nodulation genes could develop under the functional constraint of the plant.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andronov EE, Terefework Z, Roumiantseva ML, Dzyubenko NI, Onichtchouk OP, Kurchak ON, Dresler-Nurmi A, Young JP, Simarov BV, Lindström K (2003) Symbiotic and genetic diversity of Rhizobium galegae isolates collected from the Galega orientalis gene center in the Caucasus. Appl Environ Microbiol 69:1067–1074

    Article  PubMed  CAS  Google Scholar 

  • Appleby CA, Tjepkema JD, Trinick MJ (1983) Haemoglobin in a non-leguminous plant. Parasponia: possible genetic origin and function in nitrogen fixation. Science 220:951–953

    Article  PubMed  CAS  Google Scholar 

  • Ba S, Willems A, de Lajudie P, Roche P, Jeder H, Quatrini P, Neyra M, Ferro M, Prome JC, Gillis M, Boivin-Masson C, Lorquin J (2002) Symbiotic and taxonomic diversity of rhizobia isolated from Acacia tortilis ssp. raddiana in Africa. Syst Appl Microbiol 25:130–145

    Article  PubMed  CAS  Google Scholar 

  • Barnett MJ, Fisher RF, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J, Gurjal M, Hong A, Huizar L, Hyman RW, Kahn D, Kahn ML, Kalman S, Keating DH, Palm C, Peck MC, Surzycki R, Wells DH, Yeh KC, Davis RW, Federspiel NA, Long SR (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci USA 98:9883–9888

    Article  PubMed  CAS  Google Scholar 

  • Bassam BJ, Djordjevic MA, Redmond JW, Batley M, Rolfe BG (1988) Identification of a nodD-dependent locus in the Rhizobium strain NGR234 activated by phenolic factors secreted by soybeans and other legumes. Mol Plant Microbe Interact 1:161–168

    PubMed  CAS  Google Scholar 

  • Beijerinck MW (1890) Künstliche Infection von Vicia faba mit Bacillus radicola. Ernährungsbedingungen dieser Bacterie. Bot Zeitung 52:837–843

    Google Scholar 

  • Belay N, Sparling R, Daniels L (1984) Dinitrogen fixation by a thermophilic methanogenic bacterium. Nature 312:286–288

    Article  PubMed  CAS  Google Scholar 

  • Benson DR, Silvester WB (1993) Biology of Frankia strains, actionomycete symbionts of actiorhizal plants. Microbiol Rev 57:293–319

    PubMed  CAS  Google Scholar 

  • Boivin C, Ndoye I, Lortet G, Ndiaye A, De Lajudie P, Dreyfus B (1997) The Sesbania root symbionts Sinorhizobium saheli and S. teranga bv. sesbaniae can form stem nodules on Sesbania rostrata, although they are less adapted to stem nodulation than Azorhizobium caulinodans. Appl Environ Microbiol 63:1040–1047

    PubMed  CAS  Google Scholar 

  • Campbell A (1981) Evolutionary significance of accessory DNA elements in bacteria. Annu Rev Microbiol 35:55–83

    Article  PubMed  CAS  Google Scholar 

  • Cárdenas L, Dominguez J, Quinto C, Lopez-Lara IM, Lugtenberg BJ, Spaink HP, Rademaker GJ, Haverkamp J, Thomas-Oates JE (1995) Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol Biol 29:453–464

    Article  PubMed  Google Scholar 

  • Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by beta-Poteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  PubMed  CAS  Google Scholar 

  • Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735

    PubMed  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311(5765):1283–1287

    Article  PubMed  CAS  Google Scholar 

  • Cohan FM (2002) What are bacterial species. Annu Rev Microbiol 56:457–487

    Article  PubMed  CAS  Google Scholar 

  • Coenye T, Vandamme P (2003) Intragenomic heterogeneity between multiple 16S ribosomal RNA operons in sequenced bacterial genomes. FEMS Microbiol Lett 228:45–49

    Article  PubMed  CAS  Google Scholar 

  • Davey RB, Reanney DC (1980) Extrachromosomal genetic elements and the adaptive evolution of bacteria. Evol Biol 13:113–147

    Google Scholar 

  • de Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins MD, Lindström K, Dreyfus B, Gillis M (1998) Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol 48:369–382

    PubMed  Google Scholar 

  • de Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins MD, Dreyfus B, Kersters K, Gillis M (1994) Polyphasic taxonomy of rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 44:715–733

    Google Scholar 

  • Dobert RC, Breil BT, Triplett EW (1994) DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Mol Plant Microbe Interact 7:564–572

    PubMed  CAS  Google Scholar 

  • Doignon-Bourcier F, Willems A, Coopman R, Laguerre G, Gillis M, de Lajudie P (2000) Genotypic characterization of Bradyrhizobium strains nodulating small Senegalese legumes by 16S-23S rRNA intergenic gene spacers and Amplified Fragment Length Polymorphism fingerprint analyses. Appl Environ Microbiol 66:3987–3997

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ (1994) Phylogeny of the legume family: An approach to understanding the origin of nodulation. Ann Rev Ecol Syst 25:325–349

    Article  Google Scholar 

  • Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131:900–910

    Article  PubMed  CAS  Google Scholar 

  • Eardly B, van Berkum P (2005) Use of population genetic structure to define species limits in Rhizobiaceae. Symbiosis 38:109–122

    CAS  Google Scholar 

  • Finan TM, Weidner S, Wong K, Buhrmester J, Chain P, Vorholter FJ, Hernández-Lucas I, Becker A, Cowie A, Gouzy J, Golding B, Puhler A (2001) The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci USA 98:9889–9894

    Article  PubMed  CAS  Google Scholar 

  • Fred EB, Baldwin IL, McCoy E (1932) Root nodule bacteria and leguminous plants. University of Wisconsin Press, Madison, WI, USA

    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

    Article  PubMed  CAS  Google Scholar 

  • Galibert F, Finan TM, Long SR, Pühler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    Article  PubMed  CAS  Google Scholar 

  • Gao J, Terefework Z, Chen W, Lindström K (2001) Genetic diversity of rhizobia isolated from Astragalus adsurgens growing in different geographical regions of China. J Biotech 91:155–168

    Article  CAS  Google Scholar 

  • Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JP (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048

    PubMed  CAS  Google Scholar 

  • González V, Santamaria RI, Bustos P, Hernandez-Gonzalez I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramirez MA, Jimenez-Jacinto V, Collado-Vides J, Davila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103:3834–3839

    Article  PubMed  Google Scholar 

  • Guo XW, Zhang XX, Zhang ZM, Li FD (1999) Characterization of Astragalus sinicus rhizobia by restriction fragment length polymorphism analysis of chromosomal and nodulation genes regions. Curr Microbiol 39:358–364

    Article  PubMed  CAS  Google Scholar 

  • Haukka K, Lindström K (1994) Pulsed-field gel electrophoresis for genotypic comparison of Rhizobium bacteria that nodulate leguminous trees. FEMS Microbiol Lett 119:215–2201

    Article  CAS  Google Scholar 

  • Haukka K, Lindström K, Young JP (1998) Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64:419–426

    PubMed  CAS  Google Scholar 

  • Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia–legume symbiosis so special? Plant Physiol 127:1484–1492

    Article  PubMed  CAS  Google Scholar 

  • Honma MA, Asomaning M, Ausubel FM (1990) Rhizobium meliloti nodD genes mediate host-specific activation of nodABC. J Bacteriol 172:901–911

    PubMed  CAS  Google Scholar 

  • Jarvis BDW, Sivacumaran S, Tighe SW, Gillis M (1996) Identification of Agrobacterium and Rhizobium species based on cellular fatty acids composition. Plant Soil 184:143–158

    Article  CAS  Google Scholar 

  • Jarvis BDW, Tighe SW (1994) Rapid identification of Rhizobium species based on cellular fatty acid analysis. Plant Soil 161:31–41

    Article  CAS  Google Scholar 

  • Jourand P, Giraud E, Bena G, Sy A, Willems A, Gillis M, Dreyfus B, de Lajudie P (2004) Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule forming and nitrogen fixung bacteria. Int J Syst Evol Microbiol 54:2269–2273

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (supplement). DNA Res 31:381–406

    Article  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    Article  PubMed  Google Scholar 

  • Kondorosi E, Banfalvi Z, Kondorosi A (1984) Physical and genetic analysis of a symbiotic region of Rhizobium meliloti: identification of nodulation genes. Mol Gen Genet 193:445–452

    Article  CAS  Google Scholar 

  • Krishnan HB, Pueppke SG (1994) Host range, RFLP, and antigenic relationships between Rhizobium fredii strains and Rhizobium sp. NGR234. Plant Soil 161:21–29

    Article  CAS  Google Scholar 

  • Laguerre G, Allard MR, Revoy F, Amarger N (1994) Rapid identification of rhizobia by restriction fragment polymorpfism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 60:56–63

    PubMed  CAS  Google Scholar 

  • Laguerre G, Fernandez MP, Edel V, Normand P, Amarger N (1993) Genomic heterogeneity among french Rhizobium strains isolated from Phaseolus vulgaris L. Int J Syst Bacteriol 43:761–767

    PubMed  CAS  Google Scholar 

  • Laguerre G, Louvrier P, Allard MR, Amarger N (2003) Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulation of host legumes. Appl Environ Microbiol 69:2276–2283

    Article  PubMed  CAS  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 Rhizobium leguminosarum and its different biovars. Appl Environ Microbiol 62:2029–2036

    PubMed  CAS  Google Scholar 

  • Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993

    PubMed  CAS  Google Scholar 

  • Lan RT, Reevers PR (2000) Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8:396–401

    Article  PubMed  CAS  Google Scholar 

  • Lan RT, Reevers PR (2001) When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends Microbiol 9:419–324

    Article  PubMed  CAS  Google Scholar 

  • Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 54:575–594

    Article  PubMed  Google Scholar 

  • Leigh JA (2000) Nitrogen fixation in methanogens: the archaeal perspective. Curr Issues Mol Biol 2:125–131

    PubMed  CAS  Google Scholar 

  • Lindstöm K (1989) Rhizobium galegae, a new species of root nodule bacteria. Int J Syst Bacteriol 39:365–367

    Google Scholar 

  • Lindström K, Gyllenberg HG (2006) The species paradigm in bacteriology: proposal for cross-disciplinary species concept. World federation of culture collections Newsletter-July 2006: 4–13 http://wdcm.nig.ac.jp/wfcc/

  • Louvrier P, Laguerre G, Amarger N (1996) Distribution of symbiotic genotypes in Rhizobium leguminosarum biovar viciae populations isolated directly from soils. Appl Environ Microbiol 62:4202–4205

    PubMed  CAS  Google Scholar 

  • Martinez E, Romero D, Palacios R (1990) The Rhizobium genome. Crit Rev Plant Sci 9:59–93

    Article  CAS  Google Scholar 

  • Martinez-Romero E, Lindström K, van Bercum P, Eardly B, Chen WX, de Lajudie P, Graham PH, Jarvis BDW, Laguerre G, Nesme X, Young JPW, Vinuesa P, Willems A (2006) ICSP Subcommittee on the taxonomy of Rhizobium and Agrobacterium-diversity, phylogeny and systematics. http://edzna.ccg.unam.mx/csb-sra/ . Last full update 16th of March 2007

  • Martinez-Romero E, Segovia L, Martins Mercante F, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. bean and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426

    PubMed  CAS  Google Scholar 

  • Martinez-Romero E, Vinuesa P, Young PJW, de Lajudie P, Eardly B, Laguerre G, van Bercum P, Willems A, Javis BDW, Lindstöm K (2007) Guidelines to propose new rhizobial species. Manuscript submitted

    Google Scholar 

  • Mayr E (1957) Species concept and definitions: In: Mayr E (ed) The species problem. The American Association for the Advancement of Science, Washinton D.C., USA, pp. 1–22

    Google Scholar 

  • Mehta MP, Baross JA (2006) Nitrogen fixation at 92 degrees C by a hydrothermalvent archaeon. Science 314:1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Moreira FMS, Gillis M, Pot B, Kersters K, Franco AA (1993) Characterization of rhizobia isolated from different divergence groups of tropical Leguminosae by comparative polyacrylamide gel electrophoresis of their total proteins. Syst Appl Microbiol 16:135–146

    Google Scholar 

  • Moschetti G, Peluso A, Protopapa A, Anastasio M, Pepe O, Defez R (2005) Use of nodulation pattern, stress tolerance, nodC gene amplification, RAPD-PCR and RFLP-16S rDNA analysis to discriminate genotypes of Rhizobium leguminosarum biovar viciae. Syst Appl Microbiol 28:619–631

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Bena G, Boivin-Masson C, Stepkowski T (2004) Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Bovin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of Poteobacteria. Nature 411:948–950

    Article  PubMed  CAS  Google Scholar 

  • Ngom A, Nakagawa Y, Sawada H, Tsukahara J, Wakabayashi S, Uchiumi T, Nuntagij A, Kotepong S, Suzuki A, Higashi S, Abe M (2004) A novel symbiotic nitrogen-fixing member of the Ochrobactrum clade isolated from root nodules of Acacia mangium. J Gen Appl Microbiol 50:17–27

    Article  PubMed  CAS  Google Scholar 

  • Nichols R (2001) Gene trees and species trees are not the same. Trends Ecol Evol 16:358–364

    Article  PubMed  Google Scholar 

  • Nick G, Lindström K (1994) Use of repetitive sequences and the polymerase chain reaction to fingerprint the genomic DNA of Rhizobium galegae strains and to identify the DNA obtained by sonicating the liquid cultures and root nodules. Syst Appl Microbiol 17:265–273

    CAS  Google Scholar 

  • Nick G, de Lajudie P, Eardly BD, Suominen S, Paulin L, Zhang X, Gillis M, Lindström K (1999) Sinorhizobium arboris sp. Nov., and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Bacteriol 49:1359–1368

    PubMed  CAS  Google Scholar 

  • Page RDM, Charleston MA (1998) Trees within trees: Phylogeny and historical associations. Trends Ecol Evol 13:356–359

    Article  CAS  PubMed  Google Scholar 

  • Palys T, Nakamura LK, Cohan FM (1997) Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int J Syst Bacteriol 47:1145–1156

    PubMed  CAS  Google Scholar 

  • Parker MA, Lafay B, Burdon J, van Berkum P (2002) Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium. Microbiol 148:2557–2565

    Google Scholar 

  • Pérez-Ramírez NO, Rogel MA, Wang E, Castellanos JZ, Martínez-Romero E (1998) Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol Ecol 26:289–296

    Google Scholar 

  • Perret X, Broughton WJ, Brenner S (1991) Canonical ordered cosmid library of the symbiotic plasmid of Rhizobium species NGR234. Proc Natl Acad Sci USA 88:1923–1927

    Article  PubMed  CAS  Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Article  PubMed  CAS  Google Scholar 

  • Postgate J (1998) Nitrogen fixation, 3rd edn. Cambridge University Press, Cambridge UK

    Google Scholar 

  • Provorov NA (1998) Coevolution of rhizobia with legumes: Facts and Hypotheses. Symbiosis 24:337–368

    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

    Article  PubMed  CAS  Google Scholar 

  • Rademaker JL, Hoste B, Louws FJ, Kersters K, Swings J, Vauterin L, Vauterin P, de Bruijn FJ (2000) Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system. Int J Syst Evol Microbiol 50:665–677

    PubMed  CAS  Google Scholar 

  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  PubMed  CAS  Google Scholar 

  • Raven PH, Polhill RM (1981) Biogeography of the Leguminosae. In: Polhill RM, Raven PH (eds) Advances in legume systematics, part 2. Royal Botanic Gardens, Kew, pp. 27–34

    Google Scholar 

  • Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554

    Article  PubMed  CAS  Google Scholar 

  • Rivas R, Velazquez E, Willems A, Vizcaino N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martinez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microbiol 68:5217–5222

    Article  PubMed  CAS  Google Scholar 

  • Roche P, Maillet F, Plazanet C, Debelle F, Ferro M, Truchet G, Prome JC, Denarie J (1996) The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc Natl Acad Sci USA 93:15305–15310

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Quiñones F, Maguire M, Wallington EJ, Gould PS, Yerko V, Downie JA, Lund PA (2005) Two of the three groEL homologues in Rhizobium leguminosarum are dispensable for normal growth. Arch Microbiol 183:253–265

    Article  PubMed  CAS  Google Scholar 

  • Ruvkun GB, Ausubel FM (1980) Interspecies homology of nitrogenase genes. Proc Natl Acad Sci USA 77:191–195

    Article  PubMed  CAS  Google Scholar 

  • Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155–179

    Article  PubMed  CAS  Google Scholar 

  • Selbitschka W, Zekri S, Schröder G, Pühler A, Toro N (1999) The Sinorhizobium meliloti insertion sequence (IS) elements ISRm102F34-1/ISRm7 and ISRm220-13-5 belong to a new family of insertion sequence elements. FEMS Microbiol Lett 172:1–7

    Article  PubMed  CAS  Google Scholar 

  • Selenska-Pobell S, Evguenieva-Hackenberg E, Radeva G, Squartini A (1996) Characterization of Rhizobium “hedysari” by RFLP analysis of PCR amplified rDNA and by genomic PCR fingerprinting. J Appl Bacteriol 5:517–528

    Google Scholar 

  • Silva C, Vinuesa P, Eguiarte LE, Martinez-Romero E, Sousa V (2003) Rhizobium etli and Rhizobium gallicum nodulate common bean (Phaseolus vulgaris) in a traditionally managed milpa plot in Mexico: population genetics and biogeographic implications. Appl Environ Microbiol 69:884–893

    Article  PubMed  CAS  Google Scholar 

  • Silva C, Vinuesa P, Eguiarte LE, Souza V, Martnez-Romero E (2005) Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol Ecol 14:4033–4050

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92:2647–2651

    Article  PubMed  CAS  Google Scholar 

  • Spaink HP, Wijffelman CA, Pees E, Okker RH, Lugtenberg BJJ (1987) Rhizobium nodulation gene nodD as a determinant of host specificity. Nature 328:337–340

    Article  CAS  Google Scholar 

  • Sprent JI (1994) evolution and diversity in the legume-rhizobium symbiosis: chaos theory? Plant Soil 161:1–10

    Article  Google Scholar 

  • Sprent JI (1995) Legume trees and shrubs in the tropics: N2 fixation in perspective. Soil Biol Biochem 27:401–407

    Article  CAS  Google Scholar 

  • Sprent JI, Sprent P (1990) Nitrogen fixing organisms. Chapman and Hall, New York

    Google Scholar 

  • Stackebrandt E, Frederiksen W, Garrity GM, Grimont PA, Kampfer P, Maiden MC, Nesme X, Rossello-Mora R, Swings J, Truper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047

    Article  PubMed  CAS  Google Scholar 

  • Stepkowski T, Czaplinska M, Miedzinska K, Moulin L (2003) The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Poteobacteria. Syst Appl Microbiol 26:483–494

    Article  PubMed  CAS  Google Scholar 

  • Stepkowski T, Moulin L, Krzyzanska A, McInnes A, Law IJ, Howieson J (2005) European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl Environ Microbiol 71:7041–7052

    Article  PubMed  CAS  Google Scholar 

  • Suominen L, Roos C, Lortet G, Paulin L, Lindström K (2001) Identification and structure of the Rhizobium galegae common nodulation genes: evidence for horizontal gene transfer. Mol Biol Evol 18:907–916

    PubMed  CAS  Google Scholar 

  • Suominen L, Luukkainen R, Roos C, Lindström K (2003) Activation of the nodA promoter by the nodD genes of Rhizobium galegae induced by synthetic flavonoids or Galega orientalis root exudate. FEMS Microbiol Lett 219:225–232

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JT, Eardly BD, van Berkum P, Ronson CW (1996) Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microbiol 62:2818–2825

    PubMed  CAS  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220

    Article  PubMed  CAS  Google Scholar 

  • Terefework Z, Kaijalainen S, Lindström K (2001) AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and G. officinalis. J Biotechnol 91:169–180

    Article  PubMed  CAS  Google Scholar 

  • Terefework Z, Lortet G, Suominen L, Lindström K (2000) Molecular evolution of interactions between rhizobia and their legume hosts. In: Triplett E (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Wymondham, UK, pp 187–206

    Google Scholar 

  • Terefework Z, Nick G, Suomalainen S, Paulin L, Lindström K (1998) Phylogeny of Rhizobium galegae with respect to other rhizobia and agrobacteria. Int J Syst Bacteriol 48:349–356

    Article  PubMed  Google Scholar 

  • Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludena D, Mateos PF, Martinez-Molina E, Velazquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Turner SL, Zhang XX, Li FD, Young JP (2002) What does a bacterial genome sequence represent? Mis-assignment of MAFF 303099 to the genospecies Mesorhizobium loti. Microbiol 148:3330–3331

    Google Scholar 

  • Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995a) Genetic diversity of N2-fixing bacteria associated with rice roots by molecular evolutionary analysis of nifD library. Can J Microbiol 41:235–240

    Article  PubMed  CAS  Google Scholar 

  • Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995b) Phylogeny of Sym plasmids of rhizobia by PCR-based sequencing of a nodC segment. J Bacteriol 177:468–472

    PubMed  CAS  Google Scholar 

  • Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995c) 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 

  • Valverde A, Velazquez E, Gutiérrez C, Cervantes E, Ventosa A, Igual J-M (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979–1983

    Article  PubMed  CAS  Google Scholar 

  • van Bercum P, Eardly BD (1998) I: Spaink HP, Kondorosi A, Hooykaas PJ (eds) JMolecular evolutionary systematics of the Rhizobiaceae. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1–24

    Google Scholar 

  • van Berkum P, Eardly BD (2002) The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl Environ Microbiol 68:1132–1136

    Article  PubMed  CAS  Google Scholar 

  • van Berkum P, Fuhrmann JJ (2000) Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int J Syst Evol Microbiol 50:2165–2172

    PubMed  Google Scholar 

  • van Berkum P, Leibold JM, Eardly BD (2006) Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst Appl Microbiol 29:207–215

    Article  PubMed  CAS  Google Scholar 

  • Vandamme P, Coenye T (2004) Taxonomy of the genus Cupravidus: a tale of lost and found. Int J Syst Evol Microbiol 54:2285–2289

    Article  PubMed  Google Scholar 

  • Vandamme P, Pot B, Gillis M, De Vos PK, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus pproach to bacterial systematics. Microbiol Rev 60:407–438

    PubMed  CAS  Google Scholar 

  • van Rhijn PJ, Feys B, Verreth C, Vanderleyden J (1993) Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J Bacteriol 175:438–447 (Erratum in: J Bacteriol (1993) 175:3692)

    PubMed  Google Scholar 

  • Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbioses: Legumes, actinorhizal plants, Parasponia sp. and cycads. Plant Soil 274:51–78

    Article  CAS  Google Scholar 

  • Vinuesa P, Leon-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Perez-Galdona R, Werner D, Martinez-Romero E (2005a) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575

    Article  PubMed  CAS  Google Scholar 

  • Vinuesa P, Silva C (2004) Species delineation and biogeography of symbiotic bacteria associated with cultivated and wild legumes. In: Werner D (ed) Biological resources and migration. Springer Verlag, Berlin, pp 143–155

    Google Scholar 

  • Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martinez-Romero E (2005b) Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol 28:702–716

    Article  PubMed  CAS  Google Scholar 

  • Vinuesa P, Silva C, Werner D, Martinez-Romero E (2005c) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 34:29–54

    Article  PubMed  CAS  Google Scholar 

  • Wang DY, Kumar S, Hedges SB (1999) Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc Biol Sci 266:163–171

    Article  PubMed  CAS  Google Scholar 

  • Wdowiak-Wrobel S, Malek W (2005) Genomic diversity of Astragalus cicer microsymbionts revealed by AFLP fingerprinting. J Gen Appl Microbiol 51:369–378

    Article  PubMed  CAS  Google Scholar 

  • Weir BS, Turner SJ, Silvester WB, Park DC, Young JM (2004) Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl Environ Microbiol 70:5980–5987

    Article  PubMed  CAS  Google Scholar 

  • Wernegreen JJ, Riley MA (1999) Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages. Mol Biol Evol 16:98–113

    PubMed  CAS  Google Scholar 

  • Widmer R, Shaffer BT, Porteous LA, Seidler J (1999) Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in the Oregon cascade mountain range. Appl Environ Microbiol 65:374–380

    PubMed  CAS  Google Scholar 

  • Willems A, Coopman R, Gillis M (2001) Comparison of sequence analysis of 16S–23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium. Int J Syst Evol Microbiol 51:623–632

    PubMed  CAS  Google Scholar 

  • Willems A, Collins MD (1993) Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol 43:305–313

    PubMed  CAS  Google Scholar 

  • Willems A, Munive A, de Lajudie P, Gillis M (2003) In most Bradyrhizobium groups sequence comparison of 16S–23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations. Syst Appl Microbiol 26:203–210

    Article  PubMed  CAS  Google Scholar 

  • Wojciechowski MF (2003) Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perspective. In: Klitgaard BB, Bruneau A (eds) Advances in legume systematics, part 10. Royal Botanic Gardens, Kew, UK

    Google Scholar 

  • Wojciechowski MF Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862

    Article  Google Scholar 

  • Wojciechowski M, Sanderson MJ, Steele KP, Liston A (2000) Molecular phylogeny of the “temperate herbaceous tribes” of papilionoid legumes: a supertree approach. In: Herendeen PS, Bruneau A (eds) Advances in legume systematics, part 9. Royal Botanic Gardens, Kew, pp 277–298

    Google Scholar 

  • Wolde-Meskel E, Terefework Z, Lindstrom K, Frostegard A (2004) Metabolic and genomic diversity of rhizobia isolated from field standing native and exotic woody legumes in southern Ethiopia. Syst Appl Microbiol 27:603–611

    Article  PubMed  CAS  Google Scholar 

  • Yanagi M, Yamasato K (1993) Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. FEMS Microbiol Lett 107:115–120

    Article  PubMed  CAS  Google Scholar 

  • Yang G-P, Debelle F, Savgnac A, Ferro M, Schiltz O, Maillet F, Prome D, Treilhou M, Vialas C, Lindström K, Denarie J, Prome J-C (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 α,β-unsaturated N-acyl substitutions. Mol Microbiol 34:227–237

    Article  PubMed  CAS  Google Scholar 

  • Young JPW (1992) Phylogenetic classification of nitrogen-fixing organisms. In Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, NY, pp 43–86

    Google Scholar 

  • Young JPY, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, 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

    Article  PubMed  CAS  Google Scholar 

  • Young JPW, Downer HL, Eardly BD (1991) Phylogeny of the phototrophic Rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J Bacteriol 173:2271–2277

    PubMed  CAS  Google Scholar 

  • Young JPW, Haukka KE (1996) Diversity and phylogeny of rhizobia. New Phytol 133:87–94

    Article  Google Scholar 

  • Young JPW, Johnston AWB (1989) The evolution of specificity in the legume-rhizobium symbiosis. Trends Ecol Evol 4:341–349

    Article  CAS  PubMed  Google Scholar 

  • Zézé A, Mutch LA, Young JP (2001) Direct amplification of nodD from community DNA reveals the genetic diversity of Rhizobium leguminosarum in soil. Environ Microbiol 3:363–370

    Article  PubMed  Google Scholar 

  • Zhang X-X, Guo X-W, Terefework Z, Cao Y-Z, Hu FR, Lindström K, Li F-D (1999) Genetic diversity among rhizobial isolates from field-grown Astragalus sinicus of Southern China. Syst Appl Microbiol 22:312–320

    Google Scholar 

  • Zhaxybayeva O, Gogarten JP (2004) Cladogenesis, coalescence and the evolution of the three domains of life. Trends Genet 20:182–177 (Erratum in: Trends Genet 2004 20:291)

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Applied Chemistry and Microbiology, Viikki Biocenter,University of Helsinki, PO Box 56 (Viikinkaari 9), 00014, Helsinki, Finland

    Aneta Dresler-Nurmi, David P. Fewer, Leena A. Räsänen & Kristina Lindström

Authors
  1. Aneta Dresler-Nurmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David P. Fewer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leena A. Räsänen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kristina Lindström
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aneta Dresler-Nurmi .

Editor information

Katharina Pawlowski

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Dresler-Nurmi, A., Fewer, D.P., Räsänen, L.A., Lindström, K. (2007). The Diversity and Evolution of Rhizobia. In: Pawlowski, K. (eds) Prokaryotic Symbionts in Plants. Microbiology Monographs, vol 8. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2007_099

Download citation

Publish with us

Policies and ethics

Search

Navigation