Abstract
The taxonomy of rhizobia, bacteria capable of nodulating leguminous plants, has changed considerably over the last 20 years, with the original genus Rhizobium, a member of the alpha-Proteobacteria, now divided into several genera. The study of new geographically dispersed host plants, has been a source of many new species and is expected to yield many more. Here we provide an overview of the history of the rhizobia, but focus on the Rhizobium–Allorhizobium–Agrobacterium relationship. Finally, we review recent reports of nodulation and nitrogen fixation with legume hosts by bacteria that are outside the traditional rhizobial phylogenetic lineages. They include species of Methylobacterium and Devosia in the alpha- Proteobacteria and of Burkholderia and Ralstonia in the beta-Proteobacteria.
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References
Alazard D 1985 Stem and root nodulation in Aeschynomene sp Appl. Evironm. Microbiol. 50: 732–734
Amarger N, Macheret V, Laguerre G 1997 Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris Int. J. Syst. Bacteriol. 47: 996–1006
Balkwill D L 2005 Genus VI. Ensifer Cassida 1982, 343VP. In: Garrity G M (eds) Bergey’s Manual of Systematic Bacteriology 2nd ed. Vol. 2, part C. Springer, New York pp. 354–358
Barrett C F, Parker M A 2006 Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp nodule bacteria on two Mimosa spp. in Costa Rica Appl. Environ. Microbiol. 72: 1198–1206
Beijerinck M W 1888 Cultur des Bacillus radicola aus den Knöllchen Bot. Ztg. 46: 740–750
Bouzar H 1994 Request for a Judicial Opinion concerning the type species of Agrobacterium Int. J. Syst. Bacteriol. 44: 373–374
Bouzar H, Jones J B 2001 Agrobacterium larrymoorei sp. nov., a pathogen isolated from aerial tumours of Ficus benjamini Int. J. Syst. Evol. Microbiol. 51: 1023–1026
Casida Jr L E 1982 Ensifer adhaerens, gen. nov., sp. nov.: A bacterial predator of bacteria in soil Int. J. Syst. Bacteriol. 32: 339–345
Chantreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, de Lajudie P, Dreyfus B 2000 Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata Appl. Environ. Microbiol. 66: 5437–5447
Chen W-M, Laevens S, Lee T-M, Coenye T, De Vos P, Mergeay M, Vandamme P 2001 Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of cystic fibrosis patients Int. J. Syst. Evol. Microbiol. 51: 1729–1735
Chen W X, Li G S, Qi Y L, Wang E T, Yuan H L, Li J L 1991 Rhizobium huakuii sp. nov. isolated from the root nodules of Astragalus sinicus Int. J. Syst. Bacteriol. 41: 275–280
Chen W-X, Tan Z-Y, Gao J-L, Li Y, Wang E T 1997 Rhizobium hainanense sp. nov., isolated from tropical legumes Int. J. Syst. Bacteriol. 47: 870–873
Chen W, Wang E, Wang S, Li Y, Chen X, Li Y 1995 Characterization of Rhizobium tianshanense sp. nov., a moderately and slow growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China Int. J. Syst. Bacteriol. 45: 153–159
Chen W X, Yan G H, Li J L 1988 Numerical taxonomic study of fast-growing soybean rhizobia and proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov Int. J. Syst. Bacteriol. 38: 392–397
Conn H J 1942 Validity of the genus Alcaligenes J. Bacteriol. 44: 353–360
Dangeard P A 1926 Recherches sur les turbercles radicaux des Légumineuses Botaniste (Paris) 16: 1–275
Date R A, Decker A M 1965 Minimal antigenic constitution of 28 strains of Rhizobium japonicum Can. J. Microbiol. 11: 1–8
de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins M D, Kersters K, Dreyfus B, Gillis M 1998a Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int. J. Syst. Bacteriol. 48: 1277–1290
de Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins M D, Lindström K, Dreyfus B, Gillis M 1998b Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov Int. J. Syst. Bacteriol. 48: 369–382
de Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins M D, 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
De Ley J, 1974 Phylogeny of Prokaryotes Taxon 23: 291–300
De Ley J, Rassel A 1965 DNA base composition, flagellation and taxonomy of the genus Rhizobium J. Gen. Microbiol. 41: 85–91
Dreyfus B, Garcia J L, Gillis M 1988 Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata Int. J. Syst. Bacteriol. 38: 89–98
Elkan G H, Bunn C R 1992 Chapter 107. The rhizobia. In: Balows A, Trüper H G, Dworkin M, Harder W, Schleifer K-H (eds) The Prokaryotes. A handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd ed., III. Springer-Verlag, New York, pp. 2197–2213
Euzéby J P 1998 Taxonomic note: Necessary correction of specific and subspecific epithets according to Rules 12c and 13b of the International Code of Nomenclature of Bacteria (1990 Revision) Int. J. Syst. Bacteriol. 48: 1073–1075
Evans W R, Fleischman D E, Calvert H E, Pyati R V, Alter G M, Subba Rao N S 1990 Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium strain BTAi1 Appl. Environ. Microbiol. 56: 3445–3449
Farrand S K, van Berkum P B, Oger P 2003 Agrobacterium is a definable member of the family Rhizobiaceae Int. J. Syst. Evol. Microbiol. 53: 1681–1687
Frank B, 1879 Ueber die Parasiten in den Wurzelanschwillungender Papilionaceen Ber. Dtsch. Bot. Ges. 37, 376–387 and 394–399
Frank B, 1889 Ueber die Pilzsymbiose der Leguminosen Ber. Deut. Bot. Ges. 7: 332–346
Fred E B, Baldwin I L, McCoy E 1932 Root Nodule Bacteria and Leguminous Plants. University of Wisconsin Studies in Science, number 5. University of Wisconsin Press, Madison
Gao J-L, Turner S L, Kan F L, Wang E T, Tan Z Y, Qiu Y H, Gu1 J, Terefework Z, Young J P W, Lindström K, Chen W X 2004 Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the northern regions of China Int. J. Syst. Evol. Microbiol. 54: 2003–2012
Ghosh W, Roy P 2006 Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant Int. J. Syst. Evol. Microbiol. 56: 91–97
Graham P H 1963 Antigenic affinities of the root-nodule bacteria of legumes Antonie van Leeuwenhoek J. Microbiol. Serol. 29: 281–291
Graham P H 1964 The application of computer techniques to the taxonomy of the root-nodule bacteria of legumes J. Gen. Microbiol. 35: 511–517
Graham P H, Sadowsky M J, Keyser H H, Barnet Y M, Bradley R S, Cooper J E, De Ley J, Jarvis B D W, Roslycky E B, Stijdom B W, Young J P W 1991 Proposed minimal standards for the description of new genera and species of root- and stem-nodulating bacteria Int. J. Syst. Bacteriol. 41: 582–587
Jarvis B D W, Downer H L, Young J P W 1992 Phylogeny of fast-growing soybean-nodulating rhizobia supports synonymy of Sinorhizobium and Rhizobium and assignment to Rhizobium fredii Int. J. Syst. Bacteriol. 42: 93–96
Jarvis B D W, Pankhurst C E, Patel J J 1982 Rhizobium loti, a new species of legume root nodule bacteria Int. J. Syst. Bacteriol. 32: 378–380
Jarvis B D W, van Berkum P, Chen W X, Nour S M, Fernandez M P, Cleyet-Marel J C, Gillis M 1997 Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov Int. J. Syst. Bacteriol. 47: 895–898
Jordan D C 1982 Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants Int. J. Syst. Bacteriol. 32: 136–139
Jordan D C 1984 Family III. Rhizobiaceae Conn 1938. In: Krieg N, Holt R G (eds) Bergey’s Manual of Systematic Bacteriology 1 1. The Williams & Wilkins Co., Baltimore, pp. 234–235
Jourand P, Giraud E, Béna 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-fixing bacteria Int. J. Syst. Evol. Microbiol. 54: 2269–2273
Judicial Commission 1970 Opinion 33. Conservation of the generic name Agrobacterium Conn 1942 Int. J. Syst. Bacteriol 20: 10
Kersters K, De Ley J 1984 Genus III. Agrobacterium Cohn 1942. In: Krieg N, Holt R G (eds) Bergey’s Manual of Systematic Bacteriology 1, 1. The Williams & Wilkins Co., Baltimore, pp. 244–254
Kuykendall L D, Saxena B, Devine T E, Udell S E 1992 Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov Can. J. Microbiol. 38: 501–505
Kuykendall L D, Young J M, Martínez-Romero E, Kerr A, Sawada H 2005 Genus I. Rhizobium Frank 1889, 338AL. In: Garrity G M (eds) Bergey’s Manual of Systematic Bacteriology, 2nd ed., Vol. 2, part C. Springer, New York, pp. 325–340
Lautrop H 1967 Agrobacterium spp. isolated from clinical specimens Acta Pathol. Microbiol. Scand. 187: 63–64
Lindström K 1989 Rhizobium galegae, a new species of legume root nodule bacteria Int. J. Syst. Bacteriol. 39: 365–367
Martínez-Romero E, Segovia L, Martins Mercante F, Franco A A, Graham P, Pardo M A 1991 Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. Beans and Leucaena sp. trees Int. J. Syst. Bacteriol. 41: 417–426
Moffet M L, Colwell R R 1968 Adansonian analysis of the Rhizobiaceae J. Gen. Microbiol. 51: 245–266
Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B, Gillis M, de Lajudie P, Masson-Boivin C 1999 Photosynthetic bradyrhizobia from Aeschynomene spp. are specific to stem-nodulated species and form a separate 16S ribosomal DNA restriction fragment length polymorphism group Appl. Environ. Microbiol. 65: 3084–3094
Moulin L, Munive A, Dreyfus B, Boivin-Masson C 2001 Nodulation of legumes by members of the β-subclass of Proteobacteria Nature 411: 948–950
Nick G, de Lajudie P, Eardly B D, Suomalainen 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
Nour S M, Cleyet-Marel J-C, Normand P, Fernandez M P 1995 Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterreaneum sp. nov Int. J. Syst. Bacteriol. 45: 640–648
Nour S M, Fernandez M P, Normand P, Cleyet-Marel J-C 1994 Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.) Int. J. Syst. Bacteriol. 44: 511–522
Ophel K, Kerr A 1990 Agrobacterium vitis sp. nov. for strains of Agrobacterium biovar 3 from grapevines Int. J. Syst. Bacteriol. 40: 236–241
Peng G X, Tan Z Y, Wang E T, Reinhold-Hurek B, Chen W F, Chen W X 2002 Identification of isolates from soybean nodules in Xinjiang region as Sinorhizobium xinjiangense and genetic differentiation of S. xinjiangense from Sinorhizobium fredii Int. J. Syst. Evol. Microbiol. 52: 457–462
Popoff M Y, Kersters K, Kiredjian M, Miras I, Coynault C 1984 Position taxonomique de souches de Agrobacterium d’origine hospitalière Ann. Microbiol. (Inst. Pasteur) 135A: 427–442
Quan Z-X, Bae H-S, Baek J-H, Chen W-F, Im W-T, Lee S-T 2005 Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor Int. J. Syst. Evol. Microbiol. 55: 2543–2549
Rasolomampianina R, Bailly X, Fetiarison R, Rabevohitra R, Bena G, Ramaroson L, Raherimandimby M, Moulin L, De Lajudie P, Dreyfus B, Avarre J C 2005 Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to alpha- and beta-Proteobacteria Mol. Ecol. 14: 4135–4146
Riley P S, Weaver R E 1977 Comparison of thirty-seven strains of Vd-3 bacteria with Agrobacterium radiobacter: Morphological and physiological observations J. Clin. Microbiol. 5: 172–177
Rivas R, Willems A, Palomo J L, García-Benavides P, Mateos P F, Martínez-Molina E, Gillis M, Velázquez E 2004 Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations Int. J. Syst. Evol. Microbiol. 54: 1271–1275
Rivas R, Willems A, Subba-Rao N, Mateos P F, Dazzo F B, Martínez-Molina E, Gillis M, Velàzquez E 2003 Description of Devosia neptunia sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India Syst. Appl. Microbiol. 26: 47–53
Rome S, Fernandez M P, Brunel B, Normand P, Cleyet-Marel J-C 1996 Sinorhizobium medicae sp. nov., isolated from annual Medicago spp Int. J. Syst. Bacteriol. 46: 972–980
Sawada H, Ieki H, Oyaizu H, Matsumoto S 1993 Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes Int. J. Syst. Bacteriol. 43: 694–702
Scholla M H, Elkan G H 1984 Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybean Int. J. Syst. Bacteriol. 34: 484–486
Schroeter J 1886 Schizomycetes. In: Cohn (eds) Kryptogamenflora von Sclesien, Bd. 3, Heft 3, Pilze. J U Kern’s Verlag, Breslau, pp. 1–814
Segovia L, Young J P W, Martínez-Romero E 1993 Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli Int. J. Syst. Bacteriol. 43: 374–377
Skerman V B D, McGowan V, Sneath P H A 1980 Approved lists of bacterial names Int. J. Syst. Bacteriol. 30: 225–420
Sprent J I 1995 Legume trees and shrubs in the tropics: N2 fixation in prespective Soil Biol. Biochem. 27: 401–407
Squartini A, Struffi P, Döring H, Selenska-Pobell S, Tola E, Giacomini A, Vendramin E, Velàzquez E, Mateos P F, Martínez-Molina E, Dazzo F B, Casella S, Nuti M P 2002 Rhizobium sullae sp. nov. (formerly ‘Rhizobium hedysari’), the root-nodule microsymbiont of Hedysarum coronarium L Int. J. Syst. Evol. Microbiol. 52: 1267–1276
Starr M P, Weiss J E 1943 Growth of phytopathogenic bacteria in a synthetic asparagine medium Phytopathology 33: 314–318
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
Tan Z Y, Kan F L, Peng G X, Wang E T, Reinholdt-Hurek B, Chen W X 2001 Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China Int. J. Syst. Evol. Microbiol. 51: 909–914
‘tMannetje L 1967 A re-examination of the taxonomy of the genus Rhizobium and related genera using numerical analysis Antonie van Leeuwenhoek J. Microbiol. Serol. 33: 477–491
Toledo I, Lloret L, Martínez-Romero E 2003 Sinorhizobium americanus sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico Syst. Appl. Microbiol. 26: 54–64
Trujillo M E, Willems A, Abril A, Planchuelo A-M, Rivas R, Ludeña D, Mateos P F, Martínez-Molina E, Velázquez E 2005 Nodulation of Lupinus by strains of Ochrobactrum lupini sp. nov Appl. Environ. Microbiol. 71: 1318–1327
Trüper H G, De’Clari L 1997 Taxonomic note: necessary correction of specific epithets formed as substantives (nouns) “in apposition” Int. J. Syst. Bacteriol. 47: 908–909
Valverde A, Velázquez E, Fernández-Santos F, Vizcaíno N, Rivas R, Gillis M, Mateos P F, Martínez-Molina E, Igual J M, Willems A 2005 Phyllobacterium trifolii sp. nov. nodulating Trifolium and Lupinus in Spanish soils Int. J. Syst. Evol. Microbiol. 55: 1985–1989
van Berkum P, Beyene D, Bao G, Campbell T A, Eardly B D 1998 Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour] Int. J. Syst. Bacteriol. 48: 13–22
van Berkum P, Eardly B D 2002 The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica Appl. Environ. Microbiol. 68: 1132–1136
van Berkum P, Leibold J M, Eardly B D 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
Vandamme P, Goris J, Chen W-M, De Vos P, Willems A 2003 Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes Syst. Appl. Microbiol. 25: 507–512
Vandamme P, Pot B, Gillis M, De Vos P, Kersters K, Swings J 1996 Polyphasic taxonomy, a consensus approach to bacterial systematics Microbiol. Rev. 60: 407–438
Velázquez E, Igual J M, Willems A, Fernández M P, Muñoz E, Mateos P F, Abril A, Toro N, Normand P, Cervantes E, Gillis M, Martínez-Molina E 2001 Description of Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina) Int. J. Syst. Evol. Microbiol. 51: 1011–1021
Vermis K, Coenye T, LiPuma J J, Mahenthiralingam E, Nelis H J, Vandamme P 2004 Proposal to accommodate Burkholderia cepacia genomovar VI as Burkholderia dolosa sp. nov Int. J. Syst. Evol. Microbiol. 54: 689–691
Vincent J M, Humphrey B A 1970 Taxonomically significant group antigens in Rhizobium J. Gen. Microbiol. 63: 379–382
Vinuesa P, León-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Pérez-Galdona R, Werner D, Martínez-Romero E 2005 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
Wang E T, van Berkum P, Beyene D, Sui X H, Dorado O, Chen W X, Martínez-Romero E 1998 Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae Int. J. Syst. Bacteriol. 48: 687–699
Wang E, Tan Z Y, Willems A, Fernández-López M, Reinhold-Hurek B, Martínez-Romero E 2002 Sinorhizobium morelense, sp. nov. a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics Int. J. Syst. Evol. Microbiol. 52: 1687–1693
Wang E T, van Berkum P, Sui X H, Beyene D, Chen W X, Martínez-Romero E 1999 Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and descritpion of Mesorhizobium amorphae sp. nov Int. J. Syst. Bacteriol. 49: 51–65
Wei G H, Tan Z Y, Zhu M E, Wang E T, Han S Z, Chen W X 2003 Characterization of rhizobia isolated from legume species within the genera Astragalus and Lespedeza grown in the Loess Plateau of China and description of Rhizobium loessense sp. nov Int. J. Syst. Evol. Microbiol. 53: 1575–1583
Wei G H, Wang E T, Tan Z Y, Zhu M E, Chen W X 2002 Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulaceae Int. J. Syst. Evol. Microbiol. 52: 2231–2239
Willems A, Coopman R, Gillis M 2001a Phylogenetic and DNA: DNA hybridization analyses of Bradyrhizobium species Int. J. Syst. Evol. Microbiol. 51: 111–117
Willems A, Coopman R, Gillis M 2001b Comparison of sequence analysis of 16S–23S spacer regions, AFLP analysis and DNA–DNA hybridizations in Bradyrhizobium Int. J. Syst. Evol. Microbiol. 51: 623–632
Willems A, Doignon-Bourcier F, Goris J, Coopman R, de Lajudie P, De Vos P, Gillis M 2001c DNA–DNA hybridization study of Bradyrhizobium strains Int. J. Syst. Evol. Microbiol. 51: 1315–1322
Willems A, Fernández-López M, Muñoz-Adelantado E, Goris J, De Vos P, Martínez-Romero E, Toro N, Gillis M 2003 Description of New Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Cassida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an Opinion Int. J. Syst. Evol. Microbiol. 53: 1207–1217
Wilson J K 1944 Over five hundred reasons for abandoning the cross inoculation groups of legumes Soil Sci. 58: 61–69
Xu M L, Ge C, Cui Z, Li J, Fan H 1995 Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans Int. J. Syst. Bacteriol. 45: 706–711
Yao Z Y, Kan F L, Wang E T, Wei G H, Chen W X 2002 Characterization of rhizobia that nodulate legume species within the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov Int. J. Syst. Evol. Microbiol. 52: 2219–2230
Young J M 2003 The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 legitimate? Request for an Opinion Int. J. Syst. Evol. Microbiol. 53: 2107–2110
Young J M 2004 Renaming of Agrobacterium larrymoorei Bouzar and Jones 2001 as Rhizobium larrymoorei (Bouzar and Jones 2001) comb. nov Int. J. Syst. Evol. Microbiol. 54: 149
Young J M, Kuykendall L D, Martínez-Romero E, Kerr A, Sawada H 2001 A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis Int. J. Syst. Evol. Microbiol. 51: 89–103
Young J M, Pennycook S R, Watson D R W 2006 Proposal that Agrobacterium radiobacter has priority over Agrobacterium tumefaciens. Request for an Opinion Int. J. Syst. Evol. Microbiol. 56: 491–493
Zakhia F, Jeder H, Willems A, Dreyfus B, de Lajudie P 2006 Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb. Ecol. 51, 375–393
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The author is grateful to the Fund for Scientific Research – Flanders for a Postdoctoral Fellowship.
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Willems, A. The taxonomy of rhizobia: an overview. Plant Soil 287, 3–14 (2006). https://doi.org/10.1007/s11104-006-9058-7
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DOI: https://doi.org/10.1007/s11104-006-9058-7