The taxonomy of rhizobia: An overview

Plant and Soil

Volumn 287, Issue 1-2, 2006, Pages 3-14

  Willems, Anne ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Agrobacterium; Review; Rhizobia; Taxonomy

Indexed keywords

HOST PLANT; LEGUME; NEW SPECIES; NITROGEN FIXATION; NODULATION; RHIZOBACTERIUM; TAXONOMY;

AGROBACTERIUM; ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; BURKHOLDERIA; DEVOSIA; FABACEAE; METHYLOBACTERIUM; RALSTONIA; RHIZOBIACEAE; RHIZOBIUM;

EID: 33749537045     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-006-9058-7     Document Type: Review

References (104)

1. Alazard D 1985 Stem and root nodulation in Aeschynomene sp. Appl. Evironm. Microbiol. 50, 732-734.
2. Amarger N, Macheret V and Laguerre G 1997 Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris. Int. J. Syst. Bacteriol. 47, 996-1006.
3. VP. In Bergey's Manual of Systematic Bacteriology 2nd ed. Vol. 2, part C. Ed. G M Garrity. pp. 354-358. Springer, New York.
4. Barrett C F and 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.
5. Beijerinck M W 1888 Cultur des Bacillus radicola aus den Knöllchen. Bot. Ztg. 46, 740-750.
6. Bouzar H 1994 Request for a Judicial Opinion concerning the type species of Agrobacterium. Int. J. Syst. Bacteriol. 44, 373-374.
7. Bouzar H and 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.
8. Casida L E Jr 1982 Ensifer adhaerens, gen. nov., sp. nov.: A bacterial predator of bacteria in soil. Int. J. Syst. Bacteriol. 32, 339-345.
9. Chantreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, de Lajudie P and Dreyfus B 2000 Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66, 5437-5447.
10. Chen W-M, Laevens S, Lee T-M, Coenye T, De Vos P, Mergeay M and 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.
11. Chen W X, Li G S, Qi Y L, Wang E T, Yuan H L and Li J L 1991 Rhizobium huakuii sp. nov. isolated from the root nodules of Astragalus sinicus. Int. J. Syst. Bacteriol. 41, 275-280.
12. Chen W-X, Tan Z-Y, Gao J-L, Li Y and Wang E T 1997 Rhizobium hainanense sp. nov., isolated from tropical legumes. Int. J. Syst. Bacteriol. 47, 870-873.
13. Chen W, Wang E, Wang S, Li Y, Chen X and 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.
14. Chen W X, Yan G H and 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.
15. Conn H J 1942 Validity of the genus Alcaligenes. J. Bacteriol. 44, 353-360.
16. Dangeard P A 1926 Recherches sur les turbercles radicaux des Légumineuses. Botaniste (Paris) 16, 1-275.
17. Date R A and Decker A M 1965 Minimal antigenic constitution of 28 strains of Rhizobium japonicum. Can. J. Microbiol. 11, 1-8.
18. de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins M D, Kersters K, Dreyfus B and 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.
19. de Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins M D, Lindström K, Dreyfus B and Gillis M 1998b Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int. J. Syst. Bacteriol. 48, 369-382.
20. de Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins M D, Dreyfus B, Kersters K and 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.
21. De Ley J 1974 Phylogeny of Prokaryotes. Taxon 23, 291-300.
22. De Ley J and Rassel A 1965 DNA base composition, flagellation and taxonomy of the genus Rhizobium. J. Gen. Microbiol. 41, 85-91.
23. Dreyfus B, Garcia J L and 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.
24. Elkan G H and Bunn C R 1992 Chapter 107. The rhizobia. In The Prokaryotes. A handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications. Eds. A Balows, H G Trüper, M Dworkin, W Harder and K-H Schleifer. pp. 2197-2213. 2nd edition, Vol. III Springer-Verlag, New York.
25. 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.
26. Evans W R, Fleischman D E, Calvert H E, Pyati R V, Alter G M and Subba Rao N S 1990 Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium strain BTAi1. Appl. Environ. Microbiol. 56, 3445-3449.
27. Farrand S K, van Berkum P B and Oger P 2003 Agrobacterium is a definable member of the family Rhizobiaceae. Int. J. Syst. Evol. Microbiol. 53, 1681-1687.
28. Frank B, 1879 Ueber die Parasiten in den Wurzelanschwillungender Papilionaceen Ber. Dtsch. Bot. Ges. 37, 376-387 and 394-399.
29. Frank B 1889 Ueber die Pilzsymbiose der Leguminosen. Ber. Deut. Bot. Ges. 7, 332-346.
30. Fred E B, Baldwin I L and McCoy E 1932 Root Nodule Bacteria and Leguminous Plants. University of Wisconsin Studies in Science, number 5. University of Wisconsin Press, Madison.
31. 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 and 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.
32. Ghosh W and 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.
33. Graham P H 1963 Antigenic affinities of the root-nodule bacteria of legumes. Antonie van Leeuwenhoek J. Microbiol. Serol. 29, 281-291.
34. 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.
35. 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 and 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.
36. Jarvis B D W, Downer H L and 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.
37. Jarvis B D W, Pankhurst C E and Patel J J 1982 Rhizobium loti, a new species of legume root nodule bacteria. Int. J. Syst. Bacteriol. 32, 378-380.
38. Jarvis B D W, van Berkum P, Chen W X, Nour S M, Fernandez M P, Cleyet-Marel J C and 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.
39. 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.
40. Jordan D C 1984 Family III. Rhizobiaceae Conn 1938. In Bergey's Manual of Systematic Bacteriology. Eds. N Krieg and R G Holt. pp. 234-235. 1st edition, Vol. 1 The Williams & Wilkins Co, Baltimore.
41. Jourand P, Giraud E, Béna G, Sy A, Willems A, Gillis M, Dreyfus B and 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.
42. Judicial Commission 1970 Opinion 33. Conservation of the generic name Agrobacterium Conn 1942. Int. J. Syst. Bacteriol 20, 10.
43. Kersters K and De Ley J 1984 Genus III. Agrobacterium Cohn 1942. In Bergey's Manual of Systematic Bacteriology. Eds. N Krieg and R G Holt. pp. 244-254. 1st edition, Vol. 1 The Williams & Wilkins Co, Baltimore.
44. Kuykendall L D, Saxena B, Devine T E and 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.
45. AL. In Bergey's Manual of Systematic Bacteriology, 2nd ed., Vol. 2, part C. Ed. G M Garrity. pp. 325-340. Springer, New York.
46. Lautrop H 1967 Agrobacterium spp. isolated from clinical specimens. Acta Pathol. Microbiol. Scand. 187, 63-64.
47. Lindström K 1989 Rhizobium galegae, a new species of legume root nodule bacteria. Int. J. Syst. Bacteriol. 39, 365-367.
48. Martínez-Romero E, Segovia L, Martins Mercante F, Franco A A, Graham P and 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.
49. Moffet M L and Colwell R R 1968 Adansonian analysis of the Rhizobiaceae. J. Gen. Microbiol. 51, 245-266.
50. Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B, Gillis M, de Lajudie P and 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.
51. Moulin L, Munive A, Dreyfus B and Boivin-Masson C 2001 Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411, 948-950.
52. Nick G, de Lajudie P, Eardly B D, Suomalainen S, Paulin L, Zhang X, Gillis M and 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.
53. Nour S M, Cleyet-Marel J-C, Normand P and 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.
54. Nour S M, Fernandez M P, Normand P and 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.
55. Ophel K and Kerr A 1990 Agrobacterium vitis sp. nov. for strains of Agrobacterium biovar 3 from grapevines. Int. J. Syst. Bacteriol. 40, 236-241.
56. Peng G X, Tan Z Y, Wang E T, Reinhold-Hurek B, Chen W F and 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.
57. Popoff M Y, Kersters K, Kiredjian M, Miras I and Coynault C 1984 Position taxonomique de souches de Agrobacterium d'origine hospitalière. Ann. Microbiol. (Inst. Pasteur) 135A, 427-442.
58. Quan Z-X, Bae H-S, Baek J-H, Chen W-F, Im W-T and Lee S-T 2005 Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor. Int. J. Syst. Evol. Microbiol. 55, 2543-2549.
59. Rasolomampianina R, Bailly X, Fetiarison R, Rabevohitra R, Bena G, Ramaroson L, Raherimandimby M, Moulin L, De Lajudie P, Dreyfus B and 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.
60. Riley P S and 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.
61. Rivas R, Willems A, Palomo J L, García-Benavides P, Mateos P F, Martínez-Molina E, Gillis M and 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.
62. Rivas R, Willems A, Subba-Rao N, Mateos P F, Dazzo F B, Martínez-Molina E, Gillis M and 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.
63. Rome S, Fernandez M P, Brunel B, Normand P and Cleyet-Marel J-C 1996 Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int. J. Syst. Bacteriol. 46, 972-980.
64. Sawada H, Ieki H, Oyaizu H and 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.
65. Scholla M H and Elkan G H 1984 Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybean. Int. J. Syst. Bacteriol. 34, 484-486.
66. Schroeter J 1886 Schizomycetes. In Kryptogamenflora von Sclesien, Bd. 3, Heft 3, Pilze. Ed. Cohn. pp. 1-814. J U Kern's Verlag, Breslau.
67. Segovia L, Young J P W and Martínez-Romero E 1993 Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli. Int. J. Syst. Bacteriol. 43, 374-377.
68. Skerman V B D, McGowan V and Sneath P H A 1980 Approved lists of bacterial names. Int. J. Syst. Bacteriol. 30, 225-420.
69. 2 fixation in prespective. Soil Biol. Biochem. 27, 401-407.
70. 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 and 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.
71. Starr M P and Weiss J E 1943 Growth of phytopathogenic bacteria in a synthetic asparagine medium. Phytopathology 33, 314-318.
72. Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C and Dreyfus B 2001 Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183, 214-220.
73. Tan Z Y, Kan F L, Peng G X, Wang E T, Reinholdt-Hurek B and 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.
74. '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.
75. Toledo I, Lloret L and Martínez-Romero E 2003 Sinorhizobium americanus sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst. Appl. Microbiol. 26, 54-64.
76. Trujillo M E, Willems A, Abril A, Planchuelo A-M, Rivas R, Ludeña D, Mateos P F, Martínez-Molina E and Velázquez E 2005 Nodulation of Lupinus by strains of Ochrobactrum lupini sp. nov. Appl. Environ. Microbiol. 71, 1318-1327.
77. Trüper H G and De'Clari L 1997 Taxonomic note: necessary correction of specific epithets formed as substantives (nouns) "in apposition". Int. J. Syst. Bacteriol. 47, 908-909.
78. Valverde A, Velázquez E, Fernández-Santos F, Vizcaíno N, Rivas R, Gillis M, Mateos P F, Martínez-Molina E, Igual J M and Willems 2005 Phyllobacterium trifolii sp. nov. nodulating Trifolium and Lupinus in Spanish soils. Int. J. Syst. Evol. Microbiol. 55, 1985-1989.
79. van Berkum P, Beyene D, Bao G, Campbell T A and 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.
80. van Berkum P and Eardly B D 2002 The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl. Environ. Microbiol. 68, 1132-1136.
81. van Berkum P, Leibold J M and 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.
82. Vandamme P, Goris J, Chen W-M, De Vos P and Willems A 2003 Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst. Appl. Microbiol. 25, 507-512.
83. Vandamme P, Pot B, Gillis M, De Vos P, Kersters K and Swings J 1996 Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol. Rev. 60, 407-438.
84. 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 and 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.
85. Vermis K, Coenye T, LiPuma J J, Mahenthiralingam E, Nelis H J and Vandamme P 2004 Proposal to accommodate Burkholderia cepacia genomovar VI as Burkholderia dolosa sp. nov. Int. J. Syst. Evol. Microbiol. 54, 689-691.
86. Vincent J M and Humphrey B A 1970 Taxonomically significant group antigens in Rhizobium. J. Gen. Microbiol. 63, 379-382.
87. Vinuesa P, León-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Pérez-Galdona R, Werner D and 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.
88. Wang E T, van Berkum P, Beyene D, Sui X H, Dorado O, Chen W X and 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.
89. Wang E, Tan Z Y, Willems A, Fernández-López M, Reinhold-Hurek B and 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.
90. Wang E T, van Berkum P, Sui X H, Beyene D, Chen W X and 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.
91. Wei G H, Tan Z Y, Zhu M E, Wang E T, Han S Z and 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.
92. Wei G H, Wang E T, Tan Z Y, Zhu M E and 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.
93. Willems A, Coopman R and Gillis M 2001a Phylogenetic and DNA: DNA hybridization analyses of Bradyrhizobium species. Int. J. Syst. Evol. Microbiol. 51, 111-117.
94. Willems A, Coopman R and 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.
95. Willems A, Doignon-Bourcier F, Goris J, Coopman R, de Lajudie P, De Vos P and Gillis M 2001c DNA-DNA hybridization study of Bradyrhizobium strains. Int. J. Syst. Evol. Microbiol. 51, 1315-1322.
96. Willems A, Fernández-López M, Muñoz-Adelantado E, Goris J, De Vos P, Martínez-Romero E, Toro N and 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.
97. Wilson J K 1944 Over five hundred reasons for abandoning the cross inoculation groups of legumes. Soil Sci. 58, 61-69.
98. Xu M L, Ge C, Cui Z, Li J and Fan H 1995 Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int. J. Syst. Bacteriol. 45, 706-711.
99. Yao Z Y, Kan F L, Wang E T, Wei G H and 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.
100. 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.
101. 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.
102. Young J M, Kuykendall L D, Martínez-Romero E, Kerr A and 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.
103. Young J M, Pennycook S R and 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.
104. 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.