Symbiovars in rhizobia reflect bacterial adaptation to legumes

Systematic and Applied Microbiology

Volumn 34, Issue 2, 2011, Pages 96-104

  Rogel, Marco A ^a   Ormeño Orrillo, Ernesto ^a   Martinez Romero, Esperanza ^a  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

Legumes; Nitrogen fixation; Rhizobium diversity; Symbiosis

Indexed keywords

ACACIA; ACACIA TORTILIS; ACACIELLA ANGUSTISSIMA; ADAPTATION; ALFALFA; AZORHIZOBIUM CAULINODANS; BARREL MEDIC; BIOTYPE; BISERRULA PELECINUS; BRADYRHIZOBIUM; BRADYRHIZOBIUM CANARIENSE; BRADYRHIZOBIUM JAPONICUM; BRADYRHIZOBIUM LIAONINGENSE; CHICKPEA; CLOVER; COMMON VETCH; ECOLOGICAL NICHE; GALEGA OFFICINALIS; GALEGA ORIENTALIS; GENE SEQUENCE; GENISTA; HOST; HOST RANGE; LEGUME; LEUCAENA LEUCOCEPHALA; LOTA; LOTUS LANCEROTTENSE; MEDICAGO LACINIATA; MEDICAGO RUTHENICA; MESORHIZOBIUM; MESORHIZOBIUM AMORPHAE; MESORHIZOBIUM CARAGANAE; MESORHIZOBIUM CICERI; MESORHIZOBIUM GOBIENSE; MESORHIZOBIUM HUAKUII; MESORHIZOBIUM LOTI; MESORHIZOBIUM MEDITERRANEUM; MESORHIZOBIUM OPPORTUNISTUM; MESORHIZOBIUM SEPTENTRIONALE; MESORHIZOBIUM TARIMENSE; MESORHIZOBIUM TEMPERATUM; MESORHIZOBIUM TIANSHANENSE; MIMOSA AFFINIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASEOLUS VULGARIS; PRIORITY JOURNAL; RHIZOBIACEAE; RHIZOBIUM; RHIZOBIUM ETLI; RHIZOBIUM FABAE; RHIZOBIUM GALEGAE; RHIZOBIUM GALLICUM; RHIZOBIUM GIARDINII; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM MONGOLENSE; RHIZOBIUM PHASEOLI; RHIZOBIUM PISI; SESBANIA; SHORT SURVEY; SINORHIZOBIUM; SINORHIZOBIUM AMERICANUM; SINORHIZOBIUM CHIAPANECUM; SINORHIZOBIUM FREDII; SINORHIZOBIUM KOSTIENSE; SINORHIZOBIUM MEDICAE; SINORHIZOBIUM MELILOTI; SINORHIZOBIUM MEXICANUM; SINORHIZOBIUM SAHELENSE; SINORHIZOBIUM TERANGAE; SPECIES COEXISTENCE; SYMBIOSIS; UNINDEXED SEQUENCE; VICIA FABA;

FABACEAE; PHYLOGENY; RHIZOBIACEAE; SYMBIOSIS; TERMINOLOGY AS TOPIC;

BACTERIA (MICROORGANISMS); RHIZOBIUM;

EID: 79952534892     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2010.11.015     Document Type: Short Survey

References (83)

1. Amadou C., Pascal G., Mangenot S., Glew M., Bontemps C., Capela D., Carrère S., Cruveiller S., Dossat C., Lajus A., Marchetti M., Poinsot V., Rouy Z., Servin B., Saad M., Schenowitz C., Barbe V., Batut J., Médigue C., Masson-Boivin C. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 2008, 18:1472-1483.
2. Amarger N., Macheret V., Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int. J. Syst. Bacteriol. 1997, 47:996-1006.
3. Andam C.P., Mondo S.J., Parker M.A. Monophyly of nodA and nifH genes across Texan and Costa Rican populations of Cupriavidus nodule symbionts. Appl. Environ. Microbiol. 2007, 73:4686-4690.
4. Andronov E.E., Terefework Z., Roumiantseva M.L., Dzyubenko N.I., Onichtchouk O.P., Kurchak O.N., Dresler-Nurmi A., Young J.P.W., Simarov B.V., Lindstrom K. Symbiotic and genetic diversity of Rhizobium galegae isolates collected from the Galega orientalis gene center in the Caucasus. Appl. Environ. Microbiol. 2003, 69:1067-1074.
5. Ba S., Willems A., de Lajudie P., Roche P., Jeder H., Quatrini P., Neyra M., Ferro M., Prome J.-C., Gillis M., Boivin-Masson C., Lorquin J. Symbiotic and taxonomic diversity of rhizobia isolated from Acacia tortilis subsp. raddiana in Africa. Syst. Appl. Microbiol. 2002, 25:130-145.
6. Bailly X., Olivieri I., Brunel B., Cleyet-Marel J.-C., Bena G. Horizontal gene transfer and homologous recombination drive the evolution of the nitrogen-fixing symbionts of Medicago species. J. Bacteriol. 2007, 189:5223-5236.
7. Boivin C., Ndoye I., Lortet G., Ndiaye A., De Lajudie P., Dreyfus B. 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. 1997, 63:1040-1047.
8. Chen W.-M., Moulin L., Bontemps C., Vandamme P., Bena G., Boivin-Masson C. Legume symbiotic nitrogen fixation by β-Proteobacteria is widespread in nature. J. Bacteriol. 2003, 185:7266-7272.
9. Chen W., Wang E., Wang S., Li Y., Chen X., Li Y. Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People's Republic of China. Int. J. Syst. Bacteriol. 1995, 45:153-159.
10. Cooper J.E. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J. Appl. Microbiol. 2007, 103:1355-1365.
11. Cullimore J., Denarie J. How legumes select their sweet talking symbionts. Science 2003, 302:575-578.
12. Cummings S.P., Gyaneshwar P., Vinuesa P., Farruggia F.T., Andrews M., Humphry D., Elliott G.N., Nelson A., Orr C., Pettitt D., Shah G.R., Santos S.R., Krishnan H.B., Odee D., Moreira F.M.S., Sprent J.I., Young J.P.W., James E.K. Nodulation of Sesbania species by Rhizobium (Agrobacterium) strain IRBG74 and other rhizobia. Environ. Microbiol. 2009, 11:2510-2525.
13. Cytryn E.J., Jitacksorn S., Giraud E., Sadowsky M.J. Insights learned from pBTAi1, a 229-kb accessory plasmid from Bradyrhizobium sp. strain BTAi1 and prevalence of accessory plasmids in other Bradyrhizobium sp. strains. ISME J. 2008, 2:158-170.
14. Depret G., Laguerre G. Plant phenology and genetic variability in root and nodule development strongly influence genetic structuring of Rhizobium leguminosarum biovar viciae populations nodulating pea. New Phytol. 2008, 179:224-235.
15. Donate-Correa J., Leon-Barrios M., Hernandez M., Perez-Galdona R., del Arco-Aguilar M. Different Mesorhizobium species sharing the same symbiotic genes nodulate the shrub legume Anagyris latifolia. Syst. Appl. Microbiol. 2007, 30:615-623.
16. Downie J.A. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol. Rev. 2010, 34:150-170.
17. Dye D.W., Bradbury J.F., Goto M., Hayward A.C., Lelliott R.A., Schroth M.N. International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotype strains. Rev. Plant Pathol. 1980, 59:153-168.
18. Flores M., Gonzalez V., Pardo M.A., Leija A., Martinez E., Romero D., Pinero D., Davila G., Palacios R. Genomic instability in Rhizobium phaseoli. J. Bacteriol. 1988, 170:1191-1196.
19. Garcia-Fraile P., Mulas-Garcia D., Peix A., Rivas R., Gonzalez-Andres F., Velazquez E. Phaseolus vulgaris is nodulated in northern Spain by Rhizobium leguminosarum strains harboring two nodC alleles present in American Rhizobium etli strains: biogeographical and evolutionary implications. Can. J. Microbiol. 2010, 56:657-666.
20. González V., Acosta J.L., Santamaría R.I., Bustos P., Fernández J.L., Hernández González I.L., Díaz R., Flores M., Palacios R., Mora J., Dávila G. Conserved symbiotic plasmid DNA sequences in the multireplicon pangenomic structure of Rhizobium etli. Appl. Environ. Microbiol. 2010, 76:1604-1614.
21. Harrison P.W., Lower R.P.J., Kim N.K.D., Young J.W. Introducing the bacterial chromid: not a chromosome, not a plasmid. Trends Microbiol. 2010, 18:141-148.
22. Haukka K., Lindstrom K., Young J.P.W. 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. 1998, 64:419-426.
23. Hungria M., Campo R.J., Mendes I.C., Graham P.H. Contribution of biological nitrogen fixation to the nitrogen nutriton of grain crops in the tropics: the success of soybean (Glycine max L. Merr) in South America. Nitrogen Nutrition in Plant Productivity 2006, Studium Press, pp. 43-93.
24. Hynes M., O'Connell M. Host plant effect on competition among strains of Rhizobium leguminosarum. Can. J. Microbiol. 1990, 36:864-869.
25. Itakura M., Saeki K., Omori H., Yokoyama T., Kaneko T., Tabata S., Ohwada T., Tajima S., Uchiumi T., Honnma K., Fujita K., Iwata H., Saeki Y., Hara Y., Ikeda S., Eda S., Mitsui H., Minamisawa K. Genomic comparison of Bradyrhizobium japonicum strains with different symbiotic nitrogen-fixing capabilities and other Bradyrhizobiaceae members. ISME J. 2009, 3:326-339.
26. Johnston A.W., Beringer J.E. Identification of the Rhizobium strains in pea root nodules using genetic markers. J. Gen. Microbiol. 1975, 87:343-350.
27. Jones K.M., Kobayashi H., Davies B.W., Taga M.E., Walker G.C. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 2007, 5:619-633.
28. Jordan D.C. Family III. Rhizohiaceae Conn (1938). Bergey's Manual of Systematic Bacteriology 1984, vol. 1. Williams & Wilkins, pp. 234-254.
29. Koch M., Delmotte N., Rehrauer H., Vorholt J.A., Pessi G., Hennecke H. Rhizobial adaptation to hosts, a new facet in the legume root-nodule symbiosis. Mol. Plant-Microbe Interact. 2010, 23:784-790.
30. Laguerre G., Geniaux E., Mazurier S.I., Casartelli R.R., Amarger N. 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. 1993, 39:412-419.
31. Laguerre G., Nour S.M., Macheret V., Sanjuan J., Drouin P., Amarger N. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 2001, 147:981-993.
32. Laguerre G., Van Berkum P., Amarger N., Prevost D. Genetic diversity of rhizobial symbionts isolated from legume species within the genera Astragalus, Oxytropis, and Onobrychis. Appl. Environ. Microbiol. 1997, 63:4748-4758.
33. Laranjo M., Alexandre A., Rivas R., Velazquez E., Young J.P.W., Oliveira S. Chickpea rhizobia symbiosis genes are highly conserved across multiple Mesorhizobium species. FEMS Microbiol. Ecol. 2008, 66:391-400.
34. Leon-Barrios M., Lorite M.J., Donate-Correa J., Sanjuan J. Ensifer meliloti bv. lancerottense establishes nitrogen-fixing symbiosis with Lotus endemic to the Canary Islands and shows distinctive symbiotic genotypes and host range. Syst. Appl. Microbiol. 2009, 32:413-420.
35. Lorquin J., Lortet G., Ferro M., Mear N., Prome J.C., Boivin C. Sinorhizobium teranga bv. acaciae ORS1073 and Rhizobium sp. strain ORS1001, two distantly related Acacia-nodulating strains, produce similar Nod factors that are O carbamoylated, N methylated, and mainly sulfated. J. Bacteriol. 1997, 179:3079-3083.
36. Lorquin J., Lortet G., Ferro M., Mear N., Dreyfus B., Prome J.C., Boivin C. Nod factors from Sinorhizobium saheli and S. teranga bv. sesbaniae are both arabinosylated and fucosylated, a structural feature specific to Sesbania rostrata symbionts. Mol. Plant-Microbe Interact. 1997, 10:879-890.
37. Lortet G., Mear N., Lorquin J., Dreyfus B., de Lajudie P., Rosenberg C., Boivin C. Nod factor thin-layer chromatography profiling as a tool to characterize symbiotic specificity of rhizobial strains: application to Sinorhizobium saheli, S. teranga, and Rhizobium sp. strains isolated from Acacia and Sesbania. Mol. Plant-Microbe Interact. 1996, 9:736-747.
38. Maatallah J., Berraho E., Munoz S., Sanjuan J., Lluch C. Phenotypic and molecular characterization of chickpea rhizobia isolated from different areas of Morocco. J. Appl. Microbiol. 2002, 93:531-540.
39. Martínez E., Pardo M.A., Cevallos M.A., Palacios R. Reiteration of nitrogen fixation gene sequences and specificity of Rhizobium in nodulation and nitrogen fixation in Phaseolus vulgaris. J. Gen. Microbiol. 1985, 131:1779-1786.
40. Martinez-Romero E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 2003, 252:11-23.
41. Martinez-Romero E. Coevolution in Rhizobium-legume symbiosis?. DNA Cell Biol. 2009, 28:361-370.
42. Martínez-Romero J., Ormeño-Orrillo E., Rogel M.A., López-López A., Martínez-Romero E. Trends in rhizobial evolution and some taxonomic remarks. Evolutionary Biology-Concepts, Molecular and Morphological Evolution 2010, Springer-Verlag. P. Pontarotti (Ed.).
43. Masson-Boivin C., Giraud E., Perret X., Batut J. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?. Trends Microbiol. 2009, 17:458-466.
44. Mhamdi R., Jebara M., Aouani M.E., Ghrir R., Mars M. Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. Biol. Fertil. Soils 1999, 28:313-320.
45. 2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 2007, 187:79-85.
46. Moulin L., Bena G., Boivin-Masson C., Stepkowski T. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol. Phylogen. Evol. 2004, 30:720-732.
47. Moulin L., Munive A., Dreyfus B., Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 2001, 411:948-950.
48. Murooka Y., Xu Y., Sandada K., Araki M., Morinaga T., Yokota A. Formation of root nodules by Rhizobium huakuii biovar. renge bv. nov. on Astragalus sinicus cv. Japan J. Ferment. Bioeng. 1993, 76:38-44.
49. Mutch L.A., Young J.P. Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol. Ecol. 2004, 13:2335-2344.
50. Nandasena K.G., O'Hara G.W., Tiwari R.P., Sezmis E., Howieson J.G. In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ. Microbiol. 2007, 9:2496-2511.
51. Nour S.M., Cleyet-Marel J.-C., Normand P., Fernandez M.P. Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int. J. Syst. Bacteriol. 1995, 45:640-648.
52. Nour S.M., Fernandez M.P., Normand P., Cleyet-Marel J.-C. Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.). Int. J. Syst. Bacteriol. 1994, 44:511-522.
53. Nuswantara S., Fujie M., Yamada T., Malek W., Inaba M., Kaneko Y., Murooka Y. Phylogenetic position of Mesorhizobium huakuii subsp. rengei, a symbiont of Astragalus sinicus cv. Japan J. Biosci. Bioeng. 1999, 87:49-55.
54. Ophel K., Kerr A. Agrobacterium vitis sp. nov. for strains of Agrobacterium biovar 3 from grapevines. Int. J. Syst. Bacteriol. 1990, 40:236-241.
55. Pacios-Bras C., van der Burgt Y.E.M., Deelder A.M., Vinuesa P., Werner D., Spaink H.P. Novel lipochitin oligosaccharide structures produced by Rhizobium. Carbohydrate Res. 2002, 337:1193-1202.
56. Peix A., Velázquez E., Silva R.L., Mateos P.F. Key molecules involved in beneficial infection process in rhizobia-legume simbiosis. Microbes for Legume Improvement 2010, 55-80. Springer-Verlag. M.S. Khan, J. Musarrat, A. Zaidi (Eds.).
57. Quinto C., De la Vega H., Flores M., Fernández L., Ballado T., Soberón G., Palacios R. Reiteration of nitrogen fixation gene sequencing in Rhizobium phaseoli. Nature 1982, 299:724-726.
58. Quispel A. Hellriegel and Wilfarth's discovery of (symbiotic) nitrogen fixation one hundred years ago. Nitrogen Fixation: One Hundred Years After 1988, 3-12. Gustav Fisher. H. Bothe, F.J. de Bruijn, W.E. Newton (Eds.).
59. Radeva G., Jurgens G., Niemi M., Nick G., Suominen L., Lindstrom K. Description of two biovars in the Rhizobium galegae species: biovar orientalis and biovar officinalis. Syst. Appl. Microbiol. 2001, 24:192-205.
60. Ramírez-Bahena M.H., García-Fraile P., Peix A., Valverde A., Rivas R., Igual J.M., Mateos P.F., Martínez-Molina E., Velázquez E. Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. Int. J. Syst. Evol. Microbiol. 2008, 58:2484-2490.
61. Reeve W.G., O'Hara G.W., Chain P., Ardley J.K., Bräu L., Nandasena K.G., Tiwari R., Malfatti S., Kiss H., Lapidus A., Copeland A., Nolan M., Land M., Ivanova N., Mavromatis K., Markowitz V., Kyrpides N., Melino V., Denton M., Yates R.J., Howieson J.G. Complete genome sequence of Rhizobium leguminosarum bv. trifolii strain WSM2304, an effective microsymbiont of the South American clover Trifolium polymorphum. Standards Genomic Sci. 2010, 2:66-76.
62. Rincón-Rosales R., Lloret L., Ponce E., Martínez-Romero E. Rhizobia with different symbiotic efficiencies nodulate Acaciella angustissima in Mexico, including Sinorhizobium chiapanecum sp. nov. which has common symbiotic genes with Sinorhizobium mexicanum. FEMS Microbiol. Ecol. 2009, 67:103-117.
63. Rivas R., Laranjo M., Mateos P.F., Oliveira S., Martínez-Molina E., Velázquez E. Strains of Mesorhizobium amorphae and Mesorhizobium tianshanense, carrying symbiotic genes of common chickpea endosymbiotic species, constitute a novel biovar (ciceri) capable of nodulating Cicer arietinum. Lett. Appl. Microbiol. 2007, 44:412-418.
64. Segovia L., Young J.P.W., Martinez-Romero E. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 1993, 43:374-377.
65. Silva C., Vinuesa P., Eguiarte L.E., Martinez-Romero E., Souza V. 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. 2003, 69:884-893.
66. Silva C., Vinuesa P., Eguiarte L.E., Souza V., Martinez-Romero E. Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol. Ecol. 2005, 14:4033-4050.
67. Slater S.C., Goldman B.S., Goodner B., Setubal J.C., Farrand S.K., Nester E.W., Burr T.J., Banta L., Dickerman A.W., Paulsen I., Otten L., Suen G., Welch R., Almeida N.F., Arnold F., Burton O.T., Du Z., Ewing A., Godsy E., Heisel S., Houmiel K.L., Jhaveri J., Lu J., Miller N.M., Norton S., Chen Q., Phoolcharoen W., Ohlin V., Ondrusek D., Pride N., Stricklin S.L., Sun J., Wheeler C., Wilson L., Zhu H., Wood D.W. Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J. Bacteriol. 2009, 191:2501-2511.
68. Sullivan J.T., Trzebiatowski J.R., Cruickshank R.W., Gouzy J., Brown S.D., Elliot R.M., Fleetwood D.J., McCallum N.G., Rossbach U., Stuart G.S., Weaver J.E., Webby R.J., de Bruijn F.J., Ronson C.W. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 2002, 184:3086-3095.
69. Sullivan J.T., Patrick H.N., Lowther W.L., Scott D.B., Ronson C.W. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:8985-8989.
70. Terefework Z., Kaijalainen S., Lindstroem K. AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega officinalis. J. Biotechnol. 2001, 91:169-180.
71. Tian C.F., Wang E.T., Wu L.J., Han T.X., Chen W.F., Gu C.T., Gu J.G., Chen W.X. Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int. J. Syst. Evol. Microbiol. 2008, 58:2871-2875.
72. Turner S.L., Zhang X.-X., Li F.-D., Young J.P.W. What does a bacterial genome sequence represent? Mis-assignment of MAFF 303099 to the genospecies Mesorhizobium loti. Microbiology 2002, 148:3330-3331.
73. van Berkum P., Beyene D., Bao G., Campbell T.A., Eardly B.D. 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. 1998, 48:13-22.
74. Vázquez M., Davalos A., de las Peñas A., Sanchez F., Quinto C. Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains. J. Bacteriol. 1991, 173:1250-1258.
75. Velázquez E., Palomo J.L., Rivas R., Guerra H., Peix A., Trujillo M.E., García-Benavides P., Mateos P.F., Wabiko H., Martínez-Molina E. Analysis of core genes supports the reclassification of strains Agrobacterium radiobacter K84 and Agrobacterium tumefaciens AKE10 into the species Rhizobium rhizogenes. Syst. Appl. Microbiol. 2010, 33:247-251.
76. Villegas M.C., Rome S., Maure L., Domergue O., Gardan L., Bailly X., Cleyet-Marel J.-C., Brunel B. Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti. Syst. Appl. Microbiol. 2006, 29:526-538.
77. Vinuesa P., Leon-Barrios M., Silva C., Willems A., Jarabo-Lorenzo A., Perez-Galdona R., Werner D., Martinez-Romero E. 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. 2005, 55:569-575.
78. Vinuesa P., Silva C., Lorite M.J., Izaguirre-Mayoral M.L., Bedmar E.J., Martínez-Romero E. 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. 2005, 28:702-716.
79. Wang E.T., Rogel M.A., Garcia-De los Santos A., Martinez-Romero J., Cevallos M.A., Martinez-Romero E. Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int. J. Syst. Bacteriol. 1999, 49:1479-1491.
80. Wang E.T., van Berkum P., Sui X.H., Beyene D., Chen W.X., Martinez-Romero E. Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int. J. Syst. Bacteriol. 1999, 49:51-65.
81. Yates R.J., Howieson J.G., Reeve W.G., Brau L., Speijers J., Nandasena K., Real D., Sezmis E., O'Hara G.W. Host-strain mediated selection for an effective nitrogen-fixing symbiosis between Trifolium spp. and Rhizobium leguminosarum biovar trifolii. Soil Biol. Biochem. 2008, 40:822-833.
82. Young J.P.W. Rhizobium population genetics: enzyme polymorphism in isolates from peas, clover, beans and lucerne grown at the same site. J. Gen. Microbiol. 1985, 131:2399-2408.
83. Young J.P.W., Crossman L.C., Johnston A.W.B., Thomson N.R., Ghazoui Z.F., Hull K.H., Wexler M., Curson A.R.J., Todd J.D., Poole P.S., Mauchline T.H., East A.K., Quail M.A., 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. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 2006, 7:R34.