Phylogenetic diversity based on rrs, atpD, recA genes and 16S–23S intergenic sequence analyses of rhizobial strains isolated from Vicia faba and Pisum sativum in Peru

Aguilar OM, López MV, Riccillo PM (2001) The diversity of rhizobia nodulating beans in Northwest Argentina as a source of more efficient inoculant strains. J Biotechnol 91:181–188

Aguilar OM, Riva O, Peltzer E (2004) Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc Natl Acad Sci USA 101:13548–13553

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

Andrade DS, Murphy PJ, Giller KE (2002) The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Appl Environ Microbiol 68:4025–4034

Bernal G, Graham PH (2001) Diversity in the rhizobia associated with Phaseolus vulgaris L. in Ecuador, and comparisons with Mexican bean rhizobia. Can J Microbiol 47:526–534

Bernal GR, Tlusty B, Estévez de Jensen C, van Berkum P, Graham PH (2004) Characteristics of rhizobia nodulating beans in the central region of Minnesota. Can J Microbiol 50:1023–1031

Beyene D, Kassa S, Ampy F, Asseffa A, Gebremedhin T, van Berkum P (2004) Ethiopian soils harbor natural populations of rhizobia that form symbioses with common bean (Phaseolus vulgaris L.). Arch Microbiol 181:129–136

Eardly BD, Wang FS, Whittam TS, Selander RK (1995) Species limit in Rhizobium populations that nodulate the common bean (Phaseolus vulgaris). Appl Environ Microbiol 61:507–512

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

Jarabo-Lorenzo A, Pérez-Galdona R, Donate-Correa J, Rivas R, Velázquez E, Hernández M, Temprano F, Martínez-Molina E, Ruiz-Argüeso T, León-Barrios M (2003) Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Syst Appl Microbiol 26:611–626

Jordan DC (1984) Family III. Rhizobiaceae. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology. Williams & Wilkins, Baltimore, pp 234–242

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

Kumar S, Tamura K, Jakobsen IB, Nei M (2001) Molecular evolutionary genetics analysis software. Arizona State University, Tempe

Kuykendall LD (2005) Family I. Rhizobiaceae Conn 1938, 321AL. In: Brenner DJ, Krieg NR, Stanley JT (eds) Bergey’s manual of systematic bacteriology, vol 2, part C. Springer, New York, pp 324–361

Kwon SW, Park JY, Kim JS, Kang JW, Cho YH, Lim CK, Parker MA, Lee GB (2005) Phylogenetic analysis of the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the basis of 16S rRNA gene and internally transcribed spacer region sequences. Int J Syst Evol Microbiol 55:263–270

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

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

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

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 to discriminate genotypes of Rhizobium leguminosarum biovar viciae. Syst Appl Microbiol 28:619–631

Mutch LA, Young JP (2004) Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol Ecol 13:2435–2444

Ormeño-Orrillo E, Vinuesa P, Zuñiga-Dávila D, Martínez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from Lima bean (Phaseolus lunatus L.) in Peru. Syst Appl Microbiol 29:253–262

Rivas R, Peix A, Mateos PF, Trujillo ME, Martínez-Molina E, Velázquez E (2006) Biodiversity of populations of phosphate solubilizing rhizobia that nodulate chickpea in different Spanish soils. Plant Soil 287:23–33

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

Saitou N, Nei M (1987) A neighbour-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol 44:406–425

Segovia L, Young JPW, Martínez-Romero E (1993) Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Bacteriol 43:374–377

Silva C, Vinuesa P, Eguiarte LE, Martínez-Romero E, Souza 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

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustal X windows interface: flexible strategies for multiple sequence alignement aided by quality analysis tools. Nucleic Acid Res 24:4876–4882

Valverde A, Igual JM, Peix A, Cervantes E, Velázquez E (2006) Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol 56:2631–2637

van Berkum P, Beyene D, Eardly BE (1996) Phylogenetics relationships among Rhizobium species nodulating the common bean (Phaseolus vulgaris L.). Int J Syst Bacteriol 46:240–244

Velázquez E, Martínez-Romero E, Rodríguez-Navarro DN, Trujillo ME, Daza A, Mateos PF, Martinez-Molina E, van Berkum P (2001) Characterization of rhizobial isolates of Phaseolus vulgaris by staircase electrophoresis of low molecular weight RNA. Appl Environ Microbiol 67:1008–1010

Velázquez E, Peix A, Zurdo-Piñeiro JL, Palomo JL, Mateos PF, Rivas R, Muñoz-Adelantado E, Toro N, García-Benavides P, Martínez-Molina E (2005) The coexistence of symbiosis and pathogenicity-determining genes in Rhizobium rhizogenes strains enables them to induce nodules and tumors or hairy roots in plants. Mol Plant Microbe Interact 18:1325–1332

Vincent JM (1970) The cultivation, isolation and maintenance of rhizobia. In: Vincent JM (ed) A manual for the practical study of root-nodule. Blackwell, Oxford, pp 1–13

Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martínez-Romero E (2005a) 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

Vinuesa P, Silva C, Werner D, Martínez-Romero E (2005b) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Plant Microbe Interact 34:29–54

Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464