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

Canadian Journal of Microbiology

Volumn 56, Issue 8, 2010, Pages 657-666

  García Fraile, Paula ^a   Mulas García, Daniel ^b   Peix, Alvaro ^c   Rivas, Raúl ^a   González Andrés, Fernando ^b   Velázquez, Encarna ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF LEÓN   (Spain)

^c INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

Author keywords

nodC gene; Phaseolus; Rhizobium

Indexed keywords

CLIMATIC CONDITIONS; COMMON BEANS; INTERGENIC SPACERS; MAJOR PRODUCERS; PHASEOLUS; PHASEOLUS VULGARIS; PHYLOGENETIC GROUPS; RHIZOBIAL STRAINS; RHIZOBIUM ETLI; RHIZOBIUM LEGUMINOSARUM; SOUTHERN SPAIN; VULGARIS;

SOILS;

GENES;

DNA 16S; DNA 23S; SPACER DNA;

ALLELE; BIOGEOGRAPHY; CLIMATE CONDITIONS; CROP PRODUCTION; LEGUME; PERSISTENCE; PHYLOGENETICS; RHIZOBACTERIUM; SOIL ECOSYSTEM; SPECIATION (BIOLOGY); SYMBIONT;

ALLELE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BEAN; CLOVER; CONTROLLED STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASEOLUS VULGARIS; PRIORITY JOURNAL; RHIZOBIUM ETLI; RHIZOBIUM LEGUMINOSARUM; SPAIN; UNINDEXED SEQUENCE;

ALLELES; BACTERIAL PROTEINS; DNA, BACTERIAL; DNA, RIBOSOMAL SPACER; EVOLUTION, MOLECULAR; N-ACETYLGLUCOSAMINYLTRANSFERASES; PHASEOLUS; RHIZOBIUM ETLI; RHIZOBIUM LEGUMINOSARUM; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 23S; ROOT NODULES, PLANT; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SPAIN; SYMBIOSIS; TRIFOLIUM; UNITED STATES; VICIA;

SPAIN;

PHASEOLUS VULGARIS; RHIZOBIUM; RHIZOBIUM ETLI; RHIZOBIUM LEGUMINOSARUM; TRIFOLIUM; VICIA;

EID: 77954921908     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W10-048     Document Type: Article

References (35)

1. Aguilar, O.M., López, M.V., Riccillo, P.M., González, R.A., Pagano, M., Grasso, D.H., et al. 1998. Prevalence of the Rhizobium etli-like allele in genes coding for 16S rRNA among the indigenous rhizobial populations found associated with wild beans from the Southern Andes in Argentina. Appl. Environ. Microbiol. 64(9): 3520-3524. PMID:9726909.
2. Aguilar, O.M., Riva, O., and 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. U.S.A. 101(37): 13548-13553. doi:10.1073/pnas.0405321101. PMID:15340138.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215(3): 403-410. PMID:2231712.
4. Álvarez-Martínez, E.R., Valverde, A., Ramírez-Bahena, M.H., García-Fraile, P., Tejedor, C., Mateos, P.F., et al. 2009. The analysis of core and symbiotic genes of rhizobia nodulating Vicia from different continents reveals their common phylogenetic origin and suggests the distribution of Rhizobium leguminosarum strains together with Vicia seeds. Arch. Microbiol. 191(8): 659-668. doi:10.1007/s00203-009-0495-6. PMID:19603151.
5. Bernal, G., and Graham, P.H. 2001. Diversity in the rhizobia associated with Phaseolus vulgaris L. in Ecuador, and comparisons with Mexican bean rhizobia. Can. J. Microbiol. 47(6): 526-534. doi:10.1139/cjm-47-6-526. PMID:11467728.
6. Bernal, G.R., Tlusty, B., Estévez de Jensen, C., van Berkum, P., and Graham, P.H. 2004. Characteristics of rhizobia nodulating beans in the central region of Minnesota. Can. J. Microbiol. 50(12): 1023-1031. doi:10.1139/w04-092. PMID:15714233.
7. Beyene, D., Kassa, S., Ampy, F., Asseffa, A., Gebremedhin, T., and van Berkum, P. 2004. Ethiopian soils harbor natural populations of rhizobia that form symbioses with common bean (Phaseolus vulgaris L.). Arch. Microbiol. 181(2): 129-136. doi:10. 1007/s00203-003-0636-2. PMID:14685648.
8. Gaunt, M.W., Turner, S.L., Rigottier-Gois, L., Lloyd-Macgilp, S.A., and Young, J.P. 2001. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 51(Pt 6): 2037-2048. PMID:11760945.
9. Herrera-Cervera, J.A., Caballero-Mellado, J., Laguerre, G., Tichy, H.V., Requena, N., Amarger, N., et al. 1999. At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol. Ecol. 30(1): 87-97. doi:10.1111/j.1574-6941. 1999.tb00638.x.
10. Iglesias, O., Rivas, R., García-Fraile, P., Abril, A., Mateos, P.F., Martínez-Molina, E., and Velázquez, E. 2007. Genetic characterization of fast-growing rhizobia able to nodulate Prosopis alba in North Spain. FEMS Microbiol. Lett. 277(2): 210-216. doi:10.1111/j.1574-6968.2007.00968.x. PMID:18031342.
11. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16(2): 111-120. doi:10.1007/ BF01731581. PMID:7463489.
12. Kwon, S.W., Park, J.Y., Kim, J.S., Kang, J.W., Cho, Y.H., Lim, C.K., et al. 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(1): 263-270. doi:10. 1099/ijs.0.63097-0. PMID:15653885.
13. Laguerre, G., Nour, S.M., Macheret, V., Sanjuan, J., Drouin, P., and Amarger, N. 2001. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology, 147(4): 981-993. PMID:11283294.
14. Mhamdi, R., Jebara, M., Aouani, M.E., Ghrir, R., and Mars, M. 1999. Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. Biol. Fertil. Soils. 28:313-320. of rhizobial lineages. Mol. Biol. Evol. 16: 98-113. PMID:10331255.
15. Michiels, J., Dombrecht, B., Vermeiren, N., Xi, C., Luyten, E., and Vanderleyden, J. 1998. Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol. Ecol. 26(3): 193-205. doi:10.1111/j.1574-6941.1998.tb00505.x.
16. 2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 187(1): 79-85. doi:10. 1007/s00203-006-0173-x. PMID:17019605.
17. Pérez-Ramírez, N.O., Rogel, M.A., Wang, E., Castellanos, J.Z., and Martínez-Romero, E. 1998. Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol. Ecol. 26: 289-296.
18. Perret, X., Staehelin, C., and Broughton, W.J. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64(1): 180-201. doi:10.1128/MMBR.64.1.180-201.2000. PMID: 10704479.
19. T) into the new species Rhizobium pisi sp. nov. Int. J. Syst. Evol. Microbiol. 58: 2484-2490. doi:10.1099/ijs.0.65621-0. PMID:18984681.
20. Ramírez-Bahena, M.H., Velázquez, E., Fernández-Santos, F., Peix, A., Martínez-Molina, E., and Mateos, P.F. 2009. Phenotypic, genotypic, and symbiotic diversities in strains nodulating clover in different soils in Spain. Can. J. Microbiol. 55(10): 1207-1216. doi:10.1139/W09-074. PMID:19935893.
21. Rivas, R., Velázquez, E., Palomo, J.L., Mateos, P., García-Benavides, P., and Martínez-Molina, E. 2002. Rapid identification of Clavibacter michiganensis subspecies sepedonicus using two primers random amplified polymorphic DNA (TP-RAPD) fingerprints. Eur. J. Plant Pathol. 108(2): 179-184. doi:10.1023/ A:1015044911913.
22. Rivas, R., García-Fraile, P., Mateos, P.F., Martínez-Molina, E., and Velázquez, E. 2007a. Characterization of xylanolytic bacteria present in the bract phyllosphere of the date palm Phoenix dactylifera. Lett. Appl. Microbiol. 44(2): 181-187. doi:10.1111/j.1472-765X.2006.02050.x. PMID:17257258.
23. Rivas, R., Laranjo, M., Velázquez, E., Mateos, P.F., Oliveira, S., and Martínez-Molina, E. 2007b. Strains of Mesorhizobium amorphae and M. tianshanense carrying symbiotic genes of common chickpea endosymbiotic species constitute a novel biovar (ciceri) able to nodulate Cicer arietinum. Lett. Appl. Microbiol. 44: 412-418. doi:10.1111/j.1472-765X.2006.02086.x. PMID:17397480.
24. Roche, P., Maillet, F., Plazanet, C., Debellé, F., Ferro, M., Truchet, G., et al. 1996. The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc. Natl. Acad. Sci. U.S.A. 93(26): 15305-15310. doi:10.1073/pnas.93.26.15305. PMID: 8986807.
25. Rodríguez-Navarro, D.N., Buendía, A.M., Camacho, M., Lucas, M., and Santamaría, C. 2000. Characterization of Rhizobium spp. bean isolates from southwest of Spain. Soil Biol. Biochem. 32(11-12): 1601-1613. doi:10.1016/S0038-0717(00)00074-2.
26. Saitou, N., and Nei, M. 1987. A neighbour-joining method: a new method for reconstructing phylogenetics trees. Mol. Biol. Evol. 44: 406-425.
27. Santillana, N., Ramírez-Bahena, M.H., García-Fraile, P., Velázquez, E., and Zúñiga, D. 2008. 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. Arch. Microbiol. 189(3): 239-247. doi:10.1007/s00203-007-0313-y. PMID:17985116.
28. Segovia, L., Young, J.P.W., and Martínez-Romero, E. 1993. Re-classification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 43(2): 374-377. doi:10.1099/00207713-43-2-374. PMID:8494746.
29. Silva, C., Vinuesa, P., Eguiarte, L.E., Martínez-Romero, E., and 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(2): 884-893. doi:10.1128/AEM.69.2.884-893.2003. PMID: 12571008.
30. Tamura, K., Dudley, J., Nei, M., and Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24(8): 1596-1599. doi:10.1093/molbev/msm092. PMID:17488738.
31. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25(24): 4876-4882. doi:10. 1093/nar/25.24.4876.
32. Valverde, A., Igual, J.M., Peix, A., Cervantes, E., and Velázquez, E. 2006. Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int. J. Syst. Evol. Microbiol. 56(11): 2631-2637. doi:10.1099/ijs.0.64402-0. PMID:17082403.
33. Velázquez, E., Martínez-Romero, E., Rodríguez-Navarro, D.N., Trujillo, M.E., Daza, A., Mateos, P.F., et al. 2001. Characterization of rhizobial isolates of Phaseolus vulgaris by staircase electrophoresis of low-molecular-weight RNA. Appl. Environ. Microbiol. 67(2): 1008-1010. doi:10.1128/AEM.67.2.1008-1010.2001. PMID:11157280.
34. Vincent, J.M. 1970. The cultivation, isolation and maintenance of rhizobia. In A manual for the practical study of root-nodule bacteria. Edited by J.M. Vincent. Blackwell Scientific Publications, Oxford, UK. pp. 1-13.
35. Zurdo-Piñeiro, J.L., García-Fraile, P., Rivas, R., Peix, A., León-Barrios, M., Willems, A., et al. 2009. Rhizobia from Lanzarote, the Canary Islands, that nodulate Phaseolus vulgaris have characteristics in common with Sinorhizobium meliloti isolates from mainland Spain. Appl. Environ. Microbiol. 75(8): 2354-2359. doi:10.1128/AEM.02811-08. PMID:19218416.