Population genetics and phylogenetic inference in bacterial molecular systematics: The roles of migration and recombination in Bradyrhizobium species cohesion and delineation

Molecular Phylogenetics and Evolution

Volumn 34, Issue 1, 2005, Pages 29-54

  Vinuesa, Pablo ^a,b   Silva, Claudia ^a   Werner, Dietrich ^b   Martínez Romero, Esperanza ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Bayes factors; Canary islands; Coalescent simulations; Gene flow; Likelihood ratio test; Model selection; Neutrality tests; Partitioned models; Prokaryotes

Indexed keywords

NITROGENASE REDUCTASE; OXIDOREDUCTASE; RECA PROTEIN;

ARTICLE; BRADYRHIZOBIUM; CLASSIFICATION; DNA FINGERPRINTING; DNA SEQUENCE; GENETIC RECOMBINATION; GENETICS; LEGUME; MICROBIOLOGY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION GENETICS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEQUENCE ALIGNMENT; STATISTICAL MODEL;

BASE SEQUENCE; BRADYRHIZOBIUM; DNA FINGERPRINTING; EVOLUTION, MOLECULAR; FABACEAE; GENETICS, POPULATION; LIKELIHOOD FUNCTIONS; OXIDOREDUCTASES; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; REC A RECOMBINASES; RECOMBINATION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM; BRADYRHIZOBIUM CANARIENSE; BRADYRHIZOBIUM JAPONICUM; PROKARYOTA; RHIZOBIACEAE;

EID: 9944222667     PISSN: 10557903     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ympev.2004.08.020     Document Type: Article

References (151)

1. M.E. Alfaro, S. Zoller, and F. Lutzoni Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence Mol. Biol. Evol. 20 2003 255 266
2. J.C. Avise Phylogeography: the History and Formation of Species 2000 Harvard University Press Cambridge, MA, USA
3. H.-J. Bandelt, and A.W.M. Dress Split decomposition: a new and useful approach to phylogenetic analysis of distance data Mol. Phylogenet. Evol. 1 1992 242 252
4. T.G. Barraclough, and S. Nee Phylogenetics and speciation Trends Ecol. Evol. 16 2001 391 399
5. L.L. Barrera, M.E. Trujillo, M. Goodfellow, F.J. Garcia, I. Hernandez-Lucas, G. Davila, P. van Berkum, and E. Martinez-Romero Biodiversity of bradyrhizobia nodulating Lupinus spp Int. J. Syst. Bacteriol. 47 1997 1086 1091
6. S.J. Bent, C.L. Gucker, Y. Oda, and L.J. Forney Spatial distribution of Rhodopseudomonas palustris ecotypes on a local scale Appl. Environ. Microbiol. 69 2003 5192 5197
7. E.W. Brown, M.L. Kotewicz, and T.A. Cebula Detection of recombination among Salmonella enterica strains using the incongruence length difference test Mol. Phylogenet. Evol. 24 2002 102 120
8. W.J. Bruno, and A.L. Halpern Topological bias and inconsistency of maximum likelihood using wrong models Mol. Biol. Evol. 16 1999 564 566
9. T.R. Buckley Model misspecification and probabilistic tests of topology: evidence from empirical data sets Syst. Biol. 51 2002 509 523
10. T.R. Buckley, C. Simon, and G.K. Chambers Exploring among-site rate variation models in a maximum likelihood framework using empirical data: effects of model assumptions on estimates of topology, branch lengths, and bootstrap support Syst. Biol. 50 2001 67 86
11. I. Carbone, and L.M. Kohn A microbial population-species interface: nested cladistic and coalescent inference with multilocus data Mol. Ecol. 10 2001 947 964
12. C. Chaintreuil, E. Giraud, Y. Prin, J. Lorquin, A. Ba, M. Gillis, P. de Lajudie, and B. Dreyfus Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata Appl. Environ. Microbiol. 66 2000 5437 5447
13. J.C. Cho, and J.M. Tiedje Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil Appl. Environ. Microbiol. 66 2000 5448 5456
14. F.M. Cohan Bacterial species and speciation Syst. Biol. 50 2001 513 524
15. F.M. Cohan What are bacterial species? Annu. Rev. Microbiol. 56 2002 457 487
16. M.P. Cummings, S.A. Handley, D.S. Myers, D.L. Reed, A. Rokas, and K. Winka Comparing bootstrap and posterior probability values in the four-taxon case Syst. Biol. 52 2003 477 487
17. P. Darlu, and G. Lecointre When does the incongruence length difference test fail? Mol. Biol. Evol. 19 2002 432 437
18. V. Daubin, N.A. Moran, and H. Ochman Phylogenetics and the cohesion of bacterial genomes Science 301 2003 829 832
19. E.F. DeLong, and N.R. Pace Environmental diversity of bacteria and archaea Syst. Biol. 2001 470 478
20. K. Dolphin, R. Belshaw, C.D. Orme, and D.L. Quicke Noise and incongruence: interpreting results of the incongruence length difference test Mol. Phylogenet. Evol. 17 2000 401 406
21. C.J. Douady, F. Delsuc, Y. Boucher, W.F. Doolittle, and E.J. Douzery Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability Mol. Biol. Evol. 20 2003 248 254
22. J.J. Doyle, and M.A. Luckow The rest of the iceberg. Legume diversity and evolution in a phylogenetic context Plant Physiol. 131 2003 900 910
23. D.E. Dykhuizen, and L. Green Recombination in Escherichia coli and the definition of biological species J. Bacteriol. 173 1991 7257 7268
24. 2-fixing Rhizobium: characteristics P.M. Gresshoff L.E. Roth G. Stacey W.L. Newton Nitrogen Fixation: Achievements and Objectives 1990 Chapman & Hall New York 805 811
25. P. Erixon, B. Svennblad, T. Britton, and B. Oxelman Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics Syst. Biol. 52 2003 665 673
26. P. Escobar-Páramo, A. Sabbagh, P. Darlu, O. Pradillon, C. Vaury, E. Denamur, and G. Lecointre Decreasing the effects of horizontal gene transfer on bacterial phylogeny: the Escherichia coli case study Mol. Phylogenet. Evol. 30 2004 243 250
27. J.S. Farris, J. Källersjö, A.G. Kluge, and C. Bult Testing significance of congruence Cladistics 10 1994 315 319
28. E.J. Feil, and B.G. Spratt Recombination and the population structures of bacterial pathogens Annu. Rev. Microbiol. 55 2001 561 590
29. J. Felsenstein Confidence limits on phylogenies: an approach using the bootstrap Evolution 39 1985 783 791
30. Felsenstein, J., 2004. PHYLIP (Phylogeny Inference Package). Distributed by the author. Department of Genetics, University of Washington, Seattle
31. B.J. Finlay Global dispersal of free-living microbial eukaryote species Science 296 2002 1061 1063
32. J. Francisco-Ortega, R.K. Jansen, and A. Santos-Guerra Chloroplast DNA evidence of colonization, adaptive radiation, and hybridization in the evolution of the Macaronesian flora Proc. Natl. Acad. Sci. USA 93 1996 4085 4090
33. J. Francisco-Ortega, M.T. Jackson, A. Santos-Guerra, M. Fernández-Galván, and B.V. Ford-Lloyd The phytogeography of Chamaecytisus proliferus (L.fil.) Link complex (Fabaceae: Genisteae) in the Canary Islands: a multivariate analysis Vegetatio 110 1994 1 17
34. Y.-X. Fu Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection Genetics 147 1997 915 925
35. Y.-X. Fu, and W.-H. Li Statistical tests of neutrality of mutations Genetics 133 1993 693 709
36. F. Galibert, T.M. Finan, S.R. Long, A. Puhler, P. Abola, F. Ampe, F. Barloy-Hubler, M.J. Barnett, A. Becker, P. Boistard, G. Bothe, M. Boutry, L. Bowser, J. Buhrmester, E. Cadieu, D. Capela, P. Chain, A. Cowie, R.W. Davis, S. Dreano, N.A. Federspiel, R.F. Fisher, S. Gloux, T. Godrie, A. Goffeau, B. Golding, J. Gouzy, M. Gurjal, I. Hernandez-Lucas, A. Hong, L. Huizar, R.W. Hyman, T. Jones, D. Kahn, M.L. Kahn, S. Kalman, D.H. Keating, E. Kiss, C. Komp, V. Lelaure, D. Masuy, C. Palm, M.C. Peck, T.M. Pohl, D. Portetelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thebault, M. Vandenbol, F.J. Vorholter, S. Weidner, D.H. Wells, K. Wong, K.C. Yeh, and J. Batut The composite genome of the legume symbiont Sinorhizobium meliloti Science 293 2001 668 672
37. M.W. Gaunt, S.L. Turner, L. Rigottier-Gois, S.A. Lloyd-Macgilp, and J.P. Young Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia Int. J. Syst. Evol. Microbiol. 51 2001 2037 2048
38. J.P. Gogarten, W.F. Doolittle, and J.G. Lawrence Prokaryotic evolution in light of gene transfer Mol. Biol. Evol. 19 2002 2226 2238
39. N. Goldman, J.P. Anderson, and A.G. Rodrigo Likelihood-based tests of topologies in phylogenetics Syst. Biol. 49 2000 652 670
40. D.W. Griffin, C.A. Kellogg, V.H. Garrison, and E.A. Shinn The global transport of dust-an intercontinental river of dust, microorganisms and toxic chemicals flows through the Earth's atmosphere Am. Sci. 90 2002 228 235
41. S. Guindon, and O. Gascuel A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood Syst. Biol. 52 2003 696 704
42. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symp. Ser., pp. 95-98
43. B. Haubold, and P.B. Rainey Genetic and ecotypic structure of a fluorescent Pseudomonas population Mol. Ecol. 5 1996 747 761
44. J. Hey, and J. Wakeley A coalescent estimator of the population recombination rate Genetics 145 1997 833 846
45. M. Holder, and P.O. Lewis Phylogeny estimation: traditional and Bayesian approaches Nat. Rev. Genet. 4 2003 275 284
46. A.B. Hollis, W.E. Kloos, and G.E. Elkan DNA: DNA hybridization studies of Rhizobium japonicum and related Rhizobiaceae J. Gen. Microbiol. 123 1981 215 222
47. R.R. Hudson Estimating the recombination parameter of a finite population model without selection Genet. Res. 50 1987 245 250
48. R.R. Hudson, and N.L. Kaplan Statistical properties of the number of recombination events in the history of a sample of DNA sequences Genetics 111 1985 147 164
49. R.R. Hudson, D.D. Boos, and N.L. Kaplan A statistical test for detecting geographic subdivision Mol. Biol. Evol. 9 1992 138 151
50. R.R. Hudson, M. Slatkin, and W.P. Maddison Estimation of levels of gene flow from DNA sequence data Genetics 132 1992 583 589
51. J.P. Huelsenbeck, and B. Rannala Phylogenetic methods come of age: testing hypotheses in an evolutionary context Science 276 1997 227 232
52. J.P. Huelsenbeck, J.J. Bull, and C.W. Cunningham Combining data in phylogenetic analysis Trends Ecol. Evol. 11 1996 152 157
53. J.P. Huelsenbeck, F. Ronquist, R. Nielsen, and J.P. Bollback Bayesian inference of phylogeny and its impact on evolutionary biology Science 294 2001 2310 2314
54. J.P. Huelsenbeck, B. Larget, R.E. Miller, and F. Ronquist Potential applications and pitfalls of Bayesian inference of phylogeny Syst. Biol. 51 2002 673 688
55. D.H. Huson SplitsTree: analyzing and visualizing evolutionary data Bioinformatics 14 1998 68 73
56. C.A. Istock, K.E. Duncan, N. Ferguson, and X. Zhou Sexuality in a natural population of bacteria-Bacillus subtilis challenges the clonal paradigm Mol. Ecol. 1 1992 95 103
57. A. Jarabo-Lorenzo, E. Velazquez, R. Perez-Galdona, M.C. Vega-Hernandez, E. Martinez-Molina, P.E. Mateos, P. Vinuesa, E. Martinez-Romero, and M. Leon-Barrios Restriction fragment length polymorphism analysis of 16S rDNA and low molecular weight RNA profiling of rhizobial isolates from shrubby legumes endemic to the Canary islands Syst. Appl. Microbiol. 23 2000 418 425
58. A. Jarabo-Lorenzo, R. Pérez-Galdona, J. Donate-Correa, R. Rivas, E. Velázquez, M. Hernández, F. Temprano, E. Martínez- Molina, T. Ruiz-Argüeso, and M. León-Barrios Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp Syst. Appl. Microbiol. 26 2003 611 623
59. B.D.W. Jarvis, M. Gillis, and J. De Ley Intra- and intergeneric similarities between the ribosomal ribonucleic cistrons of Rhizobium and Bradyrhizobium species and some related bacteria Int. J. Syst. Bacteriol. 36 1986 129 138
60. D.C. Jordan 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 1982 136 139
61. C. Juan, E. Brent, P. Oromí, and G.M. Hewitt Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands Trends Ecol. Evol. 15 2000 104 109
62. A.K. Judd, S. M., M.J. Sadowsky, and F.J. de Bruijn Use of repetitive sequences and the polymerase chain reaction technique to classify genetically related Bradyrhizobium japonicum serocluster 123 strains Appl. Environ. Microbiol. 59 1993 1702 1708
63. T. Kaneko, Y. Nakamura, S. Sato, K. Minamisawa, T. Uchiumi, S. Sasamoto, A. Watanabe, K. Idesawa, M. Iriguchi, K. Kawashima, M. Kohara, M. Matsumoto, S. Shimpo, H. Tsuruoka, T. Wada, M. Yamada, and S. Tabata Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 DNA Res. 9 2002 189 197
64. E. Käss, and M. Wink Phylogenetic relationships in the Papilionoideae (family Leguminoéqe) based on nucleotide sequences of cpDNA (rbcL) and ncDNA (ITS 1 and 2) Mol. Phylogenet. Evol. 8 1997 65 88
65. R.E. Kass, and A.E. Raftery Bayes factors J. Am. Stat. Assoc. 90 1995 773 795
66. C.R. Kelsey, K.A. Crandall, and A.F. Voevodin Different models, different trees: the geographic origin of PTLV-I Mol. Phylogenet. Evol. 13 1999 336 347
67. M. Kimura The Neutral Theory of Molecular Evolution 1983 Cambridge University Press Cambridge, MA
68. W. Kitagawa, S. Takami, K. Miyauchi, E. Masai, Y. Kamagata, J.M. Tiedje, and M. Fukuda Novel 2,4-dichlorophenoxyacetic acid degradation genes from oligotrophic Bradyrhizobium sp. strain HW13 isolated from a pristine environment J. Bacteriol. 184 2002 509 518
69. S. Kumar, and S.R. Gadagkar Disparity index: a simple statistic to measure and test the homogeneity of substitution patterns between molecular sequences Genetics 158 2001 1321 1327
70. C.G. Kurland, B. Canback, and O.G. Berg Horizontal transfer: a critical view Proc. Natl. Acad. Sci. USA 100 2003 9658 9662
71. W.F.W. Kurz, and T.A. LaRue Nitrogenase activity in rhizobia in absence of plant host Nature 256 1975 407 408
72. L.D. Kuykendall, B. Saxena, T.E. Devine, and S.E. Udell Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can. J. Microbiol. 38 1992 501 505
73. G. Laguerre, S.M. Nour, V. Macheret, J. Sanjuan, P. Drouin, and N. Amarger Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts Microbiology 147 2001 981 993
74. R. Lan, and P.R. Reeves When does a clone deserve a name? A perspective on bacterial species based on population genetics Trends Microbiol. 9 2001 419 424
75. R.T. Lan, and P.R. Reeves Intraspecies variation in bacterial genomes: the need for a species genome concept Trends Microbiol. 8 2000 396 401
76. J.G. Lawrence Gene transfer in bacteria: speciation without species? Theor. Popul. Biol. 61 2002 449 460
77. T. Leitner, S. Kumar, and J. Albert Tempo and mode of nucleotide substitutions in gag and env gene fragments in human immunodeficiency virus type 1 populations with a known transmission history J. Virol. 71 1997 4761 4770
78. A.R. Lemmon, and E.C. Moriarty The importance of proper model assumptions in Bayesian phylogenetics Syst. Biol. 53 2004 265 277
79. B.R. Levin Periodic selection, infectious gene exchange and the genetic structure of E. coli populations Genetics 99 1981 1 23
80. D. Martin, and E. Rybicki RDP: detection of recombination amongst aligned sequences Bioinformatics 16 2000 562 563
81. J. Maynard-Smith Analyzing the mosaic structure of genes J. Mol. Evol. 34 1992 126 129
82. J. Maynard-Smith, N.H. Smith, M. O'Rourke, and B.G. Spratt How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90 1993 4384 4388
83. S. Mesa, L. Velasco, M.E. Manzanera, M.J. Delgado, and E.J. Bedmar Characterization of the norCBQD genes, encoding nitric oxide reductase, in the nitrogen fixing bacterium Bradyrhizobium japonicum Microbiology 148 2002 3553 3560
84. L. Moulin, G. Béna, C. Boivin-Masson, and T. Stepkowski Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus Mol. Phylogenet. Evol. 30 2004 720 732
85. R. Nichols Gene trees and species trees are not the same Trends Ecol. Evol. 16 2001 358 364
86. J.A. Nylander, F. Ronquist, J.P. Huelsenbeck, and J.L. Nieves-Aldrey Bayesian phylogenetic analysis of combined data Syst. Biol. 53 2004 47 67
87. H. Ochman, J.G. Lawrence, and E.A. Groisman Lateral gene transfer and the nature of bacterial innovation Nature 405 2000 299 304
88. Y. Oda, B. Star, L.A. Huisman, J.C. Gottschal, and L.J. Forney Biogeography of the purple nonsulfur bacterium Rhodopseudomonas palustris Appl. Environ. Microbiol. 69 2003 5186 5191
89. R.M. Polhill Complete synopsis of legume genera, Phytochemical Dictionary of the Leguminoseae 1994 Chapman & Hall London pp. xlix-Ivii
90. D. Posada, and K.A. Crandall MODELTEST: testing the model of DNA substitution Bioinformatics 14 1998 817 818
91. D. Posada, and K.A. Crandall Evaluation of methods for detecting recombination from DNA sequences: computer simulations Proc. Natl. Acad. Sci. USA 98 2001 13757 13762
92. D. Posada, and K.A. Crandall The effect of recombination on the accuracy of phylogeny estimation J. Mol. Evol. 54 2002 396 402
93. D. Posada, K.A. Crandall, M. Nguyen, J.C. Demma, and R.P. Viscidi Population genetics of the porB gene of Neisseria gonorrhoeae: different dynamics in different homology groups Mol. Biol. Evol. 17 2000 423 436
94. J.L. Rademaker, B. Hoste, F.J. Louws, K. Kersters, J. Swings, L. Vauterin, P. Vauterin, and F.J. de Bruijn Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system Int. J. Syst. Evol. Microbiol. 50 Pt 2 2000 665 677
95. J.L.W. Rademaker, F.J. Louws, U. Rossbach, P. Vinuesa, and F.J. de Bruijn Computer-assisted pattern analysis of molecular fingerprints and database construction A.D.L. Akkermans J.E. van Elsas F.J. de Bruijn Molecular Ecology Manual 1998 Kluwer Academic Publishers Dordrecht 1 33 Chapter 37.31.33
96. S.E. Ramos-Onsins, and J. Rozas Statistical properties of new neutrality tests against population growth Mol. Biol. Evol. 19 2002 2092 2100
97. Rivas, R., Willems, A., Palomo, J.L., García-Benavides, P., Mateos, P.F., Martinez-Molina, E., Gillis, M., Velázquez, E., 2004. Bradryrhizobium betae sp. nov. isolated from roots of Beta vulgaris affected by tumor-like deformations. Int. J. Syst. Evol. Microbiol. (in press)
98. F. Ronquist, and J.P. Huelsenbeck MrBAYES 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 2003 1572 1574
99. N.A. Rosenberg The probability of topological concordance of gene trees and species trees Theor. Popul. Biol. 61 2002 225 247
100. R. Rosselló-Mora, and R. Amann The species concept for prokaryotes FEMS Microbiol. Rev. 25 2001 39 67
101. J. Rozas, J.C. Sanchez-DelBarrio, X. Messeguer, and R. Rozas DnaSP, DNA polymorphism analyses by the coalescent and other methods Bioinformatics 19 2003 2496 2497
102. A. Saito, H. Mitsui, R. Hattori, K. Minamisawa, and T. Tsutomu Hattori Slow-growing and oligotrophic soil bacteria phylogenetically close to Bradyrhizobium japonicum FEMS Microbiol. Ecol. 25 1998 277 286
103. M.O. Salminen, J.K. Carr, D.S. Burke, and F.E. McCutcham Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning AIDS Res. Hum. Retroviruses 11 1995 1423 1425
104. S.F. Sarkar, and D.S. Guttman Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen Appl. Environ. Microbiol. 70 2004 1999 2012
105. H. Sawada, L.D. Kuykendall, and J.M. Young Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts J. Gen. Appl. Microbiol. 49 2003 155 179
106. S. Sawyer Statistical tests for detecting gene conversion Mol. Biol. Evol. 6 1998 526 538
107. M.H. Schierup, and J. Hein Consequences of recombination on traditional phylogenetic analysis Genetics 156 2000 879 891
108. L. Segovia, D. Piñero, R. Palacios, and E. Martínez-Romero Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum Appl. Environ. Microbiol. 57 1991 426 433
109. R.K. Selander, D.A. Caugant, H. Ochman, J.M. Musser, M.N. Gilmour, and T.S. Whittam Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics Appl. Environ. Microbiol. 51 1986 873 884
110. H. Shimodaira, and M. Hasegawa Multiple comparisons of log-likelihoods with applications to phylogenetic inference Mol. Biol. Evol. 16 1999 1114 1116
111. C. Silva, L.E. Eguiarte, and V. Souza Reticulated and epidemic population genetic structure of Rhizobium etli biovar phaseoli in a traditionally managed locality in Mexico Mol. Ecol. 8 1999 277 287
112. C. Silva, P. Vinuesa, L.E. Eguiarte, E. Martinez-Romero, and V. Souza 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 2003 884 893
113. P.H.A. Sneath, and R.R. Sokal Numerical Taxonomy 1973 W.H. Freeman San Francisco
114. R.B. So, J.K. Ladha, and J.P. Young Photosynthetic symbionts of Aeschynomene spp. form a cluster with bradyrhizobia on the basis of fatty acid and rRNA analyses Int. J. Syst. Bacteriol. 44 1994 392 403
115. V. Souza, T.T. Nguyen, R.R. Hudson, D. Piñero, and R.E. Lenski Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proc. Natl. Acad. Sci. USA 89 1992 8389 8393
116. H.P. Spaink, A. Kondorosi, and P.J.J. Hooykaas The Rhizobiaceae 1998 Kluwer Academic Publishers Dordrecht
117. J.I. Sprent Nodulation in legumes 2001 Royal Botanic Gardens Kew p. 146
118. E. Stackebrandt, W. Frederiksen, G.M. Garrity, P.A. Grimont, P. Kampfer, M.C. Maiden, X. Nesme, R. Rossello-Mora, J. Swings, H.G. Truper, L. Vauterin, A.C. Ward, and W.B. Whitman Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology Int. J. Syst. Evol. Microbiol. 52 2002 1043 1047
119. J.T. Sullivan, B.D. Eardly, P. van Berkum, and C.W. Ronson Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus Appl. Environ. Microbiol. 62 1996 2818 2825
120. J.T. Sullivan, H.N. Patrick, W.L. Lowther, D.B. Scott, and C.W. Ronson Nodulating strains of Rhizobium loti arise through chromosomal and symbiotic gene transfer in the environment Proc. Natl. Acad. Sci. USA 92 1995 8995 8999
121. Y. Suzuki, G.V. Glazko, and M. Nei Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics Proc. Natl. Acad. Sci. USA 99 2002 16138 16143
122. D.L. Swofford PAUP*: Phylogenetic Analysis Using Parsimony and Other Methods (software) 2002 Sinuauer Associates Sunderland, MA
123. D.L. Swofford, G.J. Olsen, P.J. Waddel, and D.M. Hillis Phylogenetic inference D.M. Hillis C. Moritz B.K. Mable Molecular Systematics 1996 Sinauer Associates Sunderland, MA 407 514
124. F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 1989 585 595
125. Z. Tan, T. Hurek, P. Vinuesa, P. Muller, J.K. Ladha, and B. Reinhold-Hurek Specific detection of Bradyrhizobium and Rhizobium srains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer- targeted PCR Appl. Environ. Microbiol. 67 2001 3655 3664
126. A.R. Templeton The meaning of species and speciation: a genetic perspective D. Otte J.A. Endler Speciation and its Consecuences 1989 Sinauer Sunderland, Massachusetts 3 27
127. J.D. Thompson, T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res. 25 1997 4876 4882
128. V. Torsvik, L. Ovreas, and T.F. Thingstad Prokaryotic diversity-magnitude, dynamics, and controlling factors Science 296 2002 1064 1066
129. S.L. Turner, and J.P. Young The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications Mol. Biol. Evol. 17 2000 309 319
130. 2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences J. Bacteriol. 177 1995 1414 1417
131. P. van Berkum, and B.D. Eardly Molecular evolutionary systematics of the Rhizobiaceae H.P. Spaink A. Kondorosi P.J.J. Hooykaas The Rhizobiaceae: Molecular Biology of Plant-Associated Bacteria 1998 Kluwer Academic Publishers Dordrecht 1 24
132. P. van Berkum, and J.J. Fuhrmann Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence Int. J. Syst. Evol. Microbiol. 50 2000 2165 2172
133. P. van Berkum, and B.D. Eardly The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica Appl. Environ. Microbiol. 68 2002 1132 1136
134. P. Vandamme, B. Pot, M. Gillis, P. de Vos, K. Kersters, and J. Swings Polyphasic taxonomy, a consensus approach to bacterial systematics Microbiol. Rev. 60 1996 407 438
135. P. Vinuesa, and C. Silva Species delineation and biogeography of symbiotic bacteria associated with cultivated and wild legumes D. Werner Biological Resources and Migration 2004 Springer Verlag Berlin 143 161
136. P. Vinuesa, J.L.W. Rademaker, F.J. de Bruijn, and D. Werner Genotypic characterization of Bradyrhizobium strains nodulating endemic woody legumes of the Canary Islands by PCR-restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rDNA) and 16S-23S rDNA intergenic spacers, repetitive extragenic palindromic PCR genomic fingerprinting and partial 16S rDNA sequencing Appl. Environ. Microbiol. 64 1998 2096 2104
137. P. Vinuesa, J.L.W. Rademaker, F.J. de Bruijn, and D. Werner Characterization of Bradyrhizobium spp. strains by RFLP analysis of amplified 16S rDNA and rDNA intergenic spacer regions E. Martínez G. Hernández Highlights on Nitrogen Fixation 1999 Plenum Publishing Corporation New York 275 279
138. Vinuesa, P., León-Barrios, M., Silva, C., Willems, A., Jarabo-Lorenzo, A., Pérez-Galdona, R., Werner, D., Martínez- Romero, E., 2004. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont from the nodules of endemic woody legume species (Papilionoideae:Genisteae) growing in the Canary Islands along with B. japonicum bv. genistearum, Bradyrhizobium genospecies α and Bradyrhizobium genospecies β. Int. J. Syst. Evol. Microbiol. (in press. http://dx.doi.org/10.1099/ijs.0.63292-0)
139. D.M. Ward A natural species concept for prokaryotes Curr. Opin. Microbiol. 1 1998 271 277
140. J. Wernegreen, and M.A. Riley Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages Mol. Biol. Evol. 16 1999 98 113
141. T.S. Whittam ETDIV and ETCLUS programs 1990 Pennsylvania State University
142. A. Willems, R. Coopman, and M. Gillis Comparison of sequence analysis of 16S-23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium Int. J. Syst. Evol. Microbiol. 51 2001 623 632
143. A. Willems, R. Coopman, and M. Gillis Phylogenetic and DNA-DNA hybridization analyses of Bradyrhizobium species Int. J. Syst. Evol. Microbiol. 51 2001 111 117
144. A. Willems, A. Munive, P. de Lajudie, and M. Gillis In most Bradyrhizobium groups sequence comparison of 16S-23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations Syst. Appl. Microbiol. 26 2003 203 210
145. X. Xia, and Z. Xie DAMBE: Software package for data analysis in molecular biology and evolution J. Hered. 92 2001 371 373
146. X. Xia, Z. Xie, M. Salemi, L. Chen, and Y. Wang An index of sustitution saturation and its application Mol. Phylogenet. Evol. 26 2002 1 7
147. L.M. Xu, C. Ge, Z. Cui, J. Li, and H. Fan Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans Int. J. Syst. Bacteriol. 45 1995 706 711
148. Z. Yang Among-site rate variation and its impact on phylogenetic analyses Trends Ecol. Evol. 11 1996 367 372
149. Z.Y. Yao, F.L. Kan, E.T. Wang, G.H. Wei, and W.X. Chen Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov Int. J. Syst. Evol. Microbiol. 52 2002 2219 2230
150. X. Zhang, G. Nick, S. Kaijalainen, Z. Terefework, L. Paulin, S.W. Tighe, P.H. Graham, and K. Lindström Phylogeny and diversity of Bradyrhizobium strains isolated from the root nodules of peanut (Arachis hypogaea) in Sichuan, China Syst. Appl. Microbiol. 22 1999 378 386
151. J. Zhou, L.D. Bowler, and B.G. Spratt Interspecies recombination, and phylogenetic distortions, within the glutamine synthetase and shikimate dehydrogenase genes of Neisseria meningitidis and commensal Neisseria species Mol. Microbiol. 23 1997 799 812