Microevolution of symbiotic bradyrhizobium populations associated with soybeans in east north america

Ecology and Evolution

Volumn 2, Issue 12, 2012, Pages 2943-2961

  Tang, Jie ^a,c   Bromfield, E S P ^a   Rodrigue, N ^a,b   Cloutier, S ^a   Tambong, J T ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bradyrhizobium; Evolution; Glycine max (soybean); Homologous recombination; Inoculation; Native legumes

Indexed keywords

EID: 84887320456     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.404     Document Type: Article

References (69)

1. Appunu, C., A. N'Zoue, and G. Laguerre. 2008. Genetic diversity of native bradyrhizobia isolated from soybeans (Glycine max L.) in different agricultural-ecologicalclimatic regions of India. Appl. Environ. Microbiol. 74:5991-5996.
2. den Bakker, H., X. Didelot, E. Fortes, K. Nightingale, and M. Wiedmann. 2008. Lineage specific recombination rates and microevolution in Listeria monocytogenes. BMC Evol. Biol. 8:277.
3. van Berkum, P., P. Elia, Q. Song, and B. D. Eardly. 2012. Development and application of a multilocus sequence analysis method for the identification of genotypes within the genus Bradyrhizobium and for establishing nodule occupancy of soybean (Glycine max L. Merr). Mol. Plant Microbe Interact. 25:321-330.
4. Bromfield, E. S. P., L. R. Barran, and R. Wheatcroft. 1995. Relative genetic structure of a population of Rhizobium meliloti isolated directly from soil and from nodules of alfalfa (Medicago sativa) and sweet clover (Melilotus alba). Mol. Ecol. 4:183-188.
5. Bromfield, E. S. P., J. T. Tambong, S. Cloutier, D. Prévost, G. Laguerre, P. van Berkum, 2010. Ensifer, Phyllobacterium and Rhizobium species occupy nodules of Medicago sativa (alfalfa) and Melilotus alba (sweet clover) grown at a Canadian site without a history of cultivation. Microbiology 156:505-520.
6. Cober, E. R., H. D. Voldeng, J. A. Frégeau-Reid, and R. J. D. Guillemette. 2007. AC Glengarry soybean. Can. J. Plant Sci. 87:307-308.
7. Cregan, P. B., and H. H. Keyser. 1986. Host restriction of nodulation by Bradyrhizobium japonicum Strain USDA 123 in soybean. Crop Sci. 26:911-916.
8. Delannay, X., D. M. Rodgers, and R. G. Palmer. 1983. Relative genetic contributions among ancestral lines to North American soybean cultivars. Crop Sci. 23:944-949.
9. Didelot, X., and D. Falush. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-1266.
10. Didelot, X., and M. C. J. Maiden. 2010. Impact of recombination on bacterial evolution. Trends Microbiol. 18:315-322.
11. Didelot, X., R. Urwin, M. C. J. Maiden, and D. Falush. 2009. Genealogical typing of Neisseria meningitidis. Microbiology 155:3176-3186.
12. Doyle, J. J., and J. L. Doyle. 1993. Chloroplast DNA phylogeny of the papilionoid legume tribe Phaseoleae. Syst. Bot. 18:309-327.
13. Feil, E. J. 2010. Linkage, selection, and the clonal complex. Pp. 19-35 in D. A. Robinson, D. Falush, and E. J. Fiel, eds. Bacterial population genetics in infectious disease. Wiley-Blackwell, Hoboken, NJ.
14. Feil, E. J., and B. G. Spratt. 2001. Recombination and the population structures of bacterial pathogens. Annu. Rev. Microbiol. 55:561-90.
15. Fraser, C., E. J. Alm, M. F. Polz, B. G. Spratt, and W. P. Hanage. 2010. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741-746.
16. Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, and O. Gascuel. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321.
17. Hollis, A. B., W. E. Kloos, and G. H. Elkan. 1981. DNA:DNA hybridization studies of Rhizobium japonicum and related Rhizobiaceae. Microbiology 123:215-222.
18. Hudson, R. R., D. D. Boos, and N. L. Kaplan. 1992a. A statistical test for detecting population subdivision. Mol. Biol. Evol. 9:138-151.
19. Hudson, R. R., M. Slatkin, and W. P. Maddison. 1992b. Estimation of levels of gene flow from DNA sequence data. Genetics 132:583-589.
20. Huson, D. H., and D. Bryant. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267.
21. Itakura, M., K. Saeki, H. Omori, T. Yokoyama, T. Kaneko, S. Tabataet et al. 2009. Genomic comparison of Bradyrhizobium japonicum strains with different symbiotic nitrogen-fixing capabilities and other Bradyrhizobiaceae members. ISME. J. 3:326-339.
22. Jakobsson, M., and N. A. Rosenberg. 2010. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-1806.
23. Joseph, S. J., X. Didelot, K. Gandhi, D. Dean, and T. D. Read. 2011. Interplay of recombination and selection in the genomes of Chlamydia trachomatis. Biol. Direct 6:28.
24. Kaneko, T., Y. Nakamura, S. Sato, K. Minamisawa, T. Uchiumi, S. Sasamoto et al. 2002. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9:189-197.
25. T. Gene 2:763-787.
26. Keyser, H. H., and R. F. Griffin. 1987. Beltsville Rhizobium culture collection catalog. Agricultural Research Service, U.S. Department of Agriculture, Beltsville, MD.
27. Keyser, H. H., and F. Li. 1992. Potential for increasing biological nitrogen fixation in soybean. Plant Soil 141:119-135.
28. Kvien, C. S., G. E. Ham, and J. W. Lambert. 1981. Recovery of introduced Rhizobium japonicum strains by soybean genotypes. Agron. J. 73:900-905.
29. Lartillot, N., and H. Philippe. 2006. Computing Bayes factors using thermodynamic integration. Syst. Biol. 55:195-207.
30. Lewis-Rogers, N., K. A. Crandall, and D. Posada. 2004. Evolutionary analyses of genetic recombination. Pp. 49-78 in V. Parisi, V. De Fonzo, F. Aluffi-Pentini, eds. Dynamical Genetics. Research Signpost, Kerala, India.
31. Li, Q. Q., E. T. Wang, Y. Z. Zhang, Y. M. Zhang, C. F. Tian, X. H. Sui et al. 2011. Diversity and biogeography of rhizobia isolated from root nodules of Glycine max grown in Hebei Province, China. Microb. Ecol. 61:917-931.
32. Librado, P., and J. Rozas. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
33. Loh, J., and G. Stacey. 2003. Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Appl. Environ. Microbiol. 69:10-17.
34. Lohrke, S. M., J. H. Orf, and M. J. Sadowsky. 1996. Inheritance of host-controlled restriction of nodulation by Bradyrhizobium japonicum strain USDA 110. Crop Sci. 36:1271-1276.
35. Maiden M.C. 2006. Multilocus sequence typing of bacteria. Annu. Rev. Microbiol. 60:561-588.
36. Marr, D. L., T. E. Devine, and M. A. Parker. 1997. Nodulation restrictive genotypes of Glycine and Amphicarpaea: a comparative analysis. Plant Soil 189:181-188.
37. Martin, D. P., P. Lemey, M. Lott, V. Moulton, D. Posada, and P. Lefeuvre. 2010. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462-2463.
38. Menna, P., and M. Hungria. 2011. Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin and spread and maintenance by both horizontal and vertical transfer. Int. J. Syst. Evol. Microbiol. 61:3052-3067.
39. Menna, P., F. G. Barcellos, and M. Hungria. 2009. Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int. J. Syst. Evol. Microbiol. 59:2934-2950.
40. Moulin, L., G. Béna, C. Boivin-Masson, and T. Stezpkowski. 2004. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol. Phylogenet. Evol. 30:720-732.
41. Nandasena, K. G., G. W. O'Hara, R. P. Tiwari, E. Sezmiş, and J. G. Howieson. 2007. 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. 9:2496-2511.
42. Parker, M. A. 1999. Relationships of bradyrhizobia from the legumes Apios americana and Desmodium glutinosum. Appl. Environ. Microbiol. 65:4914-4920.
43. Parker, M. A., and D. A. Kennedy. 2006. Diversity and relationships of bradyrhizobia from legumes native to eastern North America. Can. J. Microbiol. 52:1148-1157.
44. Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.
45. Pretorius-Guth, I. M., A. Puhler, and R. Simon. 1990. Conjugal transfer of megaplasmid 2 between Rhizobium meliloti strains in alfalfa nodules. Appl. Environ. Microbiol. 56:2354-2359.
46. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
47. R Development Core Team. 2009. R: a language and environment for statistical computing. ISBN 3-900051-07-0. R Foundation for Statistical Computing, Vienna, Austria.
48. Rivas, R., M. Martens, P. de Lajudie, and A. Willems. 2009. Multilocus sequence analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 32:101-110.
49. Santos, M. A., M. A. T. Vargas, and M. Hungria. 1999. Characterization of soybean Bradyrhizobium strains adapted to the Brazilian savannas. FEMS Microbiol. Ecol. 30:261-272.
50. Schliep, K. P. 2011. Phangorn: phylogenetic analysis in R. Bioinformatics 27:592-593.
51. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, and E. B. Hollister et al. 2009. Introducing mothur: open-source, platform-independent, communitysupported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
52. Semu, E., D. J. Hume, and C. T. Corke. 1979. Influence of soybean inoculation and nitrogen levels on populations and serogroups of Rhizobium japonicum in Ontario. Can. J. Microbiol. 25:739-745.
53. Smartt, J., and T. Hymowitz. 1985. Domestication and evolution of grain legumes. Pp. 32-72 in R. J. Summerfield and E. H. Roberts, eds. Grain legume crops. Collins, London, U.K.
54. Smith, J. M., E. J. Feil, and N. H. Smith. 2000. Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22:1115-1122.
55. Spoerke, J. M., H. H. Wilkinson, and M. A. Parker. 1996. Nonrandom genotypic associations in a legume-Bradyrhizobium mutualism. Evolution 50:146-154.
56. Steenkamp, E. T., T. Stepkowski, A. Przymusiak, W. J. Botha, and I. J. Law. 2008. Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harboring nodulation genes that belong to the large pantropical clade common in Africa. Mol. Phylogenet. Evol. 48:1131-1144.
57. Stepkowski, T., L. Moulin, A. Krzyzańska, A. McInnes, I. J. Law, and J. Howieson. 2005. European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl. Environ. Microbiol. 71:7041-7052.
58. Stepkowski, T., C. E. Hughes, I. J. Law, L. Markiewicz, D. Gurda, A. Chlebicka et al. 2007. Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl. Environ. Microbiol. 73:3254-3264.
59. Sterner, J. P., and M. A. Parker. 1999. Diversity and relationships of bradyrhizobia from Amphicarpaea bracteata based on partial nod and ribosomal sequences. Syst. Appl. Microbiol. 22:387-392.
60. Streeter, J. G. 1994. Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Can. J. Microbiol. 40:513-522.
61. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
62. Tian, C. F., J. P. W. Young, E. T. Wang, S. M. Tamimi, and W. X. Chen. 2010. Population mixing of Rhizobium leguminosarum bv. viciae nodulating Vicia faba: the role of recombination and lateral gene transfer. FEMS Microbiol. Ecol. 73:563-576.
63. Vincent, J. M. 1970. A manual for the practical study of rootnodule bacteria. International Biological Program Handbook, No. 15. Blackwell Scientific Publications, Oxford, U.K.
64. Vinuesa, P., K. Rojas-Jiménez, B. Contreras-Moreira, S. K. Mahna, B. N. Prasad, H. Moe et al. 2008. Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the Asiatic continent. Appl. Environ. Microbiol. 74:6987-6996.
65. Voldeng, H. D., R. J. D. Guillemette, D. A. Leonard, and E. R. Cober. 1996. Maple Glen soybean. Can. J. Plant Sci. 76:475-476.
66. Voldeng, H. D., P. Turcotte, R. J. D. Guillemette, and E. R. Cober. 1999. AC Orford soybean. Can. J. Plant Sci. 79:111-112.
67. Weaver, R. W., L. R. Frederick, and L. C. Dumeril. 1972. Effect of soybean cropping and soil properties on numbers of Rhizobium japonicum in Iowa soils. Soil Sci. 114:137-141.
68. Wernersson, R., and A. G. Pedersen. 2003. RevTrans - constructing alignments of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31:3537-3539.
69. Zhu, T., L. Shi, J. J. Doyle, and P. Keim. 1995. A single nuclear locus phylogeny of soybean based on DNA sequence. Theor. Appl. Genet. 90:991-999.