Distinct Bradyrhizbium communities nodulate legumes native to temperate and tropical monsoon Australia

Molecular Phylogenetics and Evolution

Volumn 63, Issue 2, 2012, Pages 265-277

  Stepkowski, Tomasz ^a   Watkin, Elizabeth ^b   McInnes, Alison ^c,e   Gurda, Dorota ^a   Gracz, Joanna ^a   Steenkamp, Emma T ^d  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^b CURTIN UNIVERSITY   (Australia)

^c UNIVERSITY OF WESTERN SYDNEY   (Australia)

^d UNIVERSITY OF PRETORIA   (South Africa)

^e ACT Government   (Australia)

Author keywords

Australia; Biogeography; Bradyrhizobium; Climate change; Geographical isolation; Leguminosae; Multilocus sequence analysis; NodA gene

Indexed keywords

ACYLTRANSFERASE; BACTERIAL DNA; BACTERIAL PROTEIN; NODA PROTEIN, RHIZOBIALES; RIBOSOME DNA; RNA 16S;

ARTICLE; AUSTRALIA; BRADYRHIZOBIUM; CLASSIFICATION; DNA SEQUENCE; FABACEAE; GENETICS; MICROBIAL CONSORTIUM; MICROBIOLOGY; MULTIGENE FAMILY; MULTILOCUS SEQUENCE TYPING; NODULATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS;

ACYLTRANSFERASES; AUSTRALIA; BACTERIAL PROTEINS; BASE SEQUENCE; BRADYRHIZOBIUM; DNA, BACTERIAL; DNA, RIBOSOMAL; FABACEAE; MICROBIAL CONSORTIA; MULTIGENE FAMILY; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; RNA, RIBOSOMAL, 16S; ROOT NODULES, PLANT; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; FABACEAE; RHIZOBIACEAE;

EID: 84858071010     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.12.020     Document Type: Article

References (108)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of bestfit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Andam C.P., Parker M.A. Origins of Bradyrhizobium nodule symbionts from two legume trees in the Philippines. J. Biogeogr. 2008, 35:1030-1039.
3. Appunu C., N'Zoue A., Laguerre G. Genetic diversity of native bradyrhizobia isolated from soybeans (Glycine max L.) in different agricultural-ecological-climatic regions of India. Appl. Environ. Microbiol 2008, 74:5991-5996.
4. Barnet Y.M., Catt P.C. Distribution and characteristics of root-nodule bacteria isolated from Australia Acacia spp. Plant Soil 1991, 135:109-120.
5. Barnet Y.M., Catt P.C., Hearne D.H. Biological nitrogen fixation and root-nodule bacteria (Rhizobium sp. and Bradyrhizobium sp.) in two rehabilitating sand dune areas planted with Acacia spp. Aust. J. Bot. 1985, 33:595-610.
6. Bontemps C., Elliott G.N., Simon M.F., Dos Reis F.B.D., Gross E., Lawton R.C., Neto N.E., Loureiro M.D., De Faria S.M., Sprent J.I., James E.K., Young J.P.W. Burkholderia species are ancient symbionts of legumes. Mol. Ecol. 2010, 19:44-52.
7. Bowman D.M.J.S., Brown G.K., Braby M.F., Brown J.R., Cook L.G., Crisp M.D., Ford F., Haberle S., Hughes J., Isagi Y., Joseph L., McBride J., Nelson G., Ladiges P.Y. Biogeography of the Australian monsoon tropics. J. Biogeogr. 2010, 37:201-216.
8. Brennan, K., 1992. Annotated Checklist of Vascular Plants of the Alligator Rivers Region. Open File Record 62. Office of the Supervising Scientist, Alligator Rivers Region Research Institute, Jabiru, NT, Australia.
9. Byrne M., Yeates D.K., Joseph L., Kearney M., Bowler J., Williams M.A.J., Cooper S., Donnellan S.C., Keogh J.S., Leys R., Melville J., Murphy D.J., Porch N., Wyrwoll K.H. Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol. Ecol. 2008, 17:4398-4417.
10. Byrne M., Steane D.A., Joseph L., Yeates D.K., Jordan G.J., Crayn D., Aplin K., Cantrill D.J., Cook L.G., Crisp M.D., Keogh J.S., Melville J., Moritz C., Porch N., Sniderman J.M.K., Sunnucks P., Weston P.H. Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J. Biogeogr. 2011, 38:1635-1656.
11. Cardinale M., Lanza A., Bonnì M.L., Marsala S., Puglia A.M., Quatrini P. Diversity of rhizobia nodulating wild shrubs of Sicily and some neighbouring islands. Arch. Microbiol. 2008, 190:461-470.
12. Chahboune R., Carro L., Peix A., Barrijal S., Velázquez E., Bedmar E.J. Bradyrhizobium cytisi sp. nov. isolated from effective nodules of Cytisus villosus in Morocco. Int. J. Syst. Evol. Microbiol. 2011, 61:2922-2927.
13. Chaintreuil C., Boivin C., Dreyfus B., Giraud E. Characterization of the common nodulation genes of the photosynthetic Bradyrhizobium sp. ORS285 reveals the presence of a new insertion sequence upstream of nodA. FEMS Microbiol. Lett. 2001, 194:83-86.
14. Chang Y.L., Wang J.Y., Wang E.T., Liu H.C., Sui X.H., Chen W.X. Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea grown in Southern China. Int. J. Syst. Evol. Microbiol. 2011, 61:2496-2502.
15. Chen W.M., Moulin L., Bontemps C., Vandamme P., Bena G., Boivin-Masson C. Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J. Bacteriol. 2003, 185:7266-7272.
16. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucl. Acids Res. 1988, 16:10881-10890.
17. Crisp, M.D., Cook, L.G., 2003. Phylogeny and embryo sac evolution in the endemic Australasian papilionoid tribes Mirbelieae and Bossiaeeae. In: Klitgaard B.B., Bruneau, A. (Eds.), Advances in Legume Systematics, Part 10. Higher Level Systematics. The Royal Botanic Gardens, Kew, pp. 253-268.
18. Crisp M.D., Cook L.G. Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution 2009, 63:2257-2265.
19. Crisp M.D., Laffan S., Linder H.P., Monro A. Endemism in the Australian flora. J. Biogeogr. 2001, 28:183-198.
20. Crisp M., Cook L., Steane D. Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities?. Philos. Trans. Roy. Soc. B. 2004, 359:1551-1571.
21. Dalton H. The cultivation of diazotrohic organisms. Methods for Evaluating Biological Nitrogen Fixation 1980, 13-64. Wiley and Sons, Chichester. F.J. Bergerson (Ed.).
22. 2. Nature 2003, 421:245-249.
23. Dénarié J., Debellé F., Promé J.C. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 1996, 65:503-535.
24. Doignon-Bourcier F., Sy A., Willems A., Torck U., Dreyfus B., Gillis M., de Lajudie P. Diversity of bradyrhizobia from 27 tropical leguminosae species native of Senegal. Syst. Appl. Microbiol. 1999, 22:647-661.
25. Doolittle W.F., Papke R.T. Genomics and the bacterial species problem. Genome Biol. 2006, 7:116.
26. Doyle J.J. Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci. 1998, 3:473-478.
27. Florindo F., Cooper A.K., O'Brien P.E. Introduction to 'Antarctic Cenozoic palaeoenvironments: geologic record and models'. Palaeogeogr. Palaeoclimat. 2003, 198:1-9.
28. Gevers D., Cohan F.M., Lawrence J.G., Spratt B.G., Coenye T., Feil E.J., Stackebrandt E., Van de Peer Y., Vandamme P., Thompson F.L., Swings J. Opinion: re-evaluating prokaryotic species. Nat. Rev. Microbiol. 2005, 3:733-739.
29. Green J.L., Bohannan B.J.M., Whitaker R.J. Microbial biogeography: from taxonomy to traits. Science 2008, 320:1039-1043.
30. Gu C.T., Wang E.T., Sui X.H., Chen W.F., Chen W.X. Diversity and geographical distribution of rhizobia associated with Lespedeza spp. in temperate and subtropical regions of China. Arch. Microbiol. 2007, 188:355-365.
31. Gueye F., Moulin L., Sylla S., Ndoye I., Béna G. Genetic diversity and distribution of Bradyrhizobium and Azorhizobium strains associated with the herb legume Zornia glochidiata sampled from across Senegal. Syst. Appl. Microbiol. 2009, 32:387-399.
32. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
33. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999, 41:95-98.
34. Han T.X., Tian C.F., Wang E.T., Chen W.X. Associations among rhizobial chromosomal background, nod genes, and host plants based on the analysis of symbiosis of indigenous rhizobia and wild legumes native to Xinjiang. Microb. Ecol. 2010, 59:311-323.
35. Hill R.S. Origins of the southeastern Australian vegetation. Philos. Trans. Roy. Soc. B 2004, 359:1537-1549.
36. Hopper S.D., Gioia P. The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity. Ann. Rev. Ecol. Evol. Syst. 2004, 35:623-650.
37. Hoque M.S., Broadhurst L.M., Thrall P.H. Genetic characterisation of root nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across southeastern Australia. Int. J. Evol. Syst. Microbiol. 2011, 61:299-309.
38. Hudson R.R., Boos D.D., Kaplan N.L. A statistical test for detecting population subdivision. Mol. Biol. Evol. 1992, 9:138-151.
39. Hudson R.R., Slatkin M., Maddison W.P. Estimation of levels of gene flow from DNA sequence data. Genetics 1992, 132:583-589.
40. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
41. Islam M.S., Kawasaki H., Muramatsu Y., Nakagawa Y., Seki T. Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci. Biotechnol. Biochem. 2008, 72:1416-1429.
42. Jarabo-Lorenzo A., Perez-Galdona R., Donate-Correa J., Rivas R., Velazquez E., Hernandez M., Temprano F., Martinez-Molina E., Ruiz-Argueso T., Leon-Barrios M. Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Syst. Appl. Microbiol. 2003, 26:611-623.
43. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 1992, 8:275-282.
44. Jordan J.C. 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. 1982, 32:136-139.
45. Kellogg C.A., Griffin D.W. Aerobiology and the global transport of desert dust. Trends Ecol. Evol. 2006, 21:638-644.
46. Kuykendall L.M., Saxena B., Devine T.E., Udell S.E. Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can. J. Microbiol. 1992, 38:501-503.
47. Lafay B., Burdon J.J. Molecular diversity of rhizobia occurring on native shrubby legumes in southeastern Australia. Appl. Environ. Microbiol. 1998, 64:3989-3997.
48. Lafay B., Burdon J.J. Small-subunit rRNA genotyping of rhizobia nodulating Australian Acacia spp. Appl. Environ. Microbiol. 2001, 67:396-402.
49. Lafay B., Burdon J.J. Molecular diversity of rhizobia nodulating the invasive legume Cytisus scoparius in Australia. J. Appl. Microbiol. 2006, 100:1228-1238.
50. Lafay, B., Burdon, J.J., 2007. Molecular diversity of legume root-nodule bacteria in Kakadu National Park, Northern Territory, Australia. PLoS ONE 7;2(3): e277.
51. Lafay B., Bullier E., Burdon J.J. Bradyrhizobia isolated from root nodules of Parasponia (Ulmaceae) do not constitute a separate coherent lineage. Int. J. Syst. Evol. Microbiol. 2006, 56:1013-1018.
52. Lange R.T. Nodule bacteria associated with the indigenous Leguminosae of south-western Australia. J. Gen. Microbiol. 1961, 61:351-359.
53. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
54. Lavin M., Herendeen P.S., Wojciechowski M.F. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst. Biol. 2005, 54:575-594.
55. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
56. Lin D.X., Man C.X., Wang E.T., Chen W.X. Diverse rhizobia that nodulate two species of Kummerowia in China. Arch. Microbiol. 2007, 188:495-507.
57. Marsudi N.D.S., Glenn A.R., Dilworth M.J. Identification and characterization of fast-and slow-growing root nodule bacteria from South-Western Australian soils able to nodulate Acacia saligna. Soil Biol. Biochem. 1999, 31:1229-1238.
58. Martens M., Dawyndt P., Coopman R., Gillis M., De Vos P., Willems A. Advantages of Multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer. Int. J. Syst. Evol. Microbiol. 2008, 58:200-214.
59. Martin H.A. Cenozoic climatic change and the development of the arid vegetation in Australia. J. Arid Environ. 2006, 66:533-563.
60. Martiny J.B.H., Bohannan B.J.M., Brown J.H., Colwell R.K., Fuhrman J.A., Green J.L., Horner-Devine M.C., Kane M., Krumins J.A., Kuske C.R., Morin P.J., Naeem S., Ovreås L., Reysenbach A.L., Smith V.H., Staley J.T. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 2006, 4:102-112.
61. 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.
62. McInnes, A., Ashwath, N., 1992. Techniques for the Collection, Isolation, Authentication and Maintenance of Rhizobia. Internal Report 84. Supervising Scientist for the Alligator Rivers Region, Jabiru, NT, Australia.
63. McInnes A., Date R.A. Improving the survival of rhizobia on Stylosanthes and Desmanthus seed at high temperature. Aust. J. Exp. Agricult. 2005, 45:171-182.
64. 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.
65. Moulin L., Béna G., Boivin-Masson C., Stepkowski T. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol. Phyl. Evol. 2004, 30:720-732.
66. Muñoz V., Ibañez F., Tonelli M.L., Valetti L., Anzuay M.S., Fabra A. Phenotypic and phylogenetic characterization of native peanut Bradyrhizobium isolates obtained from Córdoba, Argentina. Syst. Appl. Microbiol. 2011, 34:446-452.
67. Murphy D.J., Brown G.K., Miller J.T., Ladiges P.Y. Molecular phylogeny of Acacia Mill. (Mimosoideae: Leguminosae): evidence for major clades and informal classification. Taxon 2010, 59:7-19.
68. Nei M. Molecular Evolutionary Genetics 1987, Columbia Univ. Press, New York.
69. Ngom A., Nakagawa Y., Sawada H., Tsukahara J., Wakabayashi S., Uchiumi T., Nuntagij A., Kotepong S., Suzuki A., Higashi S., Abe M. A novel symbiotic nitrogen-fixing member of the Ochrobactrum clade isolated from root nodules of Acacia mangium. J. Gen. Appl. Microbiol. 2004, 50:17-27.
70. Ormeno-Orillo E., Vinuesa P., Zuniga-Davila D., Marti{dotless}nez-Romero E. Molecular diversity of native bradyrhizobia isolated from Lima bean (Phaseolus lunatus L.) in Peru. Syst. Appl. Microbiol. 2006, 29:253-262.
71. Papke R.T., Ramsing N.B., Bateson M.M., Ward D.M. Geographical isolation in spring cyanobacteria. Environ. Microbiol. 2003, 5:650-659.
72. Parker M.A. Symbiotic relationships of legumes and nodule bacteria on Barro Colorado Island, Panama: a review. Microb. Ecol. 2008, 55:662-672.
73. Parker M.A., Lafay B., Burdon J.J., Van Berkum P. Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium. Microbiology 2002, 148:2557-2565.
74. Parker M.A., Wurtz A.K., Paynter Q. Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biol. Invasions 2007, 9:127-138.
75. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
76. Radutoiu S., Madsen L.H., Madsen E.B., Felle H.H., Umehara Y., Gronlund M., Sato S., Nakamura Y., Tabata S., Sandal N., Stougaard J. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003, 425:585-592.
77. Ramirez-Bahena M.H., Peix A., Rivas R., Camacho M., Rodriguez-Navarro D.N., Mateos P.F., Martinez-Molina E., Willems A., Velazquez E. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov. isolated from effective nodules of Pachyrhizus erosus. Int. J. Syst. Evol. Microbiol. 2009, 59:1929-1934.
78. Rivas R., Velazquez E., Willems A., Vizcaino N., Subba-Rao N.S., Mateos P.F., Gillis M., Dazzo F.B., Martinez-Molina E. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl. Environ. Microbiol. 2002, 68:5217-5222.
79. Rivas R., Willems A., Palomo J.L., García-Benavides P., Mateos P.F., Martínez-Molina E., Gillis M., Velázquez E. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int. J. Syst. Evol. Microbiol. 2004, 54:1271-1275.
80. Rivas R., Martens M., de Lajudie P., Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2009, 32:101-110.
81. Rodríguez-Echeverría S. Rhizobial hitchhikers from Down Under: invasional meltdown in a plant-bacteria mutualism?. J. Biogeogr. 2010, 37:1611-1622.
82. Sawada H., Kuykendall L.D., Young J.M. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J. Gen. Appl. Microbiol. 2003, 49:155-179.
83. Schmidt S.K., Lynch R.C., King A.J., Karki D., Robeson M.S., Nagy L., Williams M.W., Mitter M.S., Freeman K.R. Phylogeography of microbial phototrophs in the dry valleys of the high Himalayas and Antarctica. Proc. Roy. Soc. B 2011, 278:702-708.
84. Schrire B.D., Lewis G.P., Lavin M. Biogeography of Leguminosae. Legumes of World 2005, 21-56. The Royal Botanic Gardens, Kew. G. Lewis, B. Schrire, B. MacKinder, M. Lock (Eds.).
85. Schrire B.D., Lavin M., Barker N.P., Forest F. Phylogeny of the tribe Indigofereae (Leguminosae-Papilionoideae): geographically structured more in succulent-rich and temperate settings than in grass-rich environments. Am. J. Bot. 2009, 96:816-852.
86. Short, P.S., Albrecht, D.E., Cowie, I.D., Lewis, D.L., Stuckey, B.M., 2011. Checklist of the Vascular Plants of the Northern Territory. Northern Territory Herbarium, Department of Natural Resources, Environment, the Arts and Sport, NT.
87. Sjöström A., Gross C.L. Life-history characters and phylogeny are correlated with extinction risk in the Australian angiosperms. J. Biogeogr. 2006, 33:271-290.
88. Sniderman J.M.K., Jordan G.J. Extent and timing of floristic exchange between Australian and Asian rain forests. J. Biogeogr. 2011, 38:1445-1455.
89. Sprent J.I. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol. 2007, 174:11-25.
90. Steenkamp E.T., Stepkowski T., Przymusiak A., Botha W.J., Law I.J. 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. Phyl. Evol. 2008, 48:1131-1144.
91. Stepkowski T., Moulin L., Krzyzańska A., McInnes A., Law I.J., Howieson J. European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl. Environ. Microbiol. 2005, 71:7041-7052.
92. Stepkowski T., Hughes C.E., Law I.J., Markiewicz L., Gurda D., Chlebicka A., Moulin L. Diversification of lupin Bradyrhizobium strains: evidence from nodulation gene trees. Appl. Environ. Microbiol. 2007, 73:3254-3264.
93. Stepkowski T., zak M., Moulin L., Króliczak J., Golińska B., Narozna D., Safronova V.I., Madrzak C.J. Bradyrhizobium canariense and Bradyrhizobium japonicum are the two dominant rhizobium species in root nodules of lupin and serradella plants growing in Europe. Syst. Appl. Microbiol. 2011, 34:368-375.
94. Suenaga H. Targeted metagenomics: a high-resolution metagenomics approach for specific gene clusters in complex microbial communities. Environ. Microbiol. 2012, 14:13-22.
95. Sullivan J.T., Ronson C.W. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci. USA 1998, 95:5145-5149.
96. Sy A., Giraud E., Jourand P., Garcia N., Willems A., de Lajudie P., Prin Y., Neyra M., Gillis M., Boivin-Masson C., Dreyfus B. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 2001, 183:214-220.
97. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Some Mathematical Questions in Biology - DNA Sequence Analysis 1986, 57-86. Amer. Math. Soc, Providence, RI. R.M. Miura (Ed.).
98. Valverde A., Velazquez E., Fernandez-Santos F., Vizcaino N., Rivas R., Mateos P.F., Martinez-Molina E., Igual J.M., Willems A. Phyllobacterium trifolii sp nov., nodulating Trifolium and Lupinus in Spanish soils. Int. J. Syst. Evol. Microbiol. 2005, 55:1985-1989.
99. Vincent J.M. A Manual for the Practical Study of Root-Nodule Bacteria 1970, Blackwell Scientific Publications, Ltd., Oxford.
100. 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 genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies α and Bradyrhizobium genospecies β. Int. J. Syst. Evol. Microbiol. 2005, 55:569-575.
101. Vinuesa P., Silva C., Werner D., Martinez-Romero E. Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol. Phyl. Evol. 2005, 34:29-54.
102. Vinuesa P., Rojas-Jiménez K., Contreras-Moreira B., Mahnam S.K., Prasad B.N., Moe H., Selvaraju S.B., Thierfelder H., Werner D. 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. 2008, 74:6987-6996.
103. Whitaker R.J., Grogan D.W., Taylor J.W. Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 2003, 301:976-978.
104. Willems A., Coopman R., Gillis M. Comparison of sequence analysis of 16S-23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium. Syst. Appl. Microbiol. 2001, 51:623-632.
105. Willems A., Coopman R., Gillis M. Phylogenetic and DNA-DNA hybridization analyses of Bradyrhizobium species. Int. J. Syst. Evol. Microbiol. 2001, 51:111-117.
106. Xu L.M., Ge C., Cui Z., Li J., Fan H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybean. Int. J. Syst. Bacteriol. 1995, 45:706-711.
107. Yao Z.Y., Kan F.L., Wang E.T., Wei G.H., Chen W.X. Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int. J. Syst. Evol. Microbiol. 2002, 52:2219-2230.
108. Zhang Y.F., Wang E.T., Tian C.F., Wang F.Q., Han L.L., Chen W.F., Chen W.X. Bradyrhizobium elkanii, Bradyrhizobium yuanmingense and Bradyrhizobium japonicum are the main rhizobia associated with Vigna unguiculata and Vigna radiata in the subtropical region of China. FEMS Microbiol. Lett. 2008, 285:146-154.