Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium)

Soil Biology and Biochemistry

Volumn 43, Issue 12, 2011, Pages 2384-2396

  De Meyer, Sofie E ^a   Van Hoorde, Koenraad ^a,b   Vekeman, Bram ^a   Braeckman, Tamara ^a   Willems, Anne ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY COLLEGE GHENT   (Belgium)

Author keywords

Belgium; Bradyrhizobium; Ensifer; Flanders; Indigenous legumes; Mesorhizobium; Rhizobia; Rhizobium; Root nodules; Symbiotic genes nodC and nifH

Indexed keywords

BELGIUM; BRADYRHIZOBIUM; ENSIFER; FLANDERS; INDIGENOUS LEGUMES; MESORHIZOBIUM; RHIZOBIA; RHIZOBIUM; ROOT NODULES; SYMBIOTIC GENES NODC AND NIFH;

AMINO ACIDS; BACTERIA; BACTERIOLOGY; RNA;

GENES;

BACTERIUM; CLUSTER ANALYSIS; CORRELATION; GENE EXPRESSION; GENETIC DIFFERENTIATION; HOST PLANT; HOST-SYMBIONT INTERACTION; INVASIVE SPECIES; LEGUME; OPTIMIZATION; PHYLOGENETICS; POLYMERASE CHAIN REACTION; RHIZOBACTERIUM; SPECIES DIVERSITY; SYMBIOSIS; VARIANCE ANALYSIS;

BELGIUM; FLANDERS;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM; ENSIFER; MESORHIZOBIUM; ONONIS; RHIZOBIACEAE; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM; RHODOPSEUDOMONAS; ROBINIA; SINORHIZOBIUM; WISTERIA;

EID: 80052527285     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2011.08.005     Document Type: Article

References (90)

1. Alvarez-Martinez E.R., Valverde A., Ramirez-Bahena M.H., Garcia-Fraile P., Tejedor C., Mateos P.F., Santillana N., Zuniga D., Peix A., Velazquez E. 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. Archives of Microbiology 2009, 191:659-668.
2. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 2009, 161:105-121. APGIII.
3. Ba S., Willems A., De Lajudie P., Roche P., Jeder H., Quatrini P., Neyra M., Ferro M., Prome J.C., Gillis M., Boivin-Masson C., Lorquin J. Symbiotic and taxonomic diversity of rhizobia isolated from Acacia tortilis subsp. raddiana in Africa. Systematic and Applied Microbiology 2002, 25:130-145.
4. Baele M., Baele P., Vaneechoutte M., Storms V., Butaye P., Devriese L.A., Verschraegen G., Gillis M., Haesebrouck F. Application of tRNA intergenic spacer PCR for identification of Enterococcus species. Journal of Clinical Microbiology 2000, 38:4201-4207.
5. Bailly X., Olivieri I., Brunel B., Cleyet-Marel J.C., Bena G. Horizontal gene transfer and homologous recombination drive the evolution of the nitrogen-fixing symbionts of Medicago species. Journal of Bacteriology 2007, 189:5223-5236.
6. Boivin C., Ndoye I., Lortet G., Ndiaye A., De Lajudie P., Dreyfus B. The Sesbania root symbionts Sinorhizobium saheli and S. teranga bv. sesbaniae can form stem nodules on Sesbania rostrata, although they are less adapted to stem nodulation than Azorhizobium caulinodans. Applied and Environmental Microbiology 1997, 63:1040-1047.
7. Bottomley P.J., Cheng H.H., Strain S.R. Genetic structure and symbiotic characteristics of a Bradyrhizobium population recovered from a pasture soil. Applied and Environmental Microbiology 1994, 60:1754-1761.
8. Bromfield E.S.P., Tambong J.T., Cloutier S., Prevost D., Laguerre G., van Berkum P., Thi T.V.T., Assabgui R., Barran L.R. 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 2010, 156:505-520.
9. Chen W.M., de Faria S.M., Straliotto R., Pitard R.M., Simoes-Araujo J.L., Chou J.F., Chou Y.J., Barrios E., Prescott A.R., Elliott G.N., Sprent J.I., Young J.P.W., James E.K. Proof that Burkholderia strains form effective symbioses with legumes: a study of novel mimosa-nodulating strains from South America. Applied and Environmental Microbiology 2005, 71:7461-7471.
10. 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. Journal of Bacteriology 2003, 185:7266-7272.
11. Cooper J.E. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. Journal of Applied Microbiology 2007, 103:1355-1365.
12. Dedysh S.N., Ricke P., Liesack W. NifH and NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria. Microbiology-SGM 2004, 150:1301-1313.
13. Deng Z.S., Zhao L.F., Kong Z.Y., Yang W.Q., Lindström K., Wang E.T., Wei G.H. Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiology Ecology 2011, 76:463-475.
14. Depret G., Laguerre G. Plant phenology and genetic variability in root and nodule development strongly influence genetic structuring of Rhizobium leguminosarum biovar viciae populations nodulating pea. New Phytologist 2008, 179:224-235.
15. Diouf D., Fall D., Chantreuil C., Ba A.T., Dreyfus B., Neyra M., Ndoye I., Moulin L. Phylogenetic analyses of symbiotic genes and characterization of functional traits of Mesorhizobium spp. strains associated with the promiscuous species Acacia seyal Del. Journal of Applied Microbiology 2010, 108:818-830.
16. Dobert R.C., Brei B.T., Triplett E.W. DNA-sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Molecular Plant-Microbe Interactions 1994, 7:564-572.
17. Downie J.A. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiology Reviews 2010, 34:150-170.
18. Dresler-Nurmi A., Fewer D.P., Räsänen L.A., Lindström K. The diversity and evolution of rhizobia. Microbiology Monographs 2007.
19. Eardly B.D., Young J.P.W., Selander R.K. Phylogenetic position of Rhizobium sp strain or-191, a symbiont of both Medicago sativa and Phaseolus vulgaris, based on partial sequences of the 16s ribosomal-RNA and nifH genes. Applied and Environmental Microbiology 1992, 58:1809-1815.
20. Estrella M.J., Munoz S., Soto M.J., Ruiz O., Sanjuan J. Genetic diversity and host range of rhizobia nodulating Lotus tenuis in typical soils of the Salado river basin (Argentina). Applied and Environmental Microbiology 2009, 75:1088-1098.
21. Farida B., Géraldine D., Abdelghani B., Djellali B., Said B., Gisèle L. Retama species growing in different ecological-climatic areas of northeastern Algeria have a narrow range of rhizobia that form a novel phylogenetic clade within the Bradyrhizobium genus. Systematic and Applied Microbiology 2009, 32:245-255.
22. Flores M., Gonzalez V., Pardo M.A., Leija A., Martinez E., Romero D., Pinero D., Davila G., Palacios R. Genomic instability in Rhizobium phaseoli. Journal of Bacteriology 1988, 170:1191-1196.
23. Fred E.B., Baldwin I.L., McCoy E. Root Nodule Bacteria and Leguminous Plants 1932, University of Wisconsin Press, Madison.
24. Freitas A.D.S., Sampaio E., Santos C., Fernandes A.R. Biological nitrogen fixation in tree legumes of the Brazilian semi-arid caatinga. Journal of Arid Environments 2010, 74:344-349.
25. Gaunt M.W., Turner S.L., Rigottier-Gois L., Lloyd-Macgilp S.A., Young J.P.W. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. International Journal of Systematic and Evolutionary Microbiology 2001, 51:2037-2048.
26. Gevers D., Huys G., Swings J. Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiology Letters 2001, 205:31-36.
27. Han T.X., Han L.L., Wu L.J., Chen W.F., Sui X.H., Gu J.G., Wang E.T., Chen W.X. Mesorhizobium gobiense sp. nov. and Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China. International Journal of Systematic and Evolutionary Microbiology 2008, 58:2610-2618.
28. Haukka K., Lindström K., Young J.P.W. Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Applied and Environmental Microbiology 1998, 64:419-426.
29. Hou B.C., Wang E.T., Li Y., Jia R.Z., Chen W.F., Man C.X., Sui X.H., Chen W.X. Rhizobial resource associated with epidemic legumes in Tibet. Microbial Ecology 2009, 57:69-81.
30. Howieson J.G., O'Hara G.W., Carr S.J. Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crops Research 2000, 65:107-122.
31. Hynes M.F., Oconnell M.P. Host plant effect on competition among strains of Rhizobium leguminosarum. Canadian Journal of Microbiology 1990, 36:864-869.
32. Ibáñez F., Angelini J., Taurian T., Tonelli M.L., Fabra A. Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. Systematic and Applied Microbiology 2009, 32:49-55.
33. 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. Genetic diversity of Bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Systematic and Applied Microbiology 2003, 26:611-623.
34. Jarvis B.D.W., VanBerkum P., Chen W.X., Nour S.M., Fernandez M.P., CleyetMarel J.C., Gillis M. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. International Journal of Systematic Bacteriology 1997, 47:895-898.
35. Kan F.L., Chen Z.Y., Wang E.T., Tian C.F., Sui X.H., Chen W.X. Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Archives of Microbiology 2007, 188:103-115.
36. Lafay B., Burdon J.J. Molecular diversity of rhizobia nodulating the invasive legume Cytisus scoparius in Australia. Journal of Applied Microbiology 2006, 100:1228-1238.
37. Lambinon J., Langhe J.D., Delvosalle L., Duvigneaud J. Flora van België, het Groothertogdom Luxemburg, Noord-Frankrijk en de Aangrenzende Gebieden, Derde ruk ed 1998, De Nationale Plantentuin van België, Meise.
38. Lorite M.J., Donate-Correa J., del Arco-Aguilar M., Galdona R.P., Sanjuan J., Leon-Barrios M. Lotus endemic to the Canary Islands are nodulated by diverse and novel rhizobial species and symbiotypes. Systematic and Applied Microbiology 2010, 33:282-290.
39. Maâtallah J., Berraho E.B., Muñoz S., Sanjuan J., Lluch C. Phenotypic and molecular characterization of chickpea rhizobia isolated from different areas of Morocco. Journal of Applied Microbiology 2002, 93:531-540.
40. Martens M., Delaere M., Coopman R., De Vos P., Gillis M., Willems A. Multilocus sequence analysis of Ensifer and related taxa. International Journal of Systematic and Evolutionary Microbiology 2007, 57:489-503.
41. Masson-Boivin C., Giraud E., Perret X., Batut J. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?. Trends in Microbiology 2009, 17:458-466.
42. Menna P., Barcellos F.G., Hungria M. 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. International Journal of Systematic and Evolutionary Microbiology 2009, 59:2934-2950.
43. Merabet C., Martens M., Mahdhi M., Zakhia F., Sy A., Le Roux C., Domergue O., Coopman R., Bekki A., Mars M., Willems A., de Lajudie P. Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov. International Journal of Systematic and Evolutionary Microbiology 2010, 60:664-674.
44. Mergaert P., Van Montagu M., Holsters M. Molecular mechanisms of Nod factor diversity. Molecular Microbiology 1997, 25:811-817.
45. Mierzwa B., Wdowiak-Wrobel S., Kalita M., Gnat S., Malek W. Insight into the evolutionary history of symbiotic genes of Robinia pseudoacacia rhizobia deriving from Poland and Japan. Archives of Microbiology 2010, 192:341-350.
46. Mierzwa B., Wdowiak-Wrobel S., Maek W. Phenotypic, genomic and phylogenetic characteristics of rhizobia isolated from root nodules of Robinia pseudoacacia (black locust) growing in Poland and Japan. Archives of Microbiology 2009, 191:697-710.
47. Mierzwa B., Wdowiak-Wrobel S., Malek W. Robinia pseudoacacia in Poland and Japan is nodulated by Mesorhizobium amorphae strains. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2010, 97:351-361.
48. Mnasri B., Badri Y., Saidi S., de Lajudie P., Mhamdi R. Symbiotic diversity of Ensifer meliloti strains recovered from various legume species in Tunisia. Systematic and Applied Microbiology 2009, 32:583-592.
49. 2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Archives of Microbiology 2007, 187:79-85.
50. Moulin L., Bena G., Boivin-Masson C., Stepkowski T. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Molecular Phylogenetics and Evolution 2004, 30:720-732.
51. Muresu R., Maddau G., Delogu G., Cappuccinelli P., Squartini A. Bacteria colonizing root nodules of wild legumes exhibit virulence-associated properties of mammalian pathogens. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2010, 97:143-153.
52. Mutch L.A., Young J.P.W. Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Molecular Ecology 2004, 13:2435-2444.
53. Palaniappan P., Chauhan P.S., Saravanan V.S., Anandham R., Sa T.M. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biology and Fertility of Soils 2010, 46:807-816.
54. Pankhurst C.E., Craig A.S., Jones W.T. Effectiveness of Lotus root-nodules. 1. Morphology and flavolan content of nodules formed on Lotus pedunculatus by fast-growing Lotus rhizobia. Journal of Experimental Botany 1979, 30:1085-1093.
55. Pearson W.R. Rapid and sensitive sequence comparison with Fastp and Fasta. Methods in Enzymology 1990, 183:63-98.
56. Perez-Fernandez M.A., Lamont B.B. Nodulation and performance of exotic and native legumes in Australian soils. Australian Journal of Botany 2003, 51:543-553.
57. Perret X., Staehelin C., Broughton W.J. Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews 2000, 64:180-201.
58. Radeva G., Jurgens G., Niemi M., Nick G., Suominen L., Lindström K. Description of two biovars in the Rhizobium galegae species: biovar orientalis and biovar officinalis. Systematic and Applied Microbiology 2001, 24:192-205.
59. Ramirez-Bahena M.H., Velazquez E., Fernandez-Santos F., Peix A., Martinez-Molina E., Mateos P.F. Phenotypic, genotypic, and symbiotic diversities in strains nodulating clover in different soils in Spain. Canadian Journal of Microbiology 2009, 55:1207-1216.
60. Raymond J., Siefert J.L., Staples C.R., Blankenship R.E. The natural history of nitrogen fixation. Molecular Biology and Evolution 2004, 21:541-554.
61. Rincon A., Arenal F., Gonzalez I., Manrique E., Lucas M.M., Pueyo J.J. Diversity of rhizobial bacteria isolated from nodules of the gypsophyte Ononis tridentata L. growing in spanish soils. Microbial Ecology 2008, 56:223-233.
62. Rivas R., Martens M., de Lajudie P., Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Systematic and Applied Microbiology 2009, 32:101-110.
63. Rogel M.A., Ormeño-Orrillo E., Martinez Romero E. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Systematic and Applied Microbiology 2011, 34:96-104.
64. Sajnaga E., Malek W., Lotocka B., Stepkowski T., Legocki A. The root-nodule symbiosis between Sarothamnus scoparius L. and its microsymbionts. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2001, 79:385-391.
65. Sarita S., Sharma P.K., Priefer U.B., Prell J. Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiology Ecology 2005, 54:1-11.
66. 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. Molecular Phylogenetics and Evolution 2008, 48:1131-1144.
67. Suominen L., Roos C., Lortet G., Paulin L., Lindström K. Identification and structure of the Rhizobium galegae common nodulation genes: evidence for horizontal gene transfer. Molecular Biology and Evolution 2001, 18:907-916.
68. 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. Journal of Bacteriology 2001, 183:214-220.
69. Tamura, K., Peterson, D., Peterson, N., Stecher G., Nei, M., Kumar, S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parismony methods. Molecular Biology and Evolution, Advance Access published May 4, 2011. doi:10.1093/molbev/msr121.
70. Trujillo M.E., Alonso-Vega P., Rodriguez R., Carro L., Cerda E., Alonso P., Martinez-Molina E. The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. The ISME Journal 2010, 4:1265-1281.
71. Turner S.L., Zhang X.-X., Li F.-D., Young J.P.W. What does a bacterial genome sequence represent? Mis-assignment of MAFF 303099 to the genospecies Mesorhizobium loti. Microbiology 2002, 148:3330-3331.
72. Ulrich A., Zaspel I. Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L. Microbiology-Uk 2000, 146:2997-3005.
73. Van Landuyt W., Hoste I., Vanhecke L., Vercruysse W., Van Den Bremt P., De Beer D. Atlas van de Flora van Vlaanderen en het Brussels Gewest 2006, INBO and Nationale Plantentuin van België, Brussels.
74. Van Landuyt W., Vanhecke L., Hoste I. Rode Lijst van de vaatplanten van Vlaanderen en het Brussels Hoofdstedelijk Gewest. Atlas van de Flora van Vlaanderen en het Brussels Gewest 2006, INBO and Nationale Plantentuin van België, Brussels. W. Van Landuyt, I. Hoste, L. Vanhecke, W. Vercruysse, P. Van Den Bremt, D. De Beer (Eds.).
75. Van Landuyt W., Vanhecke L., Hoste I., Bauwens D. Do the distribution patterns of vascular plant species correspond to biogeographical classifications based on environmental data? A case study from northern Belgium. Landscape and Urban Planning 2011, 99:93-103.
76. Vancanneyt M., Mengaud J., Cleenwerck I., Vanhonacker K., Hoste B., Dawyndt P., Degivry M.C., Ringuet D., Janssens D., Swings J. Reclassification of Lactobacillus kefirgranum Takizawa et al. 1994 as Lactobacillus kefiranofaciens subsp. kefirgranum subsp. nov. and emended description of L-kefiranofaciens Fujisawa, et al. 1988. International Journal of Systematic and Evolutionary Microbiology 2004, 54:551-556.
77. Vandamme P., Goris J., Chen W.M., de Vos P., Willems A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Systematic and Applied Microbiology 2002, 25:507-512.
78. Velazquez E., Valverde A., Rivas R., Gomis V., Peix A., Gantois I., Igual J.M., Leon-Barrios M., Willems A., Mateos P.F., Martinez-Molina E. Strains nodulating Lupinus albus on different continents belong to several new chromosomal and symbiotic lineages within Bradyrhizobium. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2010, 97:363-376.
79. Versalovic J., Schneider M., De Bruijn F.J., Lupski J.R. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cellular Biology 1994, 5:25-40.
80. Villegas M.D., Rome S., Maure L., Domergue O., Gardan L., Bailly X., Cleyet-Marel J.C., Brunel B. Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti. Systematic and Applied Microbiology 2006, 29:526-538.
81. Vincent J.M. A Manual for the Practical Study of the Root-nodule Bacteria 1970, IBP Handbook 15.
82. 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 endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. International Journal of Systematic and Evolutionary Microbiology 2005, 55:569-575.
83. Wdowiak-Wrobel S., Malek W. Following phylogenetic tracks of Astragalus cicer microsymbionts. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2010, 97:21-34.
84. Wei G.H., Chen W.M., Zhu W.F., Chen C., Young J.P.W., Bontemps C. Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiology Ecology 2009, 68:320-328.
85. Weir B.S., Turner S.J., Silvester W.B., Park D.C., Young J.A. Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Applied and Environmental Microbiology 2004, 70:5980-5987.
86. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 16s ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 1991, 173:697-703.
87. Wielbo J., Marek-Kozaczuk M., Mazur A., Kubik-Komar A., Skorupska A. Genetic and metabolic divergence within a Rhizobium leguminosarum bv. trifolii population recovered from clover nodules. Applied and Environmental Microbiology 2010, 76:4593-4600.
88. Willems A. The taxonomy of rhizobia: an overview. Plant and Soil 2006, 287:3-14.
89. Willems A., Collins M.D. Phylogenetic analysis of rhizobia and agrobacteria based on 16s ribosomal-RNA gene sequences. International Journal of Systematic Bacteriology 1993, 43:305-313.
90. Zakhia F.R., Jeder H., Domergue O., Willems A., Cleyet-Marel J.C., Gillis M., Dreyfus B., de Lajudie P. Characterisation of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Systematic and Applied Microbiology 2004, 27:380-395.