Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia

Systematic and Applied Microbiology

Volumn 35, Issue 2, 2012, Pages 120-131

  Aserse, Aregu Amsalu ^a,b   Räsänen, Leena A ^a   Assefa, Fassil ^b   Hailemariam, Asfaw ^c   Lindström, Kristina ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b ADDIS ABABA UNIVERSITY   (Ethiopia)

^c Ministry of Agriculture Ethiopia   (Ethiopia)

Author keywords

AFLP; Diversity; MLSA; Phaseolus vulgaris; Phylogeny; Rhizobium

Indexed keywords

RNA 16S; RNA POLYMERASE BETA SUBUNIT;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ETHIOPIA; GENE; GENE SEQUENCE; GENETIC VARIABILITY; GLNII GENE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHASEOLUS VULGARIS; PHYLOGENY; PRIORITY JOURNAL; RECA GENE; RHIZOBIACEAE; RHIZOBIUM ETLI; RHIZOBIUM GIARDINII; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM PHASEOLI; RHIZOBIUM RADIOBACTER;

AGROBACTERIUM TUMEFACIENS; PHASEOLUS VULGARIS; RADIOBACTER; RHIZOBIUM; RHIZOBIUM ETLI; RHIZOBIUM GIARDINII; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM PHASEOLI;

EID: 84856688649     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2011.11.005     Document Type: Article

References (81)

1. Amann R.I., Lin C.H., Key R., Montgomery L., Stahl D.A. Diversity among fibrobacter strains: towards a phylogenetic classification. Syst. Appl. Microbiol. 1992, 15:23-32.
2. Amarger N., Macheret V., Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int. J. Syst. Bacteriol. 1997, 47:996-1006.
3. Anderson J.M., Ingram J.S.I. Tropical soil biology and fertility: A handbook of methods 1993, CAB International, Wallingford, UK.
4. Anyango B., Wilson K.J., Beynon J.L., Giller K.E. Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Appl. Environ. Microbiol. 1995, 61:4016-4021.
5. Assefa T., Assefa H., Kimani P. Development of improved haricot bean germplasm for the mid and low-altitude sub-humid agroecologies of Ethiopia. Workshop on food and forage legumes of Ethiopia 2006, 87-94. ICARDA, Aleppo, Syria. K. Ali, S. Ahmed, S. Beniwal, G. Kenneni, S.M. Rajandra, K. Makkouk (Eds.).
6. Bailly X., Olivieri I., De Mita S., Cleyet-Marel J.C., Bena G. Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago. Mol. Ecol. 2006, 15:2719-2734.
7. Beyene B., Tsige A. Conserving microorganisms in the soil. Soil science research in Ethiopia. Proceedings of the first soil science research review workshop 1986.
8. Beyene D. The state of research on biological nitrogen fixation in Ethiopia. Biological nitrogen fixation in Africa 1985, 72-84. Matianum, Nairobi. H. Ssali, S.O. Keya (Eds.).
9. Beyene D., Kassa S., Ampy F., Asseffa A., Gebremedhin T., van Berkum P. Ethiopian soils harbor natural populations of rhizobia that form symbioses with common bean (Phaseolus vulgaris L.). Arch. Microbiol. 2004, 181:129-136.
10. Boudon S., Manceau C., Nottéghem J.L. Structure and origin of Xanthomonas arboricola pv. pruni populations causing bacterial spot of stone fruit trees in Western Europe. Phytopathology 2005, 95:1081-1088.
11. Broughton W.J., Hernandez G., Blair M., Beebe S., Gepts P., Vanderleyden J. Beans (Phaseolus spp.): model food legumes. Plant Soil 2003, 252:55-128.
12. Charles L., Carbone I., Davies K.G., Bird D., Burke M., Kerry B.R., Opperman C.H. Phylogenetic analysis of Pasteuria penetrans by use of multiple genetic loci. J. Bacteriol. 2005, 187:5700-5708.
13. Dawit T., Asfaw T., Geletu B. Genetic resources in Ethiopia. Cool-season food legumes of Ethiopia. Proceeding of the first national cool-season food legumes review conference 1994, 79-96. ICARDA/IAR, ICARDA, Syria. T. Asfaw, B. Geletu, M.C. Saxena, M.B. Solh (Eds.).
14. Degefu T., Wolde-meskel E., Frostegård A. Multilocus sequence analyses reveal several unnamed Mesorhizobium genospecies nodulating Acacia species and Sesbania sesban trees in Southern regions of Ethiopia. Syst. Appl. Microbiol. 2011, 34:216-226.
15. Diouf A., de Lajudie P., Neyra M., Kersters K., Gillis M., Martínez-Romero E., Gueye M. Polyphasic characterization of rhizobia that nodulate Phaseolus vulgaris in West Africa (Senegal and Gambia). Int. J. Syst. Evol. Microbiol. 2000, 50:159-170.
16. Dowton M., Austin A.D. Increased congruence does not necessarily indicate increased phylogenetic accuracy the behavior of the incongruence length difference test in mixed-model analyses. Syst. Biol. 2002, 51:19-31.
17. Ferris, S., Kaganzi, E. (2008) Evaluating market opportunities for haricot beans in Ethiopia. IPMS (Improving Marketing Success) of Ethiopian farmers Project working paper 7, ILRI (international Livestock Research Institute). Nairobi, Kenya, p. 68.
18. Gao J., Terefework Z., Chen W., Lindström L. Genetic diversity of rhizobia isolated from Astragalusadsurgens growing in different geographical regions of China. J. Biotechnol. 2001, 91:155-168.
19. Gaunt M.W., Turner S.L., Rigottier-Gois L., Lloyd-Macgilp S.A., Young J.P. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 2001, 51:2037-2048.
20. Gepts P., Debouck D. Origin, domestication and evolution of the common bean (Phaseolus vulgaris L.). Common beans, research for crop improvement. 1991, 7-53. CAB, Wallingford, UK, Cali-Colombia. A. van Schoonhoven, O. Voysest (Eds.).
21. Germano M.G., Menna P., Mostasso F.L., Hungria M. RFLP analysis of the RNA operon of a Brazilian collection of bradyrhizobial strains from thirty-three legume species. Int. J. Syst. Evol. Microbiol. 2006, 56:217-229.
22. Hailu M., Abebe D., Abebe T. Pulse crops of Ethiopia. Plant genetic resources of Ethiopia 1991, 328-343. Cambridge University Press. J.M.M. Engels, J.G. Hawkes, Melaku Worede (Eds.).
23. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 2004, 41:95-98.
24. Han T.X., Wang E.T., Wu L.J., Chen W.F., Gu J.G., Gu C.T., Tian C.F., Chen W.X. Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang China. Int. J. Syst. Evol. Microbiol. 2008, 58:1693-1699.
25. Haukka K., Lindström K., Young J.P.W. Diversity of partial 16S rRNA sequences among and within strains of African rhizobia isolated from Acacia and Prosopis. Syst. Appl. Microbiol. 1996, 19:352-359.
26. Huys G., Coopman R., Janssen P., Kersters K. High-resolution genotypic analysis of the genus Aeromonas by AFLP fingerprinting. Int. J. Syst. Bacteriol. 1996, 4:572-580.
27. Jordan D.C. Rhizobiaceae. Bergey's manual of systematic bacteriology 1984, 234-244. Williams Wilkins, Baltimore, USA. N.R. Krieg, J.R. Holt (Eds.).
28. Kaplan L. Archeology and domestication in American Phaseolus (beans). Econ. Bot. 1965, 19:358-368.
29. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16:111-120.
30. Konstantinidis K.T., Ramette A., Tiedje J.M. Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl. Environ. Microbiol. 2006, 72:7286-7293.
31. Laguerre G., Nour S.M., Macheret V., Sanjuan J., Drouin P., Amarger N. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 2001, 147:981-993.
32. Li L., Sinkko H., Montonen L., Wei G., Lindström K., Räsänen A.L. Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol. Ecol. 2011, Published online 17 October 2011. 10.1111/j.1574-6941.2011.01198.x.
33. Lindström K., Gyllenberg H.G. The species paradigm in bacteriology: proposal for a cross-disciplinary species concept. World Federation for Culture Collections Newsletter 2006, 42:4-13.
34. Lindström K., Sarsa M.L., Polkunen J.P. Symbiotic nitrogen fixation of Rhizobium (Galega) in acid soils, and its survival in soil under acid and cold stress. Plant Soil 1985, 87:293-302.
35. Lindström K., Young J.P.W. International Committee on systematics of prokaryotes subcommittee on the taxonomy of Agrobacterium and Rhizobium. Minutes of the meeting, 7 September 2010, Geneva, Switzerland. Int. J. Syst. Evol. Microbiol. 2011, 61:3089-3093.
36. Martens M., Dawyndt P., Coopman R., Gillis M., Vos P.D., Willems A. Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int. J. Syst. Evol. Microbiol. 2008, 58:200-214.
37. Martens M., Delaere M., Coopman R., De Vos P., Gillis M., Willems A. Multilocus sequence analysis of Ensifer and related taxa. Int. J. Syst. Evol. Microbiol. 2007, 57:489-503.
38. Martínez-Romero E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 2003, 252:11-23.
39. Martínez-Romero E., Palacios R. The Rhizobium genome. Crit. Rev. Plant. Sci. 1990, 9:17-29.
40. Martínez-Romero E., Pardo M.A., Palacios R., Cevallos M.A. Reiteration of nitrogen fixation gene sequences and specificity to Rhizobium in nodulation and nitrogen fixation in Phaseolus vulgaris. J. Gen. Microbiol. 1985, 131:1779-1786.
41. Martínez-Romero E., Segovia L., Mercante F.M., Franco A.A., Graham P., Pardo M.A. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 1991, 41:417-426.
42. 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. Int. J. Syst. Evol. Microbiol. 2010, 60:664-674.
43. Mhamdi R., Mrabet M., Laguerre G., Tiwari R., Elarbi Aouani M. Colonization of Phaseolus vulgaris nodules by Agrobacterium-like strains. Can. J. Microbiol. 2005, 51:105-111.
44. 2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 2007, 187(1):79-85.
45. Nzoué A., Miché L., Klonowska A., Laguerre G., de Lajudie P., Moulin L. Multilocus sequence analysis of bradyrhizobia isolated from Aeschynomene species in senegal. Syst. Appl. Microbiol. 2009, 32:400-412.
46. Peng G.X., Tan Z.Y., Wang E.T., Reinhold-Hurek B., Chen W.F., Chen W.X. Identification of isolates from soybean nodules in Xinjiang Region as Sinorhizobium xinjiangense and genetic differentiation of S. xinjiangense from Sinorhizobium fredii. Int. J. Syst. Evol. Microbiol. 2002, 52:457-462.
47. Pérez-Ramírez N.O., Rogel M.A., Wang E.T., Castellanos J.Z., Martínez-Romero E. Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol. Ecol. 1998, 26:289-296.
48. Perret X., Staehelin C., Broughton W.J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 2000, 64:180-201.
49. Portier P., Saux M.F.L., Mougel C., Lerondelle C., Chapulliot D., Thioulouse J., Nesme X. Identification of genomic species in Agrobacterium biovar 1 by AFLP genomic markers. Appl. Environ. Microbiol. 2006, 72(11):7123-7131.
50. Poupot R., Martinez-Romero E., Gautier N., Prome J.C. Wild type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors. J. Biol. Chem. 1995, 270:6050-6055.
51. Poupot R., Martinez-Romero E., Promé J.C. Nodulation factors from Rhizobium tropici are sulfated or non-sulfated chitopentasaccharides containing an N-methyl-N-acylglucosamine terminus. Biochemistry 1993, 32:10430-10435.
52. Rademaker J.L.W., Hoste B., Louws F.J., Kersters K., Swings J., Vauterin L., Vauterin P., de Bruijn F.J. Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system. Int. J. Syst. Evol. Microbiol. 2000, 50:665-677.
53. Ribeiro R.A., Barcellos Fe.G., Thompson F.L., Hungria M. Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Res. Microbiol. 2009, 160(4):297-306.
54. Ribeiro R.A., Rogel M.A., López-López A., Ormeño-Orrillo E., Barcellos F.G., Martínez J., Thompson F.L., Martínez-Romero E., Hungria M. Reclassification of Rhizobium tropici type A strains as 1 Rhizobium leucaenae sp. nov. Int. J. Syst. Evol. Microbiol. 2011, Published July 8, 2011. 10.1099/ijs.0.032912-0.
55. Rivas R., Martens M., de Lajudie P., Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2009, 32(2):101-110.
56. Rivas R., Velázquez E., Willems A., Vizcaino N., Subba-Rao N.S., Mateos P.F., Gillis M., Dazzo F.B., Martínez-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.
57. Rogel M.A., Ormerino-Orrillo E., Martinez-Romero E. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst. Appl. Microbiol. 2011, 34:96-104.
58. Rosselló-Mora R. DNA-DNA reassociation methods applied to microbial taxonomy and their critical evaluation. Molecular identification, systematics, and population structure of prokaryotes 2006, 23-50. Springer, Heidelberg. E. Stackebrandt (Ed.).
59. 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 Microbiol. Ecol. 2005, 54:1-11.
60. Segovia L., Young J.P.W., Martinez-Romero E. Reclassification of American Rhizobium leguminasorum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 1993, 43:374-377.
61. Seishiro A., Tetsuya K., Danielle P., Sayuri N., Tadashi K., Motomi I. Genotypic and phenotypic diversity of rhizobia isolated from Lathyrus japonicus indigenous to Japan. Syst. Appl. Microbiol. 2010, 33(7):383-397.
62. Singh S.P. Integrated genetic improvement. Common bean improvement in the twenty first century. Developments in plant breeding 1999, vol. 7:133-165. Kluwer Academic Publishers, Dordrecht.
63. Somasegaran P., Hoben H.J. Handbook for rhizobia: Methods in legume Rhizobium technology 1994, Springer-Verlag, New York, p. 450.
64. Stackebrandt E., Frederiksen W., Garrity G.M., Grimont P.A., Kämpfer P., Maiden M.C.J., Nesme X., Rosselló-Mora R., Swings J. Report of the ad hoc committee for the reevaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 2002, 52:1043-1047.
65. Staden R., Beal K.F., Bonfield J.K. The Staden package. Methods Mol. Biol. 1998, 132:115-130.
66. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Mol. Biol. 2011, 28:2731-2739.
67. Terefework Z., Kaijalainen S., Lindström K. AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega officinalis. J. Biotechnol. 2001, 91(2-3):169-180.
68. Turner S.L., Young J.P.W. The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol. Biol. Evol. 2000, 17:309-319.
69. van Berkum P., Terefework Z., Paulin L., Suomalainen S., Lindström K., Eardly B.D. Discordant phylogenies within the rrn loci of rhizobia. J. Bacteriol. 2003, 185:2988-2998.
70. Vincent J.M. A manual for the practical study of root nodule bacteria. IBP Handbook No. 15 1970, Black Well Scientific Publications, Oxford, p. 164.
71. Vinuesa P., Rojas-Jimenez K., Contreras-Moreira B., Mahna S.K., Prasad B.N., Moe H., Salvaraju S.B., Thierfelder H., Werner D. Multilocus sequence analysis of 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.
72. Vinuesa P., Silva C., Lorite M.J., Izaguirre-Mayoral M.L., Bedmar E.J., Martínez-Romero E. Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst. Appl. Microbiol. 2005, 28:702-716.
73. Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995, 23:4407-4414.
74. Wei G.H., Wang E.T., Tan Z.Y., Zhu M.E., Chen W.X. Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int. J. Syst. Evol. Microbiol. 2002, 52:2231-2239.
75. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 1991, 17:697-703.
76. Willems A., Doignon-Bourcier F., Coopman R., Hoste B., de Lajudie P., Gillis M. AFLP finngerprint analysis of Bradyrhizobium strains isolated from Faidherbia albida and Aeschynomene species. Syst. Appl. Microbiol. 2000, 23:137-147.
77. Wolde-meskel E., Berg T., Peters N.K., Frostegård å. Nodulation status of native woody legumes and phenotypic characteristics of associated rhizobia in soils of southern Ethiopia. Biol. Fert. Soils 2004, 40(1):55-66.
78. World Bank (2006) National fertilizer sector project: Implementation completion report Africa Region. The World Bank, Washington, D.C.
79. Wortmann C.S., Kirkby R.A., Elude C.A., Allen D.J. Atlas of common bean (Phaseolus vulgaris L.) production in Africa. CIAT Publication, 297 1998, 133.
80. Xia X., Xie Z. DAMBE: software package for data analysis in molecular biology and evolution. J. Hered. 2001, 92:371-373.
81. Xia X., Xie Z., Salemi M., Chen L., Wang Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 2003, 26:1-7.