Eco-geographical diversity of cowpea bradyrhizobia in Senegal is marked by dominance of two genetic types

Systematic and Applied Microbiology

Volumn 37, Issue 2, 2014, Pages 129-139

  Wade, Tatiana Krasova ^a   Le Quéré, Antoine ^b   Laguerre, Gisèle ^c   N'Zoué, Angèle ^b   Ndione, Jacques André ^d   doRego, Francis ^a   Sadio, Omar ^e   Ndoye, Ibrahima ^a   Neyra, Marc ^a,b,f  

^a Centre IRD de Bel Air   (Senegal)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^c CIRAD   (France)

^d Third World Forum Dakar   (Senegal)

^e Universite de Bretagne Occidentale   (France)

^f UR MALY   (France)

Author keywords

16S 23S rDNA IGS; Housekeeping genes; Native bradyrhizobia diversity; NifH; NodC; Vigna unguiculata

Indexed keywords

DNA 16S; DNA 23S; RAIN;

ARTICLE; BRADYRHIZOBIUM; BRADYRHIZOBIUM YUANMINGENSE; CHEMICAL PARAMETERS; CONTROLLED STUDY; COWPEA; GENE SEQUENCE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HOUSEKEEPING GENE; HUMIDITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENETICS; PLANT TAXONOMY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SENEGAL; SOIL ACIDITY; SOIL MOISTURE; SOIL PROPERTY; SOIL TEXTURE;

BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; BRADYRHIZOBIUM YUANMINGENSE; VIGNA UNGUICULATA;

16S-23S RDNA IGS; HOUSEKEEPING GENES; NATIVE BRADYRHIZOBIA DIVERSITY; NIFH; NODC; VIGNA UNGUICULATA;

BACTERIAL PROTEINS; BIOTA; BRADYRHIZOBIUM; CULTURE MEDIA; DNA, RIBOSOMAL SPACER; FABACEAE; GENES, ESSENTIAL; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; OSMOTIC PRESSURE; PHYLOGEOGRAPHY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; ROOT NODULES, PLANT; SENEGAL; STRESS, PHYSIOLOGICAL;

EID: 84896736648     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2013.10.002     Document Type: Article

References (68)

1. Allen O.N., Allen E.K. The Leguminosae. A Source Book of Characteristics, Uses, and Nodulation 1981, University of Wisconsin Press, USA.
2. André S., Galiana A., Le Roux C., Prin Y., Neyra M., Duponnois R. Ectomycorrhizal symbiosis enhanced the efficiency of inoculation with two Bradyrhizobium strains and Acacia holosericea growth. Mycorrhiza 2005, 15:357-364.
3. Appunu C., N'Zoué 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. Appunu C., Sasi Rekha N., Prabavathy V.R., Nair S. A significant proportion of indigenous rhizobia from India associated with soybean [Glycine max (L.)] are distinctly belong to Bradyrhizobium and Ensifer genera. Biol. Fertil. Soils 2009, 46:57-63.
5. Appunu C., N'Zoue A., Moulin L., Depret G., Laguerre G. Vigna mungo, V. radiata and V. unguiculata plants sampled in different agronomical-ecological-climatic regions of India are nodulated by Bradyrhizobium yuanmingense. Syst. Appl. Microbiol. 2009, 32:460-470.
6. Appunu C., Ganesan G., Kalita M., Kaushik R., Saranya B., Prabavathy V.R., Sudha N. Phylogenetic diversity of rhizobia associated with horsegram (Macrotyloma uniflorum (Lam.) Verdc.) grown in South India based on glnII, recA and 16S-23S intergenic sequence analyses. Curr. Microbiol. 2011, 62:1230-1238.
7. Bâ A.M., Samba R., Sylla S.N., Le Roux C., Neyra M., Rousteau A., Imbert D., Toribio A. Caractérisation de la diversité des microorganismes symbiotiques de Pterocarpus officinalis dans des forêts marécageuses de Guadeloupe et de Martinique. Rev. Ecol. Terre-Vie 2004, 59:163-170.
8. Borcard D., Buttler A. Ecologie numérique 2001, Université de Montréal et Université de Franche-Comté.
9. Bushby H.V.A., Date R.A., Butler K.L. Rhizobium strain evaluation of Glycine max cv. Davis Vigna mungo cv. Regure and V. unguiculata cv. Caloona for three soils in glasshouse and field experiments. Aust. J. Exp. Agric. Anim. Husb. 1983, 23:43-53.
10. Chahboune R., Carro L., Peix A., Ramírez-Bahena M.H., Barrijal S., Velázquez E., Bedmar E.J. Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst. Appl. Microbiol. 2012, 35(5):302-305.
11. Chang Y.L., Wang E.T., Sui X.H., Zhang X.X., Chen W.X. Molecular diversity and phylogeny of rhizobia associated with Lablab purpureus (Linn.) grown in Southern China. Syst. Appl. Microbiol. 2011, 34(4):276-284.
12. Cissé N., Hall A.E. Traditional Cowpea in Senegal, a Case Study 2003, 27. http://www.fao.org/ag/AGP/AGPC/doc/publicat/cowpea_Cisse/cowpea_cisse_e.htm.
13. Dakora F.D., Keya S.O. Contribution of legume nitrogen fixation to sustainable agriculture in sub-Saharan Africa. Soil Biol. Biochem. 1997, 29:809-817.
14. Delamuta J.R.M., Ribeiro R.A., Ormeño-Orrillo E., Melo I.S., Martínez-Romero E., Hungria M. Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum Group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int. J. Syst. Evol. Microbiol. 2013, 10.1099/ijs.0.049130-0.
15. Depret G., Houot S., Allard M.-R., Breuil M.-C., Nouaïm R., Laguerre G. Long-term effects of crop management on Rhizobium leguminosarum biovar viciae populations. FEMS Microb. Ecol. 2004, 51:87-97.
16. Doignon-Bourcier F., Willems A., Coopman R., Laguerre G., Gillis M., de Lajudie P. Genotypic characterization of Bradyrhizobium strains nodulating small senegalese legumes by 16S-23S rRNA intergenic gene spacers and amplified fragment length polymorphism fingerprint analyses. Appl. Environ. Microbiol. 2000, 66:3987-3997.
17. Jensen M.A., Webster J.A., Straus N. Rapid identification of bacteria on the basis of polymerase chain reaction-amplified ribosomal DNA spacer polymorphism. Appl. Environ. Microbiol. 1993, 59:945-952.
18. Jordan D.C. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov. a genus of slow-growing, root nodules bacteria from leguminous plants. Int. J. Syst. Bacteriol. 1982, 32:136-139.
19. George T., Bohlool B.B., Singleton P.W. Bradyrhizobium japonicum-environment interaction: nodulation and interstrain competition in soils along an elevational transect. Appl. Environ. Microbiol. 1987, 53:1113-1117.
20. 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.
21. Gürtler V., Stanisich A. New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 1996, 142:3-7.
22. Excoffier L., Laval G., Schneider S. Arlequin ver 3.0: an integrated software package for population genetics data analysis. Evol. Bioinforma. Online 2005, 1:47-50.
23. FAO Agricultural Database 2012, http://faostat.fao.org/site/567/default.aspx#ancor (update 02.2012; accessed 08.2012).
24. Fatokun C.A., Boukar O. Gene flow in cowpea: longevity of wild and cultivated cowpea seeds in the field. 5th World Cowpea Research Conference 2010, (Abstract).
25. Kouakou C.K., Macauley H.R., Gueye M.C., Otto M.C., Rami J.F., Cissé N., Pasquet R.S. Diversité génétique des variétés traditionnelles de niébé [Vigna unguiculata (L.) Walp.] au Sénégal: étude préliminaire. Plant Genet. Resour. Newsl. 2007, 152:33-44.
26. Krasova-Wade T., Ndoye I., Braconnier S., Sarr B., de Lajudie P., Neyra M. Diversity of indigeneous bradyrhizobia associated with three cowpea cultivars (Vigna unguiculata (L.) Walp.) grow under limited and favorable water conditions in Senegal (West Africa). Afr. J. Biotechnol. 2003, 2(1):13-22.
27. Krasova Wade T. Etude de la diversité des rhizobiums nodulants le niébé [Vigna unguiculata (L.) Walp.] au Sénégal 2003, Ph.D. Thesis, Department of Vegetal Biology, University of Cheikh Anta Diop, Dakar, Senegal.
28. Krebs C.J. Species diversity measures. Ecological Methodology 1989, 328-370. Harper Collins, New York. C.J. Krebs (Ed.).
29. Lafay B., Burdon J.J. Molecular diversity of rhizobia occurring on native shrubby legumes in Southeastern Australia. Appl. Environ. Microbiol. 1998, 64:3989-3997.
30. 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.
31. Leblond-Bourget N., Decaris B. La séquence de l'Espace Intergenique 16S-23S: méthode rapide et fiable d'identification des souches bactériennes. Bull. Soc. Fr. Microbiol. 1996, 111:7-10.
32. Li Q.Q., Wang E.T., Zhang Y.Z., Zhang Y.M., Tian C.F., Sui X.H., Chen W.F., Chen W.X. Diversity and biogeography of rhizobia isolated from root nodules of Glycine max grown in Hebei province, China. Microbiol. Ecol. 2011, 61:917-931.
33. Lin D.X., Man C.X., Wang E.T., Chen W.X. Diverse rhizobia that nodulate two species of Kummerowia. Arch. Microbiol. 2007, 188:495-507.
34. Martins L.M.V., Neves M.C.P., Rumjanek N.G. Growth characteristics and symbiotic efficiency of rhizobia isolated from cowpea nodules of the north-east region of Brazil. Soil Biol. Biochem. 1997, 29:1005-1010.
35. Menna P., Barcellos F.G., Hungria M. Phylogeny and taxonomy of adverse collection of Bradyrhizobium strain based on multilocus sequence analysis of the 16S rDNA gene ITS region and glnII, recA, atpD and dnaK genes. Int. J. Syst. Evol. Bicrobiol. 2009, 59:2934-2950.
36. Nei M., Kumar S. Molecular Evolution and Phylogenetics 2000, Oxford University Press, New York.
37. Normand P., Cournoyer B., Simonet P., Nazaret S. Analysis of a ribosomal RNA operon in the actinomycete Frankia. Gene 1992, 111:119-124.
38. Normand P., Ponsonnet C., Nesme X., Neyra M., Simonet P. ITS analysis of prokariotes. Mol. Microb. Ecol. Man. 1996, 3.4.5:1-12.
39. N'Zoué 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.
40. Palmer K.M., Young J.P.W. Higher diversity of Rhizobium leguminosarum biovar viciae population in arable soils than in grass soils. Appl. Environ. Microbiol. 2000, 66:2445-2450.
41. Pule-Meulenberg F., Belane A.K., Krasova Wade T., Dakora F.D. Symbiotic functioning and bradyrhizobial biodiversity of cowpea (Vigna unguiculata L. Walp.) in Africa. BMC Microbiol. 2010, 10:89-100.
42. Ramírez-Bahena M.H., Peix A., Rivas R., Camacho M., Rodríguez-Navarro D.N., Mateos P.F., Martínez-Molina E., Willems A., Velázquez E. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int. J. Syst. Evol. Microbiol. 2009, 8:1929-1934.
43. Rivas R., Willems A., Palomo J.L., Garcia-Benavides P., Mateos P.F., Martinez-Molina E., Gillis M., Vélaz E. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumor-like deformations. Int. J. Syst. Evol. Microbiol. 2004, 54:1271-1275.
44. Rivas R., Martens M., de Lajudie P., Willems A. Multilocus sequences analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2009, 32:101-110.
45. Rousk J., Bââth E., Brookes P.C., Lauber C.L., Lozupone C., Caporaso J.G., Knight R., Fierer N. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 2010, 2010:1-12.
46. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
47. Sarr P.S., Yamakawa T., Saeki Y., Guissé A. Phylogenetic diversity of indigenous cowpea bradyrhizobia from soils in Japan based on sequence analysis of the 16S-23S rRNA internal transcribed spacer (ITS). Syst. Appl. Microbiol. 2011, 34:285-292.
48. Singh B.B., Ehlers J.D., Sharma B., Freire Filho F.R. Recent progress in cowpea breeding. Challenges and Opportunities for Enhancing Sustainable Cowpea Production 2002, 22-40. IITA, Ibadan, Nigeria. C.A. Fatokun, S.A. Tarawali, B.B. Singh, P.M. Kormawa, M. Tamo (Eds.).
49. Singh B.B. Short-duration cowpea varieties and intensive cowpea-cereals cropping systems for increased household food security and enhanced family nutrition in the tropics. 5th World Cowpea Research Conference 2010, (Abstract).
50. Sprent J.I. Evolution and diversity in the legume-rhizobium symbiosis: chaos theory?. Plant Soil 1994, 161:1-10.
51. Steenkamp E., Stepkowski T., Przymusiak A., Botha W.J., Law I.J. Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harbouring nodulation genes that belong to the large pan tropical called common in Africa. Mol. Phylogenet. Evol. 2008, 48:1131-1144.
52. Streeter J.G. Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Can. J. Microbiol. 1994, 40:513-522.
53. 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. Evol. 2011, 28:2731-2739.
54. Thies J.E., Bohlool B.B., Singleton P.W. Subgroups of cowpea miscellany: symbiotic specificity within Bradyrhizobium spp. for Vigna unguiculata, Phaseolus lunatus, Arachis hypogaea, and Macroptilium atropurpureum. Appl. Environ. Microbiol. 1991, 57:1540-1545.
55. Thies J.E., Bohlool B.B., Singleton P.W. Environmental effects on competition for nodules occupancy between introduced and indigenous rhizobia and among introduced strains. Can. J. Microbiol. 1992, 38:493-500.
56. van Berkum P., Leibold J.M., Eardly B.D. Proposal for combining Bradyrhizobium spp (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst. Appl. Microbiol. 2006, 29:207-215.
57. Venkateswarlu B., Hari K., Katyal J.C. Influence of soil and crop factors on the native rhizobial populations in soils under dryland farming. Appl. Soil Ecol. 1997, 7:1-10.
58. Vincent J.M. A Manual for the Practical Study of Root-Nodule Bacteria 1970, Blackwell Scientific Publications Ltd., Oxford, UK.
59. Vinuesa P., n-Barrios M.L., Silva C., Willems A., Jarabe-Lorenzo A., Pérez-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 Island, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int. J. Syst. Evol. Microbiol. 2005, 55:569-575.
60. Vinuesa P., Rojas-Jiménez K., Contreras-Moreira B., Mahna S.K., Prasad B.N., Moe H., Selvaraju S.B., Thierfelder H., Werner D. Biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the Asiatic continent, assessed by multilocus sequence analysis. Appl. Environ. Microbiol. 2008, 74:6987-6996.
61. Wang R., Chang Y.L., Zheng W.T., Zhang D., Zhang X.X., Sui X.H., Wang E.T., Hu J.Q., Zhang L.Y., Chen W.X. Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst. Appl. Microbiol. 2013, 36(2):101-105.
62. Willems A., Doignon-Bourcier F., Goris J., Coopman R., de Lajudie P., De Vos P., Gillis M. DNA-DNA hybridization study of Bradyrhizobium strains. Int. J. Syst. Evol. Microbiol. 2001, 51:1315-1322.
63. Willems A., Munive A., de Lajudie P., Gillis M. In most Bradyrhizobium groups sequence comparison of 16S-23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations. Syst. Appl. Microbiol. 2003, 26(2):203-210.
64. Woomer P., Singleton P.W., Bohlool B.B. Ecological indicators of native rhizobia in tropical soils. Appl. Environ. Microbiol. 1988, 54:1112-1116.
65. Yao Z.Y., Kan F.L., Wang E.T., 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.
66. Zhang S., Xie F., Li Y. Phylogenetic of bradyrhizobia from Chinese cowpea miscellany inferred from 16S rRNA, atpD, glnII, and 16S-23S intregenic spacer sequences. Can. J. Microbiol. 2011, 57:316-327.
67. 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.
68. Zhang Y.M., Li Y., Chen W.F., Wang E.T., Tian C.F., Li Q.Q., Zhang Y.Z., Sui X.H., Chen W.X. Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China plain. Appl. Environ. Microbiol. 2011, 77:6331-6342.