New insights into the origins and evolution of rhizobia that nodulate common bean (Phaseolus vulgaris) in Brazil

Soil Biology and Biochemistry

Volumn 39, Issue 4, 2007, Pages 867-876

  Grange, Luciana ^a,b   Hungria, Mariangela ^b   Graham, Peter H ^c   Martínez Romero, Esperanza ^d  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b EMBRAPA CERRADOS   (Brazil)

^c UNIVERSITY OF MINNESOTA   (United States)

^d INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

Biological nitrogen fixation; Evolution of the symbiosis; Phaseolus vulgaris; Rhizobium etli; Rhizobium tropici

Indexed keywords

ECOSYSTEMS; GENETIC ENGINEERING; NITROGEN FIXATION; PLANTS (BOTANY); RNA; SOILS;

BANDING PATTERNS; GENETIC DIVERSIFICATION; PHASEOLUS VULGARIS; RHIZOBIUM ETLI; RHIZOBIUM TROPICI;

BACTERIA;

CLADISTICS; EVOLUTION; GENETIC ANALYSIS; LEGUME; NITROGEN FIXATION; NODULATION; POLYMERASE CHAIN REACTION; RELATEDNESS; RHIZOBACTERIUM; RNA; SYMBIOSIS; WILD POPULATION;

BRAZIL; SOUTH AMERICA;

PHASEOLUS VULGARIS; RHIZOBIACEAE; RHIZOBIUM ETLI; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM TROPICI;

EID: 33846585978     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2006.10.008     Document Type: Article

References (67)

1. Acosta-Durán C., and Martínez-Romero E. Diversity of rhizobia from nodules of the leguminous tree Gliricidia sepium, a natural host of Rhizobium tropici. Archives of Microbiology 178 (2002) 161-164
2. Aguilar O.M., Lópes M.V., Riccillo P.M., González R.A., Pagano M., Grasso D.H., Pühler A., and Favelukes G. Prevalence of the Rhizobium-etli like allele in genes coding for 16S rRNA among the indigenous rhizobial populations found associated with wild beans from the Southern Andes in Argentina. Applied and Environmental Microbiology 64 (1998) 3520-3524
3. Aguilar O.M., Riva O., and Peltzer E. Analysis of Rhizobium etli and its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proceedings of the National Academy of Sciences of the United States of America 101 (2004) 13548-13553
4. Alberton O., Kaschuk G., and Hungria M. Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biology & Biochemistry 38 (2006) 1298-1307
5. Amarger N., Bours M., Revoy F., Allard M.R., and Laguerre G. Rhizobium tropici nodulates field-grown Phaseolus vulgaris in France. Plant and Soil 161 (1994) 147-156
6. Amarger N., Macheret V., and Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. International Journal of Systematic Bacteriology 47 (1997) 996-1006
7. Andrade D.S., Murphy P.J., and Giller K.E. The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Applied and Environmental Microbiology 68 (2002) 4025-4034
8. Anyango B., Wilson K.J., Beynon J.L., and Giller K.E. Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Applied and Environmental Microbiology 61 (1995) 4016-4021
9. Bernal G.R., and Graham P.H. Diversity in the rhizobia associated with Phaseolus vulgaris L. in Ecuador, and comparisons with Mexican bean rhizobia. Canadian Journal of Microbiology 47 (2001) 526-534
10. Bernal G.R., Tlusty B., Estevez de Jensen C., van Berkum P., and Graham P.H. Characteristics of rhizobia nodulating beans in the central region of Minnesota. Canadian Journal of Microbiology 50 (2004) 1023-1031
11. Beyhaut E., Tlusty B., van Berkum P., and Graham P.H. Rhizobium giardinii is the microsymbiont of Illinois bundleflower (Demanthus illinoensis (Michx.) Macmillan) in Midwestern prairies. Canadian Journal of Microbiology 52 (2006) 903-907
12. a safra)-Brasil-Série histórica. Retrieved in 6 April 2006 from 〈http://www.conab.gov.br/download/safra/FeijaoTotalSerieHist.xls
13. Dagutat H., and Steyn P.L. Taxonomy and distribution of rhizobia indigenous to South African soils. In: Tikhnovich I.A., Provorov N.A., Romanov V.I., and Newton W.E. (Eds). Nitrogen Fixation: Fundamentals and Applications (1995), Kluwer, Boston 683-686
14. Debouck D.G. Primary diversification of Phaseolus in the Americas: three centers?. Plant Genetic Resources Newsletter 67 (1986) 2-8
15. Debouck D.G., Toro O., Paredes M., Johnson W.C., and Gepts P. Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabacea) in northwestern South America. Economic Botany 47 (1983) 408-423
16. Emygdio B.M., Antunes I.F., Nedel J.L., and Choer E. Diversidade genética em cultivares locais e comerciais de feijão baseada em marcadores RAPD. Pesquisa Agropecuária Brasileira 38 (2003) 1165-1171
17. Franco M.C., Cassini S.T.A., Oliveira V.R., Vieira C., and Tsai S.M. Nodulação em cultivares de feijão dos conjuntos gênicos andino e meso-americano. Pesquisa Agropecuária Brasileira 37 (2002) 1145-1150
18. Freitas F.O. Evidências genético-arqueológicas sobre a origem do feijão comum no Brasil. Pesquisa Agropecuária Brasileira 41 (2006) 1199-1203
19. FUNAI (Fundação Nacional do Índio), 2005. Povos indígenas. Retrieved in 14 September 2005, from 〈http://www.funai.gov.br〉.
20. Gepts P. Biochemical evidence bearing on the domestication of Phaseolus (Fabaceae) beans. Economic Botany 44 (1990) 28-38
21. Gepts P., and Debouck D. Origin, domestication, and evolution of the common bean (Phaseolus vulgaris L.). In: van Schoonhoven A., and Voysest O. (Eds). Common Beans: Research for Crop Improvement (1991), CAB, Wallingford-UK, Cali-Colombia 7-53
22. Graham P.H. Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris L.: a review. Field Crops Research 4 (1981) 93-112
23. Graham P.H., Viteri S.E., Mackie F., Vargas A.T., and Palacios A. Variation in acid soil tolerance among strains of Rhizobium phaseoli. Field Crops Research 5 (1982) 121-128
24. Graham P.H., Draeger K.J., Ferrey M.L., Conroy M.J., Hammer B.E., Martínez E., Aarons S.R., and Quinto C. Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Canadian Journal of Microbiology 40 (1994) 198-207
25. Grange L., and Hungria M. Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biology & Biochemistry 36 (2004) 1389-1398
26. Gutiérrez-Zamora M.L., and Martínez-Romero E. Natural endophytic association between Rhizobium etli and maize (Zea mays L.). Journal of Biotechnology 91 (2001) 117-126
27. Hardarson G. Methods for enhancing symbiotic nitrogen fixation. Plant and Soil 152 (1993) 1-17
28. Harlan J.R. Agricultural origins: centers and non-centers. Science 174 (1971) 468-474
29. Haukka K., Lindström K., and Young J.P.W. Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolated from leguminous trees growing in Africa and Latin America. Applied and Environmental Microbiology 64 (1998) 419-426
30. Hernandez-Lucas I., Segovia L., Martínez-Romero E., and Pueppke S.G. Phylogenetic relationships and host range of Rhizobium spp. that nodulate Phaseolus vulgaris L. Applied and Environmental Microbiology 61 (1995) 2775-2779
31. Herrera-Cervera J.A., Caballero-Mellado J., Laguerre G., Tichy H.V., Requena N., Amarger N., Martínez-Romero E., Olivares J., and Sanjuan J. At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiology Ecology 30 (1999) 87-97
32. Hungria M., Franco A.A., and Sprent J.I. New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris L. Plant and Soil 149 (1993) 103-109
33. Hungria M., Vargas M.A.T., and Araújo R.S. Fixação biológica do nitrogênio em feijoeiro. In: Vargas M.A.T., and Hungria M. (Eds). Biologia dos Solos dos Cerrados (1997), EMBRAPA-CPAC, Planaltina, Brazil 189-294
34. Hungria M., Andrade D.S., Chueire L.M.O., Probanza A., Guttierrez-Mañero F.J., and Megías M. Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biology & Biochemistry 32 (2000) 1515-1528
35. Hungria M., Campo R.J., and Mendes I.C. Benefits of inoculation of common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biology and Fertility of Soils 39 (2003) 88-93
36. Jaccard P. The distribution of flora in the alpine zone. New Phytologist 11 (1912) 37-50
37. Jordan D.C. Rhizobiaceae Conn 1938. In: Krieg N.R., and Holt J.G. (Eds). Bergey's Manual of Systematic Bacteriology (1984), The Williams & Wilkins Co., Baltimore-London 235-244
38. Kaplan L. Archeology and domestication in American Phaseolus (beans). Economic Botany 19 (1965) 358-368
39. Kaplan L. What is the origin of the common bean?. Economic Botany 35 (1980) 240-254
40. Kaschuk G., Hungria M., Santos J.C., and Berton-Junior J.F. Differences in common bean rhizobial populations associated with soil tillage management in southern Brazil. Soil and Tillage Research 87 (2006) 205-207
41. Kipe-Nolt J.A., Montealegre C.M., and Tohme J. Restriction of nodulation by the broad host range Rhizobium tropici CIAT899 in wild accessions of Phaseolus vulgaris L. New Phytologist 120 (1992) 489-494
42. Lafay B., and Burdon J.J. Molecular diversity of rhizobia occurring on native shrubby legumes in southeastern Australia. Applied and Environmental Microbiology 64 (1998) 3989-3997
43. Laguerre G., Nour S.M., Macheret V., Sanjuan J., Drouin P., and Amarger N. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147 (2001) 981-993
44. Martinez-Romero E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant and Soil 252 (2003) 11-23
45. Martínez Romero E., Segovia L., Mercante F.M., Franco A.A., Graham P.H., and Pardo M.A. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. International Journal of Systematic Bacteriology 41 (1991) 417-426
46. 2. Plant and Soil 204 (1998) 89-94
47. Menna P., Hungria M., Barcellos F.G., Bangel E.V., and Martínez-Romero E. Molecular phylogeny based on the 16S rRNA gene and host specificity of elite rhizobial strains used in Brazilian commercial inoculants. Systematic and Applied Microbiology 29 (2006) 315-332
48. Mercante F.M., Cunha C.O., Straliotto R., Ribeiro-Junior W.Q., Vanderleyden J., and Franco A.A. Leucaena leucocephala as a trap-host for Rhizobium tropici strains from the Brazilian "cerrado" region. Revista de Microbiologia 29 (1998) 49-58
49. Michiels J., Dombrecht B., Vermeiren N., Xi C., Luyten E., and Vanderleyden J. Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiology Ecology 26 (1998) 193-205
50. Mostasso L., Mostasso F.L., Dias B.G., Vargas M.A.T., and Hungria M. Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Research 73 (2002) 121-132
51. Münchbach M., Nocker A., and Narberhaus F. Multiple small heat shock proteins in rhizobia. Journal of Bacteriology 181 (1999) 83-90
52. Nodari R.O., Tsai S.M., Guzmán P., Gilbertson R.L., and Gepts P. Toward an integrated linkage map of common bean, III: mapping genetic factors controlling host-bacteria interactions. Genetics 134 (1993) 341-350
53. Pérez-Ramírez N.O., Rogel M.A., Wang E., Castellanos J.Z., and Martínez-Romero E. Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiology Ecology 26 (1998) 289-296
54. Pinto P.P., Raposeiras R., Macedo A.M., Seldin L., Paiva E., and Sá N.M.H. Effects of high temperature on survival, symbiotic performance and genomic modifications of bean nodulating Rhizobium strains. Revista de Microbiologia 29 (1998) 117-125
55. Piñero D., Martínez E., and Selander R.K. Genetic diversity and relationships among isolates of Rhizobium leguminosarum biovar phaseoli. Applied and Environmental Microbiology 54 (1988) 2825-2832
56. Prous A. O povoamento da América visto do Brasil: uma perspectiva crítica. Dossiê surgimento do homem na América. Revista USP 34 (1997) 8-21 jun./ago
57. Segovia L., Young J.P.W., and Martínez-Romero E. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. International Journal of Systematic Bacteriology 43 (1993) 374-377
58. Silva C., Vinuesa P., Eguarte L.E., Martínez-Romero E., and Souza V. Rhizobium etli and Rhizobium gallicum nodulate common bean (Phaseolus vulgaris) in a traditionally managed milpa plot in Mexico: populations genetics and biogeographic implications. Applied and Environmental Microbiology 69 (2003) 884-893
59. Sneath P.H.A., and Sokal R.R. Numerical Taxonomy (1973), W.H. Freeman & Co., San Francisco
60. Souza V., Eguiarte L., Avila G., Cappelo R., Gallardo C., Montoya J., and Piñero D. Genetic structure of Rhizobium etli biovar phaseoli associated with wild and cultivated bean plants (Phaseolus vulgaris and Phaseolus coccineus) in Morelos, Mexico. Applied and Environmental Microbiology 60 (1994) 1260-1268
61. Straliotto R., Cunha C.O., Mercante F.M., Franco A.A., and Rumjanek N.G. Diversity of rhizobia nodulating common beans (Phaseolus vulgaris L.) isolated from Brazilian tropical soils. Anais da Academia Brasileira de Ciências 71 (1999) 3-11
62. Tlusty B., van Berkum P., and Graham P.H. Characteristics of the rhizobia associated with Dalea spp. in the Ordway, Kellogg-Weaver dunes and Hayden prairies. Canadian Journal of Microbiology 51 (2005) 15-23
63. Vincent J.M. Manual for the Practical Sudy of Root Nodule Bacteria (1970), Blackwell, Oxford (IBP Handbook No. 15)
64. Wang E.T., Rogel M.A., Garcia de los Santos A., Martinez-Romero J., Cevallos M.A., and Martinez-Romero E. Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. International Journal of Systematic Bacteriology 49 (1999) 1479-1491
65. Wernegreen J.J., and Riley M.A. Comparison of the evolutionary dynamics of symbiotic and hosekeeping loci: a case for the genetic coherence of rhizobial lineages. Molecular Biology and Evolution 16 (1999) 98-113
66. Young J.P.W., Downer H.L., and Eardly B.D. Phylogeny of the phototrophic Rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. Journal of Bacteriology 173 (1991) 2271-2277
67. Zhang X., Turner S.L., Guo X., Yang H., Debellé F., Yang G., Dénarié J., Young J.P.W., and Li F. The common nodulation genes of Astragalus sinicus rhizobia are conserved despite chromosomal diversity. Applied and Environmental Microbiology 66 (2000) 2988-2995