Rescue and genetic assessment of soybean-nodulating Bradyrhizobium strains from an experimental field thirty years after inoculation
Abstract
As the long-term phenotype and genetic stability of bacteria used as inoculant are important parameters in their ecology and for agricultural purposes, this study aimed genotypically characterize several-rescued bradyrhizobia of an experimental field thirty years after the first inoculation. A high genetic diversity of 30 bradyrhizobia isolates was observed, either by AFLP (H = 4.87) or rep-PCR (H = 4.18). The results indicate that the Bradyrhizobium population that persists in the Eldorado soil is genetically very diverse and different from the parental strains. All isolates were infective and trapped in IAS-5 soybean variety maintaining their nodulation and nitrogen fixation properties. Given that many rhizobia in a soil can lost the infective capacity and that the host genotype can affect the spectrum of rhizobial genotype selected from a soil, the genetic diversity of the complete bradyrhizobia population in Eldorado soil could be even higher than the identified in this work.
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ALBERTON, O.; KASCHUK, G.; HUNGRIA, M. Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biology and Biochemistry, Amsterdam, v.38, n.6, p. 1298–1307, jun 2006. DOI: https://doi.org/10.1016/j.soilbio.2005.08.018
ANDRADE, D.S.; MURPHY, P.J.; 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, Washington, v.68, n.8, p. 4025–4034, ago 2002 DOI: https://doi.org/10.1128/AEM.68.8.4025-4034.2002
ATLAS, R.M.; BARTHA, R. Microbial ecology: Fundamentals and applications. 4.ed. Menlo Park: Benjamin/Cummings, 1998. 694p.
BATISTA, J.S.S.; HUNGRIA, M.; BARCELLOS, F.G.; FERREIRA, M.C.; MENDES, I.C. Variability in Bradyrhizobium japonicum and B. elkanii seven years after introduction of both the exotic microsymbiont and the soybean host in a Cerrados soil. Microbial Ecology, New York, v.53, n.2, p.270-284, fev 2007. DOI: https://doi.org/10.1007/s00248-006-9149-2
BODDEY L.H.; HUNGRIA, M. Phenotypic grouping of Brazilian Bradyrhizobium strains which nodulate soybean. Biology and Fertility of Soils, Berlin, v.25, n.4, p.407-415, out 1997. DOI: https://doi.org/10.1007/s003740050333
BRUNEL, B.; CLEYET-MAREL, J.C.; NORMAND, P.; BARDIN, R. Stability of Bradyrhizobium japonicum inoculants after introduction into soil. Applied and Environmental Microbiology, Washington, v.54, n.11, p.2636–2642, nov 1988. DOI: https://doi.org/10.1128/aem.54.11.2636-2642.1988
CARVALHO, F. G.; SELBACH, P. A.; BIZARRO, M. J. Eficiência e competitividade de variantes espontâneos isolados de estirpes de Bradyrhizobium spp recomendadas para a cultura da soja (Glycine max). Revista Brasileira de Ciência do Solo, Viçosa, v.29, n.6, p.883-891, nov 2005. DOI: https://doi.org/10.1590/S0100-06832005000600006
CHEN, L.S.; FIGUEREDO, A.; PEDROSA, F.O.; HUNGRIA, M. Genetic characterization of soybean rhizobia in Paraguay. Applied and Environmental Microbiology, Washington, v.66, n.11, p.5099–5103, nov 2000. DOI: https://doi.org/10.1128/AEM.66.11.5099-5103.2000
COUTINHO, H. L. C.; OLIVEIRA, V. M.; LOVATO, A.; MAIA, A. H. N.; MANFIO, G. P. Evaluation of the diversity of rhizobia in Brazilian agricultural soils cultivated with soybeans. Applied Soil Ecology, Amsterdam, v.13, n.2, p. 159-167, 1999. DOI: https://doi.org/10.1016/S0929-1393(99)00031-1
DE BRUIJN F.J. Use of repetitive extragenic palindromic and enterobacterial repetitive intergenic consensus sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Applied and Environmental Microbiology, Washington, v.58, n.7, p.2180-2187, jul 1992. DOI: https://doi.org/10.1128/aem.58.7.2180-2187.1992
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 Microbiology Ecology, Malden, v.51, n.1, p.87-97, dez 2004. DOI: https://doi.org/10.1016/j.femsec.2004.07.009
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. Applied and Environmental Microbiology, Washington, v.66, n.9, p.3987–3997, set 2000. DOI: https://doi.org/10.1128/AEM.66.9.3987-3997.2000
FERREIRA, M.C.; ANDRADE, D.S.; CHUEIRE, L.M.O.; TAKEMURA, S.M.; HUNGRIA, M. Tillage method and crop rotation effects on the population sizes and diversity of bradyrhizobia nodulating soybean. Soil Biology and Biochemistry, Oxford, v.32, n.5, p.627–637, mai 2000. DOI: https://doi.org/10.1016/S0038-0717(99)00189-3
FERREIRA, M.C.; HUNGRIA, M. Recovery of soybean inoculant strains from uncropped soils in Brazil. Field Crops Research, Amsterdam, v. 79, n. 2/3, p. 139-152, dec 2002. DOI: https://doi.org/10.1016/S0378-4290(02)00119-3
FREIBERG, C.; FELLAY, R.; BAIROCH, A.; BROUGHTON, W. ROSENTHAL, A. PERRET, X. Molecular basis of symbiosis between Rhizobium and legumes. Nature, London, v. 387, n.6631; p.394–401, mai 1997. DOI: https://doi.org/10.1038/387394a0
FREIRE, J.R.J. Inoculation of soybean. In: VINCENT, J.M.; WHITNEY, A.S.; BOSE, J. (Ed.) Exploiting the legume-Rhizobium symbiosis in tropical agriculture Hawaii. University of Hawaii, Honolulu, 1977. P. 335-379.
FREIRE, J.R.J. ; KOLLING, J.; VIDOR, C.; PEREIRA, G.; KOLLING, I.G.; MENDES, N. G. Sobrevivência e competição por sítios de nodulação de estirpes de Rhizobium japonicum na cultura da soja. Revista Brasileira de Ciência do Solo, Campinas, v.7, n.1, p. 47-53, jan 1983.
GALLI-TERASAWA, L.; GLIENKE-BLANCO, C.; HUNGRIA, M. Diversity of a soybean rhizobial population adapted to a Cerrados soil. World Journal of Microbiology and Biotechnology, Heidelberg, v.19, n.9 p.933–939, dez 2003. DOI: https://doi.org/10.1023/B:WIBI.0000007324.50022.c0
GIBSON, A.H.; DEMEZAS, D.H.; GAULT, R.R.; BHUVANESWARI, T.V.; BROCKWELL, J. Genetic stability of rhizobia in the field. In: KEISTER, D.L.; CREGAN, P.B. (Ed.) The Rhizosphere and Plant Growth. Kluwer Academic Publishers, Dordrecht, 1991. p .141-148. DOI: https://doi.org/10.1007/978-94-011-3336-4_29
GIONGO, A.; AMBROSINI, A.; JARDIM-FREIRE, J.R.; BODANESE-ZANETTINI, M.H.; PASSAGLIA, L.M.P. Amplification of 16S rRNA gene sequences to differentiate two highly related bradyrhizobia species. Pesquisa Agropecuária Brasileira, Brasília, v.42, n.9, p.1361-1364, set 2007. DOI: https://doi.org/10.1590/S0100-204X2007000900019
GÖTTFERT, M.; RÖTHLISBERGER, S, KÜNDIG, C.; BECK, C.; MARTY, R.; HENNECKE, H; Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. Journal of Bacteriology, Washington, v.183, n.4, p.1405-1412, fev 2001. DOI: https://doi.org/10.1128/JB.183.4.1405-1412.2001
HUNGRIA, M.; FRANCO, A.A.; SPRENT, J.I. New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris L. Plant and Soil, The Hague, v.149, n.1, p.103-109, jan 1993. DOI: https://doi.org/10.1007/BF00010767
HUNGRIA, M.; VARGAS, M.A.T. Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Research, Amsterdam, v. 65, n.1, p.151-164, jan 2000. DOI: https://doi.org/10.1016/S0378-4290(99)00084-2
HUNGRIA, M.; CHUEIRE, L.M.O.; COCA, R.G.; MEGIAS, M. Preliminary characterization of fast growing rhizobial strains isolated from soybean nodules in Brazil. Soil Biology and Biochemistry, Amsterdam, v.33, n. 10, p.1349-1361, out 2001. DOI: https://doi.org/10.1016/S0038-0717(01)00040-2
KANEKO, T.et al. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Research, Oxford, v.9, n.6, p.189–197, dez 2002. DOI: https://doi.org/10.1093/dnares/9.6.189
LABERGE, S.; MIDDLETON, A.T.; WHEATCROFT, R. Characterization, nucleotide sequence, and conserved genomic locations of insertion sequence ISRm5 in Rhizobium meliloti. Journal of Bacteriology, Washington, v.177, n.11, p.3133–3142, jun 1995. DOI: https://doi.org/10.1128/jb.177.11.3133-3142.1995
LAGUERRE, G.; LOUVRIER, P.; ALLARD, M.R.; AMARGER, N. Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulation of host legumes. Applied and Environmental Microbiology, Washington, v.69, n.4, p.2276–2283, abr 2003. DOI: https://doi.org/10.1128/AEM.69.4.2276-2283.2003
LÕHMUS, K.; TRUU, M.; TRUU, J.; OSTONEN, I.; KAAR, E.; VARES, A.; URI, V.; ALAMA, S.; KANAL, A. Functional diversity of culturable bacterial communities in the rhizosphere in relation to fine-root and soil parameters in alder stands on forest, abandoned agricultural and oil-shale mining areas. Plant and Soil, The Hague, v.283, n.1/2, p.1–10, mai 2006. DOI: https://doi.org/10.1007/s11104-005-2509-8
MAGURRAN, A.E. Ecological diversity and its measurement. New Jersey: Princeton, 1987. 179p. DOI: https://doi.org/10.1007/978-94-015-7358-0
MARILLEY, L.; VOGT, G.; BLANC, M.; ARAGNO, M. Bacterial diversity in the bulk soil and rhizosphere fractions of Lolium perenne and Trifolium repens as revealed by PCR restriction analysis of 16S rDNA. Plant and Soil, The Hague, v.198, n.2, p.219–224, jan 1998 DOI: https://doi.org/10.1023/A:1004309008799
MARTINEZ-ROMERO, E.; CABALLERO-MELLADO, J. Rhizobium phylogenies and bacterial diversity. Critical Reviews in Plant Sciences, Amsterdam, v.15, n.2, p.113–140, mar 1996. DOI: https://doi.org/10.1080/07352689609701938
OBATON, M.; BOUNIOLS, A.; PIVA, G.; VALDEZ, V. Are Bradyrhizobium japonicum stable during a long stay in soil? Plant and Soil, The Hague, v.245, n.2, p.315–326, ago 2002. DOI: https://doi.org/10.1023/A:1020447928911
PALMER, K.M.; YOUNG, J.P.W. Higher diversity of Rhizobium leguminosarum biovar viciae populations in arable soils than in grass soils. Applied and Environmental Microbiology, Washington, v.66, n.6, p.2445–2450, jun 2000. DOI: https://doi.org/10.1128/AEM.66.6.2445-2450.2000
PARKER, M.A. Relationships of bradyrhizobia from the legumes Apios americana and Desmodium glutinosum. Applied and Environmental Microbiology, Washington, v.65, n.11, p.4914–4920, nov 1999. DOI: https://doi.org/10.1128/AEM.65.11.4914-4920.1999
PERES, J.R.R.; VIDOR, C. Seleção de estirpes de Rhizobium japonicum e competitividade por sítios de infecção nodular em estirpes de soja. Agronomia Sulriograndense, Porto Alegre, v.16, n.2, p.205-219, jan 1980.
PROVOROV, N.A.; VOROBEV, N.I. Evolutionary genetics of nodule bacteria: molecular and population aspects. Russian Journal of Genetics, Moscow, v.36, n.12, p.1323–1335, dez 2000. DOI: https://doi.org/10.1023/A:1009029703470
REVELLIN, C.; PINOCHET, X.; BEAUCLAIR, P.; CATROUX, G; Influence of soil properties and soybean cropping history on the Bradyrhizobium japonicum population in some French Soils. European Journal of Soil Science, Oxford, v.47, n.4, p.505–510, dez 1996. DOI: https://doi.org/10.1111/j.1365-2389.1996.tb01850.x
SAMBROOK, J.; RUSSEL, D.W. Molecular cloning: a laboratory manual. 3.ed. New York: Cold Spring Harbor Laboratory Press, 2001. 2344p.
SANTOS, M. A.; VARGAS, M. A. T.; HUNGRIA, M. Characterization of soybean bradyrhizobia strains adapted to the Brazilian cerrados region. FEMS Microbiology Ecology, Amsterdam, v.30, n.3, p. 261-272, nov 1999. DOI: https://doi.org/10.1111/j.1574-6941.1999.tb00654.x
SHANNON, C.E; WEAVER, W. The mathematical theory of communication. Urbana: University of Illinois Press, 1949. 132 p.
SIKORA, S.; REDZEPOVIC, S Genotypic characterization of indigenous soybean rhizobia by PCR-RFLP of 16S rDNA, rep-PCR and RAPD analysis. Food Technology and Biotechnology, Zagreb, v.41, n.1, p.61-67, jan 2003.
SILVA, C.; VINUESA, P.; EGUIARTE, L.E.; MARTINEZ-ROMERO, E.; SOUZA, V; Rhizobium etli and Rhizobium gallicum nodulate common bean (Phaseolus vulgaris) in a traditionally managed milpa plot in Mexico: population genetics and biogeographic implications. Applied and Environmental Microbiology, Washington, v.69, n.2, p.884–893, fev 2003. DOI: https://doi.org/10.1128/AEM.69.2.884-893.2003
SINGH, D.V.; MATTE, M.H.; MATTE, G.R.; JIANG, S.; SABEENA, F.; SHUKLA, B.N.; SANYAL, S.C.; HUQ, A.; COLWELL, R.R. Molecular analysis of Vibrio cholerae O1, O139, non-O1, and non-O139 strains: clonal relationships between clinical and environmental isolates. Applied and Environmental Microbiology, Washington, v.67, n.2, p.910–921, fev 2001. DOI: https://doi.org/10.1128/AEM.67.2.910-921.2001
SOIL SURVEY STAFF. Keys to Soil Taxonomy. 11 ed. Washington: Natural Resources Conservation Services, 2010. 338 p.
SOMASEGARAM, P.; HOBEN, M.J. Handbook for Rhizobia: Methods in legume-Rhizobium technology. New York, Springer-Verlag, 1994. 450p.
SUGAWARA, M.; TSUKUI, T.; KANEKO, T.; OHTSUBO, Y.; SATO, S.; NAGATA, Y.; TSUDA, M.; MITSUI, H.; MINAMISAWA, K. Complete genome sequence of Bradyrhizobium diazoefficiens USDA 122, a nitrogen-fixing soybean symbiont. Genome announcements, Washington, v.5, n.9, e01743-16, mar 2017. DOI: https://doi.org/10.1128/genomeA.01743-16
SULLIVAN, J.T.; RONSON, C.W. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proceedings of the National Academy of Sciences of the United States of America, Washington, v.95, n. 9 p. 5145-5149, abr 1998. DOI: https://doi.org/10.1073/pnas.95.9.5145
VARGAS, M.A.T.; MENDES, I.C.; SUHET, A.R.; PERES, J.R.R. Serological distribution of Bradyrhizobium japonicum from Brazilian cerrados areas under soybean cultivation. Revista de Microbiologia, São Paulo, v.24, n.4, p.239–243, out 1993.
VARGAS, M.A.T.; HUNGRIA, M. Biologia dos Solos de Cerrados. Planaltina: EMBRAPA-CPAC, 1997. 524 p.
VARGAS, L.K.; LISBOA, B.B.; SCHOLLES, D.; SILVEIRA, J.R.P.; JUNG, G.C.; GRANADA, C.E.; NEVES, A.G.; BRAGA, M.M.; NEGREIROS, T.A. Diversidade genética e eficiência simbiótica de rizóbios noduladores de acácia-negra de solos do Rio Grande do Sul. Revista Brasileira de Ciência do Solo, Viçosa, v. 31, n.4, p.647-654, jul 2007. DOI: https://doi.org/10.1590/S0100-06832007000400005
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, New York, v.5, n.1, p.:25-40, jan 1994.
VINCENT, J.M. A manual for the practical study of root nodule bacteria. Oxford: Blackwell Scientific, 1970. 200p.
WONG, H.L.; YEOH, H.H.; LIM, S.H. Customization of AFLP analysis for cassava varietals identification. Phytochemistry, London, v.50, n.6, p.919-24, mar 1999. DOI: https://doi.org/10.1016/S0031-9422(98)00628-1
ZILLI, J.E.; VALISHESKI, R.R.; FREIRE FILHO, F.R.; NEVES, M.C.P.; RUMJANEK, N.G. Assessment of cowpea Rhizobium diversity in Cerrado areas of northeastern Brazil. Brazilian Journal of Microbiology, São Paulo, v.35, n.4, p.281-287, out 2004. DOI: https://doi.org/10.1590/S1517-83822004000300002
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