Historia de la investigación en la simbiosis leguminosa bacteria:Una perspectiva didáctica

  1. Marta-Helena Ramírez-Bahena 1
  2. Álvaro Peix 1
  3. Encarna Velázquez 2
  4. Eulogio J. Bedmar 1
  1. 1 Consejo Superior de Investigaciones Científicas
    info

    Consejo Superior de Investigaciones Científicas

    Madrid, España

    ROR https://ror.org/02gfc7t72

  2. 2 Universidad de Salamanca
    info

    Universidad de Salamanca

    Salamanca, España

    ROR https://ror.org/02f40zc51

Revista:
Arbor: Ciencia, pensamiento y cultura

ISSN: 0210-1963

Any de publicació: 2016

Títol de l'exemplar: Las leguminosas en la agricultura del futuro

Volum: 192

Número: 779

Tipus: Article

DOI: 10.3989/ARBOR.2016.779N3009 DIALNET GOOGLE SCHOLAR

Altres publicacions en: Arbor: Ciencia, pensamiento y cultura

Resum

After cereals, legumes constitute the second most important family of crops for human and animal consumption. However, in contrast to the former, legumes are capable of growing in arid soils of low fertility, due to their ability to establish symbiotic associations with soil bacteria called rhizobia. These microorganisms form special organs in the roots of legumes called nodules, where atmospheric dinitrogen (N2 ) is transformed into ammonium that is exported to the plant for growth. Since their discovery in legume nodules until today, knowledge of the bacteria capable of establishing symbiosis with these plants has advanced in many aspects. Especially, advances in molecular techniques for bacterial identification and access to unexplored places have confirmed that the interaction of legumes with rhizobia is older, and that N2 -fixing bacteria are more abundant and diverse, than considered previously. Here, we attempt to relate the history of an association whose development is key in the history of mankind as we know it now.

Referències bibliogràfiques

  • Agron, P. G., Ditta, G. S. y Helinski, D. R. (1992). Mutational analysis of the Rhizobium meliloti nifA promoter. Journal of Bacteriology, 174, pp. 4120-4129. PMid:1597427 PMCid:PMC206124
  • Balassa, R. (1954). Transformation mechanisms of Rhizobia. I-III. Acta microbiologica Academiae Scientiarum Hungaricae Magyar Tudományos Akadémia, 2, 1-2, pp. 51-78.
  • Balassa, G. (1963). Genetic transformation in Rhizobium: A review of the work of R. Balassa. Bacteriological Reviews, 27, pp. 228- 241. PMid:16350181 PMCid:PMC441180
  • Baldwin, I. L. y Fred, E. B. (1929). Nomenclature of the root-nodule bacteria of Leguminosae. Journal of Bacteriology, 17, pp. 141- 150. PMid:16559355 PMCid:PMC375049
  • Bedmar, E. J., González, J. J., Lluch, C. y Rodelas, B. (2006). Fijación de Nitrógeno: Fundamentos y Aplicaciones. Sociedad Espa-ola de Fijación de Nitrógeno.
  • Beijerinck, M. W. (1888). Cultur des Bacillus radicicola aus den Knöllchen. Botanishe Zeitung, 46, pp. 740–750.
  • Biswasa, J. C., Ladhaa, J. K. y Dazzob F. B. (2000). Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Science Society American Journal, 64, pp. 1644-1650. http:// dx.doi.org/10.2136/sssaj2000.6451644x http://dx.doi.org/10.2136/sssaj2000.6451644x
  • Brock, T. D. (1961). Milestones in Microbiology. Englewood Cliffs: Prentice-Hall. Disponible en: https://archive.org/details/MilestonesinMicrobiology.
  • Buchanan, R. E. (1915) Nomenclature of the Coccaceae. Journal of Infectious Diseases, 17, pp. 528-541. http://dx.doi.org/10.1093/infdis/17.3.528
  • Charles, T. C. y Finan, T. M. (1990). Genetic map of Rhizobium meliloti megaplasmid pRme SU47b. Journal of Bacteriology, 172, pp. 2469-2476. PMid:2158971 PMCid:PMC208885
  • Cohn, F. (1875). Untersuchungen ueber Bakterien. Beitraege zur Biologie der Planzen. En: Brock, T. D. (1961). Milestones in Microbiology. Englewood Cliffs: Prentice-Hall, pp. 127-222. Disponible en: https://archive.org/details/MilestonesinMicrobiology.
  • Collard, P. (1976). The Development of Microbiology. Cambridge, London: Cambridge University Press. PMCid:PMC1667259
  • Davis, J. C. (2007). La increíble historia de la humanidad: de la Edad de Piedra a nuestros tiempos. Barcelona: Planeta.
  • Downie, J. A., Knight, C. D., Johnston, A. W. B. y Rossen, L. (1985). Identification of genes and gene products involved in the nodulation of peas by Rhizobium leguminosarum. Molecular General Genetics, 198, pp. 255-262. http://dx.doi.org/10.1007/BF00383003
  • Egelhoff, T. T. y Long, S. R. (1985). Rhizobium meliloti nodulation genes: identification of nodDABC gene products, purification of NodA protein, and expression of nodA in Rhizobium meliloti. Journal of Bacteriology, 164, pp. 591-599. PMid:2997121 PMCid:PMC214293
  • FAO Statistical Pocketbook (2015). Disponible en: http://www.fao. org/3/a-i4691e.pdf.
  • Faucher, C., Maillet, F., Vasse, J., Rosenberg, C., van Brussel, A. A. N., Truchet, G. y Dénarié, J. (1988). Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal. Journal of Bacteriology, 170, pp. 5489-5499. PMid:3056902 PMCid:PMC211642
  • Frank, B. (1889). Ueber die Pilzsymbiose der Leguminosen. Berichte der Deutschen Chemischen Gesellschaft, 7, pp. 332-346.
  • Freiberg, C., Fellay, R., Bairoch, A., Broughton, W. J., Rosenthal, A. y Perret, X. (1997). Molecular basis of symbiosis between Rhizobium and legumes. Nature, 387, pp. 394-401. http://dx.doi.org/10.1038/387394a0 PMid:9163424
  • Frioni, L. (1990). Ecología Microbiana del Suelo. Montevideo: Universidad de la República.
  • Glazebrook, J. y Walker, G. C. (1989). A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell, 56, pp. 661- 672. http://dx.doi.org/10.1016/0092-8674(89)90588-6
  • Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J. C., Jaubert, M., Simon, D., Cartieaux, F., Prin, Y., Bena, G., Hannibal, L., Fardoux, J., (2007). Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science, 316, pp. 1307-1312. http://dx.doi.org/10.1126/science.1139548 PMid:17540897
  • García-Fraile, P., Carro, L., Robledo, M., Ramírez-Bahena, M. H., Flores-Félix, J. D., Fernández, M. T., Mateos, P. F., Rivas, R., Igual, J. M., Martínez-Molina, E., Peix, A. y Velázquez, E. (2012). Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS ONE 7, e38122. http://dx.doi.org/10.1371/journal.pone.0038122 PMid:22675441 PMCid:PMC3364997
  • Graham, P. H. (1992). Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soils conditions. Canadian Journal of Microbiology, 38, pp. 475-484. http://dx.doi.org/10.1139/m92-079
  • Hellriegel, H. y Wilfarth, H. (1888). Untersuchungen über die Stickstoffnahrung der Gramineon und Leguminosen. Berlin: Buchdruckerei der "Post" Kayssler. Disponible en: https://archive.org/ details/untersuchungen00hell.
  • Higashi, S. (1967). Transfer of clover infectivity of Rhizobium trifolii to Rhizobium phaseoli as mediated by an episomic factor. Journal of General and Applied Microbiology, 13, pp. 391-403. http://dx.doi.org/10.2323/jgam.13.391
  • Honeycutt, R. J., McClelland, M. y Sobral, B.W. (1993). Physical map of the genome of Rhizobium meliloti 1021. Journal of Bacteriology, 175, pp. 6945-6452. PMid:8226638 PMCid:PMC206821
  • Horvath, B., Bachem, C. W. B., Schell, J. y Kondorosi, A. (1987). Host specific regulation of nodulation genes in Rhizobium mediated by a plant-signal, interacting with the nodD product. EMBO Journal, 6, pp. 841-848. PMid:16453758 PMCid:PMC553473
  • Jabbouri, S., Reli?, B., Hanin, M., Kamalaprija, P., Burger, U., Promé, J. C. y Broughton, W. J. (1998). nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors. Journal of Biological Chemistry, 273, pp. 12047-12055.
  • Kowalski, M. (1967). Transducing phages of Rhizobium meliloti. Acta Microbiologica Polonica, 16, pp. 7-12. PMid:4166074
  • Krishnan, H. B. y Pueppke S. G. (1991). nolC, a Rhizobium fredii gene involved in cultivar-specific nodulation of soybean, shares homology with a heat-shock gene. Molecular Microbiology, 5, pp. 737-745. http://dx.doi.org/10.1111/j.1365-2958.1991.tb00744.x PMid:1646377
  • Kündig, C., Hennecke, H. y Göttfert, M. (1993). Correlated physical and genetic map of the Bradyrhizobium japonicum 110 genome. Journal of Bacteriology, 175, pp. 613-622. PMid:8423135 PMCid:PMC196196
  • Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J. C. y Dénarié, J. (1990). Symbiotic host specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature, 344, pp. 781-784. http://dx.doi.org/10.1038/344781a0 PMid:2330031
  • Migula, W. (1897). System der Bakterien. Handbuch der Morphologie, entwicklungsgeschichte und systematik der bakterien (volume 1). Publisher Jena, Fischer. Disponible en: https://archive. org/details/systemderbakter02migugoog
  • Nobbe, F. y Hiltner, L. (1896). Bodenimpfung für anbau von leguminosen. Sächsische. Landwirtschaftliche Zeitschrift, 44, pp. 90-92.
  • Nuti, M. P., Ledeboer, A. M., Lepidi, A. A. y Schilperoort, R. A. (1977). Large plasmids in diferent Rhizobium species. Journal of General Microbiology, 100, pp. 241-248. http://dx.doi.org/10.1099/00221287-100-2-241
  • Orla-Jensen, S. (1909). Die Hauptlinien des Natürlichen Bacteriensystems nebst einer Uebersicht der Gärungsphenomene. Zentralblatt für Bacteriologie Parasitenkunds Infectionskrankheiten und Hygiene Ableitung, II Bd 22, pp. 305-346.
  • Rogel, M. A., Orme-o-Orrillo, E. y Martinez-Romero, E. (2011). Symbiovars in rhizobia reflect bacterial adaptation to legumes. Systematic and Applied Microbiology, 34, pp. 96-104. http://dx.doi.org/10.1016/j.syapm.2010.11.015 PMid:21306854
  • Peix, A., Ramírez-Bahena, M. H., Velázquez, E. y Bedmar, E. J. (2015). Bacterial asociations with legumes. CRC Critical Reviews in Plant Sciences, 34, pp. 17-42. http://dx.doi.org/10.1080/07352689.2014.897899
  • Peters, N. K., Frost, J. W. y Long, S. R. (1986). A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science, 233, pp. 977-980. http://dx.doi.org/10.1126/science.3738520 PMid:3738520
  • Prazmowski, A. (1890). Die wurzelknöllchen der erbse. Landwirtschaflichen Versuchsstat, 37, pp. 161-238.
  • Prescott, L. M., Harley, J. P. y Klein, D. A. (2004). Microbiología. Madrid: McGraw-Hill Interamericana.
  • Price, N. P., Reli?, B., Talmont, F., Lewin, A., Promé, D., Pueppke, S. G., Maillet, F., Dénarié, J. Promé, J. C., Broughton, W. J. (1992). Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Molecular Microbiology, 6, pp. 3575-3584. http://dx.doi.org/10.1111/j.1365-2958.1992.tb01793.x PMid:1474899
  • Ramírez-Bahena, M. H., García-Fraile, P., Peix, A., Valverde, A., Rivas, R., Igual, J. M., Mateos, P. F., Martínez-Molina, E. y Velázquez, E. (2008). Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889, Rhizobium phaseoli Dangeard ... leguminosarum DSM 30132T (=NCIMB 11478T) into the new species Rhizobium pisi sp. nov. International Journal of Systematic and Evolutionary Microbiology, 58, pp. 2484-2490. http://dx.doi.org/10.1099/ijs.0.65621-0 PMid:18984681
  • Schindler, F. (1885). Über die biologische bedeutung der wurzelknöllchen bei den Papilionaceen. Journal die Landwirtschaft, 33, pp. 325-336.
  • Schlaman, H. R. M., Spaink, H. P., Okker, R. J. H. y Lugtenberg, B. J. J. (1989). Subcellular localization of the nodD gene product in Rhizobium leguminosarum. Journal of Bacteriology, 171, pp. 4686-4693. PMid:2670892 PMCid:PMC210268
  • Schlegel, H. G. (1990). Microbiología General. Barcelona: Ediciones Omega.
  • Schmidt, J., Wingender, R., John, M., Wieneke, U. y Schell, J. (1988). Rhizobium meliloti nodA and nodB genes are involved in generating compounds that stimulate mitosis of plant cells. Proceedings of the National Academy of Sciences of U. S. A., 85, pp. 8578-8582. http://dx.doi.org/10.1073/pnas.85.22.8578
  • Török, I. y Kondorosi, A. (1981). Nucleotide sequence of Rhizobium meliloti nitrogenase reductase (nifH) gene. Nucleic Acids Research, 9, pp. 5711-5723. http://dx.doi.org/10.1093/nar/9.21.5711 PMid:6273806 PMCid:PMC327555
  • Vinuesa, P., Silva, C., Lorite, M. J., Izaguirre-Mayoral, M. L., Bedmar, E. J. y Martínez-Romero, E. (2005). 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. Systematic and Applied Microbiology, 28, pp. 702-716. http://dx.doi.org/10.1016/j.syapm.2005.05.007 PMid:16261860
  • Ward, H. M. (1887). On the tubercular swellings on the root of Vicia faba. Philosophical Transactions B, 178, pp. 539-562. http://dx.doi.org/10.1098/rstb.1887.0018
  • Woese, C. R. y Fox, G. E. (1977). Phylogenetic structure of the procaryotic domain: The primary kingdoms. Proceedings of the National Academy of Sciences of U. S. A., 74, pp. 5088-5090. http://dx.doi.org/10.1073/pnas.74.11.5088
  • Woese, C. R., Kandler, O. y Wheels M.L. (1990) Towards a natural system of organisms: proposal for the domains of Archaea, Bacteria, and Eucarya. Proceedings of the National Academy of Sciences of U. S. A., 87, pp. 4576-4579. http://dx.doi.org/10.1073/pnas.87.12.4576
  • Yanni, Y. G., Rizk, R.Y., Corich, V., Squartini, A., Ninke, K., Philip-Hollingsworth, S., Orgambide, G., de Bruijn, F., Stoltzfus, J., Buckley, D., Schmidt, T. M., Mateos, P. F., Ladha, J. K. y Dazzo, F. B. (1997). Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant and Soil, 194, pp. 99-114 http://dx.doi.org/10.1023/A:1004269902246