Skip to main content
SpringerLink
Log in

Control of the expression of bacterial genes involved in symbiotic nitrogen fixation

  • Special Topic Review: Control of Gene Expression Microorganisms. Edited by Miguel Vicente
  • Special Topic Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Several genera of N2-fixing bacteria establish symbiotic associations with plants. Among these, the genus Rhizobium has the most significant contribution, in terms of yield, in many important crop plants. The establishment of the Rhizobium-legume symbiosis is a very complex process involving many genes which need to be co-ordinately regulated. In the first instance, plant signal molecules, known to be flavonoids, trigger the expression of host-specific genes in the bacterial partner through the action of the regulatory NodD protein. In response to these signals, Rhizobium bacteria synthesize lipo-oligosaccharide molecules which in turn cause cell differentiation and nodule development. Once the nodule has formed, Rhizobium cells differentiate into bacteroids and another set of genes is activated. These genes, designated nif and fix, are responsible for N2 fixation. In this system, several regulatory proteins are involved in a complex manner, the most important being NifA and a two component (FixK and FixL) regulatory system. Our knowledge about the establishment of these symbioses has advanced recently, although there are many questions yet to be solved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albright, C.M., Huala, E. & Ausubel, F.M. 1989 Procaryotic signal transduction mediated by sensor and regulatory protein pairs. Annual Review of Genetics 23, 311–336

    Google Scholar 

  • Anthamatten, D. & Hennecke, H. 1991 The regulatory status of the fixL-and fixJ-like genes in Bradyrhizobium japonicum may be different from that in Rhizobium meliloti. Molecular and General Genetics 225, 38–48.

    Google Scholar 

  • Baev, N., Endre, G., Petrovics, G., Banfalvi, Z. & Kondorosi, A. 1991 Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes d-glucosamine synthetase. Molecular and General Genetics 228, 113–124.

    Google Scholar 

  • Baev, N. & Kondorosi, A. 1992 Nucleotide sequence of the R. meliloti nodL gene located in locus n5 of the nod regulon. Plant Molecular Biology 18, 843–846.

    Google Scholar 

  • Banfalvi, Z., Nieuwkoop, A., Schell, M., Best, L. & Stacey, G. 1988 Regulation of nod gene expression in Bradyrhizobium japonicum. Molecular and General Genetics 214, 420–424.

    Google Scholar 

  • Barbour, W.M., Hattermann, D.R. & Stacey, G. 1991 Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Applied and Environmental Microbiology 57, 2635–2639.

    Google Scholar 

  • Bassam, B.J., Djorjevic, M.A., Redmond, J.W., Batley, M. & Rolfe, B.G. 1988 Identification of a nodD-dependent locus in the Rhizobium strain NGR 234 activated by phenolic factors secreted by soybeans and other legumes. Molecular Plant-Microbe Interactions 1, 161–168.

    Google Scholar 

  • Batut, J., Daveran-Mingot, M.L., David, M., Jacobs, J., Garnerone, A.M. & Kahn, D. 1989 FixK a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. EMBO Journal 8, 1279–1286.

    Google Scholar 

  • Batut, J., Santero, E. & Kustu, S. 1991 In vitro activity of the nitrogen fixation regulatory protein FixJ from R. meliloti. Journal of Bacteriology 173, 5914–5917.

    Google Scholar 

  • Better, M., Lewis, B., Corbin, D., Ditta, G. & Helinski, D.R. 1985 Structural relationships among Rhizobium meliloti symbiotic promoters. Cell 35, 479–485.

    Google Scholar 

  • Bhuvaneswari, T.V., Turgeon, G. & Bauer, W.D. 1980 Early stages in the infection of soybean (Glycine max L Merr) by Rhizobium japonicum. 1. Localization of infective root cells. Plant Physiology 66, 1027–1031.

    Google Scholar 

  • Bibb, M.J., Biro, S., Motamedi, H., Collins, J. F. & Hutchinson, C.R. 1989 Analysis of the nucleotide sequence of the Streptomyces glaucescens tcml genes provides key information about enzymology of poliketide antibiotic biosynthesis. EMBO Journal 8, 2727–2736.

    Google Scholar 

  • Birkenhead, K., Nooman, B., Reville, W.J., Boesten, B., Manian, S.S. & O'Gara, F. 1990 Carbon utilization and regulation of nitrogen fixation genes in Rhizobium meliloti. Molecular Plant-Microbe Interactions 3, 167–173.

    Google Scholar 

  • Bloemberg, G.V., Lugtenberg, B.J.J. & Spaink, H.P. 1992 In vitro transacetylating activity of the nodL protein of Rhizobium leguminosarum bv. viciae. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA. 11–16 July 1992.

  • Buck, M. & Cannon, W. 1987 Frameshifts close to the Klebsiella pneumoniae promoter prevent multicopy inhibition by hybrid nifH plasmids. Molecular and General Genetics 207, 492–498.

    Google Scholar 

  • Bulawa, C.E. & Wasco, W. 1991 Chitin and nodulation. Nature 353, 710.

    Google Scholar 

  • Caetano-Anolles, G., Crist-Estes, D.K. & Bauer, W.D. 1988 Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. Journal of Bacteriology 170, 3164–3169.

    Google Scholar 

  • Canter-Cremers, H.C.J., Spaink, H.P., Wijfjes, A.H.M., Pees, E., Wijffelman, C.A., Okker, R.J.H. & Lubtenberg, B.J.J. 1989 Additional nodulation genes on the Sym plasmid of Rhizobium leguminosarum biovar viciae. Plant Molecular Biology 13, 163–174.

    Google Scholar 

  • Cervantes, E., Sharman, S.B., Maillet, F., Vasse, J., Truchet, G. & Rosenberg, C. 1989 The Rhizobium meliloti host range nodQ gene encodes a protein which shares homology with translation elongation and initiation factors. Molecular Microbiology 3, 745–755.

    Google Scholar 

  • Colonna-Romano, S., Arnold, S., Schluter, A., Boistard, P. & Puhler, A. 1990 An Fnr-like protein encoded in Rhizobium leguminosarum biovar viciae shows structural and functional homology to Rhizobium meliloti FixK. Molecular and General Genetics 223, 138–147.

    Google Scholar 

  • David, M., Daveran, M.-L., Batut, J., Dedieu, A., Domergue, O., Ghai, J., Hertig, C., Boistard, P. & Kahn, D. 1988 Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54, 671–683.

    Google Scholar 

  • Davis, E.O. & Johnston, A.W.B. 1990 Regulatory functions of the three nodD genes of Rhizobium leguminosarum bv. phaseoli. Molecular Microbiology 3, 1567–1577.

    Google Scholar 

  • Débellé, F. & Sharma, S.B. 1986 Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation. Nucleic Acids Research 14, 7453–7472.

    Google Scholar 

  • DeBruijn, F., Hilgert, U., Stigter, I., Schneider, M., Meyer, H., Klosse, U. & Pawlowski, K. 1990 Regulation of nitrogen fixation and assimilation genes in the free-living versus symbiotic state. In Nitrogen Fixation: Achievements and Objectives, eds Gresshof, P.M., Roth, L.E., Stacey, G. & Newton, W.E. pp. 33–44. New York: Chapman and Hall.

    Google Scholar 

  • Demont, N., Roche, P., Aurelle, H., Talmont, F., Promé, D., Promé, J.C., Price, N.P.J., Relic, B., Broughton, W.J., Débellé, F., Ardourel, M.Y., Maillet, F., Rosenberg, C., Truchet, G. & Dénarié, J. 1992 Rhizobium nodulation factors: variations on a theme. In Molecular Genetics of Plant Microbe Interactions, eds Nester, E.W. & Verma, D.P.S. pp. 133–141. Dordrecht: Kluwer Academic.

    Google Scholar 

  • DePhilip, P., Batut, J. & Boistard, P. 1990 Rhizobium meliloti FixL is an oxygen sensor and regulates R. meliloti nifA and fixK genes differently in Escherichia coli. Journal of Bacteriology 172, 4255–4262.

    Google Scholar 

  • Ditta, G., Virts, E. & Helinski, D. 1988 Oxygen regulation of nif genes in Rhizobium meliloti. In Molecular Plant-Microbe Interactions, eds Verma, D.P.S. & Palacios, R. pp. 109–110. St. Paul MN: APS Press.

    Google Scholar 

  • Ditta, G., Virts, E., Palomares, A.J. & Kim, C.H. 1987 The nifA gene of Rhizobium meliloti is oxygen regulated. Journal of Bacteriology 169, 3217–3223.

    Google Scholar 

  • Djordjevic, M.A., Redmond, J.W., Batley, M. & Rolfe, B.G. 1987 Clovers secrete specific phenolic compounds which either stimulate or repress nod gene expression in Rhizobium trifolii. EMBO Journal 6, 1173–1179.

    Google Scholar 

  • Downie, J.A. 1989 The nodL gene from Rhizobium leguminosarum is homologous to the acetyl transferases encoded by lacA and cysE. Molecular Microbiology 3, 1649–1651.

    Google Scholar 

  • Downie, J.A., Sutton, J.M. & Lea, E.J.A. 1992 nodO: a nodulation protein that forms pores in membranes. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA, 11–16 July 1992 p. S13.

  • Drummond, M., Whitty, P. & Wooton, J. 1986 Sequence and domain relationships of ntrC and nifA from Klebsiella pneumoniae: homologies to other regulatory proteins. EMBO Journal 5, 441–447.

    Google Scholar 

  • Dudley, M.E., Jacobs, T.W. & Long, S.R. 1987 Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta 171, 289–301.

    Google Scholar 

  • Dusha, I., Bakos, A., Kondorosi, A., DeBruijn, F. & Shell, J. 1989 The Rhizobium meliloti early nodulation genes (nod ABC) are nitrogen regulated: isolation of a mutant strain with efficient nodulation capacity on alfalfa in the presence of ammonium. Molecular and General Genetics 219, 89–96.

    Google Scholar 

  • Dylan, T., Ielpi, L., Stanfield, S., Kashyap, L., Douglas, C., Yanosfsky, M., Nester, E., Helinski, D.R. & Ditta, G. 1986 Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proceedings of the National Academy of Science of the United States of America 83, 4403–4407.

    Google Scholar 

  • Earl, C.D., Ronson, C.W. & Ausubel, F.M. 1987 Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. Journal of Bacteriology 169,1127–1136.

    Google Scholar 

  • Economou, A. & Downie, J.A. 1992. The nodulation of legumes by rhizobia. In Nitrogen Fixation and its Research in China, ed Hong, G.-F., pp. 315–339. Berlin and Heidelberg: Springer-Verlag.

    Google Scholar 

  • Evans, I.J. & Downie, J.A. 1986 The nodI gene product of Rhizobium leguminosarum is closely related to ATP-binding bacterial transport proteins; nucleotide sequence analysis of the nodI and nodJ genes. Gene 43, 95–101.

    Google Scholar 

  • Firmin, J.L., Wilson, K.E., Rossen, L. & Johnston, A.W.B. 1986 Flavonoid activation of nodullation genes in Rhizobium reversed by other compounds present in plants. Nature 324, 90–92.

    Google Scholar 

  • Fischer, R.F. & Long, S.R. 1992 Rhizobium-plant signal exchange. Nature 357, 655–660.

    Google Scholar 

  • Folch, J.L., Spaink, H.P., Sousa, C., Quinto, C. & Megias, M. 1992 Rhizobium tropici CIAT899 nodulation genes and signals. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA, 11–16 July, 1992 p. 67.

  • Geelen, D., Goormachtig, S., Van Den Eede, G., Van Montagu, M. & Holster, M. 1992 Organization and functional analysis of the nod locus 1 genes from Azorhizobium caulinodans In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA, 11–16 July, 1992, p. 68.

  • Geiger, O., Spaink, H.P. & Lugtenberg, B.J.J. 1992 Phospholipids of Rhizobium contain nodE-determined highly unsaturated fatty acid moieties. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA, 11–16 July, 1992, p. 69.

  • Gilles-Gonzalez, M.A., Ditta, G.S. & Helinski, D.R. 1991 A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 350, 170–172.

    Google Scholar 

  • Götz, R., Limmer, N., Ober, K. & Schmit, R. 1982. Motility and chemotaxis in two strains of Rhizobium with complex flagella. Journal of General Microbiology 128, 789–798.

    Google Scholar 

  • Gubler, M. & Hennecke, H. 1986. fixA, B and C genes are essential for symbiotic and free-living, microaerobic nitrogen fixation. European Journal of Biochemistry 146, 193–199.

    Google Scholar 

  • Gussin, G.N., Ronson, C.W. & Ausubel, F.M. 1986 Regulation of nitrogen fixation genes. Annual Review of Genetics 20, 567–591.

    Google Scholar 

  • Györgypal, Z, Iyer, N. & Kondorosi, A. 1988 Three regulatory nodD alleles of diverged flavonoid-specificity are involved in host-dependent nodulation by Rhizobium meliloti. Molecular and General Genetics 212, 85–92.

    Google Scholar 

  • Hennecke, H., Alvarez-Morales, A., Betancourt-Alvarez, M., Ebeling, E., Filser, M., Fischer, H.-M., Gubler, M., Hahn, M., Kalusa, K., Lamb, J.W., Meyer, L., Regensburger, B., Studer, D. & Weber, J. 1985. Organization and regulation of symbiotic nitrogen fixation genes from Bradyrhizobium japonicum. In Nitrogen Fixation Research Progress, eds Evans, H.J., Bottomley, P.J. & Newton, W.E. pp. 157–163. The Hague: Nihjoff/Junk.

    Google Scholar 

  • Holsters, M., Geelen, D., Goethals, K., VanMontagu, M., Geremia, R., Promé, J.C. & Mergaert, P. 1992 Nod factor production by Azorhizobium caulinodans strain ORS571. In New Horizons in Nitrogen Fixation, eds Palacios, R., Mora, J. & Newton, W.E. pp. 191–196. Dordrecht: Kluwer Academic.

    Google Scholar 

  • Hontelez, J.G.J., Mol, P., VanDun, C., Schetgens, R., VanKammen, A. & Van DenBos, R.C. 1984 Expression of sym-plasmid genes in bacteroids of Rhizobium leguminosarum. In Advances in Nitrogen Fixation Research, eds Veeger, C. & Newton, W.E. p. 686. The Hague: Nihjoff/Junk.

    Google Scholar 

  • Horvath, B., Bachem, C.W.B., Schell, J. & Kondorosi, A. 1987 Host specific regulation of nodulation genes in Rhizobium is mediated by a plant signal, interacting with the nodD gene product. EMBO Journal 6, 841–848.

    Google Scholar 

  • Huala, E. & Ausubel, F.M. 1989 The central domain of Rhizobium meliloti NifA is sufficient to activate transcription from the R. meliloti nifH promoter. Journal of Bacteriology 171, 3354–3365.

    Google Scholar 

  • Johnston, A.W.B., Beynon, J.L., Buchanan-Wollaston, A.V., Setchell, S.M., Hirsch, P.R. & Beringer, J.E. 1978 High frequency transfer of nodulating ability between strains and species of Rhizobium. Nature 276, 634–636.

    Google Scholar 

  • Kahn, D., David, M., Domergue, O., Daveran, M.-L., Ghai, J., Hirsch, P.R. & Batut, J. 1989 Rhizobium meliloti fixGHI sequence predicts involvement of a specific cation pump in symbiotic nitrogen fixation. Journal of Bacteriology 171, 929–939.

    Google Scholar 

  • Kaminski, P.A. & Elmerich, C. 1991 Involvement of fixLJ in the regulation of nitrogen fixation in Azorhizobium caulinodans. Molecular Microbiology 5, 665–673.

    Google Scholar 

  • Kondorosi, E., Banfalvi, Z. & Kondorosi, A. 1984 Physical and genetic analysis of a symbiotic region of Rhizobium meliloti: identification of nodulation genes. Molecular and General Genetics 193, 445–452.

    Google Scholar 

  • Kondorosi, E., Gyuris, J., Schmidt, J., John, M., Duda, E., Hoffman, B., Schell, J. & Kondorosi, A. 1989 Positive and negative control of nod gene expression in Rhizobium meliloti is required for optimal nodulation. EMBO Journal 8, 1331–1340.

    Google Scholar 

  • Kustu, S., Weiss, D.S., Klose, K., Porter, S., North, A. & Wedel, A. 1992 Prokaryotic enhancers and enhancer binding proteins. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington USA, 11–16 July, 1992, p. S20.

  • Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Prome, J.C. & Denarie, J. 1990 Symbiotic host-specificity of Rhizobium meliloti is determined by sulphated and acylated glucosamine oligosaccharide signal. Nature 344, 781–784.

    Google Scholar 

  • Long, S.R. 1989. Rhizobium-legume nodulation: life together in the underground. Cell 56, 203–214.

    Google Scholar 

  • Long, S.R. 1992 Expression and action of Rhizobium nod genes: recent results. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA, 11–16 July 1992, p. S11.

  • Maillet, F., Débellé, F. & Dénarié, J. 1990. Role of the nodD and SyrM genes in the activation of the regulatory gene nodD3 and of the common and host-specific nod genes of Rhizobium meliloti. Molecular Microbiology 4, 1975–1984.

    Google Scholar 

  • Mergaert, P., VanMontagu, M., Prome, J.C. & Holsters 1992. The Nod factors of Azorhizobium caulinodans strain ORS571. In New Horizons in Nitrogen Fixation, eds Palacios, R., Mora, J. & Newton, W.E. pp. 191–196. Dordrecht: Kluwer Academic.

    Google Scholar 

  • Nap, J.-P. & Bisseling, T. 1990 Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science 250, 948–954.

    Google Scholar 

  • Nooman, B., Motherway, M. & O'Gara, F. 1992 Ammonia regulation of the Rhizobium meliloti nitrogenase structural and regulatory genes under free-living conditions-involvement of the fixL gene product. Molecular and General Genetics 234, 423–428.

    Google Scholar 

  • Norel, F., Kush, A., Denefle, P., Charpin, N. & Elmerich, C. 1984 Nitrogen fixation in a tropical Rhizobium associated with Sesbania rostrata. In Advances in Nitrogen Fixation Research, eds Veeger, C. & Newton, W.E. p. 694. The Hague: Nihjoff/Junk.

    Google Scholar 

  • Nuti, M.P., Lepidi, A.A., Prakash, R.K., Schilperoort, R.A. & Cannon, F.C. 1979 Evidence for nitrogen fixation genes on indigenous Rhizobium plasmids. Nature 282, 533–535.

    Google Scholar 

  • Peters, N.K. & Long, S.R. 1988 Alfalfa root exudate and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiology 88, 396–400.

    Google Scholar 

  • Redmond, J.W., Batley, M., Djordjevic, M.A., Innes, R.W., Kuempel, P.L. & Rolfe, B.G. 1986 Flavones induced expression of nodulation genes Rhizobium. Nature 323, 632–635.

    Google Scholar 

  • Ridge, R.W. & Rolfe, B.G. 1986 Rhizobium sp. degradation of legume root hair cell wall at the site of infection thread origin. Applied and Environmental Microbiology 50, 717–750.

    Google Scholar 

  • Rodriguez-Quiñones, F., Banfalvi, Z., Murphy, P. & Kondorosi, A. 1987. Interspecies homology of nodulation genes in Rhizobium. Plant Molecular Biology 8, 61–67.

    Google Scholar 

  • Rodriguez-Quiñones, F., Fernandez-Burriel, M., Banfalvi, Z., Megias, M. & Kondorosi, A. 1989 Identification of a conserved, reiterated DNA region that influences the efficiency of nodulation in strain RS1051. Molecular Plant-Microbe Interactions 2, 75–83.

    Google Scholar 

  • Ronson, C.W., Nixon, B.T. & Ausubel, F.M. 1987 Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell 49, 579–581.

    Google Scholar 

  • Rossen, L., Shearman, C.A., Johnston, A.W.B. & Downie, J.A. 1985 The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant exudate induces the nodABC genes. EMBO Journal 4, 3369–3373.

    Google Scholar 

  • Ruvkun, G.B. & Ausubel, F.M. 1980 Interspecies homology of nitrogenase genes. Proceedings of the National Academy of Sciences of the United States of America. 77, 191–195.

    Google Scholar 

  • Sanjuan, J., Carlson, R.W., Spaink, H.P., Bhat, U.R., Barbour, W.M., Glushka, J. & Stacey, G. 1992 A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proceedings of the National Academy of Sciences of the United States of America. 89, 8789–8793.

    Google Scholar 

  • Schlaman, H.R.M., Okker, R.J.H. & Lugtenberg, B.J.J. 1992 Regulation of nodulation gene expression by NodD in rhizobia. Journal of Bacteriology 174, 5177–5182.

    Google Scholar 

  • Schmidt, J., Wingender, R., John, M., Wieneke, U. & 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 the United States of America. 85, 8578–8582.

    Google Scholar 

  • Schofield, P.R. & Watson, J.M. 1986 DNA sequence of Rhizobium trifolii nodulation genes reveals a reiterated and potentially regulatory sequence proceedings nodAB and nodF. Nucleic Acids Research 14, 2891–2903.

    Google Scholar 

  • Schultze, M., Quiclet-Sire, B., Kondorosi, E., Virelizier, H., Glushka, J.N., Endre, G., Gero, S.D. & Kondorosi, A. 1992 Rhizobium meliloti produces a family of sulphated lipo-oligosaccharides exhibiting different degrees of plant host specificity. Proceedings of the National Academy of Sciences of the United States of America, 89, 192–196.

    Google Scholar 

  • Schwedock, J. & Long, S.R. 1990 ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348, 644–647.

    Google Scholar 

  • Shearman, C.A., Rossen, L., Johston, A.W.B. & Downie, J.A. 1986 The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl-carrier protein and is regulated by nodD plus a factor of pea root exudates. EMBO Journal 5, 647–652.

    Google Scholar 

  • Sheldon, P.S., Kelwick, R.G.O., Sidebottom, C., Smith, C.G. & Slabas, A.R. 1990 3-Oxoacyl-(acyl-carrier protein) reductase from avocado (Persea americana) fruit mesocarp. Biochemistry 272, 713–720.

    Google Scholar 

  • Smit, G., Kijne, J.W. & Lugtenberg, B.J.J. 1987 Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. Journal of Bacteriology 169, 4294–4301.

    Google Scholar 

  • Sousa, C., Folch, J., Boloix, P., Megias, M., Nava, N. & Quinto, C. 1993 A Rhizobium tropici DNA region carrying the amino terminal-half of a nodD gene and a nod-box like sequence is responsible for host range extension. Molecular Microbiology, in press.

  • Spaink, H.P., Aarts, A., Bloemberg, G.V., Folch, J., Geiger, O., Schalman, H.R.M., Thomas-Oates, J.E., VanBrussel, A.A.N., Van DeSande, K., VanSpronsen, P., Wijfjes, A.H.M. & Lugtenberg, B.J.J. 1992 Rhizobial lipo-oligosaccharide signals: their biosynthesis and their role in the plant. In Molecular Genetics of Plant Microbe Interactions, eds Nester, E.W. & Verma, D.P.S. pp. 151–162. Dordrecht: Kluwer Academic.

    Google Scholar 

  • Spaink, H.P., Okker, R.J.H., Wijffelman, C.A., Tak, T., Goosen-De Roo, L., Pees, E., VanBrussel, A.A.N. & Lugtenberg, B.J.J. 1989b Symbiotic properties of rhizobia containing a flavonoid independent hybrid nodD product. Journal of Bacteriology 171, 4045–4053.

    Google Scholar 

  • Spaink, H.P., Sheeley, D.M., VanBrussel, A.A.N., Glushkai, J., York, W.S., Tak, T., Geiger, O., Kennedy, E.P., Reinhold, V.N. & Lugtenberg, B.J.J. 1991 A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125–130.

    Google Scholar 

  • Spaink, H.P., Winman, J., Djordjevic, M.A., Wijffelman, C.A., Okker, R.J.H. & Lugtenberg, B.J.J. 1989a Genetic analysis and cellular localization of the Rhizobium host-specificity-determining NodE protein. EMBO Journal 8, 2811–2818.

    Google Scholar 

  • Stock, J.B., Ninfa, A.J. & Stock, A.M. 1989 Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiological Reviews 53, 450–490.

    Google Scholar 

  • Szeto, W.W., Nixon, B.T., Ronson, C.W. & Ausubel, F.M. 1987 Identification and characterization of the Rhizobium meliloti ntr gene: R. meliloti has separate regulatory pathways for activation of nitrogen fixation genes in free-living and symbiotic cells. Journal of Bacteriology 169, 1423–1432.

    Google Scholar 

  • Szeto, W.W., Zimmerman, J.L., Sundaresan, V. & Ausubel, F.M. 1984 A Rhizobium meliloti symbiotic regulatory gene. Cell 36, 1035–1043.

    Google Scholar 

  • Toro, N. & Olivares, J. 1986 Analysis of R. meliloti sym mutants obtained by heat treatment. Applied and Environmental Microbiology 51, 1148–1150.

    Google Scholar 

  • VanBrussel, A.N.N., Recourt, K., Pees, E., Spaink, H.P., Tak, Y., Wijffelman, C.A., Kijne, J.W. & Lugtenberg, B.J.J. 1990 A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra. Journal of Bacteriology 172, 5394–5401.

    Google Scholar 

  • VandenBosch, K.A., Bradley, D.J., Knox, J.P., Perotto, S., Butcher, G.W. & Brewin, N.J. 1989. Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO Journal 8, 335–342.

    Google Scholar 

  • Van DenEede, G., Dreyfus, B., Goethals, K., Montagu, V.M. & Holsters, M. 1987 Identification and cloning of nodulation genes from stem-nodulating bacterium ORS571. Molecular and General Genetics 206, 291–299.

    Google Scholar 

  • Vargas, C., Martinez, L.J., Megias, M. & Quinto, C. 1990 Identification and cloning of nodulation genes and host specificity determinants of the broad host range Rhizobium leguminosarum biovar phaseoli strain CIAT899. Molecular Microbiology 4, 1899–1910.

    Google Scholar 

  • Vazquez, M., Davalos, A., De LasPeñas, A., Sanchez, F. & Quinto, C. 1991 Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains. Journal of Bacteriology 173, 1250–1258.

    Google Scholar 

  • Vazquez, M., Santana, O., Villalobos, M.A. & Quinto, C. 1992 Similarity of the nodI and NodJ products with proteins from gram negative bacteria. Organization and function of nodulation genes related sequences in Rhizobium leguminosarum bv. phaseoli strain CE3. In 6th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Seattle, Washington, USA, 11–16 July 1992, p. 140.

  • Virts, E.L., Stanfield, S.W., Helinski, D.R. & Ditta, G.S. 1988 Common regulatory elements control symbiotic and microaerobic induction of nifA in Rhizobium meliloti. Proceedings of the National Academy of Sciences of the United States of America. 85, 3062–3065.

    Google Scholar 

  • Yao, P.Y. & Vincent, J.M. 1969 Host specificity in the root hair “curling factor” of Rhizobium spp. Australian Journal of Biological Sciences 22, 413–423.

    Google Scholar 

  • Young, J.P.W. & Johnston, A.W.B. 1989 The evolution of specificity in the legume-Rhizobium symbiosis. Tree 4, 341–349.

    Google Scholar 

  • Zaat, S.A.J., Schripsema, J., Wijffelman, C.A., VanBrussel, A.A.N. & Lugtenberg, B.J.J. 1989 Analysis of the major inducers of the Rhizobium nodA promoter from Vicia sativa root exudates and their activity with different nodD genes. Plant Molecular Biology 13, 175–188.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Microbiologia y Parasitologia, Universidad de Sevilla, Apdo 874 41012, Sevilla, Spain

    M. Megías, J. L. Folch & C. Sousa

Authors
  1. M. Megías
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. L. Folch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Megías, M., Folch, J.L. & Sousa, C. Control of the expression of bacterial genes involved in symbiotic nitrogen fixation. World Journal of Microbiology and Biotechnology 9, 444–454 (1993). https://doi.org/10.1007/BF00328032

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00328032

Key words

Search

Navigation