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The Role of Microbial Surface Polysaccharides in the Rhizobium-Legume Interaction

  • Chapter
Plant-Microbe Interactions

Part of the book series: Subcellular Biochemistry ((SCBI,volume 29))

Abstract

The symbiotic interaction between the soil bacteria classified as Rhizobium or Bradyrhizobium and members of the plant family Leguminosae enables the study of cell-to-cell recognition, signal exchange, and induced morphogenesis. Rhizobia are able to enter the plant root via a sophisticated infection mechanism, induce a new plant organ, the root nodule, and differentiate within the infected plant cells into nitrogen-fixing bacteroids which have properties of an endosymbiont (Hirsch, 1992). The establishment of this symbiosis is controlled by a complex network of signals which are produced by both the bacteria and the plant. In this review we would like to draw attention to the role and functions of rhizobial surface carbohydrates during the establishment of the symbiosis. Rhizobial cells are able to synthesize several surface carbohydrates: lipopolysaccharides (LPS) bound to the outer membrane of the cell, capsular polysaccharides (CPS) and 3-deoxy-D-manno-2-octulosonic acid (KDO)-rich polysaccharides (KPS) associated with the cell surface, and exopolysaccharides (EPS) secreted to the medium.

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References

  • Albersheim, P., and Anderson-Prouty, A. J., 1975, Carbohydrates, proteins, cell surfaces, and the biochemistry of pathogenesis, Ann. Rev. Plant Physiol. 26:31–52.

    Article  CAS  Google Scholar 

  • Aldington, S., McDougall, G. J., and Fry, S. C., 1991, Structure-activity relationships of biologically active oligosaccharides, Plant Cell Environ. 14:625–636.

    Article  CAS  Google Scholar 

  • Aman, P., McNeil, M., Franzen, L.-E., Darvill, A. G., and Albersheim, P., 1981, Structural elucidation, using HPLC-MS and GLC-MS, of the acidic exopolysaccharide secreted by Rhizobium meliloti strain Rm2011, Carbohydr. Res. 95:263–282.

    Article  CAS  Google Scholar 

  • Amemura, A., Hisamatsu, M., Mitani, H., and Harada, T., 1983, Cyclic (1-2)-β-d-glucan and the octasaccharide repeating units of extracellular acidic polysaccharides produced by Rhizobium, Carbohydr. Res. 114:277–285.

    Article  CAS  Google Scholar 

  • An, J., Carlson, R. W., Glushka, J., and Streeter, J. G., 1995, The structure of a novel polysaccharide produced by Bradyrhizobium species with soybean nodules, Carbohydr. Res. 269:303–317.

    Article  PubMed  CAS  Google Scholar 

  • Ardourel, M., Demont, N., Debellé, F., Maillet, F., de Billy, F., Promé, J.-C., Dénarié, J., and Truchet, G., 1994, Rhizobium meliloti lipooligosaccharide nodulation factors: Different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses, Plant Cell 6:1357–1374.

    PubMed  CAS  Google Scholar 

  • Astete, S. G., and Leigh, J. A., 1996, mucS, a gene involved in activation of galactoglucan (EPS II) synthesis gene expression in Rhizobium meliloti, Mol. Plant-Microbe Interact. 9:395–400.

    Article  PubMed  CAS  Google Scholar 

  • Battisti, L., Lara, J. C., and Leigh, J. A., 1992, Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa, Proc. Natl. Acad. Sci. USA 89:5625–5629.

    Article  PubMed  CAS  Google Scholar 

  • Bauer, W. D., 1981, Infection of legumes by rhizobia, Annu. Rev. Plant Physiol. 32:407–449.

    Article  CAS  Google Scholar 

  • Becker, A., Kleickmann, A., Arnold, W., and Pünier, A., 1993a, Analysis of the Rhizobium meliloti exoH/exoK/exoL fragment: ExoK shows homology to excreted endo-beta-1,3-1,4-glucanases and ExoH resembles membrane proteins, Mol. Gen. Genet. 238:145–154.

    PubMed  CAS  Google Scholar 

  • Becker, A., Kleickmann, A., Arnold, W., Keller, M., and Pünier, A., 1993b, Identification and analysis of the Rhizobium meliloti exoAMONP genes involved in exopolysaccharide biosynthesis and mapping of promoters located on the exoHKLAMONP fragment, Mol. Gen. Genet. 241:367–379.

    PubMed  CAS  Google Scholar 

  • Becker, A., Kleickmann, A., Küster, H., Keller, M., Arnold, W., and Pünier, A., 1993c, Analysis of the Rhizobium meliloti genes exoU, exoV, exoW, exoT, and exoI involved in exopolysaccharide biosynthesis and nodule invasion, Mol. Plant-Microbe Interact. 6:735–744.

    Article  PubMed  CAS  Google Scholar 

  • Becker, A., Niehaus, K., and Pünier, A., 1995a, Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated ExoP protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain, Mol. Microbiol. 16:191–203.

    Article  PubMed  CAS  Google Scholar 

  • Becker, A., Küster, H., and Pühler, A., 1995b, Extension of the Rhizobium meliloti succinoglycan biosynthesis gene cluster: identification of the exs A gene encoding an ABC transporter protein, and the exs B gene which probably codes for a regulator of succinoglycan biosynthesis, Mol. Gen. Genet. 249:487–497.

    Article  PubMed  CAS  Google Scholar 

  • Becker, A., Küster, H., Roxlau, A., Keller, M., Ivashina, T., Cheng, H.-P., Walker, G. C., and Pünier, A., 1997, A 32 kb exp gene cluster of Rhizobium meliloti directing the biosynthesis of galactoglucan: Genetic organization and properties of the encoded gene products, J. Bacteriol. 179:1375–1384.

    PubMed  CAS  Google Scholar 

  • Becquart-de Kozak, I., Reuhs, B. L., Buffard, D., Breda, C., Kim, J. S., Esnault, R., and Kendorosi, A., 1997, Role of the K-antigen subgroup of capsular polysaccharides in the early recognition process between Rhizobium meliloti and alfalfa leaves, MPMI 10:114–123.

    Article  CAS  Google Scholar 

  • Bertram-Drogatz, P. A., Quester, I., Becker, A., and Pühler, A., 1998, The Sinorhizobium meliloti MucR protein is essential for the production of high molecular weight succinoglycan exopolysaccharide binds to short DNA regions upstream of exoH and exoY, Mol. Gen. Genet., in press.

    Google Scholar 

  • Bhat, U. R., and Carlson, R. W., 1992, Chemical characterization of pH-dependent structural epitopes of lipopolysaccharides from Rhizobium leguminosarum biovar phaseoli, J. Bacteriol. 174:2230–2235.

    PubMed  CAS  Google Scholar 

  • Bhat, U. R., Krishnaiah, B. S., and Carlson, R. W., 1991a, Re-examination of the structures of the lipopolysaccharide core oligosaccharides from Rhizobium leguminosarum biovar phaseoli, Carbohydr. Res. 220:219–227.

    Article  PubMed  CAS  Google Scholar 

  • Bhat, U. R., Mayer, H., Yokota, A., Hollingsworth, R. I., and Carlson, R. W., 1991b, Occurrence of lipid A variants with 27-hydroxyoctacosanoic acid in lipopolysaccharides from members of the family Rhizobiaceae, J. Bacteriol. 173:2155–2159.

    PubMed  CAS  Google Scholar 

  • Bhat, U. R., Forsberg, L. S., and Carlson, R. W., 1994, Structure of lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide: Unique nonphosphorylated lipid A containing 2-amino-2-deoxygluconate, galacturonate and glucosamine, J. Biol. Chem. 269:14402–14410.

    PubMed  CAS  Google Scholar 

  • Bhuvaneswari, T. V., Turgeon, G. B., and Bauer, W. D., 1980, Early events in the infection of soybean by Rhizobium japonicum. I. Localization of infectable root cells, Plant Physiol. 66:1027–1031.

    Article  PubMed  CAS  Google Scholar 

  • Bohlool, B. B., and Schmidt, E. L., 1974, A possible basis for specificity in the Rhizobium-legume root nodule symbiosis, Science 185:269–271.

    Article  PubMed  CAS  Google Scholar 

  • Bond, L., 1948, Origin and developmental morphology of root nodules of Pisum sativum, Bot. Gaz. 109:411–434.

    Article  Google Scholar 

  • Borthakur, D., and Johnston, A. W. B., 1987, Sequence of psi, a gene of the symbiotic plasmid of Rhizobium phaseoli which inhibits exopolysaccharide synthesis and nodulation and demonstration that its transcription is inhibited by psr, another gene on the symbiotic plasmid, Mol. Gen. Genet. 207:149–154.

    Article  PubMed  CAS  Google Scholar 

  • Borthakur, D., Barber, C. E., Lamb, J. W., Daniels, M. J., Downie, J. A., and Johnston, A. W. B., 1986, A mutation that blocks exopolysaccharide synthesis prevents nodulation of peas by Rhizobium leguminosarum but not by beans by Rhizobium phaseoli and is corrected by cloned DNA from Rhizobium or the phytopathogen Xanthomonas, Mol. Gen. Genet. 203:320–323.

    Article  CAS  Google Scholar 

  • Branca, C., De Lorenzo, G., and Cervone, F., 1988, Competitive inhibition of the auxin-induced elongation by a-d-oligogalacturonides in pea stem segments, Physiol. Plant. 72:499–504.

    Article  CAS  Google Scholar 

  • Brewin, N. J., 1991, Development of the legume root nodule, Annu. Rev. Cell Biol. 7:191–226.

    Article  PubMed  CAS  Google Scholar 

  • Brewin, N., and Kardalsky, I. V., 1997, Legume lectins and nodulation by Rhizobium, Trends in Plant Sci. 2:92–98.

    Article  Google Scholar 

  • Brewin, N. J., Wood, E. A., Larkins, A. P., Gafaré, G., and Butcher, G. W., 1986, Analysis of lipopolysaccharide from root nodule bacteroids of Rhizobium leguminosarum using monoclonal antibodies, J. Gen. Microbiol. 132:1959–1968.

    CAS  Google Scholar 

  • Brzoska, P. M., and Signer, E. R., 1991, lpsZ, a lipopolysaccharide gene involved in symbiosis of Rhizobium meliloti, J. Bacteriol. 173:3235–3237.

    PubMed  CAS  Google Scholar 

  • Buendia, A. M., Enenkel, B., Koplin, R., Niehaus, K., Arnold, W., and Pühler, A., 1991, The Rhizobium meliloti exoZl exoB fragment of megaplasmid 2: ExoB functions as a UDP-glucose 4-epimerase and ExoZ shows homology to NodX of Rhizobium leguminosarum biovar viciae strain TOM, Mol. Microbiol. 5:1519–1530.

    Article  PubMed  CAS  Google Scholar 

  • Caetano Anolles, G., and Gresshoff, P. M., 1991, Plant genetic control of nodulation, Annu. Rev. Microbiol. 45:345–382.

    Article  PubMed  CAS  Google Scholar 

  • Callaham, D. A., and Torrey, J. G., 1981, The structural basis for infection of root hairs of Trifolium repens by Rhizobium, Can. J. Bot. 59:1647–1664.

    Article  Google Scholar 

  • Canter Cremers, H. C., Stevens, K., Lugtenberg, B. J., Wijffelman, C. A., Batley, M., Redmond, J. W., Breedveld, M. W., and Zevenhuizen, L. P., 1991, Unusual structure of the exopolysaccharide of Rhizobium leguminosarum bv. viciae strain 248, Carbohydr. Res. 218:185–200.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, R. W., 1984, Heterogenicity of Rhizobium lipopolysaccharides, J. Bacteriol. 158:548–555.

    Google Scholar 

  • Carlson, R. W., and Garci, F., 1989, The structures of the lipopolysaccharide core components from Rhizobium leguminosarum biovar phaseoli CE3 and two of its symbiotic mutants, CE109 and CE309, Carbohydr. Res. 195:101–110.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, R. W., and Krishnaiah, B. S., 1992, Structures of the oligosaccharides obtained from the core regions of the lipopolysaccharides of Bradyrhizobium japonicum 61A101c and its symbiotically defective lipopolysaccharide mutant, JS314, Carbohydr. Res. 231:205–219.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, R. W., and Yadav, M., 1985, Isolation and partial characterization of the extracellular polysaccharides and lipopolysaccharides from fast-growing Rhizobium japonicum USDA205 and its nod-mutant, HC205, which lacks the symbiotic plasmid, Appl. Environ. Microbiol. 50:1219–1224.

    PubMed  CAS  Google Scholar 

  • Carlson, R. W., Hanley, B., Rolfe, B. G., and Djordjevic, M. A., 1986, A structural comparison of the acidic extracellular polysaccharides from Rhizobium trifolii mutants affected in root hair infection, Plant Physiol. 80:134–137.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, R. W., Kalembasa, S., Turowski, D., Pachori, P., and Noel, K. D., 1987a, Characterization of the lipopolysaccharide from a Rhizobium phaseoli mutant that is defective in infection thread development, J. Bacteriol. 169:4923–4928.

    PubMed  CAS  Google Scholar 

  • Carlson, R. W., Shatters, R., Duh, J.-L., Turnbull, E., Hanley, B., Rolfe, B. G., and Djordjevic, M. A., 1987b, The isolation and partial characterization of the lipopolysaccharides from several Rhizobium trifolii mutants affected in root hair infection, Plant Physiol. 84:421–427.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, R. W., Reuhs, B., Chen, T. B., Bhat, U. R., and Noel, K. D., 1995, Lipopolysaccharide core structures in Rhizobium etli and mutants deficient in O-antigen, J. Biol. Chem. 270:11783–11788.

    Article  PubMed  CAS  Google Scholar 

  • Carrion, M., Bhat, R., Rehus, B., and Carlson, R. W., 1990, Isolation and characterization of the lipopolysaccharides from Bradyrhizobium japonicum, J. Bacteriol. 172:1725–1731.

    PubMed  CAS  Google Scholar 

  • Cava, J. R., Elias, P. M., Turowski, D. A., and Noel, K. D., 1989, Rhizobium leguminosarum CNF42 genetic regions encoding lipopolysaccharide structures essential for complete nodule development on bean plants, J. Bacteriol. 171:8–15.

    PubMed  CAS  Google Scholar 

  • Chakravorty, A. K., Zurkowski, W., Shine, J., and Rolfe, B. G., 1982, Symbiotic nitrogen fixation: Molecular cloning of Rhizobium genes involved in exopolysaccharide synthesis and effective nodulation, J. Mol. Appl. Gen. 1:585–596.

    CAS  Google Scholar 

  • Chandler, M. R., 1978, Some observations on the infection of Arachis hypogaea L. by Rhizobium, J. Exp. Bot. 29:749–755.

    Article  Google Scholar 

  • Chandler, M. R., Date, R. A., and Roughley, R. J., 1982, Infection and root nodule development in Stylosanthes species by Rhizobium, J. Exp. Bot. 33:47–57.

    Article  Google Scholar 

  • Charles, T. C., and Finan, T. M., 1991, Analysis of a 1600-kilobase Rhizobium meliloti megaplasmid using defined deletions generated in vivo, Genetics 127:5–20.

    PubMed  CAS  Google Scholar 

  • Chen, H., Batley, M., Redmond, J., and Rolfe, B. G., 1985, Alteration of the effective nodulation properties of a fast growing broad host range Rhizobium due to changes in exopolysaccharide synthesis, J. Plant Physiol. 120:331–349.

    Article  CAS  Google Scholar 

  • Clover, R. H., Kieber, J., and Signer, E. R., 1989, Lipopolysaccharide mutants of Rhizobium meliloti are not defective in symbiosis, J. Bacteriol. 171:3961–3967.

    PubMed  CAS  Google Scholar 

  • Coplin, D. L., and Cook, D., 1990, Molecular genetics of extracellular polysaccharide biosynthesis in vascular phytopathogenic bacteria, Mol. Plant-Microbe Interact. 3:271–279.

    Article  PubMed  CAS  Google Scholar 

  • Cote, F., and Hahn, M. G., 1994, Oligosaccharins: Structures and signal transduction, Plant Mol. Biol. 26:1379–1411.

    Article  PubMed  CAS  Google Scholar 

  • Currier, W. W., and Strobel, G. A., 1976, Chemotaxis of Rhizobium spp. to plant root exudates, Plant Physiol. 57:820–823.

    Article  PubMed  CAS  Google Scholar 

  • Darvill, A., Augur, C., Bergmann, C., Carlson, R. W., Cheong, J. J., Eberhard, S., Hahn, M. G., Ló, V. M., Marfà, V., Meyer, B., Mohnen, D., O’Neil, M. A., Spiro, M. D., Halbeek, H., York, W. S., and Albersheim, P., 1992, Oligosaccharins—Oligosaccharides that regulate growth, development and defence responses in plants, Glycobiology 2:181–198.

    Article  PubMed  CAS  Google Scholar 

  • Dazzo, F. B., 1980, Lectins and their saccharide receptors as determinants of specificity in the Rhizobium-legume symbiosis, in The Cell Surface: Mediator of Developmental Processes (S. Subtelny and N. K. Wessells, eds.), pp. 81–104, Academic Press, New York.

    Google Scholar 

  • Dazzo, F. B., and Brill, W. J., 1977, Receptor site on clover and alfalfa roots for Rhizobium, Appl. Environ. Microbiol. 33:132–136.

    PubMed  CAS  Google Scholar 

  • Dazzo, F. B., Truchet, G. L., Sherwood, J. E., Hrabak, E. M., Abe, M., and Pankratz, S. H., 1984, Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis, Appl. Environ. Microbiol. 48:87–94.

    Google Scholar 

  • Dazzo, F. B., Truchet, G. L., Hollingsworth, R. I., Hrabak, E. M., Pankratz, H. S., Philip-Hollingsworth, S., Salzwedel, J. L., Chapman, K., Appenzeller, L., Squartini, A., etal., 1991, Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs, J. Bacteriol. 173:5371–5384.

    PubMed  CAS  Google Scholar 

  • Dazzo, F. B., Orgambide, G. G., Philip-Hollingsworth, J., Hollingsworth, R. I., Nike, K. O., and Salzwedel, J. L., 1996, Modulation of development, growth dynamics, wall crystallinity, and infection sites in white clover root hairs by membrane chitolipooligosaccharides from Rhizobium leguminosarum bv. trifolii, J. Bacteriol. 178:3621–3627.

    PubMed  CAS  Google Scholar 

  • DeMaagd, R. A., Rao, A. S., Mulders, I. H. M., Goosen-de Roo, L., VanLoosdrecht, M. C. M., Wijffelman, C. A., and Lugtenberg, B. J. J., 1989, Isolation and characterization of mutants of Rhizobium leguminosarum bv. viciae 248 with altered lipopolysaccharides: Possible role of surface charge or hydrophobicity in bacterial release from the infection thread, J. Bacteriol. 171:1143–1150.

    CAS  Google Scholar 

  • Denarie, J., Debelle, F., and Rosenberg, C., 1992, Signaling and host range variation in nodulation, Annu. Rev. Microbiol. 46:497–531.

    Article  PubMed  CAS  Google Scholar 

  • Denarie, J., Truchet, G., and Prome, J. C., 1994, Lipo-oligosacchaaride signalling: The mediation of recognition and nodule organogenesis induction in the legume-Rhizobium symbiosis, Biochem. Soc. symp. 60:51–60.

    PubMed  CAS  Google Scholar 

  • Diebold, R., and Noel, K. D., 1989, Rhizobium leguminosarum exopolysaccharide mutants: Biochemical and genetic analyses and symbiotic behaviour on three hosts, J. Bacteriol. 171:4821–4830.

    PubMed  CAS  Google Scholar 

  • Djordjevic, S. P., Rolfe, B. G., Batley, M., and Redmond, J. W., 1986, The structure of the exopolysaccharide from Rhizobium sp. strain NGR234, Carbohydr. Res. 148:87–99.

    Article  CAS  Google Scholar 

  • Djordjevic, S. P., Chen, H., Batley, M., Redmond, J. W., and Rolfe, B. G., 1987, Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides, J. Bacteriol. 169:114–126.

    Google Scholar 

  • Doherty, D., Leigh, J. A., Glazebrook, J., and Walker, G. C., 1988, Rhizobium meliloti mutants that overproduce the R. meliloti acidic Calcofluor-binding exopolysaccharide, J. Bacteriol. 170:4249–4256.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Dudman, W. F., 1978, Structural studies of the extracellular polysaccharides of Rhizobium japonicum strains 71a, CC708 and CB1795, Carbohydr. Res. 66:9–23.

    Article  CAS  Google Scholar 

  • Dylan, T., Nagpal, P., Helsinski, D. R., and Ditta, G., 1990, Symbiotic pseudorevertants of R. meliloti ndv mutants, J. Bacteriol. 172:1409–1417.

    PubMed  CAS  Google Scholar 

  • Fahraeus, G., 1957, The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique, J. Gen. Microbiol. 16:374–381.

    Article  PubMed  CAS  Google Scholar 

  • Finan, T. M., Hirsch, A. M., Leigh, J. A., Johansen, E., Kuldau, G. A., Deegan, S., Walker, G. C., and Signer, E. R., 1985, Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation, Cell 40:869–877.

    Article  PubMed  CAS  Google Scholar 

  • Finan, T. M., Kunkel, B., De Vos, G. F., and Signer, E. R., 1986, Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes, J. Bacteriol. 167:66–72.

    PubMed  CAS  Google Scholar 

  • Fischer, H. M., 1994, Genetic regulation of nitrogen fixation in rhizobia, Microbiol. Rev. 58:352–386.

    PubMed  CAS  Google Scholar 

  • Forsbery, L. S., and Reuhs, B. L., 1997, Structural characterization of the K antigens from Rhizobium fredii USDA257: Evidence for a common structural motiv, with strain specific variation, within capsular polysaccharides of Rhizobium spp., J. Bacteriol. 179:5366–5371.

    Google Scholar 

  • Gil-Serrano, A., del Junco, A. S., Tejero-Mateo, P., Megias, M., and Caviedes, M. A., 1990, Structure of the extracellular polysaccharide secreted by Rhizobium leguminosarum var. phaseoli CIAT 899, Carbohydr. Res. 204:103–107.

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook, J., and Walker, G. C., 1989, A novel exopolysaccharide can function in place of the Calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti, Cell 56:661–672.

    Article  PubMed  CAS  Google Scholar 

  • Glucksmann, M. A., Reuber, L., and Walker, G. C., 1993a, Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: A model for succinoglycan biosynthesis, J. Bacteriol. 175:7045–7055.

    PubMed  CAS  Google Scholar 

  • Glucksmann, M. A., Reuber, T. L., and Walker, G. C., 1993b, Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti, J. Bacteriol. 175:7033–7044.

    PubMed  CAS  Google Scholar 

  • Gonzales, J. E., Rehus, B. L., and Walker, G. C., 1996a, Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa, Proc. Natl. Acad. Sci. USA 93:8636–8641.

    Article  Google Scholar 

  • Gonzáles, J. E., York, G. M., and Walker, G. C., 1996b, Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function, Gene 179:141–146.

    Article  Google Scholar 

  • Gross, M., Geier, G., Geider, K., and Rodolph, K., 1992, Levan and levan sucrase synthesized by the fireblight pathogen Erwinia amylovora, Physiol. Mol. Plant Pathol. 40:371–381.

    Article  CAS  Google Scholar 

  • Grosskopf, E., Ha, D. T. C., Wingender, R., Roehrig, H., Szesci, J., Kondorosi, E., Schell, J., and Kondorosi, A., 1993, Enhanced levels of chalcone synthase in alfalfa nodules induced by a Fix negative mutant of Rhizobium meliloti, Mol. Plant-Microbe Interact. 6:173–181.

    Article  CAS  Google Scholar 

  • Gulash, M., Ames, P., LaRosiliere, R. C., and Bergman, K., 1984, Rhizobia are attracted to localized sites in legume roots, Appl. Environ. Microbiol. 48:148–152.

    Google Scholar 

  • Her, G. R., Glazebrook, J., Walker, G. C., and Reinhold, V. N., 1990, Structural studies of a novel exopolysaccharide produced by a mutant of Rhizobium meliloti strain Rm2011, Carbohydr. Res. 198:305–312.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, A. M., and Fang, Y., 1994, Plant hormones and nodulation: What’s the connection? Plant Mol. Biol. 26:5–9.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, P. R., and Spokes, J. D., 1994, Survival and dispersion of genetically modified rhizobia in the field and genetic interactions with native strains, FEMS Microbiol. Ecol. 15:147–159.

    Article  CAS  Google Scholar 

  • Hitchcock, P. J., and Brown, T. M., 1983, Morphological hetrogenicity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels, J. Bacteriol. 154:269–277.

    PubMed  CAS  Google Scholar 

  • Ho, J. C., Wang, J. L., Schindler, M., and Loh, S. T., 1994, Carbohydrate binding activities of Bradyrhizobium japonicwn: III Lectin expression, bacterial binding, and nodulation efficiency, Plant J. 5:873–884.

    Article  PubMed  CAS  Google Scholar 

  • Hollingsworth, R. I., and Dazzo, F. B., 1988, The complete structure of the trifoliin A lectin-binding capsular polysaccharaide of Rhizobium trifolii 843, Carbohydr. Res. 172:92–112.

    Article  Google Scholar 

  • Hollingsworth, R. I., Carlson, R. W., Garcia, F., and Gage, D. A., 1989, A new core tetrasaccharide component from the lipopolysaccharide ai Rhizobium trifolii ANU843, J. Biol. Chem. 264:9294–9299.

    PubMed  CAS  Google Scholar 

  • Hollingsworth, R. I., Zhang, Y., and Priefer, U. B., 1994, Structure of the unusual trisaccharide lipopolysaccharide component produced by a symbiotically defective mutant of Rhizobium leguminosarum biovar viciae, Carbohydr. Res. 264:271–280.

    Article  PubMed  CAS  Google Scholar 

  • Hotter, G. S., and Scott, D. B., 1991, Exopolysaccharide mutants of Rhizobium loti are fully effective on a determinate nodulating host but are ineffective on an indeterminate nodulating host, J. Bacteriol. 173:851–859.

    PubMed  CAS  Google Scholar 

  • Hynes, M. F., Simon, R., Müller, P., Niehaus, K., Labes, M., and Pühler, A., 1986, The two megaplasmids of Rhizobium meliloti are involved in effective nodulation of alfalfa, Mol. Gen. Genet. 1986:356–362.

    Article  Google Scholar 

  • Ielpi, L., Couso, R., and Dankert, M., 1981a, Lipid linked intermediates in the biosynthesis of xanthan gum, FEBS Lett. 130:253–256.

    Article  PubMed  CAS  Google Scholar 

  • Ielpi, L., Couso, R. O., and Dankert, M. A., 1981b, Xanthan gum biosynthesis: Pyruvic avid acetal residues are transferred from phosphoenolpyruvate to the pentasaccharide-P-P-lipid, Biochem. Biophys. Res. Commun. 102:1400–1408.

    Article  PubMed  CAS  Google Scholar 

  • Ielpi, L., Dylan, T., Ditta, G., Helinski, D. R., and Stanfield, S. W., 1990, The ndvB locus of Rhizobium meliloti encodes a 319 KDa protein involved in the production of β-1,2-glucan, J. Biol. Chem. 265:2843–2851.

    PubMed  CAS  Google Scholar 

  • James, E. K., Sprent, J. L., Sutherland, J. M., Mcinroy, S. G., and Minchin, F. R., 1992, The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena, Annu. Bot. 69:173–180.

    Google Scholar 

  • Jansson, P.-E., Kenne, L., Lindberg, B., Ljunggren, H., Lönngren, J., Rudén, U., and Svensson, S., 1977, Demonstration of an octasaccharide repeating unit in the extracellular polysaccharide of Rhizobium meliloti by sequential degradation, J. Am. Chem. Soc. 99:3812–3815.

    Article  PubMed  CAS  Google Scholar 

  • Joshi, P. A., Caetano-Anollés, G., Graham, E. T., and Gresshoff, P. M. (1991, Ontogeny and ultrastructure of spontaneous nodules in alfalfa (Medicago sativa), Protoplasma 162:1–11.

    Article  Google Scholar 

  • Kannenberg, E. L., and Brewin, N. J., 1989, Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH, J. Bacteriol. 171:4543–4548.

    PubMed  CAS  Google Scholar 

  • Kannenberg, E. L., and Brewin, N. J., 1994, Host-plant invasion by Rhizobium: The role of cell-surface components, Trends Microbiol. 2:277–283.

    Article  PubMed  CAS  Google Scholar 

  • Kannenberg, E. L., Rathbun, E. A., and Brewin, N. J., 1992, Molecular dissection of structure and function in the lipopolysaccharide of Rhizobium leguminosarum strain 3841 using monoclonal antibodies and genetic analysis, Mol. Microbiol. 6:2477–2487.

    Article  PubMed  CAS  Google Scholar 

  • Kannenberg, E. L., Perotto, S., Bianciotto, V., Rathbun, E. A., and Brewin, N. J., 1994, Lipopolysaccharide epitope expression of Rhizobium bacteroids as revealed by in situ immunolabelling of pea root nodule sections, J. Bacteriol. 176:2021–2032.

    PubMed  CAS  Google Scholar 

  • Kapp, D., Niehaus, K., Quandt, J., Müller, P., and Pühler, A., 1990, Cooperative action of Rhizobium meliloti nodulation and infection mutants during the process of forming mixed infected alfalfa nodules, Plant Cell 2:139–151.

    PubMed  Google Scholar 

  • Keller, M., Roxlau, A., Weng, W. M., Schmidt, M., Quandt, J., Niehaus, K., Jording, D., Arnold, W., and Pühler, A., 1995, Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan, Mol. Plant-Microb Interact. 8:267–277.

    Article  CAS  Google Scholar 

  • Kim, J. S., Reuhs, B. L., Rahman, M. M., Ridley, B., and Carlson, R. W., 1996. Separation of bacterial capsular and lipopolysaccharides by preparative electrophoresis, Glycobiology 6:433–437.

    Article  PubMed  CAS  Google Scholar 

  • Kiss, E., Reuhs, B. L., Kim, J. S., Kereszt, A., Petrovics, G., Putnoky, P., Dusha, I., Carlson, R. W., and Kandorosin, A., 1997, The rkp GHI and-J genes are involved in capsular polysaccharide production by Rhizobium meliloti, J. Bacteriol. 179:2132–2140.

    PubMed  CAS  Google Scholar 

  • Klein, S., Hirsch, A. M., Smith, C. A., and Signer, E. R., 1988, Interaction of nod and exo Rhizobium meliloti in alfalfa nodulation, Mol. Plant-Microbe Interact. 1:94–100.

    Article  PubMed  CAS  Google Scholar 

  • Kosch, K., Jacobi, A., Parniske, M., Werner, D., and Mueller, P., 1994, The impairment of the nodulation process induced by a Bradyrhizobium japonicum exopolysaccharide mutant is determined by the genotype of the host plant, Z. Naturforsch. C Biosci. 49:727–736.

    CAS  Google Scholar 

  • Lagares, A., Caetano Anolles, G., Niehaus, K., Lorenzen, J., Ljunggren, H. D., Pühler, A., and Favelukes, G., 1992, A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa, J. Bacteriol. 174:5941–5952.

    PubMed  CAS  Google Scholar 

  • Latchford, J. W., Borthakur, D., and Johnston, A. W., 1991, The products of Rhizobium genes, psi and pss, which affect exopolysaccharide production, are associated with the bacterial cell surface, Mol. Microbiol. 5:2107–2114.

    Article  PubMed  CAS  Google Scholar 

  • Legocki, R. P., and Verma, D. P., 1980, Identification of “nodule specific” host proteins (nodulins) involved in the development of rhizobium-legume symbiosis, Cell 20:153–163.

    Article  PubMed  CAS  Google Scholar 

  • Leigh, J. A., and Coplin, D. L., 1992, Exopolysaccharides in plant-bacterial interactions, Annu. Rev. Microbiol. 46:307–346.

    Article  PubMed  CAS  Google Scholar 

  • Leigh, J. A., and Lee, C. C., 1988, Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules, J. Bacteriol. 170:3327–3332.

    PubMed  CAS  Google Scholar 

  • Leigh, J. A., Signer, E. R., and Walker, G. C., 1985, Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules, Proc. Natl. Acad. Sci. USA 85:6231–6235.

    Article  Google Scholar 

  • Leigh, J. A., Reed, J. W., Hanks, J. F., Hirsch, A. M., and Walker, G. C., 1987, Rhizobium meliloti mutants that fail to succinylate their Calcofluor-binding exopolysaccharide are defective in nodule invasion, Cell 51:579–587.

    Article  PubMed  CAS  Google Scholar 

  • Levery, S. B., Zhan, H., Lee, C. C., Leigh, J. A., and Hakomori, S., 1991, Structural analysis of a second acidic exopolysaccharide of Rhizobium meliloti that can function in alfalfa root nodule invasion, Carbohydr. Res. 210:339–347.

    Article  PubMed  CAS  Google Scholar 

  • Libbenga, K. R., and Harkes, P. A. A., 1973, Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L., Planta 114:17–28.

    Article  Google Scholar 

  • Long, S., Reed, J. W., Himawan, J., and Walker, G. C., 1988, Genetic analysis of a cluster of genes required for synthesis of the Calcofluor-binding exopolysaccharide of Rhizobium meliloti, J. Bacteriol. 170:4239–4248.

    PubMed  CAS  Google Scholar 

  • Lopez Lara, I. M., Orgambide, G., Dazzo, F. B., Olivares, J., and Toro, N., 1993, Characterization and symbiotic importance of acidic extracellular polysaccharides of Rhizobium sp. strain GRH2 isolated from acacia nodules, J. Bacteriol. 175:2826–2832.

    PubMed  CAS  Google Scholar 

  • Lopez-Lara, I. M., Orgambide, G., Dazzo, F. B., Olivares, J., and Toro, N., 1995, Surface polysaccharide mutants of Rhizobium sp. (Acacia) strain GRH2: Major requirement of lipopolysaccharide for successful invasion of Acacia nodules and host range determination, Microbiology 141:573–581.

    Article  PubMed  CAS  Google Scholar 

  • Lorkiewicz, Z., Derylo, M., Russa, R., Skorupska, A., and Urbanik Sypniewska, T., 1993, Rhizobium leguminosarum biovar trifolii mutants altered in surface structures that are defective in nodulation or nitrogen fixation, Acta Microbiol. Polon. 42:219–234.

    CAS  Google Scholar 

  • Marfá, V., Gollin, D. J., Eberhard, S., Mohnen, D., Darvill, A., and Albersheim, P., 1991, Oligogalacturonides in suspension-cultured tobacco cells, Plant J. Cell Mol. Biol. 1:217–225.

    Article  Google Scholar 

  • Mateos, P. F., Baker, D. L., PhilipHollingsworth, S., Squartini, A., Peruffo, A. D. B., Nuti, M. P., and Dazzo, F. B., 1995, Direct in situ identification of cellulose microfibrils associated with Rhizobium leguminosarum biovar trifolii attached to the root epidermis of white clover, Can. J. Microbiol. 41:202–207.

    Article  CAS  Google Scholar 

  • Matthysse, A. G., 1983, Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infections, J. Bacteriol. 154:906–915.

    PubMed  CAS  Google Scholar 

  • Matulová, M., Toffanin, R., Navarini, L., Gilli, R., Paoletti, S., and Cesàro, A., 1994, NMR analysis of succinoglycans from different microbial sources: Partial assignment of their 1H and 13C NMR spectra and localization of the succinate and acetate groups, Carbohydr. Res. 265:167–179.

    Article  PubMed  Google Scholar 

  • Mellor, R. B., and Collinge, D. B., 1995, A simple model based on known plant defence reactions is sufficient to explain most aspects of nodulation, J. Exp. Bot. 46:1–18.

    Article  CAS  Google Scholar 

  • Mort, A. J., and Bauer, W. D., 1982, Application of two new methods for cleavage of polysaccharides into specific oligosaccharide fragments, J. Biol. Chem. 257:1870–1875.

    PubMed  CAS  Google Scholar 

  • Müller, P., Hynes, M. F., Kapp, D., Niehaus, K., and Pühler, A., 1988, Two classes of Rhizobium meliloti infection mutants differ in exopolysaccharide production and in coinoculation properties with nodulation mutants, Mol. Gen. Genet. 211:17–26.

    Article  Google Scholar 

  • Müller, P., Keller, M., Weng, W. M., Quandt, J., Arnold, W., and Pühler, A., 1993, Genetic analysis of the Rhizobium meliloti exoYFQ operon: ExoY is homologous to sugar transferases and ExoQ represents a transmembrane protein, Mol. Plant-Microbe Interact. 6:55–65.

    Article  PubMed  Google Scholar 

  • Mulligan, J. T., and Long, S. R., 1985, Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD, Proc. Natl. Acad. Sci. USA 82:6609–6613.

    Article  PubMed  CAS  Google Scholar 

  • Mulligan, J. T., and Long, S. R., 1989, A family of activator genes regulates expression of Rhizobium meliloti nodulation genes, Genetics 122:7–18.

    PubMed  CAS  Google Scholar 

  • Mutaftschiev, S., Vasse, J., and Truchet, G., 1982, Exostructures of Rhizobium meliloti, FEMS Microbiol. Lett. 13:171–175.

    Article  Google Scholar 

  • Napoli, C. A., and Hubbell, D. H., 1975, Ultrastructure of Rhizobium-induced infection threads in clover root hairs, Appl. Microbiol. 30:1003–1009.

    PubMed  CAS  Google Scholar 

  • Newcomb, W., 1981, Nodule morphogenesis and differentiation, in Biology of the Rhizobiaceae (K. L. Giles and A. G. Atherly, eds.), pp. 245–298, Academic Press, New York.

    Google Scholar 

  • Niehaus, K., Kapp, D., and Puehler, A., 1993, Plant defence and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS I)-deficient Rhizobium meliloti mutant, Planta 190:415–425.

    Article  CAS  Google Scholar 

  • Niehaus, K., Baier, R., Lorenzen, J., Meyer-Gattermann, P., Sieben, S., and Pühler, A., 1994, Plant defence in alfalfa pseudonodules induced by an exopolysaccharide (EPS I)-deficient symbiont Rhizobium meliloti, Acta Horticult. 381:258–264.

    CAS  Google Scholar 

  • Niehaus, K., Baier, R., Kohring, B., Flaschel, E., and Pühler, A., 1997a, Symbiotic suppression of the Medicago sativa plant defence system by Rhizobium meliloti oligosaccharides, in Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture (A. Legocki, H. Bothe, and A. Pühler, eds.), pp. 111–114, Springer, Heidelberg.

    Chapter  Google Scholar 

  • Niehaus, K., Lorenzen, J., Lagares, A., and Pühler, A., 1997b, A Rhizobium meliloti lipopolysaccharide mutant effective in Medicago sativa but ineffective in Medicago truncatula, submitted.

    Google Scholar 

  • Noel, K. D., VandenBosch, K. A., and Kulpaca, B., 1986, Mutations in Rhizobium phaseoli that lead to arrested development in infection threads, J. Bacteriol. 168:1392–1401.

    PubMed  CAS  Google Scholar 

  • Noel, K. D., Duelli, D. M., Tao, H., and Brewin, N. J., 1996, Antigenic change in the lipopolysaccharide of Rhizobium etli CFN42 induced by exudates of Phaseolus vulgaris, Mol. Plant-Microbe Interact. 9:180–186.

    Article  CAS  Google Scholar 

  • Østeras, M., Stanley, J., and Finan, T. M., 1995, Identification of Rhizobium-specific intergenic mosaic elements within essential two-component regulatory system of Rhizobium species, J. Bacteriol. 177:5485–5494.

    PubMed  Google Scholar 

  • Ozga, D. A., Lara, J. C., and Leigh, J. A., 1994, The regulation of exopolysaccharide production is important at two levels of nodule development in Rhizobium meliloti, Mol. Plant-Microbe Interact. 7:758–765.

    Article  PubMed  CAS  Google Scholar 

  • Parke, D., Rivelli, M., and Ornston, L. N., 1985, Chemotaxis to aromatic and hydroaromatic acids: Comparison of Bradyrhizobium japonicum and Rhizobium trifolii, J. Bacteriol. 163:417–422.

    PubMed  CAS  Google Scholar 

  • Parniske, M., Schmidt, P. E., Kosch, K., and Mueller, P., 1994, Plant defense response of host plants with determinate nodules induced by EPS-defective exoB mutants of Bradyrhizobium japonicum, Mol. Plant-Microbe Interact. 7:631–638.

    Article  CAS  Google Scholar 

  • Perotto, S., Brewin, N. J., and Kannenberg, E. L., 1994, Cytological evidence for a host defense response that reduces cell and tissue invasion in pea nodules by lipopolysaccharide-defective mutants of Rhizobium leguminosarum strain 3841, Mol. Plant-Microbe Interact. 7:99–112.

    Article  CAS  Google Scholar 

  • Petrovics, G., Putnoky, P., Reuhs, B. L., Kim, J., Thorp, T. A., Noel, K. D., Carlson, R. W., and Kondorosi, A., 1993, The presence of a novel type of surface polysaccharide in Rhizobium meliloti requires a new fatty acid synthase-like gene cluster involved in symbiotic nodule development, Mol. Microbiol. 8:1083–1094.

    Article  PubMed  CAS  Google Scholar 

  • Praveen, N., Webb, D. T., and Borthakur, D., 1996, Leucaena leucocephala nodules formed by a surface polysaccharide defective mutant of Rhizobium sp. strain TALI 145 are delayed in bacteroid development and nitrogen fixation, Mol. Plant-Microbe Interact. 9:364–372.

    Article  Google Scholar 

  • Price, N. P., Jeyaretnam, B., Carlson, R. W., Kadrmas, J. L., Raetz, C. R., and Brozek, K. A., 1995, Lipid A biosynthesis in Rhizobium leguminosarum: Role of a 2-keto-3-deoxyoctulosonate-activated 4′ phosphatase, Proc. Natl. Acad. Sci. USA 92:7352–7356.

    Article  PubMed  CAS  Google Scholar 

  • Priefer, U. B., 1989, Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae VF39, J. Bacteriol. 171:6161–6168.

    PubMed  CAS  Google Scholar 

  • Pull, S. P., Pueppke, S. G., Hymowitz, T., and Ord, J. H., 1978, Soybean lines lacking the 120,000-Dalton seed lectin, Science 200:1277–1279.

    Article  PubMed  CAS  Google Scholar 

  • Putnoky, P. E., Grosskopf, E., Ha, D. T. C., Kiss, G. B., and Kondorosi, A., 1988, Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development, J. Cell Biol. 106:597–607.

    Article  PubMed  CAS  Google Scholar 

  • Puvanesarajah, V., Schell, F. M., Gerhold, D., and Stacey, G., 1987, Cell surface polysaccharides from Bradyrhizobium japonicum and a nonnodulating mutant, J. Bacteriol. 169:137–141.

    PubMed  CAS  Google Scholar 

  • Quandt, J., Hillemann, A., Niehaus, K., Arnold, W., and Pühler, A., 1992, An osmorevertant of a Rhizobium meliloti ndvB deletion mutant forms infection threads but is defective in bacteroid development, Mol. Plant-Microbe Interact. 5:420–427.

    Article  CAS  Google Scholar 

  • Reed, J. W., and Walker, G. C., 1991a, Acidic conditions permit effective nodulation of alfalfa by invasion-deficient Rhizobium meliloti exoD mutants, Genes Dev. 5:2274–2287.

    Article  PubMed  CAS  Google Scholar 

  • Reed, J. W., and Walker, G. C., 1991b, The exoD gene of Rhizobium meliloti encodes a novel function needed for alfalfa nodule invasion, J. Bacteriol. 173:664–677.

    PubMed  CAS  Google Scholar 

  • Reed, J. W., Capage, M., and Walker, G. C., 1991a, Rhizobium meliloti exoG and exoJ mutations affect the exoX-exoY system for modulation of exopolysaccharide production, J. Bacteriol. 173:3776–3788.

    PubMed  CAS  Google Scholar 

  • Reed, J. W., Glazebrook, J., and Walker, G. C., 1991b, The exoR gene of Rhizobium meliloti affects RNA levels of other exo genes but lacks homology to known transcriptional regulators, J. Bacteriol. 173:3789–3794.

    PubMed  CAS  Google Scholar 

  • Reinhold, B. B., Chan, S. Y., Reuber, T. L., Marra, A., Walker, G. C., and Reinhold, V. N., 1994, Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021, J. Bacteriol. 176:1997–2002.

    PubMed  CAS  Google Scholar 

  • Reuber, T. L., and Walker, G. C., 1993a, The acetyl substituent of succinoglycan is not necessary for alfalfa nodule invasion by Rhizobium meliloti Rm1021, J. Bacteriol. 175:3653–3655.

    PubMed  CAS  Google Scholar 

  • Reuber, T. L., and Walker, G. C., 1993b, Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti, Cell 74:269–280.

    Article  PubMed  CAS  Google Scholar 

  • Reuber, T. L., Long, S., and Walker, G. C., 1991, Regulation of Rhizobium meliloti exo genes in free-living cells and in plants examined by using TnphoA fusions, J. Bacteriol. 173:426–434.

    PubMed  CAS  Google Scholar 

  • Reuhs, B. L., Carlson, R. W., and Kim, J. S., 1993, Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-d-manno-2-octulosonic acid-containing polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli, J. Bacteriol. 175:3570–3580.

    PubMed  CAS  Google Scholar 

  • Reuhs, B. L., Kim, J. S., Badgett, A., and Carlson, R. W., 1994, Production of cell-associated polysaccharides of Rhizobium fredii USDA205 is modulated by apigenin and host root extract, MPMI 7:240–247.

    Article  PubMed  CAS  Google Scholar 

  • Reuhs, B. L., Williams, M. N., Kim, J. S., Carlson, R. W., and Cote, F., 1995, Suppression of the Fix-phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K polysaccharide, J. Bacteriol. 177:4289–4296.

    PubMed  CAS  Google Scholar 

  • Rietschel, E. T., Brade, H., Holst, O., Brade, L., Müller-Loennies, S., Mamat, U., Zähringer, U., Beckmann, F., Seydel, U., Brandenburg, K., Ulmer, A. J., Mattern, T., Heine, H., Schletter, J., Loppnow, H., Schönbeck, U., Flad, H.-D., Hauschildt, S., Schade, U. F., Padova, D., Kusumoto, S., and Schumann, R. R., 1996, Bacterial endotoxins: Chemical constitution, biological recognition, host response, and immunological detoxification, in Pathology of Septic Shock (E. T. Rietschel and H. Wagner, eds.), pp. 40–69, Springer, Berlin.

    Chapter  Google Scholar 

  • Robertsen, B. K., Aman, P., Darvill, A. G., McNeil, M., and Albersheim, P., 1981, Host-symbiont interactions V., The structe of acidic extracellular polysaccharides secreted by Rhizobium leguminosarum and Rhizobium trifolii, Plant Physiol. 67:389–400.

    Article  PubMed  CAS  Google Scholar 

  • Rolfe, B. G., Gresshoff, P. M., Shine, J., and Vincent, J. M., 1980, Interaction between a non-nodulating and an ineffective mutant of Rhizobium trifolii resulting in effective (nitrogen fixing) nodulation, Appl. Environ. Microbiol. 39:449–452.

    PubMed  CAS  Google Scholar 

  • Rolfe, B. G., Carlson, R. W., Ridge, R. W., Dazzo, F. B., Mateos, P. F., and Pankhurst, C. E., 1996, Defective infection and nodulation of covers by exopolysaccharide mutants of Rhizobium leguminosarum bv. trifolii, Austral. J. Physiol. 23:285–303.

    Article  CAS  Google Scholar 

  • Ross, P., Mayer, R., and Benziman, M., 1991, Cellulose biosynthesis and function in bacteria, Microbiol. Rev. 55:35–58.

    PubMed  CAS  Google Scholar 

  • Roth, L. E., Jeon, K. W., and Stacey, G., 1988, Homology in endosymbiotic systems: The term “symbiosome,” in Molecular Genetics of Plant-Microbe Interactions (R. Palacios and D. P. S. Verma, eds.), Minnesota, pp. 28–28, APS Press, St. Paul.

    Google Scholar 

  • Russa, R., Urbanik Sypniewska, T., Shashkov, A. S., Kochanowski, H., and Mayer, H., 1995, The structure of the homopolymeric O-specific chain from the phenol soluble LPS of the Rhizobium luti type strain NSP2213, Carbohydr. Polym. 27:299–303.

    Article  CAS  Google Scholar 

  • Russa, R., Bruneteau, M., Shashkov, A. S., Urbanik Sypniewska, T., and Mayer, H., 1996, Characterization of the lipopolysaccharides from Rhizobium meliloti strain 102F51 and its nonnodulating mutant WL113, Arch. Microbiol. 165:26–33.

    Article  PubMed  CAS  Google Scholar 

  • Salzer, P., Hebe, G., Reith, A., Zitterell-Haid, B., Stransky, H., Gaschler, K., and Hager, A., 1996, Rapid reactions of spruce cells to elicitors released from the ectomycorrhizal fungus Hebeloma crustuliniforme, and inactivation of these elicitors by extracellular spruce cell enzymes, Planta 198:118–126.

    Article  CAS  Google Scholar 

  • Saxena, I. M., Kudlicka, K., Okuda, K., and Brown, R. M., 1994, Characterization of genes in the cellulose-synthesizing operon (acs operon) of Acetobacter xylinum: Implications for cellulose crystallization, J. Bacteriol. 176:5735–5752.

    PubMed  CAS  Google Scholar 

  • Schaede, R., 1940, Die Knöllchen der adventiven Wasserwurzeln von Neptunia oleraceae und ihre Bakteriensymbiose, Planta 31:1–21.

    Article  Google Scholar 

  • Schultze, M., and Kondorosi, A., 1995, What makes nodulation signals host-plant specific? Trends Microbiol. 3:370–372.

    Article  PubMed  CAS  Google Scholar 

  • Shiraishi, T., Yamada, T., Saitoh, K., Kato, T., Toyoda, K., Yoshioka, H., Kim, H. M., Ichinose, Y., Tahara, M., and Oku, H., 1994, Suppressors: Determinants of specificity produced by plant pathogens, Plant Cell Physiol. 35:1107–1119.

    CAS  Google Scholar 

  • Sindhu, S. S., Brewin, N. J., and Kannenberg, E. L., 1990, Immunochemical analysis of lipopolysaccharides from free-living and endosymbiotic forms of Rhizobium leguminosarum, J. Bacteriol. 172:1804–1813.

    PubMed  CAS  Google Scholar 

  • Smith, G., Kijne, J., and 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, J. Bacteriol. 169:4294–4301.

    Google Scholar 

  • Smith, G., Logman, T. J. J., Boerrigter, M. E. T. I., Kijne, J., and Lugtenberg, B. J. J., 1989, Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips, J. Bacteriol. 171:4054–4062.

    Google Scholar 

  • Smith, G., Swart, S., Lugtenberg, B. J., and Kijne, J. W., 1992, Molecular mechanisms of attachment of Rhizobium bacteria to plant roots, Mol. Microbiol. 20:2897–2903.

    Article  Google Scholar 

  • Solheim, B., and Fjellheim, K. E., 1984, Rhizobial polysaccharide-degrading enzymes from roots of legumes, Physiol. Plant 62:11–17.

    Article  CAS  Google Scholar 

  • Stacey, G., So, J. S., Roth, L. E., Lakshmi, S. B., and Carlson, R. W., 1991, A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation, Mol. Plant-Microbe Interact. 4:332–340.

    Article  PubMed  CAS  Google Scholar 

  • Tolmasky, M. E., Staneloni, R. J., and Leloir, L. F., 1982, Lipid-bound saccharides in Rhizobium meliloti, J. Biol. Chem. 257:6751–5757.

    PubMed  CAS  Google Scholar 

  • Truchet, G., Barker, D. G., Camut, S., de Billy, F., Vasse, J., and Huguet, T., 1989, Alfalfa nodulation in the absence of Rhizobium, Mol. Gen. Genet. 219:65–68.

    Article  CAS  Google Scholar 

  • Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., De Billy, F., Promé, J. C., and Dénarié, J., 1991, Sulphated lipooligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa, Nature 351:670–673.

    Article  CAS  Google Scholar 

  • Turgeon, B. G., and Bauer, W. D., 1985, Ultrastructure of infection-thread development during the infection of soybean by Rhizobium japonicum, Planta 174:3403–3406.

    Google Scholar 

  • Urzainqui, A., and Walker, G. C., 1992, Exogenous suppression of the symbiotic deficiencies of Rhizobium meliloti exo mutants, J. Bacteriol. 174:3403–3406.

    PubMed  CAS  Google Scholar 

  • Uttaro, A. D., Cangelosi, G. A., Geremia, R. A., Nester, E. W., and Ugalde, R. A., 1990, Biochemical characterization of avirulent exoC mutants of Agrobacterium tumefaciens, J. Bacteriol. 172:1640–1646.

    PubMed  CAS  Google Scholar 

  • VandenBosch, K. A., Bradley, D. J., Knox, J. P., Perotto, S., Butcher, G. W., and Brewin, N. J., 1989a, Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots, EMBO J. 8:335–242.

    PubMed  CAS  Google Scholar 

  • VandenBosch, K. A., Brewin, N. J., and Kannenberg, E. L., 1989b, Developmental regulation of a Rhizobium cell surface antigen during growth of pea root nodules, J. Bacteriol. 171:4537–4542.

    PubMed  CAS  Google Scholar 

  • van Eijsden, R., Diaz, C. L., de Pater, B. J., and Kijne, J. W., 1995, Sugar-binding activity of pea (Pisum sativum) lectin is essential for heterologous infection of transgenic white clover hairy roots by Rhizobium leguminosarum biovar viciae, Plant Mol. Biol. 29:431–439.

    Article  PubMed  Google Scholar 

  • van Spronsen, P. C., Bakhuizen, R., van Brussel, A. A., and Kijne, J. W., 1994, Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process, Eur. J. Cell Biol. 64:88–94.

    PubMed  Google Scholar 

  • Varik, A., 1993, Biological roles of oligosaccharides: All of the theories are correct, Glycobiology 3:97–130.

    Article  Google Scholar 

  • Vasse, J., DeBilly, F., Camut, S., and Truchet, J., 1990, Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules, J. Bacteriol. 172:4295–4306.

    PubMed  CAS  Google Scholar 

  • Vesper, S. J., and Bauer, D. W., 1986, Role of pili (fimbriae) in attachment of Bradyrhizobium japonicum to soybean roots, Appl. Environ. Microbiol. 52:134–141.

    PubMed  CAS  Google Scholar 

  • Vesper, S. L., Malik, N. S. A., and Bauer, W. D., 1987, Transposon mutants of Bradyrhizobium japonicum altered in attachment to host roots, Appl. Environ. Microbiol. 53:1959–1961.

    PubMed  CAS  Google Scholar 

  • Vincent, J. M., 1980, Factors controlling the legume-Rhizobium symbiosis, in Nitrogen Fixation, Vol. 2 (W. H. Newton and W. H. Orme-Johnson, eds.), pp. 103–129, University Park Press, Baltimore, Maryland.

    Google Scholar 

  • Wang, Y., and Hollingsworth, R. I., 1994, The structure of the O-antigenic chain of the lipopolysaccharide of Rhizobium trifolii 4s, Carbohydr. Res. 260:305–317.

    Article  PubMed  CAS  Google Scholar 

  • Whitfield, C., 1995, Biosynthesis of lipopolysaccharide O-antigens, Trends Microbiol. 3:178–185.

    Article  PubMed  CAS  Google Scholar 

  • Williams, M. N., Hollingsworth, R. I., Klein, S., and Signer, E. R., 1990, The sybiotic defect of Rhizobium meliloti exopolysaccharide mutants is suppressed by IpsZ,+ a gene involved in lipopolysaccharide biosynthesis, J. Bacteriol. 172:2622–2632.

    PubMed  CAS  Google Scholar 

  • Wong, H. C., Fear, A. L., Calhoon, R. D., Eichinger, G. H., Mayer, R., Amikam, D., Benziman, M., Gelfand, D. H., Meade, J. H., Emerick, A. W., Bruner, R., Ben-Bassat, A., and Tal, R., 1990, Genetic organization of the cellulose synthase operon in Acetobacter xylinum, Proc. Natl. Acad. Sci. USA 87:8130–8184.

    Article  PubMed  CAS  Google Scholar 

  • Yang, C., 1992, Ultrastructure of infection mode of Rhizobium meliloti exopolysaccharide mutant in alfalfa, Acta Microbiol. Sin. 32:191–197.

    Google Scholar 

  • Yang, C., Signer, E. R., and Hirsch, A. M., 1992, Nodules initiated by Rhizobium meliloti exopolysaccharide mutants lack a discrete, persistent nodule meristem, Plant Physiol. 98:143–151.

    Article  PubMed  CAS  Google Scholar 

  • York, G. M., and Walker, G. C., 1997, The Rhizobium meliloti exoK gene and prsD/prsE/exsH genes are components of independent degradative pathways which contribute to production of low-molecular-weight succinoglycan, Mol. Microbiol. 25:117–134.

    Article  PubMed  CAS  Google Scholar 

  • Zevenhuizen, L. P. T. M., 1986, Selective synthesis of polysaccharides by Rhizobium trifolii, strain TA-1, FEMS Microbiol. Lett. 35:43–47.

    Article  CAS  Google Scholar 

  • Zevenhuizen, L. P., and Faleschini, P., 1991, Effect of the concentration of sodium chloride in the medium on the relative proportions of poly-and oligo-saccharides excreted by Rhizobium meliloti strain YE-2SL, Carbohydr. Res. 209:203–209.

    Article  PubMed  CAS  Google Scholar 

  • Zevenhuizen, L. P. T. M., and van Neerven, A. R. W., 1983, Gel-forming capsular polysaccharide of Rhizobium leguminosarum and Rhizobium trifolii, Carbohydr. Res. 124:166–171.

    Article  CAS  Google Scholar 

  • Zevenhuizen, L. P. T. M., Scholten-Koerselman, I., and Posthumus, M. A., 1980, Lipopolysaccharides of Rhizobium, Arch. Microbiol. 125:1–8.

    Article  CAS  Google Scholar 

  • Zhan, H. J., and Leigh, J. A., 1990, Two genes that regulate exopolysaccharide production in Rhizobium meliloti, J. Bacteriol. 172:5254–5259.

    PubMed  CAS  Google Scholar 

  • Zhan, H. J., Levery, S. B., Lee, C. C., and Leigh, J. A., 1989, A second exopolysaccharide of Rhizobium meliloti strain SU47 that can function in root nodule invasion, Proc. Natl. Acad. Sci. USA 86:3055–3059.

    Article  PubMed  CAS  Google Scholar 

  • Zhan, H. J., Lee, C. C., and Leigh, J. A., 1991, Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations, J. Bacteriol. 173:7391–7394.

    PubMed  CAS  Google Scholar 

  • Zhang, Y., Hollingsworth, R. I., and Priefer, U. B., 1992, Characterization of structural defects in the lipopolysaccharides of symbiotically impaired Rhizobium leguminosarum biovar viciae VF-39 mutants, Carbohydr. Res. 231:261–271.

    Article  PubMed  CAS  Google Scholar 

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Niehaus, K., Becker, A. (1998). The Role of Microbial Surface Polysaccharides in the Rhizobium-Legume Interaction. In: Biswas, B.B., Das, H.K. (eds) Plant-Microbe Interactions. Subcellular Biochemistry, vol 29. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-1707-2_3

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