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Biosynthesis and Secretion of Rhizobial Lipochitin-Oligosaccharide Signal Molecules

  • Chapter
Plant-Microbe Interactions

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

Abstract

Plants that belong to the Leguminosae family are able to establish a symbiosis with soil bacteria belonging to the genera Rhizobium, Bradyrhizobium, and Azorhizobium (collectively called rhizobia). The result of this symbiosis is the formation of a new organ, the root nodule, in which differentiated bacteria convert atmospheric nitrogen into ammonia. The formation of a root nodule involves attachment of the bacteria to the root, invasion of the root by bacteria, development of the root nodule, and differentiation of the bacteria into nitrogen-fixing bacteroids. The exchange of molecular signals between plant and bacterium during nodule formation has been the subject of much research. This chapter will focus on the early stages of nodulation, and will present an overview of the present knowledge on the synthesis of nodulation (Nod) factors: rhizobial lipochitin oligosaccharide signal molecules which are essential for nodulation.

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References

  • Aoyama, K., Haase, A. M., and Reeves, P. R., 1994, Evidence for effect of random genetic drift on G+C content after lateral transfer of fucose pathway genes to Escherichia coli K-12, Mol. Biol. Evol. 11:829–838.

    PubMed  CAS  Google Scholar 

  • Ardourel, M., Demont, N., Debellé, F., Maillet, F., Debilly, 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 

  • Ardourel, M., Lortet, G., Maillet, F., Roche, P., Truchet, G., Promé, J. C., and Rosenberg, C., 1995, In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species, Mol. Microbiol. 17:687–699.

    Article  PubMed  CAS  Google Scholar 

  • Atkinson, E. M., Palcic, M. M., Hindsgaul, O., and Long, S. R., 1994, Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity, Proc. Natl. Acad. Sci. USA 91:8418–8422.

    Article  PubMed  CAS  Google Scholar 

  • Baev, N., Endre, G., Petrovics, G., Banfalvi, Z., and Kondorosi, A., 1991, Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase, Mol. Gen. Genet. 228:113–124.

    Article  PubMed  CAS  Google Scholar 

  • Bakkers, J., Semino, C. E., Stroband, H., Kijne, J. W., Robbins, P. W., and Spaink, H. P., 1997, An important developmental role for oligosaccharides during early embryogenesis of cyprinid fish, Proc. Natl. Acad. Sci. USA 94:7982–7986.

    Article  PubMed  CAS  Google Scholar 

  • Balatti, P. A., Kovacs, L. G., Krishnan, H. B., and Pueppke, S. G., 1995, Rhizobium sp. NGR234 contains a functional copy of the soybean cultivar specificity locus, nolXWBTUV, Mol. Plant-Microbe Interact. 8:693–699.

    Article  CAS  Google Scholar 

  • Barbour, W. M., Hattermann, D. R., and Stacey, G., 1991, Chemotaxis of Bradyrhizobium japonicum to soybean exudates, Appl. Environ. Microbiol. 57:2635–2639.

    PubMed  CAS  Google Scholar 

  • Barnett, M. J., and Long, S. R., 1990, DNA sequence and translational product of a new nodulation regulatory locus: syrM has sequence similarity to NodD proteins, J. Bacteriol. 172:3695–3700.

    PubMed  CAS  Google Scholar 

  • Barny, M. A., and Downie, J. A., 1993, Identification of the NodC protein in the inner but not the outer membrane of Rhizobium leguminosarum, Mol. Plant-Microbe Interact. 6:669–672.

    Article  CAS  Google Scholar 

  • Barny, M. A., Schoonejans, E., Economou, E. S. A., Johnston, A. W. B., and Downie, J. A., 1996, The C-terminal domain of the Rhizobium leguminosarum chitin synthase NodC is important for function and determines the orientation of the N-terminal region in the inner membrane, Mol. Microbiol. 19:443–453.

    Article  PubMed  CAS  Google Scholar 

  • Bastin, D. A., and Reeves, P. R., 1995, Sequence and analysis of the O antigen gene (rfb) cluster of Escherichia coli O111, Gene 164:17–23.

    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 

  • Bec-Ferté, M. P., Krishnan, H. B., Promé, D., Savagnac, A., Pueppke, S. G., and Promé, J. C., 1994, Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257, Biochemistry 33:11782–11788.

    Article  PubMed  Google Scholar 

  • Bec-Ferté, M. P., Krishnan, H. B., Savagnac, A., Pueppke, S. G., and Promé, J. C., 1996, Rhizobium fredii synthesizes an array of lipooligosaccharides, including a novel compound with glucose inserted into the backbone of the molecule, FEBS Lett. 393:273–279.

    Article  PubMed  Google Scholar 

  • Bibb, M. J., Biro, S., Montamedi, H., Collins, J. F., and Hutchinson, C. R., 1989, Analysis of the nucleotide sequence of the Streptomyces glaucescens tcm1 genes provides key information about the enzymology of polyketide antibiotic biosynthesis, EMBO J. 9:2727–2736.

    Google Scholar 

  • Bliss, J. M., and Silver, R. P., 1996, Coating the surface: A model for expression of capsular poiysialic acid in Escherichia coli K1, Mol. Microbiol. 21:221–231.

    Article  PubMed  CAS  Google Scholar 

  • Bloemberg, G. V., Thomas-Oates, J. E., Lugtenberg, B. J. J., and Spaink, H. P., 1994, Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro, Mol. Microbiol. 11:793–804.

    Article  PubMed  CAS  Google Scholar 

  • Bloemberg, G. V., Kamst, E., Harteveld, M., van der Drift, K. M. G. M., Haverkamp, J., Thomas-Oates, J. E., Lugtenberg, B. J. J., and Spaink, H. P., 1995a, A central domain of Rhizobium NodE protein mediates host specificity by determining the hydrophobicity of fatty acyl moieties of nodulation factors, Mol. Microbiol. 16:1123–1136.

    Article  PubMed  CAS  Google Scholar 

  • Bloemberg, G. V., Lagas, R., van Leeuwen, S., van der Marel, G., van Boom, J. H., Lugtenberg, B. J. J., and Spaink, H. P., 1995b, Substrate specificity and kinetic studies of nodulation protein NodL of Rhizobium leguminosarum, Biochemistry 34:12712–12720.

    Article  PubMed  CAS  Google Scholar 

  • Boundy-Mills, K. L., Kosslak, R. M., Tully, R. E., Pueppke, S. G., Lohrke, S., and Sadowsky, M. J., 1994, Induction of the Rhizobium fredii nod box-independent nodulation gene noIJ requires a functional nodD1 gene, Mol. Plant-Microbe Interact. 7:305–308.

    Article  CAS  Google Scholar 

  • Bourdineaud, J. P., Bono, J. J., Ranjeva, R., and Cullimore, J. V., 1995, Enzymatic radiolabelling to a high specific activity of legume lipo-oligosaccharide nodulation factors from Rhizobium meliloti, Biochem. J. 306:259–264.

    PubMed  CAS  Google Scholar 

  • Breedveld, M. W., and Miller, K. J., 1994, Cyclic β-glucans of members of the family Rhizobiaceae, Microbiol. Rev. 58:145–161.

    PubMed  CAS  Google Scholar 

  • Buendia, A. M., Enenkel, B., Köplin, R., Niehaus, K., Arnold, W., and Pühler, A., 1991, The Rhizobium meliloti exoZ/exoB fragment of megaplasmid2: 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Busch, S. J., and Sassone Corsi, P., 1990, Dimers, leucine zippers and DNA-binding domains, Trends Genet. 6:36–40.

    Article  PubMed  CAS  Google Scholar 

  • Caetano-Anolles, G., Wall, L. G., De Micheli, A. T., Macchi, E. M., Bauer, W. D., and Favelukas, G., 1988, Role of motility and chemotaxis in efficiency of nodulation by Rhizobium meliloti, Plant Physiol. 86:1228–1235.

    Article  PubMed  CAS  Google Scholar 

  • Canter Cremers, H. C. J., Wijffelman, C. A., Pees, E., Rolfe, B. G., Djordjevic, M. A., and Lugtenberg, B. J. J., 1988, Host specific nodulation of plants of the pea cross-inoculation group is influenced by genes in fast growing Rhizobium downstream nodC, J. Plant Physiol. 132:398–404.

    Article  Google Scholar 

  • Cardenas, L., Dominquez, J., Quinto, C., López-Lara, I. M., Lugtenberg, B. J. J., Spaink, H. P., Rademaker, G. J., Haverkamp, J., and Thomas-Oates, J. E., 1995, Isolation, chemical structure and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli, Plant Mol. Biol. 29:453–464.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, R. W., Sanjuan, J., Bhat, R., Glushka, J., Spaink, H. P., Wijfjes, A. H. M., van Brussel, A. A. N., Stokkermans, T. J. W., Peters, K., and Stacey, G., 1993, The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and type II strains of Bradyrhizobium japonicum, J. Biol. Chem. 268:18372–18381.

    PubMed  CAS  Google Scholar 

  • Clark, C. A., Beltrame, J., and Manning, P. A., 1991, The oac gene encoding a lipopolysaccharide O-antigen acetylase maps adjacent to the integrase-encoding gene on the genome of Shigella flexneri bacteriophage Sf6, Gene 107:43–52.

    Article  PubMed  CAS  Google Scholar 

  • Cren, M., Kondorosi, A., and Kondorosi, E., 1995, NolR controls expression of the Rhizobium meliloti nodulation genes involved in the core Nod factor synthesis, Mol. Microbiol. 15:733–747.

    Article  PubMed  CAS  Google Scholar 

  • Davis, E. O., Evans, I. J., and Johnston, A. W. B., 1988, Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas, Mol. Gen. Genet. 212:531–535.

    Article  PubMed  CAS  Google Scholar 

  • DeAngelis, P. L., Papaconstantinou, J., and Weigel, P. H., 1993, Molecular cloning, identification, and sequence of the hyaluronan synthase gene from group A Streptococcus pyogenes, J. Biol. Chem. 268:19181–19184.

    PubMed  CAS  Google Scholar 

  • Debellé, F., Rosenberg, C., Vasse, J., Maillet, F., Martinez, E., Dénarié, J., and Truchet, G., 1986, Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti, J. Bacteriol. 168:1075–1086.

    PubMed  Google Scholar 

  • Debellé, F., Roche, P., Plazanet, C., Maillet, F., Pujol, C., Ardourel, M., Demont, N., Rosenberg, C., Truchet, G., Promé, J. C., and Dénarié, J., 1995, The genetics of Rhizobium host range control: Allelic and non-allelic variation, in Nitrogen Fixation: Fundamentals and Applications (I. A. Tikhonovich, ed.), pp. 275–280. Kluwer, The Netherlands.

    Chapter  Google Scholar 

  • Debellé, F., Plazanet, C., Roche, P., Pujol, C., Savagnac, A., Rosenberg, C., Promé, J. C., and Dénarié, J., 1996, The NodA proteins of Rhizobium meliloti and Rhizobium tropici specify the N-acylation of Nod factors by different fatty acids, Mol. Microbiol. 22:303–314.

    Article  PubMed  Google Scholar 

  • De Jong, A. J., Cordewener, J. H. G., Lo Schavio, F., Terzi, M., Vandekerckhove, J., van Kammen, A., and de Vries, S., 1992, A carrot somatic embryo mutant is rescued by chitinase, Plant Cell 4:425–433.

    PubMed  Google Scholar 

  • De Jong, A. J., Heidstra, R., Spaink, H. P., Hartog, M. V., Hendriks, T., Lo Schavio, F., Terzi, M., Bisseling, T., van Kammen, A., and de Vries, S., 1993, A plant somatic embryo mutant is rescued by rhizobial lipo-oligosaccharides, Plant Cell 5:615–620.

    PubMed  Google Scholar 

  • Demont, N., Debellé, F., Aurelle, H., Dénarié, J., and Promé, J. C., 1993, Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors, J. Biol. Chem. 268:20134–20142.

    PubMed  CAS  Google Scholar 

  • Dénarié, J., Debellé, F., and Promé, J. C., 1996, Rhizobium lipo chitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis, Annu. Rev. Biochem. 65:503–535.

    Article  PubMed  Google Scholar 

  • Denk, D., and Bock, A., 1987, L-Cysteine biosynthesis in Escherichia coli: Nucleotide sequence and expression of the serine acetyltransferase (cysE) gene from the wild-type and a cysteine-excreting mutant, J. Gen. Microbiol. 133:3–25.

    Google Scholar 

  • Dillard, J. P., Vandersea, M. W., and Yother, J., 1995, Characterization of the cassette containing genes for type 3 capsular polysaccharide biosynthesis in Streptococcus pneumoniae, J. Exp. Med. 181:973–983.

    Article  PubMed  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. strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides, J. Bacteriol. 169:53–60.

    PubMed  CAS  Google Scholar 

  • Dobert, R. C., Brei, B. T., and Triplett, E. W., 1994, DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria, Mol. Plant-Microbe Interact. 7:564–572.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dutka-Malen, S., Mazodier, P., and Badet, B., 1988, Molecular cloning and overexpression of the glucosamine synthase gene from Escherichia coli, Biochimie 70:287–290.

    Article  PubMed  CAS  Google Scholar 

  • Ehrhardt, D. W., Atkinson, E. M., Faull, K. F., Freedberg, D. I., Sutherlin, D. P., Armstrong, R., and Long, S. R., 1995, In vitro sulfotransferase activity of NodH, a nodulation protein of Rhizobium meliloti required for host-specific nodulation, J. Bacteriol. 177:6237–6245.

    PubMed  CAS  Google Scholar 

  • Evans, I. J., and 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.

    Article  PubMed  CAS  Google Scholar 

  • Fath, M. J., and Kolter, R., 1993, ABC transporters: Bacterial exporters, Microbiol. Rev. 57:995–1017.

    PubMed  CAS  Google Scholar 

  • Fellay, R., Perret, X., Viprey, V., Broughton, W. J., and Brenner, S., 1995, Organization of host-inducible transcripts on the symbiotic plasmid of Rhizobium sp NGR234, Mol. Microbiol. 16:657–667.

    Article  PubMed  CAS  Google Scholar 

  • Felle, H. H., Kondorosi, E., Kondorosi, A., and Schultze, M., 1995, Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide, Plant J. 7:939–947.

    Article  CAS  Google Scholar 

  • Fernández-López, M., D’Haeze, W., Mergaert, P., Verplancke, C., Promé, J. C., van Montagu, M., and Holsters, M., 1996, Role of nodI and nodJ in lipo chitooligosaccharide secretion in Azorhizobium caulinodans and Escherichia coli, Mol. Microbiol. 20:993–1000.

    Article  PubMed  Google Scholar 

  • Firmin, J. L., Wilson, K. E., Carlson, R. W., Davies, A. E., and Downie, J. A., 1993, Resistance to nodulation of cv Afghanistan peas is overcome by nodX which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor, Mol. Microbiol. 10:351–360.

    Article  PubMed  CAS  Google Scholar 

  • Fisher, R. F., Egelhoff, T., Mulligan, J. T., and Long, S. R., 1988, Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes, Genes Dev. 2:282–293.

    Article  PubMed  CAS  Google Scholar 

  • Folch-Mallol, J. L., Marroqui, S., Sousa, S., Manyani, H., López-Lara, I. M., van der Drift, K. M. G. M., Haverkamp, J., Quinto, C., Gil-Serrano, A., Thomas-Oates, J. E., Spaink, H. P., and Megias, M., 1996, Characterization of Rhizobium tropicii CIAT899 nodulation factors: The role of nodH and nodPQ genes in their sulphation, Mol. Plant-Microbe Interact. 9:151–163.

    Article  PubMed  CAS  Google Scholar 

  • Franssen, H. J., Vijn, I., Yang, W. C., and Bisseling, T., 1992, Developmental aspects of the Rhizobium-legume symbiosis, Plant Mol. Biol. 19:89–107.

    Article  PubMed  CAS  Google Scholar 

  • Freiberg, C., Fellay, R., Bairoch, A., Broughton, W. J., Rosenthal, A., and Perret, X., 1997, Molecular basis of symbiosis between Rhizobium and Legumes, Nature 387:394–401.

    Article  PubMed  CAS  Google Scholar 

  • Gaworzewska, E. T., and Carlile, M. J., 1982, Positive chemotaxis of Rhizobium leguminosarum and other bacteria towards root exudates from legumes and other plants, J. Gen. Microbiol. 128:1179–1188.

    CAS  Google Scholar 

  • Geelen, D., Leyman, B., Mergaert, P., Klarskov, K., van Montagu, M., Geremia, R., and Holsters, M., 1995, NodS is an S-adenosyl-L-methionine-dependent methyltransferase that methylates chitooligosaccharides deacetylated at the non-reducing end, Mol. Microbiol. 17:387–397.

    Article  PubMed  CAS  Google Scholar 

  • Geiger, O., Spaink, H. P., and Kennedy, E. P., 1991, Isolation of the Rhizobium leguminosarum NodF nodulation protein: NodF carries a 4′-phosphopantetheine prosthetic group, J. Bacteriol. 173:2872–2878.

    PubMed  CAS  Google Scholar 

  • Geremia, R. A., Mergaert, P., Geelen, D., van Montagu, M., and Holsters, M., 1994, The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase, Proc. Natl. Acad. Sci. USA 91:2669–2673.

    Article  PubMed  CAS  Google Scholar 

  • Ghose, R., Geiger, O., and Prestegard, J. H., 1996, NMR investigations of the structural properties of the nodulation protein, NodF, from Rhizobium leguminosarum and its homology with Escherichia coli acyl carrier protein, FEBS Lett. 388:66–72.

    Article  PubMed  CAS  Google Scholar 

  • Goethals, K., Mergaert, P., Gao, M., Geelen, D., van Montagu, M., and Holsters, M., 1992, Identification of a new inducible nodulation gene in Azorhizobium caulinodans, Mol. Plant-Microbe Interact. 5:405–411.

    Article  PubMed  CAS  Google Scholar 

  • Göttfert, M., 1993, Regulation and function of rhizobial nodulation genes, FEMS Microbiol Rev. 104:39–64.

    Article  Google Scholar 

  • Göttfert, M., Grob, P., and Hennecke, H., 1990, Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum, Proc. Natl. Acad. Sci. USA 87:2680–2684.

    Article  PubMed  Google Scholar 

  • Götz, R., Evans, I. J., Downie, J. A., and Johnston, A. W. B., 1985, Identification of the host-range DNA which allows Rhizobium leguminosarum strain TOM to nodulate cv. Afghanistan peas, Mol Gen. Genet. 201:296–300.

    Article  Google Scholar 

  • Hanin, M., Jabbouri, S., Quesadavincens, D., Freiberg, C., Perret, X., Promé, J. C., Broughton, W. J., and Fellay, R., 1997, Sulphation of Rhizobium sp. NGR234 Nod factors is dependent on noeE, a new host specificity gene, Mol. Microbiol. 24:1119–1129.

    Article  PubMed  CAS  Google Scholar 

  • Heath, R. J., and Rock, C. O., 1995, Regulation of malonyl-CoA metabolism by acyl-acyl carrier protein and beta-ketoacyl-acyl carrier protein synthases in Escherichia coli, J. Biol. Chem. 270:15531–15538.

    Article  PubMed  CAS  Google Scholar 

  • Hediger, M. A., Johnson, D. F., Nierlich, D. P., and Zabin, I., 1985, DNA sequence of the lactose operon: The lacA gene and the transcriptional termination region, Proc. Natl. Acad. Sci. USA 82:6414–6418.

    Article  PubMed  CAS  Google Scholar 

  • Heidstra, R., and Bisseling, T., 1996, Nod factor induced host responses and mechanisms of Nod factor perception, New Phytol. 133:25–43.

    Article  CAS  Google Scholar 

  • Heidstra, R., Geurts, R., Franssen, H., Spaink, H. P., van Kammen, A., and Bisseling, T., 1994, Root hair deformation activity of nodulation factors and their fate on Vicia sativa, Plant Physiol. 105:787–797.

    PubMed  CAS  Google Scholar 

  • Higgins, C. F., Hiles, I. D., Salmond, G. P. C., Gill, D. R., Downie, J. A., Evans, I. J., Holland, I. B., Gray, L., Buckel, S. D., Bell, A. W., and Hermodson, M. A., 1986, A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria, Nature 323:448–450.

    Article  PubMed  CAS  Google Scholar 

  • Holak, T. A., Nilges, M., Prestegard, J. H., Gronenborn, A. M., and Clore, G. M., 1988, Three-dimensional structure of acyl carrier protein in solution determined by nuclear magnetic resonance and the combined use of dynamical simulated annealing and distance geometry, Eur. J. Biochem. 175:9–15.

    Article  PubMed  CAS  Google Scholar 

  • Iñón de Iannino, N., Pueppke, S. G., and Ugalde, R. A., 1995, Biosynthesis of the Nod factor chito-oligosaccharide backbone in Rhizobium fredii is controlled by the concentration of UDP-N-acetyl-D-glucosamine, Mol. Plant-Microbe Interact. 8:292–301.

    Article  Google Scholar 

  • Jabbouri, S., Fellay, R., Talmont, F., Kamalaprija, P., Burger, U., Relic, B., Promé, J. C., and Broughton, W. J., 1995, Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp NGR234 nod factors, J. Biol. Chem. 270:22968–22973.

    Article  PubMed  CAS  Google Scholar 

  • John, M., Röhrig, H., Schmidt, J., Wieneke, U., and Schell, J., 1993, Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase, Proc. Natl. Acad. Sci. USA 90:625–629.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, D., Evans Roth, L., and Stacey, G., 1989, Immunogold localization of the NodC and NodA proteins of Rhizobium meliloti, J. Bacteriol. 171:4583–4588.

    PubMed  CAS  Google Scholar 

  • Kafetzopoulos, D., Thireos, G., Vournakis, J. N., and Bouriotis, V., 1993, The primary structure of a fungal chitin deacetylase reveals the function for two bacterial gene products, Proc. Natl. Acad. Sci. USA 90:8005–8008.

    Article  PubMed  CAS  Google Scholar 

  • Kamst, E., van der Drift, K. M. G. M., Thomas-Oates, J. E., Lugtenberg, B. J. J., and Spaink, H. P., 1995, Mass spectrometric analysis of chitin oligosaccharides produced by Rhizobium NodC protein in Escherichia coli, J. Bacteriol. 177:6282–6285.

    PubMed  CAS  Google Scholar 

  • Kamst, E., Lugtenberg, B. J. J., and Spaink, H. P., 1996, Chitin-oligosaccharide synthesis by the Rhizobium NodC protein, in Chitin Enzymology (R. A. A. Muzzarelli, ed.), pp. 329–338, Atec Edizioni, Italy.

    Google Scholar 

  • Kamst, E., Pilling, J., Raamsdonk, L. M., Lugtenberg, B. J. J., and Spaink, H. P., 1997a, Rhizobium nodulation protein NodC is an important determinant of chitin oligosaccharide chain length in Nod factor biosynthesis, J. Bacteriol. 179:2103–2108.

    PubMed  CAS  Google Scholar 

  • Kamst, E., Bakkers, J., Quaedvlieg, N. E. M., Pilling, J., Kijne, J. W., Lugtenberg, B. J. J., and Spaink, H. P., 1997b, Chitin oligosaccharide synthesis by the bacterial NodC protein and zebrafish DG42 starts at the reducing terminal residue, submitted.

    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 

  • Kijne, J. W., Bakhuizen, R., van Brussel, A. A. N., Caner Cremers, H. C. J., Diaz, C. L., de Pater, B. S., Smit, G., Spaink, H. P., Swart, S., Wijffelman, C. A., and Lugtenberg, B. J. J., 1992, The Rhizobium trap: Root hair curling in root-nodule symbiosis, in Perspectives in Plant Cell Recognition (J. A. Callow and J. R. Green, eds.), pp. 267–284, Cambridge University Press, Cambridge.

    Chapter  Google Scholar 

  • Kim, Y., and Prestegard, J. H., 1990, Refinement of the NMR structures for acyl carrier protein with scalar coupling data, Proteins 8:377–385.

    Article  PubMed  CAS  Google Scholar 

  • Kredich, N. M., 1996, Biosynthesis of cysteine, in Escherichia coli and Salmonella. Cellular and Molecular Biology Vol. 2 (F. C. Neidhardt, ed.), pp. 514–527, ASM Press, Washington, D.C.

    Google Scholar 

  • Leigh, J. A., and Walker, G. C., 1994, Exopolysaccharides of Rhizobium—Synthesis, regulation and symbiotic function, Trends Genet. 10:63–67.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lewis-Henderson, W. R., and Djordjevic, M. A., 1991, nodT, a positively acting cultivar specificity determinant controlling nodulation of Trifolium subterraneum by Rhizobium leguminosarum biovar trifolii, Plant Mol. Biol. 16:515–526.

    Article  PubMed  CAS  Google Scholar 

  • Lie, T. A., 1978, Symbiotic specialization in pea plants: The requirement of specific Rhizobium strains for peas from Afghanistan, Ann. Appl. Biol. 88:462–465.

    Article  Google Scholar 

  • Loh, J., Garcia, M., and Stacey, G., 1997, NodV and NodW, a second flavonoid recognition system regulating nod gene expression in Bradyrhizobium japonicum, J. Bacteriol. 179:3013–3020.

    PubMed  CAS  Google Scholar 

  • López-Lara, I. M., van den Berg, J. D. J., Thomas-Oates, J. E., Glushka, J., Lugtenberg, B. J. J., and Spaink, H. P., 1995a, Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti, Mol. Microbiol. 15:627–638.

    Article  PubMed  Google Scholar 

  • López-Lara, I. M., van der Drift, K. M. G. M, van Brussel, A. A. N., Haverkamp, J., Lugtenberg, B. J. J., Thomas-Oates, J. E., and Spaink, H. P., 1995b, Induction of nodule primordia on Phaseolus and Acacia by lipo-chitin oligosaccharide nodulation signals from broad host range Rhizobium strain GRH2, Plant Mol. Biol. 29:465–477.

    Article  PubMed  Google Scholar 

  • López-Lara, I. M., Blok-Tip, L., Quinto, C., Garcia, M. L., Stacey, G., Bloemberg, G. V., Lamers, G. E. M., Lugtenberg, B. J. J., Thomas-Oates, J. E., and Spaink, H. P., 1996, NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals, Mol. Microbiol. 21:397–408.

    Article  PubMed  Google Scholar 

  • Luka, S., Sanjuan, J., Carlson, R. W., and Stacey, G., 1993, nolMNO genes of Bradyrhizobium japonicum are co-transcribed with nodYABCSUIJ, and nolO is involved in the synthesis of the lipo-oligosaccharide nodulation signals, J. Biol. Chem. 268:27053–27059.

    PubMed  CAS  Google Scholar 

  • Magnuson, K., Jackowski, S., Rock, C. O., and Cronan, J. E., 1993, Regulation of fatty acid biosynthesis in Escherichia coli, Microbiol. Rev. 57:522–542.

    PubMed  CAS  Google Scholar 

  • Maharaj, R., May, T. B., Wang, S. K., and Chakrabarty, A. M., 1993, Sequence of the alg8 and alg44 genes involved in the synthesis of alginate by Pseudomonas aeruginosa, Gene 136:267–269.

    Article  PubMed  CAS  Google Scholar 

  • Marie, C., Barny, M. A., and Downie, J. A., 1992, Rhizobium leguminosarum has two glucosamine synthases, GlmS and NodM, required for nodulation and development of nitrogen-fixing nodules, Mol. Microbiol. 6:843–851.

    Article  PubMed  CAS  Google Scholar 

  • Matthysse, A. G., White, S., and Lightfoot, R., 1995, Genes required for cellulose synthesis in Agrobacterium tumefaciens, J. Bacteriol. 177:1069–1075.

    PubMed  CAS  Google Scholar 

  • Mckay, I. A., and Djordjevic, M. A., 1993, Production and excretion of Nod metabolites by Rhizobium leguminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field, Appl. Env. Nicrobiol. 59:3385–3392.

    CAS  Google Scholar 

  • Meinhardt, L. W., Krishnan, H. B., Balatti, P. A., and Pueppke, S. G., 1993, Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean of Rhizobium fredii USDA257, Mol. Microbiol. 9:17–29.

    Article  PubMed  CAS  Google Scholar 

  • Mergaert, P., van Montagu, M., Promé, J. C., and Holsters, M., 1993, Three unusual modifications, a d-arabinosyl, a N-methyl, and carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571, Proc. Natl. Acad. Sci. USA 90:1551–1555.

    Article  PubMed  CAS  Google Scholar 

  • Mergaert, P., D’Haeze, W., Geelen, D., Promé, D., van Montagu, M., Geremia, R., Promé, J. C., and Holsters, M., 1995, Biosynthesis of Azorhizobium caulinodans Nod factors: Study of the activity of the NodABC proteins by expression of the genes in Escherichia coli, J. Biol. Chem. 270:29217–29223.

    Article  PubMed  CAS  Google Scholar 

  • Mergaert, P., D’Haeze, W., Fernández-López, M., Geelen, D., Goethals, K., Promé, J. C., van Montagu, M., and Holsters, M., 1996, Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: Involvement of nolK, nodZ as well as noeC and/or downstream genes, Mol. Microbiol. 21:409–419.

    Article  PubMed  CAS  Google Scholar 

  • Mergaert, P., van Montagu, M., and Holsters, M., 1997, The nodulation gene nolK of Azorhizobium caulinodans is involved in the formation of GDP fucose from GDP mannose, FEBS Lett. 409:312–316.

    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 127:7–18.

    Google Scholar 

  • Mylona, P., Pawlowski, K., and Bisseling, T., 1995, Symbiotic nitrogen fixation, Plant Cell 7:869–885.

    PubMed  CAS  Google Scholar 

  • Nagahashi, S., Sudoh, M., Ono, N., Sawada, R., Yamaguchi, E., Uchida, Y., Mio, T., Takagi, M., Arisawa, M., and Yamadaokabe, H., 1995, Characterization of chitin synthase 2 of Saccharomyces cerevisiae—Implication of two highly conserved domains as possible catalytic sites, J. Biol. Chem. 270:13961–13967.

    Article  PubMed  CAS  Google Scholar 

  • Ovtsyna, A. O., Veldhuis, A., López-Lara, I. M., Wijfjes, A. H. M., Quinto, C., Geurts, R., Bisseling, T., Scott, D. B., Tikhonovich, I. A., Lugtenberg, B. J. J., and Spaink, H. P., 1997, The host-specific role of chemical modifications at the reducing terminus of lipo-chitin oligosaccharides, in press.

    Google Scholar 

  • Parniske, M., Schmidt, P. E., Kosch, K., and Muller, P., 1994, Plant defense responses 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 

  • Paulson, I. T., Brown, M. H., and Skurray, R. A., 1996, Proton-dependent multidrug efflux systems, Microbiol. Rev. 60:575–608.

    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 

  • Peters, N. K., and Verma, D. P. S., 1990, Phenolic compounds as regulators of gene expression in plant-microbe interactions, Mol. Plant-Microbe Interact. 3:4–8.

    Article  PubMed  CAS  Google Scholar 

  • Pigeon, R. P., and Silver, R. P., 1994, Topological and mutational analysis of KpsM, the hydro-phobic component of the ABC-transporter involved in the export of polysialic acid in Escherichia coli K1, Mol. Microbiol. 14:871–881.

    Article  PubMed  CAS  Google Scholar 

  • Plazanet, C., Refregier, G., Demont, N., Truchet, G., and Rosenberg, C., 1995, The Rhizobium meliloti region located downstream of the nod box n6 is involved in the specific nodulation of Medicago lupulina, FEMS Microbiol. Lett. 133:285–291.

    Article  PubMed  CAS  Google Scholar 

  • Poupot, R., Martinez-Romero, E., and Promé, J. C., 1993, Nodulation factors from Rhizobium tropici are sulphated or non-sulphated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus, Biochemistry, 32:10430–10435.

    Article  PubMed  CAS  Google Scholar 

  • Poupot, R., Martinez-Romero, E., Gautier, N., and Promé, J. C., 1995, Wild type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors, J. Biol. Chem. 270:6050–6055.

    Article  PubMed  CAS  Google Scholar 

  • Price, N. P. J., Relic, B., Taimont, F., Lewin, A., Promé, D., Pueppke, S. G., Maillet, F., Dénarié, J., Promé, J. C., and 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, Mol. Microbiol. 6:3575–3584.

    Article  PubMed  CAS  Google Scholar 

  • Pueppke, S. G., 1996, The genetic and biochemical basis for nodulation of legumes by rhizobia, Crit. Rev. Biotech. 16:1–51.

    Article  CAS  Google Scholar 

  • Quinto, C., Wijfjes, A. H. M., Bloemberg, G. V., Blok-Tip, L., López-Lara, I. M., Lugtenberg, B. J. J., Thomas-Oates, J. E., and Spaink, H. P., 1997, Bacterial nodulation protein NolZ is a chitin oligosaccharide fucosyltransferase which can also recognize related substrates of animal origin, Proc. Natl. Acad. Sci. USA 94:4336–4341.

    Article  PubMed  CAS  Google Scholar 

  • Reizer, J., Reizer, A., and Saier, M. H., 1992, A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates, Protein Sci. 1:1326–1332.

    Article  PubMed  CAS  Google Scholar 

  • Ritsema, T., Geiger, O., van Dillewijn, P., Lugtenberg, B. J. J., and Spaink, H. P., 1994, Serine residue 45 of nodulation protein NodF from Rhizobium leguminosarum bv. viciae is essential for its biological function, J. Bacteriol. 176:7740–7743.

    PubMed  CAS  Google Scholar 

  • Ritsema, T., Wijfjes, A. H. M., Lugtenberg, B. J. J., and Spaink, H. P., 1996, Rhizobium nodulation protein NodA is a host-specific determinant of the transfer of fatty acids in Nod factor biosynthesis, Mol. Gen. Genet. 251:44–51.

    PubMed  CAS  Google Scholar 

  • Ritsema, T., Gehring, A. M., Stuitje, A. R., van der Drift, K. M. G. M., Dandal, I., Lambalot, R. H., Walsh, C. T., Thomas-Oates, J. E., Lugtenberg, B. J. J., and Spaink, H. P., 1997, Functional analysis of interspecies chimera of acyl carrier proteins indicates a specialized domain for protein recognition, Mol. Gen. Genet., in press.

    Google Scholar 

  • Rivilla R., and Downie, J. A., 1994, Identification of a Rhizobium leguminosarum gene homologous to nodT but located outside the symbiotic plasmid, Gene 144:87–91.

    Article  PubMed  CAS  Google Scholar 

  • Rivilla, R., Sutton, J. M., and Downie, J. A., 1995, Rhizobium leguminosarum NodT is related to a family of outer-membrane transport proteins that includes TolC, PrtF, CyaE and AprF, Gene 161:27–31.

    Article  PubMed  CAS  Google Scholar 

  • Robyt, J. F., 1979, Mechanisms involved in the biosynthesis of polysaccharides, Trends Biochem. Sci. 4:47–49.

    Article  CAS  Google Scholar 

  • Roche, P., Debellé, F., Maillet, F., Lerouge, P., Faucher, C., Truchet, G., Dénarié, J., and Promé, J. C., 1991, Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipooligosaccharides signals, Cell 67:1131–1143.

    Article  PubMed  CAS  Google Scholar 

  • Röhrig, H., Schmidt, J., Wieneke, U., Kondorosi, E., Barlier, I., Schell, J., and John, M., 1994, Biosynthesis of lipooligosaccharide nodulation factors—Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone, Proc. Natl. Acad. Sci. USA 91:3122–3126.

    Article  PubMed  Google Scholar 

  • Röhrig, H., Schmidt, J., Waiden, R., Czaja, I., Miklasevics, E., Wieneke, U., Schell, J., and John, M., 1995, Growth of tobacco protoplasts stimulated by synthetic lipo-chitooligosaccharides, Science 269:841–843.

    Article  PubMed  Google Scholar 

  • Rosa, F., Sargent, T. D., Rebbert, M. L., Michaels, G. S., Jamrich, M., Grunz, H., Jonas, E., Winkles, J. A., and Dawid, I. B., 1988, Accumulation and decay of DG42 gene products follow a gradient pattern during Xenopus embryogenesis, Dev. Biol. 129:114–123.

    Article  PubMed  CAS  Google Scholar 

  • Rossen, L., Johnston, A. W. B., and Downie, J. A., 1984, DNA sequence of the Rhizobium leguminosarum nodulation genes nodAB and C required for root hair induction, Nucleic Acids Res. 12:9497–9508.

    Article  PubMed  CAS  Google Scholar 

  • Sadowsky, M. J., Cregan, P. B., Gottfert, M., Sharma, A., Gerhold, D., Rodriguez Quinones, F., Keyser, H. H., Hennecke, H., and Stacey, G., 1991, The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans, Proc. Natl. Acad. Sci. USA 88:637–641.

    Article  PubMed  CAS  Google Scholar 

  • Saier, M. H., Tarn, R., Reizer, A., and Reizer, J., 1994, Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport, Mol. Microbiol. 11:841–847.

    Article  PubMed  CAS  Google Scholar 

  • Sanjuan, J., Grob, P., Göttfert, M., Hennecke, H., and Stacey, G., 1994, NodW is essential for full expression of the common nodulation genes in Bradyrhizobium japonicum, Mol. Plant-Microbe Interact. 7:364–369.

    Article  CAS  Google Scholar 

  • Saxena, I. M., and Brown, R. M., 1996, Identification of cellulose synthase(s) in higher plants: Sequence analysis of processive glycosyltransferases with the common motif D,D,D 35 Q(R/Q)XRW, Cellulose.

    Google Scholar 

  • Saxena, I. M., Kudlicka, K., Okuda, K., and Brown, R. M., 1994, Characterization of genes in the cellulose-synthesizing operon, J. Bacteriol. 176:5735–5752.

    PubMed  CAS  Google Scholar 

  • Schlaman, H. R. M., 1992, Regulation of nodulation gene expression in Rhizobium leguminosarum biovar viciae, PhD thesis, Leiden University.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schmidt, J., John, M., Wieneke, U., Krussmann, H. D., and Schell, J., 1986, Expression of the nodulation gene nodA in Rhizobium meliloti and localization of the gene product in the cytosol, Proc. Natl. Acad. Sci. USA 83:9581–9585.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, J., Wingender, R., John, M., Wieneke, U., and Schell, J., 1988, Rhizobium meliloti nodA and nodB genes are involved in generating compounds that stimulate mitosis of plant cells, Proc. Natl. Acad. Sci. USA 85:8578–8582.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, J., John, M., Wieneke, U., Stacey, G., Röhrig, H., and Schell, J., 1991, Studies of the function Rhizobium meliloti nodulation genes, in Advances in Molecular Genetics of Plant-Microbe Interactions (H. Hennecke and D. P. S. Verma, eds.), pp. 150–155, Kluwer, Dordrecht, The Netherlands.

    Chapter  Google Scholar 

  • Schmidt, J., Röhrig, H., John, M., Wieneke, U., Stacey, G., Koncz, C., and Schell, J., 1993, Alteration of plants growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules, Plant J. 4:651–658.

    Article  CAS  Google Scholar 

  • Schultze, M., and Kondorosi, A., 1996, The role of Nod signal structures in the determination of host specificity in the Rhizobium-legume symbiosis, World J. Microbiol. Biotechnol. 12:137–149.

    Article  CAS  Google Scholar 

  • Schultze, M., Quiclet-Sire, B., Kondorosi, E., Virelizier, H., Glushka, J. N., Endre, G., Géro, S. D., and Kondorosi, A., 1992, Rhizobium meliloti produces a family of sulphated lipo-oligosaccharides exhibiting different degrees of plant host specificity, Proc. Natl. Acad. Sci. USA 89:192–196.

    Article  PubMed  CAS  Google Scholar 

  • Schultze, M., Kondorosi, E., Ratet, P., Buire, M., and Kondorosi, A., 1994, Cell and molecular biology of Rhizobium-plant interactions, Int. Rev. Cytol. 156:1–75.

    Article  CAS  Google Scholar 

  • Schultze, M., Staehelin, C., Röhrig, H., John, M., Schmidt, J., Kondorosi, E., Schell, J., and Kondorosi, A., 1995, In vitro sulfotransferase activity of Rhizobium meliloti NodH protein: Lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure, Proc. Natl. Acad. Sci. USA 92:2706–2709.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schwedock, J. S., Liu, C. X., Leyh, T. S., and Long, S. R., 1994, Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity, J. Bacteriol. 176:7055–7064.

    PubMed  CAS  Google Scholar 

  • Scott, D. B., Young, C. A., Collins-Emerson, J. M., Terzaghi, E. A., Rockman, E. S., Lewis, P. E., and Pankhurst, C. E., 1996, Novel and complex chromosomal arrangement of Rhizobium loti nodulation genes, Mol. Plant-Microbe Interact. 9:187–197.

    Article  PubMed  CAS  Google Scholar 

  • Semino, C. E., and Robbins, P. W., 1995, Synthesis of “Nod”-like chitin oligosaccharides by the Xenopus developmental protein DG42, Proc. Natl. Acad. Sci. USA 92:3498–3501.

    Article  PubMed  CAS  Google Scholar 

  • Shareck, F., Biely, P., Morosoli, R., and Kluepfel, D., 1995, Analysis of DNA flanking the xlnB locus of Streptomyces lividans reveals genes encoding acetyl xylan esterase and the RNA component of ribonuclease P, Gene 153:105–109.

    Article  PubMed  CAS  Google Scholar 

  • Shearman, C. A., Rossen, L., Johnston, A. W. B., and 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 in pea root exudate, EMBO J. 5:647–652.

    PubMed  CAS  Google Scholar 

  • Sherman, D. H., Malpartida, F., Bibb, M. J., Kieser, H. M., and Hopwood, D. A., 1989, Structure and function of the granatacin-producing polyketide synthase cluster of Streptomyces violaceoruber, EMBO J. 8:2717–2725.

    PubMed  CAS  Google Scholar 

  • Slabas, A. R., Chase, D., Nishida, I., Murata, N., Sidebottom, C., Safford, R., Sheldon, P. S., Kekwick, R. G., Hardie, D. G., and Mackintosh, R. W., 1992, Molecular cloning of higher-plant 3-oxoacyl-(acyl carrier protein) reductase, Biochem J. 283:2–6.

    Google Scholar 

  • Smit, G., Swart, S., Lugtenberg, B. J. J., and Kijne, J. W., 1992, Molecular mechanisms of attachment of Rhizobium bacteria to plant roots, Mol. Microbiol. 6:2897–2903.

    Article  PubMed  CAS  Google Scholar 

  • Spaink, H. P., 1995, The molecular basis of infection and nodulation by rhizobia: The ins and outs of sympathogenesis, Annu. Rev. Phytopathol. 33:345–368.

    Article  PubMed  CAS  Google Scholar 

  • Spaink, H. P., 1996, Regulation of plant morphogenesis by lipo chitin oligosaccharides, Crit. Rev. Plant Sci. 15:559–582.

    CAS  Google Scholar 

  • Spaink, H. P., Wijffelman, C. A., Pees, E., Okker, R. J. H., and Lugtenberg, B. J. J., 1987, Rhizobium nodulation gene nodD as a determinant of host specificity, Nature 328:337–340.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Spaink, H. P., Sheeley, D. M., van Brussel, A. A. N., Glushka, J., York, W. S., Tak, T., Geiger, O., Kennedy, E. P., Reinhold, V. N., and 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.

    Article  PubMed  CAS  Google Scholar 

  • Spaink, H. P., Aarts, A., Stacey, G., Bloemberg, G. V., Lugtenberg, B. J. J., and Kennedy, E. P., 1992, Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin layer chromatography, Mol. Plant-Microbe Interact. 5:72–80.

    Article  PubMed  CAS  Google Scholar 

  • Spaink, H. P., Wijfjes, A. H. M., van Vliet, T. B., Kijne, J. W., and Lugtenberg, B. J. J., 1993, Rhizobial lipo-oligosaccharide signals and their role in plant morphogenesis: Are analogous lipophilic chitin derivatives produced by the plant? Aust. J. Plant Physiol. 20:381–392.

    Article  CAS  Google Scholar 

  • Spaink, H. P., Wijfjes, A. H. M., van der Drift, K. M. G. M., Haverkamp, J., Thomas-Oates, J. E., and Lugtenberg, B. J. J., 1994, Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum, Mol. Microbiol. 13:821–831.

    Article  PubMed  CAS  Google Scholar 

  • Spaink, H. P., Bloemberg, G. V., van Brussel, A. A. N., Lugtenberg, B. J. J., van der Drift, K. M. G. M., Haverkamp, J., and Thomas-Oates, J. E., 1995a, Host specificity of Rhizobium leguminosarum is determined by the hydrophobicity of highly unsaturated fatty acyl moieties of the nodulation factors, Mol. Plant-Microbe Interact. 8:155–164.

    Article  CAS  Google Scholar 

  • Spaink, H. P., Wijfjes, A. H. M., and Lugtenberg, B. J. J., 1995b, Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides, J. Bacteriol. 177:6276–6281.

    PubMed  CAS  Google Scholar 

  • Stacey, G., 1995, Bradyrhizobium japonicum nodulation genetics, FEMS Microbiol. Lett. 127:1–9.

    Article  PubMed  CAS  Google Scholar 

  • Stacey, G., Luka, S., Sanjuan, J., Banfalvi, Z., Nieuwkoop, A. J., Chun, J. Y., Forsberg, L. S., and Carlson, R., 1994, NodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum, J. Bacteriol. 176:620–633.

    PubMed  CAS  Google Scholar 

  • Staehelin, C., Granado, J., Muller, J., Wiemken, A., Mellor, R. B., Felix, G., Regenass, M., Broughton, W. J., and Boller, T., 1994, Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases, Proc. Natl. Acad. Sci. USA 91:2196–2200.

    Article  PubMed  CAS  Google Scholar 

  • Staehelin, C., Schultze, M., Kondorosi, E., and Kondorosi, A., 1995, Lipo-chitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa, Plant Physiol. 108:1607–1614.

    PubMed  CAS  Google Scholar 

  • Stokkermans, T. J. W., Ikeshita, S., Cohn, J., Carlson, R. W., Stacey, G., Ogawa, T., and Peters, N. K., 1995, Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja, Plant Physiol. 108:1587–1595.

    Article  PubMed  CAS  Google Scholar 

  • Stokkermans, T. J. W., Orlando, R., Kolli, V. S. K., Carlson, R. W., and Peters, N. K., 1996, Biological activities and structures of Bradyrhizobium elkanii low abundance lipo chitin oligosaccharides, Mol. Plant-Microbe Interact. 9:298–304.

    Article  CAS  Google Scholar 

  • Surin, B. P., and Downie, J. A., 1988, Characterization of the Rhizobium leguminosarum genes nodLMN involved in efficient host nodulation, Mol. Microbiol. 2:173–184.

    Article  PubMed  CAS  Google Scholar 

  • Theberge, M. C., Prevost, D., and Chalifour, F. P., 1996, The effect of different temperatures on the fatty acid composition of Rhizobium leguminosarum bv. viciae in the Faba bean symbiosis, New Phytol. 134:657–664.

    Article  CAS  Google Scholar 

  • Trinick, M. J., and Galbraith, J., 1980, The Rhizobium requirements of the non-legume Parasponia in relationship to the cross inoculation concept of legumes, New Phytol. 86:17–26.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Valdivieso, M. H., Mol, P. C., Shaw, J. A., Cabib, E., and Duran, A., 1991, CALI, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae, J. Cell. Biol. 114:101–109.

    Article  PubMed  CAS  Google Scholar 

  • Van Brussel, A. A. N., Zaat, S. A. J., Canter Cremers, H. C. J., Wijffelman, C. A., Pees, E., Tak, T., and Lugtenberg, B. J. J., 1986, Role of plant root exudate and sym plasmid-localized nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor which causes thick and short roots on common vetch, J. Bacteriol. 165:517–522.

    PubMed  Google Scholar 

  • Van Brussel, A. A. N., Bakhuizen, R., van Spronsen, P. C., Spaink, H. P., Tak, T., Lugtenberg, B. J. J., and Kijne, J. W., 1992, Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium, Science 257:70–72.

    Article  PubMed  Google Scholar 

  • Van der Drift, K. M. G. M., Spaink, H. P., Bloemberg, G. V., Van Brussel, A. A. N., Lugtenberg, B. J. J., Haverkamp, J., and Thomas-Oates, J. E., 1996, Rhizobium leguminosarum bv. trifolii produces lipo chitin oligosaccharides with nodE-dependent highly unsaturated fatty acyl moieties: An electrospray ionization and collision induced dissociation tandem mass spectrometric study, J. Biol. Chem. 271:22563–22569.

    Article  PubMed  Google Scholar 

  • Van Workum, W. A. T., Van Brussel, A. A. N., Tak, T., Wijffelman, C. A., and Kijne, J. W., 1995, Ethylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium leguminosarum bv. viciae, Mol. Plant-Microbe Interact. 8:278–285.

    Article  Google Scholar 

  • Vázquez, M., Davalos, A., de las Penas, A., Sanchez, F., and Quinto, C., 1991, Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains, J. Bacteriol. 173:1250–1258.

    PubMed  Google Scholar 

  • Vázquez, M., Santana, O., and Quinto, C., 1993, The NodI and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion proteins from Gram-negative bacteria, Mol. Microbiol. 8:369–377.

    Article  PubMed  Google Scholar 

  • Verma, N. K., Brandt, J. M., Verma, D. J., and Lindberg, A. A., 1991, Molecular characterization of the O-acetyl transferase gene of converting bacteriophage SF6 that adds group antigen 6 to Shigella flexneri, Mol. Microbiol. 5:71–75.

    Article  PubMed  CAS  Google Scholar 

  • Walker, J. E., Gay, N. J., Saraste, M., and Eberle, A. N., 1984, DNA sequence around the Escherichia coli unc operon. Completion of the sequence of a 17 kilobase segment containing asnA, oriC, unc, glmS, and phoS, Biochem. J. 224:799–815.

    PubMed  CAS  Google Scholar 

  • Wang, L., Romana, L. K., and Reeves, P. R., 1992, Molecular analysis of a Salmonella enterica group El rfb gene cluster: O antigen and the genetic basis of the major polymorphism, Genetics 130:429–443.

    PubMed  CAS  Google Scholar 

  • Whitfield, C., and Valvano, M. A., 1993, Biosynthesis and expression of cell-surface polysaccharides in Gram-negative bacteria, in Advances in Microbial Physiology (A. H. Rose, ed.), pp. 135–246, Academic Press, London.

    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., et al., 1990, Genetic organization of the cellulose synthase operon in Acetobacter xylinum, Proc. Natl. Acad. Sci. USA 87:8130–8134.

    Article  PubMed  CAS  Google Scholar 

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Kamst, E., Spaink, H.P., Kafetzopoulos, D. (1998). Biosynthesis and Secretion of Rhizobial Lipochitin-Oligosaccharide Signal Molecules. 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_2

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