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Lipopolysaccharides in Rhizobium-Legume Symbioses

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Part of the book series: Subcellular Biochemistry ((SCBI,volume 53))

Abstract

The establishment of nitrogen-fixing symbiosis between a legume plant and its rhizobial symbiont requires that the bacterium adapt to changing conditions that occur with the host plant that both promotes and allows infection of the host root nodule cell, regulates and resists the host defense response, permits the exchange of metabolites, and contributes to the overall health of the host. This adaptive process involves changes to the bacterial cell surface and, therefore, structural modifications to the lipopolysaccharide (LPS). In this chapter, we describe the structures of the LPSs from symbiont members of the Rhizobiales, the genetics and mechanism of their biosynthesis, the modifications that occur during symbiosis, and their possible functions.

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Abbreviations

COS:

core oligosaccharide

CPS:

capsular polysaccharide

EPS:

extracellular polysaccharide

ISR:

induced systemic resistance

LA:

lipid A

LCO:

lipochitin oligosaccharide

LPS:

lipopolysaccharides

OPS:

O-chain polysaccharide

VLCFA:

very long chain fatty acid

References

  • Ausubel, F.M. Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6 (2005) 973–979.

    PubMed  CAS  Google Scholar 

  • Basu, S.S., Karbarz, M.J., Raetz, C.R.H. Expression cloning and characterization of the C28 acyltransferase of lipid A biosynthesis in Rhizobium leguminosarum. J Biol Chem 277 (2002) 28959–28971.

    PubMed  CAS  Google Scholar 

  • Basu, S.S., White, K.A., Que, N.L.S., Raetz, C.R.H. A deacylase in Rhizobium leguminosarum membranes that cleaves the 3- O -linked β-hydroxymyristoyl moiety of lipid A precursors. J Biol Chem 274 (1999) 11150–11158.

    PubMed  CAS  Google Scholar 

  • Bhat, U.R., Carlson, R.W., Busch, M., Mayer, H. Distribution and phylogenetic significance of 27-hydroxy- octacosanoic acid in lipopolysaccharides from bacteria belonging to the alpha-2 subgroup of Proteobacteria. Int J Sys Bacteriol 41 (1991) 213–217.

    CAS  Google Scholar 

  • Bhat, U.R., Forsberg, L.S., Carlson, R.W. The structure of the lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide. A unique non-phosphorylated lipid A containing 2-amino-2-deoxy-gluconate, galacturonate, and glucosamine. J Biol Chem 269 (1994) 14402–14410.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bolanos, L., Redondo-Nieto, M., Rivilla, R., Brewin, N.J., Bonilla, I. Cell surface interactions of Rhizobium bacteroids and other bacterial strains with symbiosomal and peribacteroid membrane components from pea nodules. Mol Plant-Microbe Inter 17 (2004) 216–223.

    CAS  Google Scholar 

  • Brewin, N. Plant cell wall remodelling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23 (2004) 293–316.

    CAS  Google Scholar 

  • Brewin, N.J., Perotto, S., Kannenberg, E.L., Rae, A.L., Rathbun, E.A., Lucas, M.M., Kardailsky, I., Gunder, A., Bolanos, L., Donovan, N., Drobak, B.K., Nester, E.W., Verma, D.P.S. Mechanisms of cell and tissue invasion by Rhizobium leguminosarum: The role of cell surface interactions. Current Plant Science and Biotechnology in Agriculture Advances in Molecular Genetics of Plant-Microbe Interactions. Kluwer Academic Publishers, Dordrecht/Boston/London (1993), pp. 369–380.

    Google Scholar 

  • Broughton, W.J., Hanin, M., Relic, B., Kopcinska, J., Golinowski, W., Simsek, S., Ojanen-Reuhs, T., Reuhs, B., Marie, C., Kobayashi, H., Bordogna, B., Le Quere, A., Jabbouri, S., Fellay, R., Perret, X., Deakin, W.J. Flavonoid-inducible modifications to rhamnan O antigens are necessary for Rhizobium sp. strain NGR234-legume symbioses. J Bacteriol 188 (2006) 3654–3663.

    PubMed  CAS  Google Scholar 

  • Carlson, R.W. The heterogeneity of Rhizobium lipopolysaccharides. J Bacteriol 158 (1984) 1012–1017.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Carlson, R.W., Krishnaiah, B.S. 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 (1992) 205–219.

    PubMed  CAS  Google Scholar 

  • Carlson, R.W., Sanders, R.E., Napoli, C., Albersheim, P. Host-symbiont interactions III. Purification and characterization of Rhizobium lipopolysaccharides. Plant Physiol 62 (1978) 912–917.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Casabuono, A.C., D’Antuono, A.L., Sato, Y., Nonami, H., Uglade, R., Lepek, V.C., Erra-Balsells, R., Couto, A.S. A matrix-assisted laser desorption/ionization mass spectrometry approach to the lipid A from Mesorhizobium loti. Rapid Comm Mass Spectrom 20 (2006) 2175–2182.

    CAS  Google Scholar 

  • Cava, J.R., Tao, H., Noel, K.D. Mapping of complementation groups within a Rhizobium leguminosarum CFN42 chromosomal region required for lipopolysaccharide synthesis. Mol Gen Genetics 221 (1990) 125–128.

    CAS  Google Scholar 

  • Choma, A. Lipopolysaccharides from Mesorhizobium huakuii and Mesorhizobium ciceri: Chemical and immunological comparitive data. Acta Biochim Pol 49 (2002) 1043–1052.

    PubMed  CAS  Google Scholar 

  • Choma, A., Sowinski, P. Characterization of Mesorhizobium huakuii lipid A containing both D-galacturonic acid and phosphate residues. Eur J Biochem/FEBS 271 (2004) 1310–1322.

    CAS  Google Scholar 

  • Choma, A., Sowinski, P., Mayer, H. Structure of the O-specific polysaccharide of Mesorhizobium huakuii IFO15243T. Carbohydr Res 329 (2000) 459–464.

    PubMed  CAS  Google Scholar 

  • Creuzenet, C., Lam, J.S. Topological and functional characterization of WbpM, an inner membrane UDP-GlcNAc C6-dehydratase essential for lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 41 (2001) 1295–1310.

    PubMed  CAS  Google Scholar 

  • Creuzenet, C., Schur, M.J., Li, J., Wakarchuk, W.W., Lam, J.S. FlaA1, a new bifunctional UDP-GlcNAc C6-dehydratase/ C4 reductase from Helicobacter pylori. J Biol Chem 275 (2000) 34873–34880.

    PubMed  CAS  Google Scholar 

  • Cronan, G.E., Keating, D.H. Sinorhizobium meliloti sulfotransferase rhat modifies lipopolysaccharide. J Bacteriol 186 (2004) 4168–4176.

    PubMed  CAS  Google Scholar 

  • D’Antuono, A.L., Casabuono, A., Couto, A., Ugalde, R.A., Lepek, V.C. Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis. Mol Plant-Microbe Interact 18 (2005) 446–457.

    PubMed  Google Scholar 

  • D’Haeze, W., Leoff, C., Freshour, G., Noel, K.D., Carlson, R.W. Rhizobium etli CE3 Bacteroid lipopolysaccharides are structurally similar but not identical to those produced by cultured CE3 bacteria. J Biol Chem 282 (2007) 17101–17113.

    PubMed  Google Scholar 

  • De Castro, C., Bedini, E., Garozzo, D., Sturiale, L., Parrilli, M. Structural determination of the O-chain moieties of the lipopolysaccharide fraction from Agrobacterium radiobacter DSM 30147. Eur J Org Chem 2004 (2004) 3842–3849.

    Google Scholar 

  • De Castro, C., Bedini, E., Nunziata, R., Rinaldi, R., Mangoni, L., Parrilli, M. Elucidation of the O-chain structure from the lipopolysaccharide of Agrobacterium tumefaciens strain C58. Carbohydr Res 338 (2003) 1891–1894.

    PubMed  Google Scholar 

  • De Castro, C., Carannante, A., Lanzetta, R., Liparoti, V., Molinaro, A., Parrilli, M. Core oligosaccharide structure from the highly phytopathogenic Agrobacterium tumefaciens TT111 and conformational analysis of the putative rhamnan epitope. Glycobiology 16 (2006) 1272–1280.

    PubMed  Google Scholar 

  • De Castro, C., Carannante, A., Lanzetta, R., Nunziata, R., Piscopo, V., Parrilli, M. Elucidation of two O-chain structures from the lipopolysaccharide fraction of Agrobacterium tumefaciens F/1. Carbohydr Res 339 (2004) 2451–2455.

    PubMed  Google Scholar 

  • De Castro, C., De Castro, O., Molinaro, A., Parrilli, M., Structural determination of the O-chain polysaccharide from Agrobacterium tumefaciens, strain DSM 30205. Eur J Biochem/FEBS 269 (2002) 2885–2888.

    Google Scholar 

  • De Castro, C., Molinaro, A., Lanzetta, R., Silipo, A., Parrilli, M. Lipopolysaccharide structures from Agrobacterium and Rhizobiaceae species. Carbohydr Res 343 (2008) 1924–1933.

    PubMed  Google Scholar 

  • De Castro, C., Sturiale, L., Parrilli, M. Characterisation of the alpha-(1->3) homopolymer of L-glycero-d-manno-heptose units isolated from the O-chain polysaccharide of Agrobacterium radiobacter. Eur J Org Chem 2004 (2004) 2436–2440.

    Google Scholar 

  • de Maagd, R.A., Rao, A.S., Mulders, I.H.M., Goosen-de Roo, L., van Loosdrecht, M.C.M., Wijffelman, C.A., Lugtenberg, B.J.J. 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 (1989) 1143–1150.

    PubMed  Google Scholar 

  • Denison, R.F., Kiers, E.T. Lifestyle alternatives for rhizobia: Mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237 (2004) 187–193.

    PubMed  CAS  Google Scholar 

  • Dow, M., Newman, M.A., von Roepenack, E. The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu Rev Phytopathol 38 (2000) 241–261.

    PubMed  CAS  Google Scholar 

  • Duelli, D.M., Tobin, A., Box, J.M., Kolli, V.S.K., Carlson, R.W., Noel, K.D. Genetic locus required for antigenic maturation of Rhizobium etli CE3 lipopolysaccharide. J Bacteriol 183 (2001) 6054–6064.

    PubMed  CAS  Google Scholar 

  • Fauvart, M., Michiels, J. Rhizobial secreted proteins as determinants of host specificity in the Rhizobium-legume symbiosis. FEMS Microbiol Lett 285 (2008) 1–9.

    PubMed  CAS  Google Scholar 

  • Ferguson, A.D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J.W., Diederichs, K. A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Struct Fold & Design 8 (2000) 585–592.

    CAS  Google Scholar 

  • Ferguson, G.P., Datta, A., Baumgartner, J., Roop, R.M., II, Carlson, R.W., Walker, G.C. Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc Natl Acad Sci USA 101 (2004) 5012–5017.

    PubMed  CAS  Google Scholar 

  • Ferguson, G.P., Datta, A., Carlson, R.W., Walker, G.C. Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol Microbiol 56 (2005) 68–80.

    PubMed  CAS  Google Scholar 

  • Ferguson, G.P., Jansen, A., Marlow, V.L., Walker, G.C. BacA-mediated bleomycin sensitivity in Sinorhizobium meliloti is independent of the unusual lipid A modification. J Bacteriol 188 (2006) 3143–3148.

    PubMed  CAS  Google Scholar 

  • Fernandez de Cordoba, F.J., Rodreguez-Carvajal, M.A., Tejero-Mateo, P., Corzo, J., Gil-Serrano, A.M. Structure of the O-antigen of the main lipopolysaccharide isolated from Sinorhizobium fredii SMH12. Biomacromolecules 9 (2008) 678–685.

    Google Scholar 

  • Forsberg, L.S., Bhat, U.R., Carlson, R.W. Structural characterization of the O-antigenic polysaccharide of the lipopolysaccharide from Rhizobium etli strain CE3. A unique O-acetylated glycan of discrete size, containing 3-O-methyl-6-deoxy-L-talose and 2,3,4-tri-O-methyl-L-fucose. J Biol Chem 275 (2000) 18851–18863.

    PubMed  CAS  Google Scholar 

  • Forsberg, L.S., Carlson, R.W. The structures of the lipopolysaccharides from Rhizobium etli strains CE358 and CE359 – The complete structure of the core region of R. etli lipopolysaccharides. J Biol Chem 273 (1998) 2747–2757.

    PubMed  CAS  Google Scholar 

  • Forsberg, L.S., Carlson, R.W. Structural characterization of the primary O-antigenic polysaccharide of the Rhizobium leguminosarum 3841 lipopolysaccharide and Identification of a new 3-acetimidoylamino-3-deoxyhexuronic acid glycosyl component: A unique O-methylated glycan of uniform size containing 6-deoxy-3-O-methyl-d-talose, N-acetylquinovosamine, and rhizoaminuronic acid (3-acetimidoylamino-3-deoxy-d-gluco-hexuronic acid). J Biol Chem 283 (2008) 16037–16050.

    PubMed  CAS  Google Scholar 

  • Forsberg, L.S., Noel, K.D., Box, J., Carlson, R.W. Genetic locus and structural characterization of the biochemical defect in the O-antigenic polysaccharide of the symbiotically deficient Rhizobium etli mutant, CE166: Replacement of N-acetylquinovosamine with its hexosyl-4-ulose precursor. J Biol Chem 278 (2003) 51347–51359.

    PubMed  CAS  Google Scholar 

  • Fraysse, N., Jabbouri, S., Treilhou, M., Couderc, F., Poinsot, V. Symbiotic conditions induce structural modifications of Sinorhizobium sp. NGR234 surface polysaccharides. Glycobiology 12 (2002) 741–748.

    PubMed  CAS  Google Scholar 

  • Frugier, F., Kosuta, S., Murray, J.D., Crespi, M., Szczyglowski, K. Cytokinin: Secret agent of symbiosis. Trends Plant Sci 13 (2008) 115–120.

    PubMed  CAS  Google Scholar 

  • Gage, D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68 (2004) 280–300.

    PubMed  CAS  Google Scholar 

  • Galibert, F., Finan, T.M., Long, S.R., Puhler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M.J., Becker, A., Boistard, P., Bothe, G., Boutry, M., Bowser, L., Buhrmester, J., Cadieu, E., Capela, D., Chain, P., Cowie, A., Davis, R.W., Dreano, S., Federspiel, N.A., Fisher, R.F., Gloux, S., Godrie, T., Goffeau, A., Golding, B., Gouzy, J., Gurjal, M., Hernandez-Lucas, I., Hong, A., Huizar, L., Hyman, R.W., Jones, T., Kahn, D., Kahn, M.L., Kalman, S., Keating, D.H., Kiss, E., Komp, C., Lelaure, V., Masuy, D., Palm, C., Peck, M.C., Pohl, T.M., Portetelle, D., Purnelle, B., Ramsperger, U., Surzycki, R., Thebault, P., Vandenbol, M., Vorholter, F.-J., Weidner, S., Wells, D.H., Wong, K., Yeh, K.-C., Batut, J. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293 (2001) 668–672.

    PubMed  CAS  Google Scholar 

  • Gargiulo, V., Garozzo, D., Lanzetta, R., Molinaro, A., Sturiale, L., Castro, C.D., Parrilli, M. Rhizobium rubi: A gram-negative phytopathogenic bacterium expressing the Lewis B epitope on the outer core of its lipooligosaccharide fraction. ChemBioChem 9 (2008) 1830–1835.

    PubMed  CAS  Google Scholar 

  • Gibson, K.E., Kobayashi, H., Walker, G.C. Molecular determinants of a symbiotic chronic infection. Ann Rev Gen 42 (2008) 413.

    CAS  Google Scholar 

  • Gil-Serrano, A.M., González-Jiménez, I., Mateo, P.T., Bermabé, M., Jiménez-Barbero, J., Megí as, M., Romero-Vzquez, M.J. Structural analysis of the O-antigen of the lipopolysaccharide of Rhizobium tropici CIAT899. Carbohydr Res 275 (1995) 285–294.

    PubMed  CAS  Google Scholar 

  • Gonzalez, V., Santamaria, R.I., Bustos, P., Hernandez-Gonzalez, I., Medrano-Soto, A., Moreno-Hagelsieb, G., Janga, S.C., Ramirez, M.A., Jimenez-Jacinto, V.N., Collado-Vides, J., Dávila G. The partitioned Rhizobium etli genome: Genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103 (2006) 3834–3839.

    PubMed  Google Scholar 

  • Gudlavalleti, S.K., Forsberg, L.S. Structural Characterization of the lipid A component of Sinorhizobium sp. NGR234 rough and smooth form lipopolysaccharide. Demonstration that the distal amide-linked acyloxyacylresidue containing the long chain fatty acid is conserved in Rhizobium and Sinorhizobium sp.. J Biol Chem 278 (2003) 3957–3968.

    PubMed  CAS  Google Scholar 

  • Heiko Scheidle, Andrea Groß, Karsten Niehaus. The Lipid A substructure of the Sinorhizobium meliloti lipopolysaccharides is sufficient to suppress the oxidative burst in host plants. New Phytol 165 (2005) 559–566.

    Google Scholar 

  • Ingram, B., Sohlenkamp, C., Geiger, O., Raetz, C.R. Altered lipid A structures and polymyxin hypersensitivity of Rhizobium etli mutants lacking the LpxE and LpxF phosphatases. Biochim Biophys Acta. Biochem. Biophys. Acta 1801 (2010) 593–604.

    Google Scholar 

  • Jabbouri, S., Hanin, M., Fellay, R., Quesada-Vincens, D., Reuhs, B., Carlson, R.W., Perret, X., Freiberg, C., Rosenthal, A., Leclerc, D., Broughton, W.J., Relic, B., Stacey, G., Mullin, B., Gresshoff, P.M. Rhizobium species NGR234 host-specificity of nodulation locus III contains nod- and fix- genes. Biology of Plant-Microbe Interactions. ISMPMI, St. Paul (1996), pp. 319–324.

    Google Scholar 

  • Jeyaretnam, B., Glushka, J., Kolli, V.S.K., Carlson, R.W. Characterization of a novel lipid-A from Rhizobium species Sin-1. A unique lipid-A structure that is devoid of phosphate and has a glycosyl backbone consisting of glucosamine and 2-aminogluconic acid. J Biol Chem 277 (2002) 41802–41810.

    PubMed  CAS  Google Scholar 

  • Kadrmas, J.L., Allaway, D., Studholme, R.E., Sullivan, J.T., Ronson, C.W., Poole, P.S., Raetz, C.R.H. Cloning and overexpression of glycosyltransferases that generate the lipopolysaccharide core of Rhizobium leguminosarum. J Biol Chem 273 (1998) 26432–26440.

    PubMed  CAS  Google Scholar 

  • Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Mochizuki, Y., Nakayama, S., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M., Tabata, S. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7 (2000a) 331–338.

    PubMed  CAS  Google Scholar 

  • Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Mochizuki, Y., Nakayama, S., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M., Tabata, S. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (supplement). DNA Res 7 (2000b) 381–406.

    PubMed  CAS  Google Scholar 

  • Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Watanabe, A., Idesawa, K., Iriguchi, M., Kawashima, K., Kohara, M., Matsumoto, M., Shimpo, S., Tsuruoka, H., Wada, T., Yamada, M., Tabata, S. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9 (2002a) 189–197.

    PubMed  Google Scholar 

  • Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Watanabe, A., Idesawa, K., Iriguchi, M., Kawashima, K., Kohara, M., Matsumoto, M., Shimpo, S., Tsuruoka, H., Wada, T., Yamada, M., Tabata, S. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 (supplement). DNA Res 9 (2002b) 225–256.

    PubMed  CAS  Google Scholar 

  • Kanjilal-Kolar, S., Basu, S.S., Kanipes, M.I., Guan, Z., Garrett, T.A., Raetz, C.R.H. Expression Cloning of three Rhizobium leguminosarum lipopolysaccharide core galacturonosyltransferases. J Biol Chem 281 (2006) 12865–12878.

    PubMed  CAS  Google Scholar 

  • Kanjilal-Kolar, S., Raetz, C.R.H. Dodecaprenyl phosphate-galacturonic acid as a donor substrate for lipopolysaccharide core glycosylation in Rhizobium leguminosarum. J Biol Chem 281 (2006) 12879–12887.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kannenberg, E.L., Carlson, R.W. Lipid A, O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol 39 (2001) 379–392.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kannenberg, E.L., Rathbun, E.A., Brewin, N.J. Molecular dissection of structure and function in the lipopolysaccharide of Rhizobium leguminosarum strain 3841 using monoclonal antibodies and genetic analysis. Mol Microbiol 6(17) (1992) 2477–2487.

    PubMed  CAS  Google Scholar 

  • Kannenberg, E.L., Reuhs, B.L., Forsberg, L.S., Carlson, R.W. Lipopolysaccharides, K-antigens: Their structures, biosynthesis, and function. In: Spaink, H.P., Kondorosi, A., Hooykaas, P.J.J (eds.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Dordrecht/Boston/London (1998), pp. 119–154.

    Google Scholar 

  • Karbarz, M.J., Kalb, S.R., Cotter, R.J., Raetz, C.R.H. Expression cloning and biochemical characterization of a Rhizobium leguminosarum lipid A 1-phosphatase. J Biol Chem 278 (2003) 39269–39279.

    PubMed  CAS  Google Scholar 

  • Karbarz, M.J., Six, D.A., Raetz, C.R.H. Purification and characterization of the lipid A 1-phosphatase LpxE of Rhizobium leguminosarum. J Biol Chem 284 (2009) 414–425.

    PubMed  CAS  Google Scholar 

  • Keating, D.H. Sinorhizobium meliloti SyrA mediates the transcriptional regulation of genes involved in lipopolysaccharide sulfation and exopolysaccharide biosynthesis. J Bacteriol 189 (2007) 2510–2520.

    PubMed  CAS  Google Scholar 

  • Keating, D.H., Willits, M.G., Long, S.R. A Sinorhizobium meliloti lipopolysaccharide mutant Altered in cell surface sulfation. J Bacteriol 184 (2002) 6681–6689.

    PubMed  CAS  Google Scholar 

  • Kneidinger, B., Larocque, S., Brisson, J.-R., Cadotte, N., Lam, J.S. Biosynthesis of 2-acetamido-2,6-dideoxy-L-hexoses in bacteria follows a pattern distinct from those of the pathways of 6-deoxy-L-hexoses. Biochem J 371 (2003) 989–995.

    PubMed  CAS  Google Scholar 

  • Kosslak, R.M., Bohlool, B.B. Suppression of nodule development on one side of a split root system of soybean caused by a prior inoculation of the other side. Plant Physiol 75 (1984) 125–130.

    PubMed  CAS  Google Scholar 

  • López-Lara, I.M., Orgambide, G., Dazzo, F.B., Olivares, J., Toro, N. 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 (1995) 573–581.

    PubMed  Google Scholar 

  • Laus, M.C., Logman, T.J., van Brussel, A.A.N., Carlson, R.W., Azadi, P., Gao, M.Y., Kijne, J.W. Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra. J Bacteriol 186 (2004) 6617–6625.

    PubMed  CAS  Google Scholar 

  • Lee, K.-B., De Backer, P., Aono, T., Liu, C.-T., Suzuki, S., Suzuki, T., Kaneko, T., Yamada, M., Tabata, S., Kupfer, D., Najar, F., Wiley, G., Roe, B., Binnewies, T., Ussery, D., D’Haeze, W., Den Herder, J., Gevers, D., Vereecke, D., Holsters, M., Oyaizu, H. The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571. BMC Genomics 9 (2008) 271.

    PubMed  Google Scholar 

  • Lerouge, I., Laeremans, T., Verreth, C., Vanderleyden, J., van Soom, C., Tobin, A., Carlson, R.W. Identification of an ABC transporter for export of the O-antigen across the inner membrane in Rhizobium etli based on the genetic, functional and structural analysis of an lps mutant deficient in O-antigen. J Biol Chem 276 (2001) 17190–17198.

    PubMed  CAS  Google Scholar 

  • Lerouge, I., Vanderleyden, J. O-antigen structural variation: Mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev 26 (2002) 17–47.

    PubMed  CAS  Google Scholar 

  • Lerouge, I., Verreth, C., Michiels, J., Carlson, R.W., Datta, A., Gao, M., Vanderleyden, J. Three genes encoding for putative methyl- and acetyltransferases map adjacent to the wzm and wzt genes and are essential for O-antigen biosynthesis in Rhizobium etli CE3. Mol Plant-Microbe Interact 16 (2003) 1085–1093.

    PubMed  CAS  Google Scholar 

  • Ma, B., Reynolds, C.M., Raetz, C.R.H. Periplasmic orientation of nascent lipid A in the inner membrane of an Escherichia coli LptA mutant. Proc Natl Acad Sci USA 105 (2008) 13823–13828.

    PubMed  CAS  Google Scholar 

  • Marlow, V.L., Haag, A.F., Kobayashi, H., Fletcher, V., Scocchi, M., Walker, G.C., Ferguson, G.P. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol 191 (2009) 1519–1527.

    PubMed  CAS  Google Scholar 

  • Mayer, H., Krauss, J.H., Urbanik-Sypniewska, T., Puvanesarajah, V., Stacey, G., Auling, G. Lipid A with 2,3-diamino-2,3-dideoxyglucose in lipopolysaccharides from slow-growing members of Rhizobiaceae and from Pseudomonas carboxydovorans. Arch Microbiol 151 (1989) 111–116.

    PubMed  CAS  Google Scholar 

  • Miller, W.L., Wenzel, C.Q., Daniels, C., Larocque, S., Brisson, J.-R., Lam, J.S. Biochemical characterization of WbpA, a UDP-N-acetyl-d-glucosamine 6-dehydrogenase involved in O-antigen biosynthesis in Pseudomonas aeruginosa PAO1. J Biol Chem 279 (2004) 37551–37558.

    PubMed  CAS  Google Scholar 

  • Mishra, R., Singh, R., Jaiswal, H., Kumar, V., Maurya, S. Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Curr Microbiol 52 (2006) 383–389.

    PubMed  CAS  Google Scholar 

  • Molinaro, A., De Castro, C., Lanzetta, R., Parrilli, M., Raio, A., Zoina, A. Structural elucidation of a novel core oligosaccharide backbone of the lipopolysaccharide from the new bacterial species Agrobacterium larrymoorei. Carbohydr Res 338 (2003) 2721–2730.

    PubMed  CAS  Google Scholar 

  • Nakano, Y., Suzuki, N., Yoshida, Y., Nezu, T., Yamashita, Y., Koga, T. Thymidine diphosphate-6-deoxy-l-lyxo-4-hexulose reductase synthesizing dTDP-6-deoxy-l-talose from Actinobacillus actinomycetemcomitans. J Biol Chem 275 (2000) 6806–6812.

    PubMed  CAS  Google Scholar 

  • Newman, J., Dow, J.M., Molinaro, A., Parrilli, M. Priming, induction and modulation of plant defence responses by bacterial lipopolysaccharides. J Endotoxin Res 13 (2007) 69 - 84.

    PubMed  CAS  Google Scholar 

  • Noel, K.D., Box, J.M., Bonne, V.J 2-O-Methylation of fucosyl residues of a rhizobial lipopolysaccharideis increased in response to host exudate and is eliminated in a symbiotically defective mutant. Appl Environ Microbiol 70 (2004) 1537–1544.

    PubMed  CAS  Google Scholar 

  • Noel, K.D., Sanchez, A., Fernandez, L., Leemans, J., Cevallos, M.A. Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. J Bacteriol 158 (1984) 148–155.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nürnberger, T., Brunner, F., Kemmerling, B., Piater, L. Innate immunity in plants and animals: Striking similarities and obvious differences. Immunol Rev 198 (2004) 249–266.

    PubMed  Google Scholar 

  • Nürnberger, T., Kemmerling, B. Receptor protein kinases-pattern recognition receptors in plant immunity. Trends Plant Sci 11 (2006) 519–522.

    PubMed  Google Scholar 

  • Ojeda, K.J., Box, J.M., Noel, K.D. Genetic basis for Rhizobium etli CE3 O-antigen O-methylated residues that vary according to growth conditions. J Bacteriol (2009) JB.01154–01109.

    Google Scholar 

  • Oldroyd, G.E.D., Downie, J.A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Ann Rev Plant Biol 59 (2008) 519–546.

    CAS  Google Scholar 

  • Perotto, S., Brewin, N.J., Kannenberg, E.L. 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 (1994) 99–112.

    CAS  Google Scholar 

  • Perotto, S., VandenBosch, K.A., Butcher, G.W., Brewin, N.J. Molecular composition and development of the plant glycocalyx associated with the peribacteroid membrane of pea root nodules. Development 112 (1991) 763–773.

    CAS  Google Scholar 

  • Price, N.P.J., Jeyaretnam, B., Carlson, R.W., Kadrmas, J.L., Raetz, C.R.H., Brozek, K.A. Lipid A biosynthesis in Rhizobium leguminosarum: Role of a novel Kdo activated 4-phosphatase. Proc Natl Acad Sci USA 92 (1995) 7352–7356.

    PubMed  CAS  Google Scholar 

  • Price, N.P.J., Kelly, T.M., Raetz, C.R.H., Carlson, R.W. Biosynthesis of a structurally novel lipid A in Rhizobium leguminosarum: Identification and characterization of six metabolic steps leading from UDP-GlcNAc to Kdo2-lipid IVA. J Bacteriol 176 (1994) 4646–4655.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Que-Gewirth, N.L.S., Karbarz, M.J., Kalb, S.R., Cotter, R.J., Raetz, C.R.H. Origin of the 2-amino-2-deoxy-gluconate unit in Rhizobium leguminosarum Lipid A. Expression cloning of the outer membrane oxidase LpxQ. J Biol Chem 278 (2003a) 12120.

    PubMed  CAS  Google Scholar 

  • Que-Gewirth, N.L.S., Lin, S., Cotter, R.J., Raetz, C.R.H. An outer membrane enzyme that generates the 2-amino-2- deoxy-gluconate moiety of Rhizobium leguminosarum lipid A. J Biol Chem 278 (2003b) 12109.

    PubMed  CAS  Google Scholar 

  • Que, N.L.S., Lin, S.H., Cotter, R.J., Raetz, C.R.H. Purification and mass spectrometry of six lipid A species from the bacterial endosymbiont Rhizobium etli - Demonstration of a conserved distal unit and a variable proximal portion. J Biol Chem 275 (2000a) 28006–28016.

    PubMed  CAS  Google Scholar 

  • Que, N.L.S., Ribeiro, A.A., Raetz, C.R.H. Two-dimensional NMR spectroscopy and structures of six lipid A species from Rhizobium etli CE3-Detection of an acyloxyacyl residue in each component and origin of the aminogluconate moiety. J Biol Chem 275 (2000b) 28017–28027.

    PubMed  CAS  Google Scholar 

  • Raetz, C.R.H., Reynolds, C.M., Trent, M.S., Bishop, R.E. Lipid Amodification systems in gram-negative bacteria. Ann Rev Biochem 76 (2007) 295–329.

    PubMed  CAS  Google Scholar 

  • Raetz, C.R.H., Whitfield, C. Lipopolysaccharide endotoxins. Ann Rev Biochem 71 (2002) 635–700.

    PubMed  CAS  Google Scholar 

  • Reuhs, B.L., Geller, D.P., Kim, J.S., Fox, J.E., Kolli, V.S.K., Pueppke, S.G. Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific K antigens. Appl Environ Microbiol 64 (1998) 4930–4938.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Reuhs, B.L., Relic, B., Forsberg, L.S., Marie, C., Ojanen-Reuhs, T., Stephens, S.B., Wong, C.-H., Jabbouri, S., Broughton, W.J. Structural characterization of a flavonoid-inducible Pseudomonas aeruginosa A-band-Like O antigen of Rhizobium sp. strain NGR234, required for the formation of nitrogen-fixing nodules. J Bacteriol 187 (2005) 6479–6487.

    PubMed  CAS  Google Scholar 

  • Reuhs, B.L., Stephens, S.B., Geller, D.P., Kim, J.S., Glenn, J., Przytycki, J., Ojanen-Reuhs, T. Epitope identification for a panel of anti-Sinorhizobium meliloti monoclonal antibodies and application to the analysis of K antigens and lipopolysaccharides from bacteroids. Appl Environ Microbiol 65 (1999) 5186–5191.

    PubMed  CAS  Google Scholar 

  • Ridley, B.L., Jeyaretnam, B.S., Carlson, R.W. The type and yield of lipopolysaccharide from symbiotically deficient Rhizobium lipopolysaccharide mutants vary depending on the extraction method. Glycobiology 10 (2000) 1013–1023.

    PubMed  CAS  Google Scholar 

  • Rocchetta, H.L., Burrows, L.L., Lam, J.S. Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 63 (1999) 523–553.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Russa, R., Urbanik-Sypniewska, T., Shashkov, A.S., Banaszek, A., Zamojski, A., Mayer, H. Partial structure of lipopolysaccharide isolated from Rhizobium leguminosarum bv. trifolii 24 and its GalA-negative Exo- mutant. System Appl Microbiol 19 (1996) 1–8.

    CAS  Google Scholar 

  • Russa, R., Urbanik-Sypniewska, T., Shashkov, A.S., Kochanowski, H., Mayer, H. The structure of the homopolymeric O-specific chain from the phenol soluble LPS of the Rhizobium loti type strain NZP2213. Carbohydrate Polymers 27 (1995) 299–303.

    CAS  Google Scholar 

  • Sanchez-Contreras, M., Bauer, W.D., Gao, M., Robinson, J.B., Allan Downie, J. Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Phil Trans Royal Soc Biol Sci 362 (2007) 1149–1163.

    CAS  Google Scholar 

  • Sargent, L., Huang, S.Z., Rolfe, B.G., Djordjevic, M. Split-root assays using Trifolium subterraneum show that Rhizobium infection induces a systemic response that can inhibit nodulation of another invasive Rhizobium strain. Appl Environ Microbiol 53 (1987) 1611–1619.

    PubMed  CAS  Google Scholar 

  • Sawada, H., Kuykendall, L.D., Young, J.M. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49 (2003) 155–179.

    PubMed  CAS  Google Scholar 

  • Schmeisser, C., Liesegang, H., Krysciak, D., Bakkou, N., Le Quere, A., Wollherr, A., Heinemeyer, I., Morgenstern, B., Pommerening-Roser, A., Flores, M., Palacios, R., Brenner, S., Gottschalk, G., Schmitz, R.A., Broughton, W.J., Perret, X., Strittmatter, A.W., Streit, W.R. Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75 (2009) 4035–4045.

    PubMed  CAS  Google Scholar 

  • Shah, J. Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Ann Rev Phytopathol 43 (2005) 229–260.

    CAS  Google Scholar 

  • Sharypova, L.A., Niehaus, K., Scheidle, H., Holst, O., Becker, A. Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide. J Biol Chem 278 (2003) 12946–12954.

    PubMed  CAS  Google Scholar 

  • Silipo, A., De Castro, C., Lanzetta, R., Molinaro, A., Parrilli, M. Full structural characterization of the lipid A components from the Agrobacterium tumefaciens strain C58 lipopolysaccharide fraction. Glycobiology 14 (2004) 805–815.

    PubMed  CAS  Google Scholar 

  • Silipo, A., Sturiale, L., Garozzo, D., Erbs, G., Tandrup, T., Lanzetta, J.R., Dow, J.M., Parrilli, M., Newman, M.-A., Molinaro, A. The acylation and phosphorylation pattern of lipid A from Xanthomonas campestris strongly influence its ability to trigger theinnate immune response in Arabidopsis. ChemBioChem 9 (2008) 896–904.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sindhu, S.S., Kannenberg, E.L., Brewin, N.J. Lipopolysaccharide maturation in pea and bean bacteroids. In: Bothe, de, Newton, B. (eds), Nitrogen Fixation: Hundred Years After. Gustav Fischer, Stuttgartand New York (1988), p. 480.

    Google Scholar 

  • Soto, M.J., Domínguez-Ferreras, A., Pérez-Mendoza, D., Sanjuán, J., Olivares, J. Mutualism versus pathogenesis: The give-and-take in plant-bacteria interactions. Cell Microbiol 11 (2009) 381–388.

    PubMed  CAS  Google Scholar 

  • Sprent, J.I. Evolving ideas of legume evolution and diversity: A taxonomic perspective on the occurrence of nodulation. New Phytol 174 (2007) 11–25.

    PubMed  CAS  Google Scholar 

  • Stacey, G., Libault, M., Brechenmacher, L., Wan, J., May, G.D. Genetics and functional genomics of legume nodulation. Curr Op Plant Biol 9 (2006) 110–121.

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Suzuki, N., Nakano, Y., Yoshida, Y., Nezu, T., Terada, Y., Yamashita, Y., Koga, T. Guanosine diphosphate-4-keto-6-deoxy-d-mannose reductase in the pathway for the synthesis of GDP-6-deoxy-D-talose in Actinobacillus actinomycetemcomitans. Eur J Biochem 269 (2002) 5963–5971.

    PubMed  CAS  Google Scholar 

  • Sweet, C.R., Ribeiro, A.A., Raetz, C.R.H. Oxidation and transamination of the 3-position of UDP-N-acetylglucosamine by enzymes from Acidithiobacillus ferrooxidans: Role in the formation of lipid A molecules with four amide-linked acyl chains. J Biol Chem 279 (2004a) 25400–25410.

    PubMed  CAS  Google Scholar 

  • Sweet, C.R., Williams, A.H., Karbarz, M.J., Werts, C., Kalb, S.R., Cotter, R.J., Raetz, C.R.H. Enzymatic synthesis of lipid A molecules with four amide-linked acyl chains: LpxA acyltransferases selective for an analog of UDP-N-acetylglucosamine in which an amine replaces the 3-hydroxyl group. J Biol Chem 279 (2004b) 25411–25419.

    PubMed  CAS  Google Scholar 

  • Tan, X.-J., Cheng, Y., Li, Y.-X., Li, Y.-G., Zhou, J.-C. BacA is indispensable for successful Mesorhizobium–Astragalus symbiosis. Appl Microbiol Biotech 84 (2009) 519–526.

    CAS  Google Scholar 

  • Tao, H., Brewin, N.J., Noel, K.D. Rhizobium leguminosarum CFN42 lipopolysaccharide antigenic changes induced by environmental conditions. J Bacteriol 174 (1992) 2222–2229.

    PubMed  CAS  Google Scholar 

  • Tao, H., Noel, D. Lipopolysaccharide epitopes missing from bean bacteroids. In: Gresshoff, P.M., Roth, L.E., Stacey, G., Newton, W.E. (eds), Nitrogen Fixation: Achievements and Objectives Proceedings of the 8th International Congress on Nitrogen Fixation. Knoxville, Tennessee, USA, May 20–26, 1990. Chapman and Hall, New York and London (1990), p. 276.

    Google Scholar 

  • Tellstrom, V., Usadel, B., Thimm, O., Stitt, M., Kuster, H., Niehaus, K. The lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula. Plant Physiol 143 (2007) 825–837.

    PubMed  Google Scholar 

  • Townsend, G.E., II, Forsberg, L.S., Keating, D.H. Mesorhizobium loti produces nodPQ-dependent sulfated cell surface polysaccharides. J Bacteriol 188 (2006) 8560–8572.

    PubMed  CAS  Google Scholar 

  • Trent, M.S., Pabich, W., Raetz, C.R.H., Miller, S.I. A PhoP/PhoQ-induced lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J Biol Chem 276 (2001) 9083–9092.

    PubMed  CAS  Google Scholar 

  • Turska-Szewczuk, A., Lotocka, B., Kutkowska, J., Król, J., Urbanik-Sypniewska, T., Russa, R. The incomplete substitution of lipopolysaccharide with O-chain prevents the establishment of effective symbiosis between Mesorhizobium loti NZP2213.1 and Lotus corniculatus. Microbiol Res 164 (2009) 163–173.

    PubMed  CAS  Google Scholar 

  • Turska-Szewczuk, A., Palusinska-Szysz, M., Russa, R. Structural studies of the O-polysaccharide chain from the lipopolysaccharide of symbiotically enhanced mutant Mlo-13 of Mesorhizobium loti NZP2213. Carbohydr Res 343 (2008) 477–482.

    PubMed  CAS  Google Scholar 

  • Turska-Szewczuk, A., Pietras, H., Borucki, W., Russa, R. Alteration of O-specific polysaccharide structure of symbiotically defective Mesorhizobium 2213.1 derived from strain NZP2213. Acta Biochim Pol 55 (2008) 191–199.

    PubMed  CAS  Google Scholar 

  • van de Wiel, C., Norris, J.H., Bochenek, B., Dickstein, R., Bisseling, T., Hirsch, A.M. Nodulin gene expression and ENOD2 localization in effective, nitrogen-fixing and ineffective, bacteria-free nodules of alfalfa. Plant Cell 2 (1990) 1009–1017.

    Google Scholar 

  • VandenBosch, K.A., Brewin, N.J., Kannenberg, E.L. Developmental regulation of a rhizobium cell-surface antigen during growth of pea root-nodules. J Bacteriol 171 (1989) 4537–4542.

    PubMed  CAS  Google Scholar 

  • VandenBosch, K.A., Noel, K.D., Kaneko, Y., Newcomb, E.H. Nodule initiation elicited by noninfective mutants of Rhizobium phaseoli. J Bacteriol 162 (1985) 950–959.

    PubMed  CAS  Google Scholar 

  • Vanderlinde, E.M., Muszynski, A., Harrison, J.J., Koval, S.F., Foreman, D.L., Ceri, H., Kannenberg, E.L., Carlson, R.W., Yost, C.K. Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155 (2009) 3055–3069.

    PubMed  CAS  Google Scholar 

  • Vedam, V., Haynes, J.G., Kannenberg, E.L., Carlson, R.W., Sherrier, D.J. A Rhizobium leguminosarum lipopolysaccharide lipid A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol Plant-Microbe Interact 17 (2004) 283–291.

    PubMed  CAS  Google Scholar 

  • Vedam, V., Kannenberg, E., Datta, A., Brown, D., Haynes-Gann, J.G., Sherrier, D.J., Carlson, R.W. The pea nodule environment restores the ability of a Rhizobium leguminosarum lipopolysaccharide acpXL mutant to add 27-hydroxyoctacosanoic acid to its lipid A. J Bacteriol 188 (2006) 2126–2133.

    PubMed  CAS  Google Scholar 

  • Vedam, V., Kannenberg, E.L., Haynes, J.G., Sherrier, D.J., Datta, A., Carlson, R.W. A Rhizobium leguminosarum acpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J Bacteriol 185 (2003) 1841–1850.

    PubMed  CAS  Google Scholar 

  • Wang, X., Karbarz, M.J., McGrath, S.C., Cotter, R.J., Raetz, C.R.H. MsbA transporter-dependent lipid A 1-dephosphorylation on theperiplasmic surface of the inner membrane: Topography of Francisella novicida LpxE expressed in Escherichia coli. J Biol Chem 279 (2004) 49470–49478.

    PubMed  CAS  Google Scholar 

  • Wang, X., McGrath, S.C., Cotter, R.J., Raetz, C.R.H. Expression cloning and periplasmic orientation of the Francisella novicida lipid A 4'-phosphatase LpxF. J Biol Chem 281 (2006) 9321–9330.

    PubMed  CAS  Google Scholar 

  • Wang, X., Ribeiro, A.A., Guan, Z., Abraham, S.N., Raetz, C.R.H. Attenuated virulence of a Francisella mutant lacking the lipid A 4'-phosphatase. Proc Natl Acad Sci USA 104 (2007) 4136–4141.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Westphal, O., Jann, K., Bacterial lipopolysaccharides, Meth Carbohydr Chem, 5 (1965) 83–91.

    CAS  Google Scholar 

  • Wood, D.W., Setubal, J.C., Kaul, R., Monks, D.E., Kitajima, J.P., Okura, V.K., Zhou, Y., Chen, L., Wood, G.E., Almeida, N.F., Jr., Woo, L., Chen, Y., Paulsen, I.T., Eisen, J.A., Karp, P.D., Bovee, D., Sr., Chapman, P., Clendenning, J., Deatherage, G., Gillet, W., Grant, C., Kutyavin, T., Levy, R., Li, M.-J., McClelland, E., Palmieri, A., Raymond, C., Rouse, G., Saenphimmachak, C., Wu, Z., Romero, P., Gordon, D., Zhang, S., Yoo, H., Tao, Y., Biddle, P., Jung, M., Krespan, W., Perry, M., Gordon-Kamm, B., Liao, L., Kim, S., Hendrick, C., Zhao, Z.-Y., Dolan, M., Chumley, F., Tingey, S.V., Tomb, J.-F., Gordon, M.P., Olson, M.V., Nester, E.W. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294 (2001) 2317–2323.

    PubMed  CAS  Google Scholar 

  • Wood, E.A., Butcher, G.W., Brewin, N.J., Kannenberg, E.L. Genetic derepression of a developmentally regulated lipopolysaccharide antigen from Rhizobium leguminosarum 3841. J Bacteriol 171 (1989) 4549–4555.

    PubMed  CAS  Google Scholar 

  • Wyckoff, T.J.O., Lin, S., Cotter, R.J., Dotson, G.D., Raetz, C.R.H. Hydrocarbon rulers in UDP- N -acetylglucosamine acyltransferases. J Biol Chem 273 (1998) 32369–32372.

    PubMed  CAS  Google Scholar 

  • Young, J.P., Crossman, L., Johnston, A., Thomson, N., Ghazoui, Z., Hull, K., Wexler, M., Curson, A., Todd, J., Poole, P., Mauchline, T., East, A., Quail, M., Churcher, C., Arrowsmith, C., Cherevach, I., Chillingworth, T., Clarke, K., Cronin, A., Davis, P., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Mungall, K., Norbertczak, H., Rabbinowitsch, E., Sanders, M., Simmonds, M., Whitehead, S., Parkhill, J. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7 (2006) R34.

    PubMed  Google Scholar 

  • Zahringer, U., Knirel, Y.A., Lindner, B., Helbig, J.H., Sonnesson, A., Marre, R., Rietschel, E.T. The lipopolysaccharide of Legionella pneumophila serogroup I (strain Philadelphia 1): Chemical structure and biological significance. Prog Clin Biol Res 392 (1995) 113–139.

    PubMed  CAS  Google Scholar 

  • Zavaleta-Pastor, M., Sohlenkamp, C., Gao, J.-L., Guan, Z., Zaheer, R., Finan, T.M., Raetz, C.R.H., López-Lara, I.M., Geiger, O. Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation. Proc Natl Acad Sci USA 107 (2010) 302–307.

    PubMed  CAS  Google Scholar 

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Carlson, R.W., Forsberg, L.S., Kannenberg, E.L. (2010). Lipopolysaccharides in Rhizobium-Legume Symbioses. In: Wang, X., Quinn, P. (eds) Endotoxins: Structure, Function and Recognition. Subcellular Biochemistry, vol 53. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9078-2_16

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