Synthesis of the flavonoid-induced lipopolysaccharide of Rhizobium sp. strain NGR234 requires rhamnosyl transferases encoded by genes rgpF and wbgA

Molecular Plant-Microbe Interactions

Volumn 24, Issue 12, 2011, Pages 1513-1521

  Ardissone, Silvia ^a   Dale Noel, K ^b   Klement, Mitchell ^b   Broughton, William J ^a,d   Deakin, William J ^a,c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b MARQUETTE UNIVERSITY   (United States)

^c Lipoprotein Research Group   (Switzerland)

^d BAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; FLAVONOID; LIPOPOLYSACCHARIDE; RHAMNOSE; TRANSFERASE;

ARTICLE; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; FABACEAE; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; MUTATION; NODULATION; PHENOTYPE; PHYSIOLOGY; RHIZOBIUM; SYMBIOSIS;

BACTERIAL PROTEINS; FABACEAE; FLAVONOIDS; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPOLYSACCHARIDES; MULTIGENE FAMILY; MUTATION; PHENOTYPE; PLANT ROOT NODULATION; POLYSACCHARIDES, BACTERIAL; RHAMNOSE; RHIZOBIUM; SYMBIOSIS; TRANSFERASES;

BACTERIA (MICROORGANISMS); FABACEAE; RHIZOBIUM; RHIZOBIUM SP.; VIGNA UNGUICULATA;

EID: 81255177055     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-05-11-0143     Document Type: Article

References (41)

1. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. 1991. Current Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
2. Becker, A., Fraysse, N., and Sharypova, L. 2005. Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol. Plant-Microbe Interact. 18:899-905. (Pubitemid 41170154)
3. Beringer, J. E. 1974. R-factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:188-198.
4. Broughton, W. J., Wong, C.-H., Lewin, A., Samrey, U., Myint, H., Meyer z. A., H., Dowling, D. N., and Simon, R. 1986. Identification of Rhizobium plasmid sequences involved in recognition of Psophocarpus, Vigna, and other legumes. J. Cell Biol. 102:1173-1182.
5. Broughton, W. J., Jabbouri, S., and Perret, X. 2000. Keys to symbiotic harmony. J. Bacteriol. 182:5641-5652.
6. Broughton, W. J., Hanin, M., Relić, B., Kopciñska, J., Golinowski, W., Şimşek, Ş., Ojanen-Reuhs, T., Reuhs, B., Marie, C., Kobayashi, H., Bordogna, B., Le Quéré, A. J.-L., Jabbouri, S., Fellay, R., Perret, X., and Deakin, W. J. 2006. Flavonoid-inducible modifications to rhamnan O antigens are necessary for Rhizobium sp. strain NGR234-legume symbioses. J. Bacteriol. 188:3654-3663. (Pubitemid 43739273)
7. Campbell, G. R. O., Reuhs, B. L., and Walker, G. C. 2002. Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc. Natl. Acad. Sci. U. S. A. 99:3938-3943. (Pubitemid 34252209)
8. Cava, J. R., Elias, P. M., Turowski, D. A., and Noel, K. D. 1989. Rhizobium leguminosarum CFN42 genetic regions encoding lipopolysaccharide structures essential for complete nodule development on bean plants. J. Bacteriol. 171:8-15.
9. Deakin, W. J., and Broughton, W. J. 2009. Symbiotic use of pathogenic strategies: Rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:312-320.
10. D'Haeze, W., Leoff, C., Freshour, G., Noel, K. D., and Carlson, R. W. 2007. Rhizobium etli CE3 bacteroid lipopolysaccharides are structurally similar but not identical to those produced by cultured CE3 bacteria. J. Biol. Chem. 282:17101-17113. (Pubitemid 47093218)
11. Fellay, R., Frey, J., and Krisch, H. 1987. Interposon mutagenesis of soil and water bacteria: A family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52:147-154. (Pubitemid 17090743)
12. Figurski, D. H., and Helinski, D. R. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652. (Pubitemid 9175374)
13. Forsberg, L. S., Bhat, U. R., and Carlson, R. W. 2000. 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. 275:18851-18863.
14. 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. (Pubitemid 27227203)
15. Gibson, K. E., Kobayashi, H., and Walker, G. C. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42:413-441.
16. Gudlavalleti, S. K., and Forsberg, L. S. 2003. Structural characterization of the lipid A component of Sinorhizobium sp. NGR234 rough and smooth form lipopolysaccharide. J. Biol. Chem. 278:3957-3968.
17. Hitchcock, P. J., and Brown, T. M. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277. (Pubitemid 13115445)
18. Jones, K. M., Kobayashi, H., Davies, B. W., and Walker, G. C. 2007. How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619-633. (Pubitemid 47074117)
19. Kanipes, M. I., Kalb, S. R., Cotter, R. J., Hozbor, D. F., Lagares, A., and Raetz, C. R. 2003. Relaxed sugar donor selectivity of a Sinorhizobium meliloti ortholog of the Rhizobium leguminosarum mannosyl transferase LpcC. Role of the lipopolysaccharide core in symbiosis of Rhizobiaceae with plants. J. Biol. Chem. 278:16365-16371. (Pubitemid 36799763)
20. Kannenberg, E. L., and Carlson, R. W. 2001. Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol. Microbiol. 39:379-391. (Pubitemid 32114162)
21. Kobayashi, H., Naciri-Graven, Y., Broughton, W. J., and Perret, X. 2004. Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol. Microbiol. 51:335-347. (Pubitemid 38142124)
22. Lagares, A., Hozbor, D. F., Niehaus, K., Otero, A. J., Lorenzen, J., Arnold, W., and Puhler, A. 2001. Genetic characterization of a Sinorhizobium meliloti chromosomal region in lipopolysaccharide biosynthesis. J. Bacteriol. 183:1248-1258. (Pubitemid 32107721)
23. Le Quéré, A. J.-L., Deakin, W. J., Schmeisser, C., Carlson, R. W., Streit, W. R., Broughton, W. J., and Forsberg, L. S. 2006. Structural characterization of a K-antigen capsular polysaccharide essential for normal symbiotic infection in Rhizobium sp. NGR234. J. Biol. Chem. 281:28981-28992.
24. Marie, C., Deakin, W. J., Ojanen-Reuhs, T., Diallo, E., Reuhs, B., Broughton, W. J., and Perret, X. 2004. TtsI, a key regulator of Rhizobium species NGR234 is required for type III-dependent protein secretion and synthesis of rhamnose-rich polysaccharides. Mol. Plant-Microbe Interact. 17:958-966. (Pubitemid 39098884)
25. Miller, W. G., Leveau, J. H., and Lindow, S. E. 2000. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol. Plant-Microbe Interact. 13:1243-1250.
26. Noel, K. D., Vandenbosch, K. A., and Kulpaca, B. 1986. Mutations in Rhizobium phaseoli that lead to arrested development of infection threads. J. Bacteriol. 168:1392-1401. (Pubitemid 17226832)
27. Noel, K. D., Forsberg, L. S., and Carlson, R. W. 2000. Varying the abundance of O antigen in Rhizobium etli and its effect on symbiosis with Phaseolus vulgaris. J. Bacteriol. 182:5317-5324.
28. Noel, K. D., Box, J. M., and Bonne, V. J. 2004. 2-O-methylation of fucosyl residues of a rhizobial lipopolysaccharide is increased in response to host exudate and is eliminated in a symbiotically defective mutant. Appl. Environ. Microbiol. 70:1537-1544. (Pubitemid 38365136)
29. Ojeda, K. J., Box, J. M., and Noel, K. D. 2010. Genetic basis for Rhizobium etli CE3 O-antigen O-methylated residues that vary according to growth conditions. J. Bacteriol. 192:679-690.
30. Peterson, A. A., and McGroarty, E. J. 1985. High-molecular-weight components in lipopolysaccharides of Salmonella typhimurium, Salmonella minnesota, and Escherichia coli. J. Bacteriol. 162:738-745. (Pubitemid 15059749)
31. Poon, K. K., Westman, E. L., Vinogradov, E., Jin, S., and Lam, J. S. 2008. Functional characterization of MigA and WapR: Putative rhamnosyltransferases involved in outer core oligosaccharide biosynthesis of Pseudomonas aeruginosa. J. Bacteriol. 190:1857-1865. (Pubitemid 351355308)
32. Pueppke, S. G., and Broughton, W. J. 1999. Rhizobium sp. strain NGR234 and R.fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant-Microbe Interact. 12:293-318. (Pubitemid 29167304)
33. Quandt, J., and Hynes, M. F. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21. (Pubitemid 23140440)
34. Reuhs, B. L., Kim, J. S., Badgett, A., and Carlson, R. W. 1994. Production of cell-associated polysaccharides of Rhizobium fredii USDA205 is modulated by apigenin and host root extract. Mol. Plant-Microbe Interact. 7:240-247. (Pubitemid 2085749)
35. Reuhs, B. L., Relić, B., Forsberg, L. S., Marie, C., Ojanen-Reuhs, T., Stephens, S. B., Wong, C. H., Jabbouri, S., and Broughton, W. J. 2005. 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. 187:6479-6487. (Pubitemid 41318407)
36. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
37. Schmeisser, C., Liesegang, H., Krysciak, D., Bakkou, N., Le Quéré, 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., and Streit, W. R. 2009. Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl. Environ. Microbiol. 75:4035-4045.
38. Skorpil, P., Saad, M. M., Boukli, N. M., Kobayashi, H., Ares-Orpel, F., Broughton, W. J., and Deakin, W. J. 2005. NopP, a phosphorylated effector of Rhizobium sp. strain NGR234, is a major determinant of nodulation of the tropical legumes Flemingia congesta and Tephrosia vogelii. Mol. Microbiol. 57:1304-1317. (Pubitemid 41176525)
39. Stanley, J., Dowling, D. N., and Broughton, W. J. 1988. Cloning of hemA from Rhizobium sp. NGR234 and symbiotic phenotype of a genedirected mutant in diverse legume genera. Mol. Gen. Genet. 215:32-37.
40. Wassem, R., Kobayashi, H., Kambara, K., Le Quéré, A. J.-L., Walker, G. C., Broughton, W. J., and Deakin, W. J. 2008. TtsI regulates symbiotic genes in Rhizobium species NGR234 by binding to tts boxes. Mol. Microbiol. 68:736-748. (Pubitemid 351490192)
41. Whitfield, C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75:39-68. (Pubitemid 44118025)