Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis

Molecular Plant-Microbe Interactions

Volumn 18, Issue 5, 2005, Pages 446-457

  D'Antuono, Alejandra L ^a   Casabuono, Adriana ^b   Couto, Alicia ^b   Ugalde, Rodolfo A ^a   Lepek, Viviana C ^a,c  

^a CONICET ^*  (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c INSTITUTO NACIONAL DE TECNOLOGÍA INDUSTRIAL   (Argentina)

Author keywords

Epimerase dehydratase family; Glycosyltransferases; LPS and (1 2) cyclic glucan mutants

Indexed keywords

CALCIUM; LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIAL GENE; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENETICS; LOTUS; METABOLISM; MICROBIOLOGY; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT ROOT; RHIZOBIACEAE;

CALCIUM; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LIPOPOLYSACCHARIDES; LOTUS; MUTATION; PHENOTYPE; PLANT ROOTS; RHIZOBIACEAE;

LOTUS TENUIS; MESORHIZOBIUM LOTI;

EID: 17644425706     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-18-0446     Document Type: Article

References (69)

1. Allard, S. T. M., Giraud, M., Whitfield, C., Graninger, M., Messner, P., and Naismith, J. H. 2001. The crystal structure of dTDP-D-glucose 4.6 dehydratase (RmlB) from Salmonella enterica serovar thyphimurium, the second enzyme in the dTDP-L-rhamnose pathway. J. Mol. Biol. 307:283-295.
2. Almirón-Roig, E., Mulholland, F., Gasson, M. J., and Griffin, A. M. 2000. The complete cps gene cluster from Streptococcus thermophilus NCFB 2393 involved in the biosynthesis of a new exopolysaccharide. Microbiology 146:2793-2802.
3. Baghwat, A. A., and Keister, D. L. 1995. Site-directed mutagenesis of the cyclic β-(1 → 3)(1 → 6)-glucan synthesis locus of Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 8:366-370.
4. Baghwat A. A., Tully, R. E., and Keister, D. L. 1992. Isolation and characterization of and ndvB locus from Rhizobium fredii. Mol. Microbiol. 6:2159-2165.
5. Baghwat A. A., Mithofer, A., Pfeffer, P. E., Kraus, C., Spickers, N., Hotckiss, A., Ebel, J., and Keister, D. L. 1999. Further studies of the role of cyclic β-glucans in symbiosis. A ndvC mutant of Bradyrhizobium japonicum synthesizes cyclodecakis-(1 → 3)-β-glucosyl. Plant Physiol. 119:1057-1064.
6. Banta, L. M., Bohne, S. D., Lovejoy, D., and Dostal, K. 1998. Stability of the Agrobacterium tumefaciens VirB10 protein is modulated by growth temperature and periplasmic osmoadaption. J. Bacteriol. 180:6597-6606.
7. Bash, R., and Matthysse, A. G. 2002. Attachment to roots and virulence of a chvB mutant of Agrobacterium tumefaciens are temperature sensitive. Mol. Plant-Microbe Interact. 15:160-163.
8. Borthakur, D., Barber, C. E., Lamb, J. E., Daniels, M. J., Downie, J. A., and Johnston, W. B. 1986. A mutation that blocks exopolysaccharide synthesis prevents nodulation of peas by Rhizobium leguminosarum but not beans by R. phaseoli and corrected by cloned DNA from Rhizobium of the phylopathogen Xanthomonas. Mol. Gen. Genet. 203:320-323.
9. Breedveld, M. B., and Miller, K. 1994. Cyclic glucan of members of family Rhizobiaceae. Microbiol. Rev. 58:145-161.
10. Brewin, N. J. 1998. Tissue and cell invasion by Rhizobium: Structure and development of infection threads and symbiosomes. Pages 417-429 in: The Rhizobiaceae. H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
11. Briones, G., Iñon de Iannino, N., Roset, M., Vigliocco, A., Silva Paulo, P., and Ugalde, R. 2001. Brucella abortus cyclic β-1,2-glucan mutants have reduced virulence in mice and are defective in intracellular replication in HeLa cells Infect. Immun. 69:4528-4535.
12. Campbell, G. R. O., Reuhs, B. E., 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. 99:3928-3943.
13. Campbell, G. R. O., Sharypova, E. A., Scheidle, H., Jones, K. M., Niehaus, K., Becker, A., and Walker, G. C. 2003. Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J. Bacteriol. 185:3853-3862.
14. Carlson, R. W., Kalembasa, W. S., Turowski, D., Pachori, P., and Noel, K. D. 1987. Characterization of the lipopolysaccharide from a Rhizobium phaseoli mutant that is defective in infection thread development. J. Bacteriol. 158:1012-1017.
15. Carlson, R. W., Reuhs, B., Chen, T. B., Bhat, U. R., and Noel, K. D. 1995. Lipopolysaccharide core structures in Rhizobium etli and mutants deficient in O-antigen. J. Biol. Chem. 270:11783-11788.
16. Cava, J. R., Elías, 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.
17. Colebatch, G., Kloska, S., Trevaskis, B., Freund, S., Altmann, T., and Udvardi, M. K. 2002. Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol. Plant-Microbe Interact. 15:411-420.
18. Douglas, C. J., Staneloni, R. J., Rubin, R. A., and Nester, E. W. 1985. Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region. J. Bacteriol. 161:850-860.
19. Dunlap, J., Minami, E., Bhagwat, A. A., Keister, D. L., and Stacey, G. 1996. Nodule development induced by mutants of Bradyrhizobium Japonicum defective in cyclic β-glucan synthesis. Mol. Plant-Microbe Interact. 9:546-555.
20. Erhardt, D. W., Wais, R., and Long, S. R. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673-681.
21. Fahraeus, G. 1957. The infection of clover root hair by nodule bacteria studied by a single slide technique. J. Gen. Microbiol. 16:374-381.
22. Freer, E., Moreno, E., Moriyón, I., Pizarro-Cerdá, J., Weintraub, A., and Gorvel, J. P. 1996. Brucella-Salmonella lipopolysaccharide chimeras are less permeable to hydrophobic probes and more sensitive to cationic peptides and EDTA than are their native Brucella sp. counterparts. J. Bacteriol. 178:5867-5876.
23. Gage, D. J., Bobo, T., and Long, S. R. 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178:7159-7166.
24. García de los Santos, A., and Brom, S. 1997. Characterization of two plasmid-borne lpsβ loci of Rhizobium etli required for lipopolysaccharide synthesis and for optimal interaction with plants. Mol. Plant-Microbe Interact. 10:891-902.
25. Geremía, R., Cavaignac, S., Zorreguieta, A., Toro, N., Olivares, J., and Ugalde, R., 1987. A Rhizobium meliloti mutant that forms ineffective pseudonodules in alfalfa produces exopolysaccharides but fails to form β(1-2)glucan. J. Bacteriol. 169:880-884.
26. Geurts, R., and Bisseling, T. 2002. Rhizobium Nod factor perception and signaling. Plant Cell 14:S239-S249.
27. Graninger, M., Nidetzky, B., Heinrichs, D., E., Whitfield, C., and Messner, P. 1999. Characterization of dTDP-dehydrorhamnose 3,5-epimerase and dTDP-dehydrorhamnose reductase, required for dTDP-L-rhamnose biosynthesis in Salmonella enterica serovar Thyphimurium LT2. J. Biol. Chem. 274:25069-25077.
28. Graninger, M., Kneidinger, B., Bruno, K., Scheber I. A., and Messner, P. 2002. Homolgs of the Rml enzymes from Salmonella enterica are responsible for dTDP-β-L-rhamnose biosynthesis in the gram-positive thermophile Aneurinibacillus thermoaerophilus DSM 10155. Appl. Environ. Microbiol. 68:3708-3715.
29. Gudlavalleti, S. K., and Forsberg, L. S. 2003. Structural characterization of the lipid A component of Sinorhizobium sp. NGR234 rough and smooth form lipopolysaccharide. Demonstration that the distal amide-linked acyloxyacyl residue containing the long chain fatty acid is conserved in Rhizobium and Sinorhizobium sp. J. Biol. Chem. 278:3957-3968.
30. Hitchcock, P. J., and Brown, T. M. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
31. Hotter, G. S., and Scott D. B. 1991. Exopolysaccharide mutants of Rhizobium loti are fully effective on a determinate nodulating host but are ineffective on an indeterminate nodulating host. J. Bacteriol. 173:851-859.
32. Iñon de Iannino, N., Briones, G., Kreiman, G., and Ugalde, R. 1996. Characterization of the biosynthesis of β(1-2) cyclic glucan in R. fredii. β(1-2) glucan has no apparent role in nodule invasion of MC Call and Peking soybean cultivars. Cell. Mol. Biol. 42:617-629.
33. 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., and Tabata, S. 2000a. Complete genome structure of the nitrogen-fixing bacterium Mesorhizobium loti. DNA Res. 7:331-338.
34. 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., and Tabata, S. 2000b. Complete genome structure of the nitrogen-fixing bacterium Mesorhizobium loti. Supplement. DNA Res. 7:381-406.
35. 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.
36. Kannenberg, E. L., Reuhs, B. L., Forsberg, L. S., and Carlson, R. W. 1998. Lipopolysaccharides and K-antigens: their structures, biosynthesis and function. Pages 119-154 in: The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
37. Kijne, J. W. 1992. The Rhizobium infection process. Pages 349-398 in: Biological Nitrogen Fixation. G. Stacey, R. H. Burris, and H. J. Evans, eds. Chapman and Hall, New York.
38. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop II, R. M., and Peterson, K. M. 1995. Four new derivatives of the broad-host-range cloning vector pBBRIMCs, carrying different antibiotic-resistance cassettes. Gene 166-175-176.
39. Lagares, A., Hozbor, D. F., Niehaus, K., Pich Otero, A. J. L., Lorenzen, J., Arnold, W., and Puhler, A. 1992. Genetic characterization of a Sinorhizobium meliloti chromosomal region involved in lipopolysaccharide biosynthesis. J. Bacteriol. 183:1248-1258.
40. Lepek, V. C., Navarro de Navarro, Y., and Ugalde, R. A. 1990. Synthesis of β(1-2) glucan in Rhizobium loti. Arch. Microbiol. 155:35-41.
41. Lepek, V. C., D'Antuono, A. L., Tomatis, P. E., Ugalde, J. E., Giambiagi, S., and Ugalde, R. A. 2002. Analysis of Mesorhizobium loti glycogen operon: Effect of phosphoglucomutase (pgm) and glycogen synthase (glgA) null mutants on nodulation of Lotus tenuis. Mol. Plant-Microbe Interact. 15:368-375.
42. Lerouge, I., and Vanderleyden, J. 2001. O-antigen structural variation: Mechanisms and possible roles in animal/plant-microbe interactions. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 26:17-47.
43. Miller, K. J., Kennedy, E. P., and Reinhold, V. N. 1986. Osmotic adaptation by gram-negative bacteria: Possible role for periplasmic oligosaccharides. Science 231:48-51.
44. Noel, K. D., and Duelli, D. M. 2000. Rhizobium lipopolysaccharide and its role in symbiosis. Pages 415-431 in: Prokaryotic Nitrogen Fixation: A Model System for Analysis of a Biological Process. E. W. Triplett, ed. Horizon Scientific Press, Wymondham, U.K.
45. 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.
46. + metabolism in Rhizobium-plant symbiosis. Microbiol. Mol. Biol. Rev. 66:203-222.
47. Pellock, B. J., Cheng, H., and Walker, G. C. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182:4310-4318.
48. 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.
49. Peschel, A., Jack, R. W., Otto, M., Collins, L. V., Staubitz, P., Nicholson, G., Kalbacher, H., Nieuweenhuizen, W. F., Jung, G., Tarkowski, A., van Kessel, K. P., and wan Strijp, J. A. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with 1-lysine. J. Exp. Med. 193:1067-1076.
50. Piekarowicz, A., and Stein, D. C. 2002. Biochemical properties of Neisseria gonorrhoeae LgtE. J. Bacteriol. 184:6410-6416.
51. Reuhs, B. L., Williams, M. N. V., Kim, J. S., Carlson, R. W., and Coté, F. 1995. Suppression of the Fix phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K polysaccharide. J. Bacteriol. 177:4289-4296.
52. Reuhs, B. L., Geller, D. P., Kim, J. S., Fox, J. E., Kumar Kolli, V. S., and Pueppke, S. G. 1998. Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific K antigens. Appl. Environ. Microbiol. 64:4930-4938.
53. Robinson, J. B., Tuovinen, O. H., and Bauer, W. D. 1992. Role of divalent cations in the subunit associations of complex flagella from Rhizobium meliloti. J. Bacteriol. 174:3896-3902.
54. Russa, R., Urbanik-Sypniewska, T., Lindstrom, K., and Mayer, H. 1995. Chemical characterization of two lipopolysaccharides species isolated from Rhizobium loti NZP2213. Arch. Microbiol. 163:345-351.
55. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Schagger, H., and von Jagow, G. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
57. Spaink, H. P. 2000. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54:257-288.
58. Stacey, G., So, J.-S., Roth, L. E., Lakshmi, S. K. B., and Carlson, R. W. 1991. A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol. Plant-Microbe Interact. 4:332-340.
59. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneky, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K., and Parniske, M. 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959-962.
60. Swart, S., Logman, T. J. J., Lugtenberg, B. J. J., Smit, G., and Kijne, J. W. 1994. Several phcnotypic changes in the cell envelope of Agrobacterium tumefaciens chvB mutants are prevented by calcium limitation. Arch. Microbiol. 161:310-315.
61. Trevelyan, V. E., Procter, D. P., and Harrison, J. S. 1950. Detection of sugar on paper chromatography. Nature (Lond.) 166:444-445.
62. Tsai, C., and Frisch, C. E. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
63. Turner, S. L., Zhang, X., Li, F., and Young, P. W. 2002. What does bacterial genome sequence represent? Misassignment of MAFF 303099 to the genospecies Mesorhizobium loti. Microbiology 148:3330-3331.
64. Udvardi, M. K., and Day, D. A. 1997. Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. 48:493-523.
65. Ugalde, J. E., Czibener, C., Feldman, M. F., and Ugalde, R. A. 2000. Identification and characterization of the Brucella abortus phosphoglucomutase gen: Role of lipopolysaccharide in virulence and intracellular multiplication. Infect. Immun. 68:5716-5723.
66. Vinuesa, P., Nwumann-Silkow, F., Pacios-Bras, C., Spaink, H. P., Martinez-Romero, E., and Werner, D. 2003. Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol. Plant-Microbe Interact. 16:159-168.
67. Wang, S., and Gabriel, O. 1969. Biological mechanisms involved in the formation of deoxy sugars. J. Biol. Chem. 244:3430-3437.
68. Webb, K. J., Skot, L., Nicholson, M. N., Jorgensen, B., and Mizen, S. 2000. Mesorhizobium loti increases root-specific expression of a calcium-binding protein homologue identified by promoter tagging in Lotus japonicus. Mol. Plant-Microbe Interact. 13:606-616.
69. Westphal, O., and Jann, K. 1965. Bacterial lipopolysaccharides. Extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5:83-91.