A Mesorhizobium loti mutant with reduced glucan content shows defective invasion of its host plant Lotus japonicus

Microbiology

Volumn 153, Issue 12, 2007, Pages 3983-3993

  Kawaharada, Yasuyuki ^a   Eda, Shima ^a   Minamisawa, Kiwamu ^a   Mitsui, Hisayuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GLUCAN; CELL PROTEIN; ENVELOPE PROTEIN; PROTEIN CEP; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL PLANT DISEASE; BACTERIAL VIRULENCE; BIOSYNTHESIS; GENETIC CODE; LOTUS; MESORHIZOBIUM; MESORHIZOBIUM LOTI; MUTAGENESIS; NITROGEN FIXATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RHIZOBIALES; SYMBIOSIS; TRANSPOSON;

ALKALINE PHOSPHATASE; ALPHAPROTEOBACTERIA; BACTERIAL OUTER MEMBRANE PROTEINS; DNA TRANSPOSABLE ELEMENTS; GLUCANS; LOTUS; MUTAGENESIS, INSERTIONAL; MUTATION; NITROGEN FIXATION; PHENOTYPE; PLANT ROOTS; SYMBIOSIS;

LOTUS CORNICULATUS VAR. JAPONICUS; MESORHIZOBIUM LOTI;

EID: 37449028613     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/008631-0     Document Type: Article

References (62)

1. Banba, M., Siddique, A.-B. M., Kouchi, H., Izui, K. & Hata, S. (2001). Lotus japonicus forms early senescent root nodules with Rhizobium etli. Mol Plant Microbe Interact 14, 173-180.
2. Becker, A., Schmidt M., Jäger, W. & Pühler, A. (1995). New gentamicin-resistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions. Gene 162, 37-39.
3. Bhagwat, A. A., Tully, R. E. & Keister, D. L. (1992). Isolation and characterization of an ndvB locus from Rhizobium fredii. Mol Microbiol 6, 2159-2165.
4. Bhagwat, A A., Tully, R. E. & Keister, D. L. (1993). Identification and cloning of a cyclic β(1→3), β-(1→6)-D-glucan synthesis locus from Bradyrhizobium japonicum. FEMS Microbiol Lett 114, 139-144.
5. Bhagwat A. A., Gross, K. C., Tully, R. E. & Keister, D. L. (1996). β-Glucan synthesis in Bradyrhizobium japonicum: characterization of a new locus (ndvC) influencing β-(1→6) linkages. J Bacteriol 178, 4635-4642.
6. Bhagwat, A. A., Mithöfer, A., Pfeffer, P. E., Kraus, C., Spickers, N., Hotchkiss, A., Ebel, J. & Keister, D. L. (1999). Further studies of the role of cyclic β-glucans in symbiosis. An ndvC mutant of Bradyrhizobium japonicum synthesizes cycIodecakis-(1→)-β-glucosyl. Plant Physiol 119, 1057-1064.
7. Bittner, A. N., Foltz, A. & Oke, V. (2007). Only one of five groEL genes is required for viability and successful symbiosis in Sinorhizobium meliloti. J Bacteriol 189, 1884-1889.
8. Bohin, J.-P. (2000). Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol Lett 186, 11-19.
9. Breedveld, M. W. & Miller, K. J. (1994). Cyclic β-glucans of members of the family Rhizobiaceae. Microbiol Rev 58, 145-161.
10. Breedveld, M. W. & Miller, K. J. (1995). Synthesis of glycerophos-phorylated cyclic (1,2)-β-glucans in Rhizobium meliloti strain 1021 after osmotic shock. Microbiology 141, 583-588.
11. Breedveld, M. W., Zevenhuizen, L. P. T. M. & Zehnder, A. J. B. (1990). Osmotically induced oligo- and polysaccharide synthesis by Rhizobium meliloti SU-47. J Gen Microbiol 136, 2511-2519.
12. Breedveld, M. W., Hadley, J. A. & Miller, K J. (1995). A novel cyclic β-1,2-glucan mutant of Rhizobium meliloti. J Bacteriol 177, 6346-6351.
13. Broughton, W. J. & Dilworth, M. J. (1971). Control of legbaemoglobin synthesis in snake beans. Biochem J 125, 1075-1080.
14. Cangelosi, G. A., Martinetti, G. & Nester, E. W. (1990). Osmosensitivity phenotypes of Agrobacterium tumefaciens mutants that lack periplasmic β-1,2-glucan. J Bacteriol 172, 2172-2174.
15. Charles, T. C., Newcomb, W. & Finan, T. M. (1991). ndvF, a novel locus located on megaplasmid pRmeSU47b (pEXO) of Rhizobium meliloti, is required for normal nodule development. J Bacteriol 173, 3981-3992.
16. Chen, R., Bhagwat; A. A. & Keister, D. (2003). A motility revertant of the ndvB mutant of Bradyrhizobium japonicum. Curr Microbiol 47, 431-433.
17. D'Antuono, A. L., Casabuono, A., Couto, A., Ugalde, R. A. & Lepek, V. C. (2005). Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis. Mol Plant Microbe Interact 18, 446-457.
18. de lannino, N. I., Briones, G., lannino, F. & Ugaide, R. A. (2000). Osmotic regulation of cyclic 1,2-β-glucan synthesis. Microbiology 146, 1735-1742.
19. Delgado, M. J., Bedmar, E. J. & Downie, J. A. (1998). Genes involved in the formation and assembly of rhizobial cytochromes and their role in symbiotic nitrogen fixation. Adv Microb Physiol 40, 191-231.
20. Dombrecht B., Vanderleyden, J. & Michiels, J. (2001). Stable RK2-derived cloning vectors for the analysis of gene expression and gene function in Gram-negative bacteria. Mol Plant Microbe Interact 14, 426-430.
21. Dunlap, J., Minami, E., Bhagwat, A. A., Kelster, D. L. & Stacey, G. (11996). Nodule development induced by mutants of Bradyrhizobium japonicum defective in cyclic β-glucan synthesis. Mol Plant Microbe Interact 9, 546-555.
22. Dylan, T., lelpi, L., Stanfield, S., Kashyap, L., Douglas, C., Yanofsky, M., Nester, E., Helinski, D. R. & Ditta, G. (1986). Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 83, 4403-4407.
23. Dylan, T., Helinski, D. R. & Ditta, G. S. (1990a). Hypoosmotic adaptation in Rhizobium meliloti requires β-(I→2)-glucan. J Bacteriol 172, 1400-1409.
24. Dylan, T., Nagpal, P., Helinski, D. R. & Ditta, G. S. (1990b). Symbiotic pseudorevertants of Rhizobium meliloti ndv mutants. J Bacteriol 172, 1409-1417.
25. Finan, T. M., Kunkel, B., De Vos, G. F. & Signer, E. R. (1986). Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysac-charide and thiamine synthesis genes. J Bacteriol 167, 66-72.
26. Fraysse, N., Couderc, F. & Poinsot, V. (2003). Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 270, 1365-1380.
27. Galibert, F., Finan, T. M., Long, S. R., Puhler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A. & other authors (2001). The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668-672.
28. Geiger, O., Weissborn, A. C. & Kennedy, E. P. (1991). Biosynthesis and excretion of cyclic glucans by Rhizobium meliloti 1021. J Bacteriol 173, 3021-3024.
29. Glazebrook, J. & Walker, G. C. (1991). Genetic techniques in Rhizobium meliloti. Methods Enzymol 204, 398-418.
30. González, V., Santamaría, R. I., Bustos, P., Hernández-González, I., Medrano-Soto, A., Moreno-Hagelsieb, G., Janga, S. C., Ramirez, M. A., Jiménez-Jacinto, V. & other authors (2006). The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci U S A 103, 3834-3839.
31. Hadri, A.-E. & Bisseling, T. (1998). Responses of the plant to Nod factors. In The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria, pp. 403-416. Edited by H. P. Spaink, A. Dondorosi & P. J. J. Hooykaas. Dordrecht, The Netherlands: Kluwer Academic Publishers.
32. Hailing, S. M., Peterson-Burch, B. D., Bricker, B. J., Zuerner, R. L., Qing, Z., U, L.-L., Kapur, V., Alt, D. P. & Olsen, S. C. (2005). Completion of the genome sequence of Brucella abortus and comparison to the highly similar genomes of Brucella melitensis and Brucella suis. J Bacteriol 187, 2715-2726.
33. Handberg, K. & Stougaard, J. (1992). Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J 2, 487-496.
34. Hattori, Y., Omori, H., Hanyu, M., Kaseda, N., Mishima, E., Kaneko, T., Tabata, S. & Saeki, K. (2002). Ordered cosmid library of the Mesorhizobium loti MAFF303099 genome for systematic gene disruption and complementation analysis. Plant Cell Physiol 43, 1542-1557.
35. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K, Ishikawa, A. & other authors (2000). Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7, 331-338.
36. Koehler, L. H. (1952). Differentiation of carbohydrates by anthrone reaction rate and color intensity. Anal Chem 24, 1576-1579.
37. Lepek, V., Navarro de Navarro, Y. & Ugaide, R. A. (1990). Synthesis of β(1-2)glucan in Rhizobium loti. Arch Microbiol 155, 35-41.
38. Lodwig, E. & Poole, P. (2003). Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22, 37-78.
39. Long, S., McCune, S. & Walker, G. C. (1988). Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis. J Bacteriol 170, 4257-4265.
40. Manoil, C. & Beckwith, J. (1985). TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A 82, 8129-8133.
41. Miller, J. H. (1992). A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
42. Miller, K. J., Kennedy, E. P. & Reinhold, V. N. (1986). Osmotic adaptation by Gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231, 48-51.
43. Miller, K. J., Reinhold, V. N., Weissborn, A. C. & Kennedy, E. P. (1987). Cyclic glucans produced by Agrobacterium tumefaciens are substituted with sn-1-phosphoglycerol residues. Biochim Biophys Acta 901, 112-118.
44. Miller, K. J., Gore, R. S. & Benesi, A. J. (1988). Phosphoglycerol substituents present on the cyclic β-1,2-glucans of Rhizobium meliloti 1021 are derived from phosphatidylglycerol. J Bacteriol 170, 4569-4575.
45. Miller, K. J., Gore, R. S., Johnson, R., Benesi, A. J. & Reinhold, V. N. (1990). Cell-associated oligosaccharides of Bradyrhizobium spp. J Bacteriol 172, 136-142.
46. Mithöfer, A., Bhagwat, A. A., Feger, M. & Ebel, J. (1996). Suppression of fungal β-glucan-induced plant defence in soybean (Glycine max L.) by cyclic 1,3-1,6-β-glucans from the symbiont Bradyrhizobium japonicum. Planta 199, 270-275.
47. 1 is required for effective nitrogen-fixing symbiosis with alfalfa. Mol Genet Genomics 271, 416-425.
48. Müller, P., Klaucke, A. & Wegel, E. (1995). TnphoA-induced symbiotic mutants of Bradyrhizobium japonicum that impair cell and tissue differentiation in Glycine max nodules. Planta 197, 163-175.
49. Niwa, S., Kawaguchi, M., Imaizumi-Anraku, H., Chechetka, S. A., Ishizaka, M., Ikuta, A. & Kouchi, H. (2001). Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. Mol Plant Microbe Interact 14, 848-856.
50. Park, J. T. & Johnson, M. J. (1949). A submicrodetermination of glucose. J Biol Chem 181, 149-151.
51. Prentki, P. & Krisch, H. M. (1984). In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29, 303-313.
52. Pugsley, A. P. (1993). The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57, 50-108.
53. Quandt, J., Hillemann, A., Niehaus, K., Arnold, W. & Pühler, A. (1992). An osmorevertant of a Rhizobium meliloti ndvB deletion mutant forms infection threads but is defective in bacteroid development. Mol Plant Microbe Interact 5, 420-427.
54. Roset, M. S., Ciocchini, A. E., Ugalde, R. A. & Iñón de Iannino, N. (2004). Molecular cloning and characterization of cgt, the Brucella abortus cyclic β-1,2-glucan transporter gene, and its role in virulence. Infect Immun 72, 2263-2271.
55. Rumley, M. K., Therisod, H., Weissborn, A. C. & Kennedy, E. P. (1992). Mechanisms of regulation of the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. J Biol Chem 267, 11806-11810.
56. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
57. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G. & Pühler, A. (1994). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73.
58. Stock, J. B., Rauch, B. & Roseman, S. (1977). Periplasmic space in Salmonella typhimurium and Escherichia coli. J Biol Chem 252, 7850-7861.
59. Tully, R. E., Keister, D. L. & Gross, K. C. (1990). Fractionation of the β-linked glucans of Bradyrhizobium japonicum and their response to osmotic potential. Appl Environ Microbiol 56, 1518-1522.
60. Young, J. P. W., Crossman, L. C., Johnston, A. W. B., Thomson, N. R., Ghazoui, Z. F., Hull, K H., Wexler, M., Curson, A. R., Todd, J. D. & other authors (2006). The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7, R34.
61. Zevenhuizen, L. P. T. M. & Van Neerven, A. R. W. (1983). (1→2)-β-D-Glucan and acidic oligosaccharides produced by Rhizobium meliloti. Carbohydr Res 118, 127-134.
62. Zorreguieta, A., Cavaignac, S., Geremia, R. A. & Ugalde, R. A. (1990). Osmotic regulation of β(1-2)-glucan synthesis in members of the family Rhizobiaceae. J Bacteriol 172, 4701-4704.