Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii USDA257

Molecular Plant-Microbe Interactions

Volumn 16, Issue 7, 2003, Pages 617-625

  Krishnan, Hari B ^a,c   Lorio, Julio ^a   Kim, Won Seok ^a   Jiang, Guoqiao ^a,d   Kim, Kil Yong ^b   DeBoer, Margreet ^a   Pueppke, Steven G ^a,e  

^a UNIVERSITY OF MISSOURI   (United States)

^b Chonnam National University   (South Korea)

^c U S DEPARTMENT OF AGRICULTURE   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); GLYCINE MAX; MACROPTILIUM; MACROPTILIUM ATROPURPUREUM; NEGIBACTERIA; RHIZOBIUM; RHIZOBIUM SP.; SINORHIZOBIUM; SINORHIZOBIUM FREDII;

EID: 0038545909     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2003.16.7.617     Document Type: Article

References (41)

1. Anderson, D. M., and Schneewind, O. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140-1143.
2. Brown, I. R., Mansfield, J. W., Taira, S., Roine, E., and Romantschuk, M. 2001. Immunocytochemical localization of HrpA and HrpZ supports a role for the Hrp pilus in the transfer of effector proteins from Pseudomonas syringae pv. tomato across the host cell wall. Mol. Plant-Microbe Interact. 14:394-404.
3. Baker, B., Zambryski, P., Staskawicz, B., and Dinesh-Kumar, S. P. 1997. Signaling in plant-microbe interactions. Science 276:726-733.
4. Broughton, W. J., Jabbouri, S., and Perret, X. 2000. Keys to symbiotic harmony. J. Bacteriol. 182:5641-5672.
5. Burnett, W. N. 1981. Western blotting: Electrophoretic transfer of proteins from SDS-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein-A. Anal. Biochem. 112:195-203.
6. Casper-Lindley, C., Dahlbeck, D., Clark, E. T., and Staskawicz, B. J. 2002. Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc. Natl. Acad. Sci. U.S.A. 99:8336-8341.
7. Cornelis, G. R., and Wolf-Watz, H. 1997. The Yersinia Yop virulon: A bacterial system for subverting eukaryotic cells. Mol. Microbiol. 87:861-867.
8. 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.
9. 2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U.S.A. 76:1648-1652.
10. Galan, J. E., and Collmer, A. 1999. Type III secretion machines: Bacterial devices for protein delivery into host cells. Science 284:1322-1328.
11. Ginocchio, C., Olmsted, S. B., Wells, C. L., and Galan, J. E. 1994. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76:717-724.
12. Göttfert, M., Rothlisberger, S., Kundig, C., Beck, C., Marty, R., and Hennecke, H. 2001. Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J. Bacteriol. 183:1405-1412.
13. He, S. Y. 1998. Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopathol. 36:363-392.
14. Heron, D. S., and Pueppke, S. G. 1984. Mode of infection, nodulation specificity, and indigenous plasmids of 11 fast-growing Rhizobium japonicum strains. J. Bacteriol. 160:1061-1066.
15. Jin, Q., and He, S.-Y. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-2558.
16. 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. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7:331-338.
17. Knutton, S., Rosenshine, I., Pallen, M. J., Nisan, I., Neves, B. C., Bain, C., Wolff, C., Dougan, G., and Frankel, G. 1998. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO (Eur. Mol. Biol. Organ.) J. 17:2166-2176.
18. Krishnan, H. B. 2002. NolX of Sinorhizobium fredii USDA257, a type III-secreted protein involved in host range determination, is localized in the infection threads of cowpea (Vigna unguiculata [L.] Walp) and soybean (Glycine max [L.] Merr.) nodules. J. Bacteriol. 184:831-839.
19. Krishnan, H. B., and Pueppke, S. G. 1991. Sequence and analysis of the nodABC region of Rhizobium fredii USDA257, a nitrogen-fixing symbiont of soybean and other legumes. Mol. Plant-Microbe Interact. 4:512-520.
20. Krishnan, H. B., and Pueppke, S. G. 1993. Flavonoid inducers of nodulation genes stimulate Rhizobium fredii USDA257 to export proteins into the environment. Mol. Plant-Microbe Interact. 6:107-113.
21. Krishnan, H. B., Kuo, C.-I., and Pueppke, S. G. 1995. Elaboration of flavonoid-induced proteins by the nitrogen-fixing soybean symbiont Rhizobium fredii is regulated by both nodD1 and nodD2, and is dependent on the cultivar-specificity locus, nolXWBTUV. Microbiology 141:2245-2251.
22. Krupski, G., Gotz, R., Ober, K., Pleier, E., and Schmitt, R. 1985. Structure of complex flagellar filaments in Rhizobium meliloti. J. Bacteriol. 162:361-366.
23. Kubori, T., Yamaguchi, S., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galan, J. E., and Aizawa, S. I. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602-605.
24. Lloyd, S. A., Sjostrom, M., Andersson, S., and Wolf-Watz, H. 2002. Molecular characterization of type III secretion signals via analysis of synthetic N-terminal amino acid sequences. Mol. Microbiol. 43:51-59.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Lee, C. A. 1997. Type III secretion systems: Machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol. 5:149-156.
27. Leigh, J. A., Signer, E. R., and Walker, G. C. 1985. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. U.S.A. 85:6231-6235.
28. Marie, C., Broughton, W. J., and Deakin, W. J. 2001. Rhizobium type III secretion systems: Legume charmers or alarmers? Curr. Opin. Plant Biol. 4:336-342.
29. 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 by Rhizobium fredii USDA257. Mol. Microbiol. 9:17-29.
30. Perret, X., Fellay, R., Bjourson, A. J., Cooper, J. E., Brenner, S., and Broughton, W. J. 1994. Subtraction hybridization and shot-gun sequencing: A novel approach to identify symbiotic loci. Nucleic Acids Res. 22:1335-1341.
31. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., and Gustafson, M. 1996. Modulation of virulence factor expression by pathogen target cell contact. Science 273:1231-1233.
32. Price, N. P. J., Relić B., Talmont, F., Lewin, A., Promé, D., Pueppke, S. G., Maillet, F., Dénarié, J., Prome, J.-C., and Broughton, W. J. 1992. Broad-host-range Rhizobium species NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6:3575-3584.
33. 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.
34. Quandt, U., and Hynes, M. F. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21.
35. Relić B., Perret, X., Estrada-Garcia, M. T., Kopcinska, J., Golinowski, W., Krishnan, H. B., Pueppke, S. G., and Broughton, W. J. 1994. Nod factors of Rhizobium are a key to the legume door. Mol. Microbiol. 13:171-178.
36. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, N., Kalkkinen, N., Romantschuk, M., and He, S. Y. 1997. Hrp pilus: An hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 94:3459-3464.
37. 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.
38. Sutton, J. M., Lea, E. J., and Downie, J. A. 1994. The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc. Natl. Acad. Sci. U.S.A. 91:9990-9994.
39. Van Gijsegem, F., Vasse, J., Camus, J. C., Marenda, M., and Boucher, C. 2000. Ralstonia solanacearum produces hrp-dependent pili that are required for PopA secretion but not for attachment of bacteria to plant cells. Mol. Microbiol. 36:249-260.
40. Vincent, J. M. 1970. A Manual for the Practical Study of Root-Nodule Bacteria. Blackwell Scientific, Oxford, U.K.
41. Viprey, V., Greco, A. D., Golinowski, W., Broughton, W. J., and Perret, X. 1998. Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28:1381-1389.