The putative secreted serine protease chp-7 Is required for full virulence and induction of a nonhost hypersensitive response by clavibacter michiganensis subsp. sepedonicus

Molecular Plant-Microbe Interactions

Volumn 22, Issue 7, 2009, Pages 809-819

  Nissinen, Riitta ^a,d   Xia, Yunjian ^a,e   Mattinen, Laura ^a   Ishimaru, Carol A ^b   Knudson, Dennis L ^c   Knudson, Susan E ^c   Metzler, Mary ^a,f   Pirhonen, Minna ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF MINNESOTA   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

^e NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^f NONE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA; SERINE PROTEINASE;

ACTINOMYCETALES; ARTICLE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETIC COMPLEMENTATION; GENETICS; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; POTATO; SOUTHERN BLOTTING; TOBACCO; VIRULENCE;

ACTINOMYCETALES; BACTERIAL PROTEINS; BLOTTING, SOUTHERN; GENE LIBRARY; GENETIC COMPLEMENTATION TEST; MUTAGENESIS, INSERTIONAL; MUTATION; POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SOLANUM TUBEROSUM; TOBACCO; VIRULENCE;

BACTERIA (MICROORGANISMS); CLAVIBACTER MICHIGANENSIS SUBSP. SEPEDONICUS; NICOTIANA TABACUM; SOLANUM TUBEROSUM;

EID: 67649502341     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-22-7-0809     Document Type: Article

References (35)

1. Bentley, S. D., Corton, C., Brown, S. E., Barron, A., Clark, L., Doggert, J., Harris, B., Ormond, D., Quail, M. A., May, G., Francis, D., Knudson, D., Parkhill, J., and Ishimaru, C. A. 2008. Genome of the actinomycete plant pathogen Clavibacter michiganensis subsp. sepedonicus suggests recent niche adaptation. J. Bacteriol. 190:2150-2160.
2. Brown, S. E., Reilley, A. A., Knudson, D. L., and Ishimaru, CA. 2002. Genomic fingerprinting of virulent and avirulent strains of Clavibacter michiganensis subspecies sepedonicus. Curr. Microbiol. 44:112-119.
3. Burger, A., Gräfen, I., Engemann, J., Niermann, E., Pieper, M., Kirchner, O., Gartemann, K.-H., and Eichenlaub, R. 2005. Identification, of homologues to the pathogenicity factor Pat-1, a putative serine protease of Clavibacter michiganensis subsp. michiganensis. Microbiol. Res. 160:417-427.
4. Comai, L., and Kosuge, T. 1983. Transposable element that causes mutations in a plant pathogenic Pseudomonas sp. J. Bacteriol. 154:1162-1167.
5. Davis, M. J., Gillaspie, Jr., A. G., Vidaver, A. K., and Harris, R. W. 1984. Clavibacter: A new genus containing some phytopathogenic coryneform bacteria, including Clavibacter xyli subsp. xyli sp. nov., subsp. nov. andClavibacter xyli subsp. cynodontis subsp. nov. , pathogens that cause ratoon stunting disease of sugarcane and bermudagrass stunting disease. Int. J. Syst. Bacteriol. 34:107-117.
6. De Boer, S. H., and Copeman, R. J. 1980. Bacterial ring rot testing with, the indirect fluorescent antibody staining procedure. Am. Potato J. 57:457-465.
7. Dow, J. M., Clarke, B. R., Milligan, D. E., Tang, J. L., and Daniels, M. J. 1990. Extracellular proteases from Xanthomonas campestris pv. campestris, the black rot pathogen. Appl. Environ. Microbiol. 56:29942998.
8. Dreier, J., Meletzus, D., and Eichenlaub, R. 1997. Characterization of the plasmid encoded virulence region pat-1 of phytopathogenic Clavibacter michiganensis subsp. michiganensis. Mol. Plant-Microbe Interact. 10:195-206.
9. Eichenlaub, R., Gartemann, K.-H., and Burger, A. 2006. Clavibacter michiganensis, a group of gram-positive phytopathogenic bacteria. Pages 385-421 in: Plant-associated bacteria, S. S. Gnanamanickam, ed. Springer Netherlands.
10. Elphinstone, J. G. 2004. Page 45 in: Potato ring rot (Clavibacter michiganensis subsp. sepedonicus): The facts. British Potato Council, Oxford, U.K.
11. Gartemann., K.-H., and Eichenlaub, R. 2001. Isolation and characterization of IS 1409, an insertion element of 4-chlorobenzoate- degrading Arthrobacter sp. strain TM1 and development of a system for transposon mutagenesis. J. Bacteriol. 183:3729-3736.
12. Gartemann, K., Abt, B., Bekel, T., Burger, A., Engemann, J., Flugel, M., Gaigalat, L., Goesmann, A., Grafen, I., Kalinowski, J., Kaup, O., Kirchner, O., Krause, L., Linke, B., McHardy, A., Meyer, F., Pohle, S., Ruckert, C., Schneiker, S., Zellermann, E.-M., Puhler, A., Eichenlaub, R., Kaiser, O., and Bartels, D. 2008. The genome sequence of the tomato-pathogenic actinomycete Clavibacter michiganensis subsp. michiganensis NCPPB382 reveals a large island involved in pathogenicity. J. Bacteriol. 190:2138-2149.
13. Heath., M. C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44:321-334.
14. Holt, J. G., Krieg, N. R., Sneath, P. H. A., Staley, J. T., and Williams, S. T. 1994. Pages 571-591 in: Bergey's Manual of Determinative Bacteriology, 9th ed. Williams and Wilkins, Baltimore.
15. Holtsmark, I., Takle, G. W., and Brurberg, M. B. 2008. Expression of putative virulence factors in. the potato pathogen Clavibacter michiganensis subsp. sepedonicus during infection. Arch. Microbiol. 189:131-139.
16. Hotson, A., and Mudgett, M. B. 2004. Cysteine proteases in phytopathogenic bacteria: Identification of plant targets and activation of innate immunity. Curr. Opin. Plant Biol. 7:384-390
17. Kirchner, O., Gartemann, K.-H., Zellermann, E.-M., Eichenlaub, R., and Burger, A. 2001. A highly efficient transposon mutagenesis system, for the tomato pathogen Clavibacter michiganensis subsp. michiganensis. Mol. Plant-Microbe Interact. 14:1312-1318.
18. Laine, M. J., Nakhei, H., Dreier, J., Lehtilä, K., Meletzus, D., Eichenlaub, R., and Metzler, M. C. 1996. Stable transformation of the gram-positive bacterium. Clavibacter michiganensis subsp. sepedonicus with several cloning vectors. Appl. Environ. Microbiol. 62:1500-1506.
19. Louws, F. J., Bell, J., Medina-Mora, C. M., Smart, C. D., Opgenorth, D., Ishimaru, C. A., Hausbeck, M. K., de Bruijn, E J., and Fulbright, D. W. 1998. rep-PCR-mediated genomic fingerprinting: A rapid and effective method to identify Clavibacter michiganensis. Phytopathology 88:862868.
20. Madden, J. C., Ruiz, N., and Caparon, M. 2001. Cytolysin-mediated translocation (CMT): A functional equivalent of Type III secretion in grampositive bacteria. Cell 104:143-152.
21. Marits, R., Koiv, V., Laasik, E., and Mäe, A. 1999. Isolation of an extracellular protease gene of Erwinia carotovora subsp. carotovora strain SCC3193 by transposon mutagenesis and the role of protease in phytopathogenicity. Microbiology 145:1959-1966.
22. McDonough, J. A., Hacker, K. E., Flores, A. R., Pavelka, M. S., Jr., and Braunstein, M. 2005. The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for die export of mycobacterial beta-lactamases. J. Bacteriol. 187:7667-79.
23. Monteiro-Vitorello, C. B., Camargo, L. E. A., Van Sluys, M. A., Kitajima, J. P., Truffi, D., do Amaral, A. M., Harakava, R., de Oliveira, J. C. F., Wood, D., de Oliveira, M. C., Miyaki, C., Takita, M. A., da Silva, A. C. R., Furlan, L. R., Carraro, D. M., Camarotte, G., Almeida N. F., Jr., Career, H., Coutinho, L. L., El-Dorry, H. A., Ferro, M. I. T., Gagliardi, P. R., Giglioti, E., Goldman, M. H. S., Goldman, G. H., Kimura, E. T., Ferro, E. S., Kuramae, E. E., Lemos, E. G. M., Lemos, M. V. F., Mauro, S. M. Z., Machado, M. A., Marino.C. L., Menck, C. F., Nunes, L. R., Oliveira, R. C., Pereira, G. G., Siqueira, W., de Souza, A. A., Tsai, S. M., Zanca, A. S., Simpson, A. J. G., Brumbley, S. M., and Setúbal, J. C. 2004. The genome sequence of the grampositive sugarcane pauthogen Leifsonia xyli subsp. xyli. Mol. PlantMicrobe Interact. 17:827-836.
24. Nissinen, R. 2000. Gram, positive phytopathogenic bacterium. Clavibacter michiganensis subsp. Sepedonicus: Virulence factors and interactions with plants. Page 114. Annales Universitatis Turkuensis ser. All, Turku, Finland.
25. Nissinen, R., Lai, F. M., Laine, M. J., Bauer, P. J., Reilley, A. A., Li, X., De Boer, S. H., Ishimaru C. A., and Metzler, M. C. 1997. Clavibacter michiganensis subsp. sepedonicus elicits a hypersensitive response in tobacco and secrets hypersensitive response-inducing protein(s). Phytopathology 87:678-684.
26. Nissinen, R., Kassuwi, S., Peltola, R., and Metzler, M. C. 2001. Strains of C. michiganensis subsp. sepedonicus impaired in cellulase production or induction of hypersensitive response can. partially compensate each other's deficiencies to enhance virulence in planta. Eur. J. Phytopathol. 107:175-182.
27. O'Toole, G., and Kolter, R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: A genetic analysis. Mol. Micro. 28:449-461.
28. Pallen, M. J. 2002. The ESAT-6/WXG100 superfamily-and a new grampositive secretion system? Trends Microbiol. 10:209-212.
29. Parkhill, J., Achtman, M., James, K. D., Bentley, S. D., Churcher, C., Klee, S. R., Morelli, G., Basham, D., Brown, D., Chillingworth, T., Davies, R. M., Davis, P., Devlin, K., Feltwell, T., Hamlin, N., Holroyd, S., Jagels, K., Leather, S., Moule, S., Mungall, K., Quail, M. A., Rajandream, M.A., Rutherford, K. M. Simmonds, M. Skelton, J. Whitehead, S. Spratt, B. G., and Barrell, B. G. 2000. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404:502-506.
30. Rosch, J. W., and Caparon, M. G. 2005. The ExPortal: An. organelle dedicated to the biogenesis of secreted proteins in Streptococcus pyogenes. Mol. Microbiol. 58:959-68.
31. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989 Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., U.S.A. Shao, F., Merritt, P. M., Bao, Z., Innes R. W., and Dixon, J. E. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-588.
32. Stork, I., Gartemann, K.-H., Burger, A., and Eichenlaub, R. 2008. A family of serine proteases of Clavibacter michiganensis subsp. michiganensis: chpC plays a role in colonization of the host plant tomato. Mol. Plant Pathol. 9:599-608.
33. van der Wolf, J. M., van Beckhoven, J. R. C. M., Hukkanen, A., Karjalainen, R., and Müller, P. 2005. Fate of Clavibacter michiganensis ssp. epedonicus, the causal organism of bacterial ring rot of potato, in weeds and field crops. J. Phytopathol. 153:358-365.
34. Xu, G.W., and Gonzalez, CF. 1989. Evaluation of TN4431-induced protease mutants of Xanthomonas campestris pv. oryzae for growth in plants and pathogenicity. Phytopathol. 79:1210-1215.
35. Zhang,Y., Bak, D. D., Heid, H., and Geider, K. 1999. Molecular characterization of a protease secreted by Erwinia amylovora. J. Mol. Biology 289:1239-1251.