Characterization of HrpB2 from Xanthomonas campestris pv. vesicatoria identifies protein regions that are essential for type III secretion pilus formation

Microbiology

Volumn 158, Issue 5, 2012, Pages 1334-1349

  Hartmann, Nadine ^a   Schulz, Steve ^a   Lorenz, Christian ^a,b   Fraas, Simone ^a   Hause, Gerd ^a   Büttner, Daniela ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PENTAPEPTIDE; PROTEIN HRPB2; PROTEIN HRPF; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; GENE INSERTION SEQUENCE; GENETIC COMPLEMENTATION; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN SECRETION; TRANSMISSION ELECTRON MICROSCOPY; TRANSPOSON; TYPE III SECRETION SYSTEM; XANTHOMONAS CAMPESTRIS;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CAPSICUM; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MUTAGENESIS, INSERTIONAL; PERIPLASM; POINT MUTATION; SEQUENCE DELETION; XANTHOMONAS CAMPESTRIS; XANTHOMONAS VESICATORIA;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; XANTHOMONAS CAMPESTRIS PV. VESICATORIA;

EID: 84860503185     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.057604-0     Document Type: Article

References (57)

1. Agrain, C., Callebaut, I., Journet, L., Sorg, I., Paroz, C., Mota, L. J. & Cornelis, G. R. (2005). Characterization of a type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol Microbiol 56, 54-67.
2. Alegria, M. C., Docena, C., Khater, L., Ramos, C. H., da Silva, A. C. & Farah, C. S. (2004). New protein-protein interactions identified for the regulatory and structural components and substrates of the type III secretion system of the phytopathogen Xanthomonas axonopodis pathovar citri. J Bacteriol 186, 6186-6197.
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1996). Current Protocols in Molecular Biology. New York: Wiley.
4. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., Sansonetti, P. & Allaoui, A. (2001). Structure and composition of the Shigella flexneri "needle complex", a part of its type III secreton. Mol Microbiol 39, 652-663.
5. Bolchi, A., Ottonello, S. & Petrucco, S. (2005). A general one-step method for the cloning of PCR products. Biotechnol Appl Biochem 42, 205-209.
6. Bonas, U., Schulte, R., Fenselau, S., Minsavage, G. V., Staskawicz, B. J. & Stall, R. E. (1991). Isolation of a gene-cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol Plant Microbe Interact 4, 81-88.
7. Botteaux, A., Sani, M., Kayath, C. A., Boekema, E. J. & Allaoui, A. (2008). Spa32 interaction with the inner-membrane Spa40 component of the type III secretion system of Shigella flexneri is required for the control of the needle length by a molecular tape measure mechanism. Mol Microbiol 70, 1515-1528.
8. Büttner, D. & Bonas, U. (2010). Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34, 107-133.
9. Büttner, D. & He, S. Y. (2009). Type III protein secretion in plant pathogenic bacteria. Plant Physiol 150, 1656-1664.
10. Büttner, D., Nennstiel, D., Klüsener, B. & Bonas, U. (2002). Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J Bacteriol 184, 2389-2398.
11. Büttner, D., Lorenz, C., Weber, E. & Bonas, U. (2006). Targeting of two effector protein classes to the type III secretion system by a HpaC-and HpaB-dependent protein complex from Xanthomonas campestris pv. vesicatoria. Mol Microbiol 59, 513-527.
12. Büttner, D., Noël, L., Stuttmann, J. & Bonas, U. (2007). Characterization of the nonconserved hpaB-hrpF region in the hrp pathogenicity island from Xanthomonas campestris pv. vesicatoria. Mol Plant Microbe Interact 20, 1063-1074.
13. Canteros, B. I. (1990). Diversity of plasmids and plasmid-encoded phenotypic traits in Xanthomonas campestris pv. vesicatoria. PhD thesis, University of Florida.
14. Cappelletti, P. A., dos Santos, R. F., do Amaral, A. M., Homem, R. A., Souza, T. S., Machado, M. A. & Farah, C. S. (2011). Structurefunction analysis of the HrpB2-HrcU interaction in the Xanthomonas citri type III secretion system. PLoS ONE 6, e17614.
15. Daniels, M. J., Barber, C. E., Turner, P. C., Sawczyc, M. K., Byrde, R. J. W. & Fielding, A. H. (1984). Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J 3, 3323-3328.
16. Deane, J. E., Abrusci, P., Johnson, S. & Lea, S. M. (2010). Timing is everything: the regulation of type III secretion. Cell Mol Life Sci 67, 1065-1075.
17. Engler, C., Kandzia, R. & Marillonnet, S. (2008). A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3, e3647.
18. Erhardt, M., Namba, K. & Hughes, K. T. (2010). Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2, a000299.
19. Escolar, L., Van Den Ackerveken, G., Pieplow, S., Rossier, O. & Bonas, U. (2001). Type III secretion and in planta recognition of the Xanthomonas avirulence proteins AvrBs1 and AvrBsT. Mol Plant Pathol 2, 287-296.
20. Ferris, H. U., Furukawa, Y., Minamino, T., Kroetz, M. B., Kihara, M., Namba, K. & Macnab, R. M. (2005). FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280, 41236-41242.
21. Figurski, D. H. & Helinski, D. R. (1979). Replication of an origincontaining derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648-1652.
22. Ghosh, P. (2004). Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68, 771-795.
23. He, S. Y., Nomura, K. & Whittam, T. S. (2004). Type III protein secretion mechanism in mammalian and plant pathogens. Biochim Biophys Acta 1694, 181-206.
24. Huguet, E., Hahn, K., Wengelnik, K. & Bonas, U. (1998). hpaA mutants of Xanthomonas campestris pv. vesicatoria are affected in pathogenicity but retain the ability to induce host-specific hypersensitive reaction. Mol Microbiol 29, 1379-1390.
25. Jones, J. D. & Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329.
26. Jones, J. B., Lacy, G. H., Bouzar, H., Stall, R. E. & Schaad, N. W. (2004). Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst Appl Microbiol 27, 755-762.
27. Kousik, C. S. & Ritchie, D. F. (1998). Response of bell pepper cultivars to bacterial spot pathogen races that individually overcome major resistance genes. Plant Dis 82, 181-186.
28. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., II & Peterson, K. M. (1995). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175-176.
29. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galán, J. E. & Aizawa, S. I. (1998). Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602-605.
30. Lavander, M., Sundberg, L., Edqvist, P. J., Lloyd, S. A., Wolf-Watz, H. & Forsberg, A. (2002). Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J Bacteriol 184, 4500-4509.
31. Lorenz, C. & Büttner, D. (2011). Secretion of early and late substrates of the type III secretion system from Xanthomonas is controlled by HpaC and the C-terminal domain of HrcU. Mol Microbiol 79, 447-467.
32. Lorenz, C., Schulz, S., Wolsch, T., Rossier, O., Bonas, U. & Büttner, D. (2008). HpaC controls substrate specificity of the Xanthomonas type III secretion system. PLoS Pathog 4, e1000094.
33. Marlovits, T. C., Kubori, T., Sukhan, A., Thomas, D. R., Galán, J. E. & Unger, V. M. (2004). Structural insights into the assembly of the type III secretion needle complex. Science 306, 1040-1042.
34. Marlovits, T. C., Kubori, T., Lara-Tejero, M., Thomas, D., Unger, V. M. & Galán, J. E. (2006). Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 441, 637-640.
35. Matteï, P. J., Faudry, E., Job, V., Izoré, T., Attree, I. & Dessen, A. (2011). Membrane targeting and pore formation by the type III secretion system translocon. FEBS J 278, 414-426.
36. Ménard, R., Sansonetti, P. J. & Parsot, C. (1993). Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175, 5899-5906.
37. Minamino, T. & MacNab, R. M. (2000). Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35, 1052-1064.
38. Minsavage, G. V., Dahlbeck, D., Whalen, M. C., Kearny, B., Bonas, U., Staskawicz, B. J. & Stall, R. E. (1990). Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria-pepper interactions. Mol Plant Microbe Interact 3, 41-47.
39. Morbitzer, R., Elsaesser, J., Hausner, J. & Lahaye, T. (2011). Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res 39, 5790-5799.
40. Ogino, T., Ohno, R., Sekiya, K., Kuwae, A., Matsuzawa, T., Nonaka, T., Fukuda, H., Imajoh-Ohmi, S. & Abe, A. (2006). Assembly of the type III secretion apparatus of enteropathogenic Escherichia coli. J Bacteriol 188, 2801-2811.
41. Ronald, P. C. & Staskawicz, B. J. (1988). The avirulence gene avrBs1 from Xanthomonas campestris pv. vesicatoria encodes a 50-kD protein. Mol Plant Microbe Interact 1, 191-198.
42. Rossier, O., Wengelnik, K., Hahn, K. & Bonas, U. (1999). The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. Proc Natl Acad Sci U S A 96, 9368-9373.
43. Rossier, O., Van den Ackerveken, G. & Bonas, U. (2000). HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol Microbiol 38, 828-838.
44. Ryan, R. P., Vorhölter, F. J., Potnis, N., Jones, J. B., Van Sluys, M. A., Bogdanove, A. J. & Dow, J. M. (2011). Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 9, 344-355.
45. Sal-Man, N., Deng, W. & Finlay, B. B. (2012). EscI-a crucial component of the type III secretion system forms the inner rod structure in enteropathogenic Escherichia coli. Biochem J 442, 119-125.
46. Sani, M., Allaoui, A., Fusetti, F., Oostergetel, G. T., Keegstra, W. & Boekema, E. J. (2007). Structural organization of the needle complex of the type III secretion apparatus of Shigella flexneri. Micron 38, 291-301.
47. Schulz, S. & Büttner, D. (2011). Functional characterization of the type III secretion substrate specificity switch protein HpaC from Xanthomonas campestris pv. vesicatoria. Infect Immun 79, 2998-3011.
48. Sorg, I., Wagner, S., Amstutz, M., Müller, S. A., Broz, P., Lussi, Y., Engel, A. & Cornelis, G. R. (2007). YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J 26, 3015-3024.
49. Szczesny, R., Jordan, M., Schramm, C., Schulz, S., Cogez, V., Bonas, U. & Büttner, D. (2010). Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. New Phytol 187, 983-1002.
50. Thein, M., Sauer, G., Paramasivam, N., Grin, I. & Linke, D. (2010). Efficient subfractionation of Gram-negative bacteria for proteomics studies. J Proteome Res 9, 6135-6147.
51. Vieira, J. & Messing, J. (1987). Production of single-stranded plasmid DNA. Methods Enzymol 153, 3-11.
52. Weber, E., Ojanen-Reuhs, T., Huguet, E., Hause, G., Romantschuk, M., Korhonen, T. K., Bonas, U. & Koebnik, R. (2005). The type III-dependent Hrp pilus is required for productive interaction of Xanthomonas campestris pv. vesicatoria with pepper host plants. J Bacteriol 187, 2458-2468.
53. Weber, E., Berger, C., Bonas, U. & Koebnik, R. (2007). Refinement of the Xanthomonas campestris pv. vesicatoria hrpD and hrpE operon structure. Mol Plant Microbe Interact 20, 559-567.
54. Wengelnik, K., Marie, C., Russel, M. & Bonas, U. (1996a). Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction. J Bacteriol 178, 1061-1069.
55. Wengelnik, K., Van den Ackerveken, G. & Bonas, U. (1996b). HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol Plant Microbe Interact 9, 704-712.
56. Wengelnik, K., Rossier, O. & Bonas, U. (1999). Mutations in the regulatory gene hrpG of Xanthomonas campestris pv. vesicatoria result in constitutive expression of all hrp genes. J Bacteriol 181, 6828-6831.
57. Wood, S. E., Jin, J. & Lloyd, S. A. (2008). YscP and YscU switch the substrate specificity of the Yersinia type III secretion system by regulating export of the inner rod protein YscI. J Bacteriol 190, 4252-4262.