Pseudomonas syringae HrpP is a type III secretion substrate specificity switch domain protein that is translocated into plant cells but functions atypically for a substrate-switching protein

Journal of Bacteriology

Volumn 191, Issue 9, 2009, Pages 3120-3131

  Morello, Joanne E ^a   Collmer, Alan ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; HRPA PROTEIN; HRPP PROTEIN; PILIN; PROTEIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; YSCP PROTEIN; VIRULENCE FACTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL SECRETION; CONTROLLED STUDY; ENZYME SPECIFICITY; GENE DELETION; GENE EXPRESSION; GENE SWITCHING; GENE TRANSLOCATION; IN VITRO STUDY; MUTANT; NONHUMAN; PATHOGENICITY; PATHOTYPE; PLANT CELL; PLANT DISEASE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOMONAS SYRINGAE; TOBACCO; TOMATO; TRANS ISOMER; TYPE III SECRETION; GENETIC COMPLEMENTATION; GENETICS; MICROBIOLOGY; PHYSIOLOGY;

LYCOPERSICON ESCULENTUM; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM; PSEUDOMONAS SYRINGAE; YERSINIA;

BACTERIAL PROTEINS; GENE DELETION; GENETIC COMPLEMENTATION TEST; LYCOPERSICON ESCULENTUM; PLANT DISEASES; PSEUDOMONAS SYRINGAE; SEQUENCE DELETION; TOBACCO; VIRULENCE FACTORS;

EID: 65549156199     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01623-08     Document Type: Article

References (51)

1. Agrain, C., I. Callebaut, L. Journet, I. Sorg, C. Paroz, L. J. Mota, and G. R. Cornelis. 2005. Characterization of a type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol. Microbiol. 56:54-67.
2. Agrain, C., I. Sorg, C. Paroz, and G. R. Cornelis. 2005. Secretion of YscP from Yersinia enterocolitica is essential to control the length of the injecti- some needle but not to change the type III secretion substrate specificity. Mol. Microbiol. 57:1415-1427.
3. Akeda, Y., and J. E. Galan. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911-915.
4. Alfano, J. R., A. O. Charkowski, W.-L. Deng, J. L. Badel, T. Petnicki- Ocwieja, K. van Dijk, and A. Collmer. 2000. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. USA 97:4856-4861.
5. Badel, J. L., R. Shimizu, H.-S. Oh, and A. Collmer. 2006. A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol. Plant-Microbe Interact. 19:99-111.
6. Block, A., G. Li, Z. Q. Fu, and J. R. Alfano. 2008. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11:396-403.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 72:248-254.
8. Buell, C. R., V. Joardar, M. Lindeberg, J. Selengut, I. T. Paulsen, M. L. Gwinn, R. J. Dodson, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, S. Daugherty, L. Brinkac, M. J. Beanan, D. H. Haft, W. C. Nelson, T.Davidsen, J. Liu, Q. Yuan, H. Khouri, N. Fedorova, B. Tran, D. Russell, K. Berry, T. Utterback, S. E. Vanaken, T. V. Feldblyum, M. D'Ascenzo, W.-L. Deng, A. R. Ramos, J. R. Alfano, S. Cartinhour, A. K. Chatterjee, T. P. Delaney, S. G. Lazarowitz, G. B. Martin, D. J. Schneider, X. Tang, C. L. Bender, O. White, C. M. Fraser, and A. Collmer. 2003. The complete sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100:10181-10186.
9. Büttner, D., and U. Bonas. 2002. Getting across-bacterial type III effector proteins on their way to the plant cell. EMBO J. 21:5313-5322.
10. Bü'ttner, D., C. Lorenz, E. Weber, and U. Bonas. 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.
11. Chang, J. H., J. M. Urbach, T. F. Law, L. W. Arnold, A. Hu, S. Gombar, S. R. Grant, F. M. Ausubel, and J. L. Dangl. 2005. A high-throughput, near- saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl. Acad. Sci. USA 102:2549-2554.
12. Collmer, A., J. L. Badel, A. O. Charkowski, W.-L. Deng, D. E. Fouts, A. R. Ramos, A. H. Rehm, D. M. Anderson, O. Schneewind, K. van Dijk, and J. R. Alfano. 2000. Pseudomonas syringae Hrp type III secretion system and effector proteins. Proc. Natl. Acad. Sci. USA 97:8770-8777.
13. Cornelis, G. R. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811-825.
14. Cuppels, D. A. 1986. Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl. Environ. Microbiol. 51:323-327.
15. Edqvist, P. J., J. Olsson, M. Lavander, L. Sundberg, A. Forsberg, H. Wolf- Watz, and S. A. Lloyd. 2003. YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J. Bacteriol. 185:2259-2266.
16. Fadouloglou, V. E., A. P. Tampakaki, N. M. Glykos, M. N. Bastaki, J. M. Hadden, S. E. Phillips, N. J. Panopoulos, and M. Kokkinidis. 2004. Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems. Proc. Natl. Acad. Sci. USA 101:70-75.
17. Figurski, D., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
18. Fouts, D. E., J. L. Badel, A. R. Ramos, R. A. Rapp, and A. Collmer. 2003. A Pseudomonas syringae pv. tomato DC3000 Hrp (type III secretion) deletion mutant expressing the Hrp system of bean pathogen P. syringae pv. syringae 61 retains normal host specificity for tomato. Mol. Plant-Microbe Interact. 16:43-52.
19. Galán, J. E., and H. Wolf-Watz. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567-573.
20. Göhre, V., and S. Robatzek. 2008. Breaking the barriers: microbial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46:189-215.
21. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
22. Huang, H.-C., R.-W. Lin, C.-J. Chang, A. Collmer, and W.-L. Deng. 1995. The complete hrp gene cluster of Pseudomonas syringae pv. syringae 61 includes two blocks of genes required for harpinPss secretion that are arranged colinearly with Yersinia ysc homologs. Mol. Plant-Microbe Interact. 8:733-746.
23. Hueck, C. J. 1998. Type III proteinsecretionsystems inbacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
24. Huynh, T. V., D. Dahlbeck, and B. J. Staskawicz. 1989. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-1377.
25. Jin, Q., and S. Y. He. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-2558.
26. Journet, L., C. Agrain, P. Broz, and G. R. Cornelis. 2003. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302: 1757-1760.
27. King, E. O., M. K. Ward, and D. E. Raney. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
28. Kvitko, B. H., A. R. Ramos, J. E. Morello, H.-S. Oh, and A. Collmer. 2007. Identification of harpins in Pseudomonas syringae pv. tomato DC3000, which are functionally similar to HrpK1 in promoting translocation of type III secretion system effectors. J. Bacteriol. 189:8059-8072.
29. Li, J., H. Ochman, E. A. Groisman, E. F. Boyd, F. Solomon, K. Nelson, and R. K. Selander. 1995. Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc. Natl. Acad. Sci. USA 92:7252-7256.
30. Lindeberg, M., S. Cartinhour, C. R. Myers, L. M. Schechter, D. J. Schneider, and A. Collmer. 2006. Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol. Plant-Microbe Interact. 19:1151-1158.
31. Lorenz, C., S. Schulz, T. Wolsch, O. Rossier, U. Bonas, and D. Buttner. 2008. HpaC controls substrate specificity of the Xanthomonas type III secretion system. PLoS Pathog. 4:e1000094.
32. Makishima, S., K. Komoriya, S. Yamaguchi, and S. I. Aizawa. 2001. Length of the flagellar hook and the capacity of the type III export apparatus. Science 291:2411-2413.
33. Marlovits, T. C., T. Kubori, M. Lara-Tejero, D. Thomas, V. M. Unger, and J. E. Galan. 2006. Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 441:637-640.
34. Moriya, N., T. Minamino, K. T. Hughes, R. M. Macnab, and K. Namba. 2006. The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J. Mol. Biol. 359:466-477.
35. Mota, L. J., L. Journet, I. Sorg, C. Agrain, and G. R. Cornelis. 2005. Bacterial injectisomes: needle length does matter. Science 307:1278.
36. Mudgett, M. B., O. Chesnokova, D. Dahlbeck, E. T. Clark, O. Rossier, U. Bonas, and B. J. Staskawicz. 2000. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. USA 97:13324-13329.
37. Oh, H.-S., B. H. Kvitko, J. E. Morello, and A. Collmer. 2007. Pseudomonas syringae lytic transglycosylases coregulated with the type III secretion system contribute to the translocation of effector proteins into plant cells. J. Bacte- riol. 189:8277-8289.
38. Payne, P. L., and S. C. Straley. 1999. YscP of Yersinia pestis is a secreted component of the Yop secretion system. J. Bacteriol. 181:2852-2862.
39. Ramos, A. R., J. E. Morello, S. Ravindran, W.-L. Deng, H.-C. Huang, and A. Collmer. 2007. Identification of Pseudomonas ssyringae pv. syringae 61 type III secretion system Hrp proteins that can travel the type III pathway and contribute to the translocation of effector proteins into plant cells. J. Bacteriol. 189:5773-5778.
40. Rose, J. 2003. The plant cell wall. Blackwell Press, Ltd., Oxford, United Kingdom.
41. Rossier, O., G. Van den Ackerveken, and U. Bonas. 2000. HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathoge- nicity and recognition by the host plant. Mol. Microbiol. 38:828-838.
42. Schechter, L. M., K. A. Roberts, Y. Jamir, J. R. Alfano, and A. Collmer. 2004. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol. 186:543-555.
43. Schechter, L. M., M. Vencato, K. L. Jordan, S. E. Schneider, D. J. Schneider, and A. Collmer. 2006. Multiple approaches to a complete inventory of Pseudomonas syringae pv. tomato DC3000 type III secretion system effector proteins. Mol. Plant-Microbe Interact. 19:1180-1192.
44. Sorg, I., S. Wagner, M. Amstutz, S. A. Muller, P. Broz, Y. Lussi, A. Engel, and G. R. Cornelis. 2007. YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J. 26:3015-3024.
45. Sory, M.-P., A. Boland, I. Lambermont, and G. R. Cornelis. 1995. Identification of the YopE and YopH domains required for secretion and internal- ization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl. Acad. Sci. USA 92:11998-12002.
46. Sory, M.-P., and G. R. Cornelis. 1994. Translocation of a hybrid YopEadenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
47. Stainier, I., S. Bleves, C. Josenhans, L. Karmani, C. Kerbourch, I. Lamber- mont, S. Totemeyer, A. Boyd, and G. R. Cornelis. 2000. YscP, a Yersinia protein required for Yop secretion that is surface exposed, and released in low Ca2+. Mol. Microbiol. 37:1005-1018.
48. Tampakaki, A. P., V. E. Fadouloglou, A. D. Gazi, N. J. Panopoulos, and M. Kokkinidis. 2004. Conserved features of type III secretion. Cell. Microbiol. 6:805-816.
49. van Dijk, K., D. E. Fouts, A. H. Rehm, A. R. Hill, A. Collmer, and J. R. Alfano. 1999. The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J. Bacteriol. 181:4790-4797.
50. Wei, W., A. Plovanich-Jones, W.-L. Deng, A. Collmer, H.-C. Huang, and S. Y. He. 2000. The gene coding for the Hrp pilus structural protein is required for type III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato. Proc. Natl. Acad. Sci. USA 97:2247-2252.
51. Wood, S. E., J. Jin, and S. A. Lloyd. 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.