Pseudomonas syringae evades host immunity by degrading flagellin monomers with alkaline protease AprA

Molecular Plant-Microbe Interactions

Volumn 27, Issue 7, 2014, Pages 603-610

  Pel, Michiel J C ^a,b   Van Dijken, Anja J H ^a   Bardoel, Bart W ^c   Seidl, Michael F ^a,b   Van Der Ent, Sjoerd ^a,b   Van Strijp, Jos A G ^c   Pieterse, Corné M J ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; MICROBIAL SERINE PROTEINASES; SERINE PROTEINASE; VIRULENCE FACTOR;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; TOMATO;

ARABIDOPSIS; FLAGELLIN; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LYCOPERSICON ESCULENTUM; PLANT DISEASES; PSEUDOMONAS SYRINGAE; SERINE ENDOPEPTIDASES; VIRULENCE FACTORS;

EID: 84901719340     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-02-14-0032-R     Document Type: Article

References (60)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gómez-Gómez, L., Boller, T., Ausubel, F. M., and Sheen, J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983. (Pubitemid 34193435)
3. Bardoel, B. W., and Van Strijp, J. A. G. 2011. Molecular battle between host and bacterium: Recognition in innate immunity. J. Mol. Recognit. 24:1077-1086.
4. Bardoel, B. W., Van der Ent, S., Pel, M. J. C., Tommassen, J., Pieterse, C. M. J., Van Kessel, K. P. M., and Van Strijp, J. A. G. 2011. Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7:e1002206.
5. Bardoel, B. W., Van Kessel, K. P. M., Van Strijp, J. A. G., and Milder, F. J. 2012. Inhibition of Pseudomonas aeruginosa virulence: Characterization of the AprA-AprI interface and species selectivity. J. Mol. Biol. 415:573-583.
6. Bethesda Research Laboratories. 1986. BRL pUC host: E. coli competent cells. Focus 8:9.
7. Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern recognition receptors. Annu. Rev. Plant Biol. 60:379-406.
8. Boller, T., and He, S. Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744.
9. Bolton, M. D., Van Esse, H. P., Vossen, J. H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., Van den Berg, G. C. M., Borras-Hidalgo, O., Dekker, H. L., De Koster, C. G., de Wit, P. J., Joosten, M. H., and Thomma, B. P. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119-136. (Pubitemid 351832760)
10. Boyer, H. M., and Roulland-Dussoix, D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
11. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L., Liu, J., Yuan, Q. Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W.-L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186. (Pubitemid 37071853)
12. Chevance, F. F. V., and Hughes, K. T. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465. (Pubitemid 351696439)
13. Clough, S. J., and Bent, A. F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.
14. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., and Scheible, W. R. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139:5-17. (Pubitemid 43951587)
15. De Jonge, R., Van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., Van der Krol, S., Shibuya, N., Joosten, M. H. A. J., and Thomma, B. P. H. J. 2010. Conserved fungal LysM effector Ecp6 prevents chitin triggered immunity in plants. Science 329:953-955.
16. Duong, F., Lazdunski, A., Cami, B., and Murgier, M. 1992. Sequence of a cluster of genes controlling synthesis and secretion of alkaline protease in Pseudomonas aeruginosa: Relationships to other secretory pathways. Gene 121:47-54.
17. Felix, G., Duran, J. D., Volko, S., and Boller, T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-276.
18. Figurski, D. H., and Helsinki, D. R. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U.S.A. 76:1648-1652. (Pubitemid 9175374)
19. Galibert, F., Finan, T. M., Long, S. R., Pühler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A., and Boistard, P. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672. (Pubitemid 32728664)
20. Gomez-Gomez, L., and Boller, T. 2000. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003-1012.
21. Gomez-Gomez, L., and Boller, T. 2002. Flagellin perception: A paradigm for innate immunity. Trends Plant Sci. 7:251-256. (Pubitemid 36726527)
22. Guzzo, J., Duong, F., Wandersman, C., Murgier, M., and Lazdunski, A. 1991. The secretion genes of Pseudomonas aeruginosa alkaline protease are functionally related to those of Erwinia chrysanthemi proteases and Escherichia coli alpha-haemolysin. Mol. Microbiol. 5:447-453. (Pubitemid 21896065)
23. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., Eng, J. K., Akira, S., Underhill, D. M., and Aderem, A. 2001. The innate immune response to bacterial flagellin is mediated by toll-like receptor 5. Nature 410:1099-1103. (Pubitemid 32391041)
24. Herrero, M., De Lorenzo, V., and Timmis, K. N. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567. (Pubitemid 20372801)
25. Hoagland, D. R., and Arnon, D. I. 1938. The water culture method for growing plants without soil. Calif. Agric. Exp. Stn. Bull. 347:36-39.
26. Hong, S. M., Bahn, S. C., Lyu, A., Jung, H. S., and Ahn, J. H. 2010. Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. Plant Cell Physiol. 51:1694-1706.
27. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. (Pubitemid 44764102)
28. Kaniga, K., Delor, I., and Cornelis, G. R. 1991. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: Inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137-141.
29. Kerkhoven, R., Van Enckevort, F. H. J., Boekhorst, J., Molenaar, D., and Siezen, R. J. 2004. Visualization for genomics: The microbial genome viewer. Bioinformatics 20:1812-1814. (Pubitemid 39162063)
30. King, E. O., Ward, M. K., and Raney, D. E. 1954. Two simple media for the demonstration of phycocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
31. Klimpel, K. R., Arora, N., and Leppla, S. H. 1994. Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol. Microbiol. 13:1093-1100. (Pubitemid 24300720)
32. Komoriya, K., Shibano, N., Higano, T., Azuma, N., Yamaguchi, S., and Aizawa, S. 1999. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34:767-779.
33. Kovach, M. E., Phillips, R. W., Elzer, P. H., Roop, R. M., and Peterson, K. M. 1994. pBBR1MCS: A broad-host-range cloning vector. Biotechniques 16:800-802. (Pubitemid 2103380)
34. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. 2004. The N terminus of bacterial elongation factor tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496-3507. (Pubitemid 41096021)
35. Létoffé, S., Delepelaire, P., and Wandersman, C. 1989. Characterization of a protein inhibitor of extracellular proteases produced by Erwinia chrysanthemi. Mol. Microbiol. 3:79-86. (Pubitemid 19239960)
36. Létoffé, S., Delepelaire, P., and Wandersman, C. 1990. Protease secretion by Erwinia chrysanthemi: The specific secretion functions are analogous to those of Escherichia coli alpha-hemolysin. EMBO (Eur. Mol. Biol. Organ.) J. 9:1375-1382.
37. Liehl, P., Blight, M., Vodovar, N., Boccard, F., and Lemaitre, B. 2006. Prevalence of local immune response against oral infection in a Drosophila/ Pseudomonas infection model. PLoS Pathog. 2:551-561.
38. Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S. V., Machado, M. A., Toth, I., Salmond, G., And Foster, G. D. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614-629.
39. Miyoshi, S., and Shinoda, S. 2000. Microbial metalloproteases and pathogenesis. Microb. Infect. 2:91-98. (Pubitemid 30077931)
40. Parmely, M., Gale, A., Clabaugh, M., Horvat, R., and Zhou, W. W. 1990. Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect. Immun. 58:3009-3014. (Pubitemid 20267696)
41. Pel, M. J. C., and Pieterse, C. M. J. 2013. Microbial recognition and evasion of host immunity. J. Exp. Bot. 64:1237-1248.
42. Preston, G. M. 2000. Pseudomonas syringae pv. tomato: The right pathogen, of the right plant, at the right time. Mol. Plant Pathol. 1:263-275.
43. Ramos, H. C., Rumbo, M., and Sirard, J. C. 2004. Bacterial flagellins: Mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12:509-517. (Pubitemid 39370733)
44. Ronald, P. C., and Beutler, B. 2010. Plant and animal sensors of conserved microbial signatures. Science 330:1061-1064.
45. Samatey, F. A., Imada, K., Nagashima, S., Vonderviszt, F., Kumasaka, T., Yamamoto, M., and Namba, K. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331-337. (Pubitemid 32246042)
46. Shan, L. B., He, P., Li, J. M., Heese, A., Peck, S. C., Nürnberger, T., Martin, G. B., and Sheen, J. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17-27. (Pubitemid 351944052)
47. Shimada, T. L., Shimada, T., and Hara-Nishimura, I. 2010. A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61:519-528.
48. Silby, M. W., Cerdeno-Tarraga, A. M., Vernikos, G. S., Giddens, S. R., ackson, R. W., Preston, G. M., Zhang, X. X., Moon, C. D., Gehrig, S. M., Godfrey, S. A. C., Knight, C. G., Malone, J. G., Robinson, Z., Spiers, A. J., Harris, S., Challis, G. L., Yaxley, A. M., Harris, D., Seeger, K., Murphy, L., Rutter, S., Squares, R., Quail, M. A., Saunders, E., Mavromatis, K., Brettin, T. S., Bentley, S. D., Hothersall, J., Stephens, E., Thomas, C. M., Parkhill, J., Levy, S. B., Rainey, P. B., and Thomson, N. R. 2009. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 10:R51.
49. Smith, K. D., Andersen-Nissen, E., Hayashi, F., Strobe, K., Bergman, M. A., Barrett, S. L. R., Cookson, B. T., and Aderem, A. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4:1247-1253. (Pubitemid 37540694)
50. Stover, C., Pham, X., Erwin, A., Mizoguchi, S., Warrener, P., Hickey, M., Brinkman, F., Hufnagle, W., Kowalik, D., Lagrou, M., Garber, R. L., Goltry, L., Tolentino, E., Westbrock-Wadman, S., Yuan, Y., Brody, L. L., Coulter, S. N., Folger, K. R., Kas, A., Larbig, K., Lim, R., Smith, K., Spencer, D., Wong, G. K.-S., Wu, Z., Paulsen, I. T., Reizer, J., Saier, M. H., Hancock, R. E. W., Lory, S., and Olson, M. V. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
51. Taylor, L. A., and Rose, R. E. 1988. A correction in the nucleotide-sequence of the Tn903 kanamycin resistance determinant in Puc4k. Nucleic Acids Res. 16:358-358.
52. Tommassen, J., Filloux, A., Bally, M., Murgier, M., and Lazdunski, A. 1992. Protein secretion in Pseudomonas aeruginosa. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 9:73-90.
53. Van Wees, S. C. M., Luijendijk, M., Smoorenburg, I., Van Loon, L. C., and Pieterse, C. M. J. 1999. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol. Biol. 41:537-549. (Pubitemid 129646155)
54. Van Wees, S. C. M., Van Pelt, J. A., Bakker, P. A. H. M., and Pieterse, C. M. J. 2013. Bioassays for assessing jasmonate-dependent defenses triggered by pathogens, herbivorous insects, or beneficial rhizobacteria. Methods Mol. Biol. 1011:35-49.
55. Verhage, A., Vlaardingerbroek, I., Raaymakers, C., Van Dam, N., Dicke, M., Van Wees, S. C. M., and Pieterse, C. M. J. 2011. Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front. Plant Sci. 2:1-12.
56. Vieira, J., and Messing, J. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268. (Pubitemid 13201666)
57. Whalen, M. C., Innes, R. W., Bent, A. F., and Staskawicz, B. J. 1991. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3:49-59. (Pubitemid 21913648)
58. Wyant, T. L., Tanner, M. K., and Sztein, M. B. 1999. Salmonella typhi flagella are potent inducers of proinflammatory cytokine secretion by human monocytes. Infect. Immun. 67:3619-3624. (Pubitemid 29291537)
59. Zeng, W., and He, S.-Y. 2010. A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv. tomato DC3000 in Arabidopsis. Plant Physiol. 153:1188-1198.
60. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D. G., Felix, G., and Boller, T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764-767. (Pubitemid 38508287)