Pseudomonas syringae CC1557: A highly virulent strain with an unusually small type iii effector repertoire that includes a novel effector

Molecular Plant-Microbe Interactions

Volumn 27, Issue 9, 2014, Pages 923-932

  Hockett, Kevin L ^a   Nishimura, Marc T ^b   Karlsrud, Erick ^a   Dougherty, Kevin ^a   Baltrus, David A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; SYRINGOMYCIN;

ARTICLE; BACTERIAL GENOME; CHEMICAL STRUCTURE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PLANT DISEASE; PLANT LEAF; PROTEIN MOTIF; PSEUDOMONAS SYRINGAE; SPECIES DIFFERENCE; TOBACCO; VIRULENCE;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GENOMICS; HOST-PATHOGEN INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT LEAVES; PSEUDOMONAS SYRINGAE; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TOBACCO; VIRULENCE;

EID: 84906241343     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-11-13-0354-R     Document Type: Article

References (41)

1. Angiuoli, S. V., Gussman, A., Klimke, W., Cochrane, G., Field, D., Garrity, G., Kodira, C. D., Kyrpides, N., Madupu, R., Markowitz, V., Tatusova, T., Thomson, N., and White, O. 2008. Toward an online repository of standard operating procedures (SOPs) for (meta)genomic annotation. OMICS 12:137-141.
2. Araki, H., Tian, D., Goss, E. M., Jakob, K., Halldorsdottir, S. S., Kreitman, M., and Bergelson, J. 2006. Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103:5887-5892.
3. Badel, J. L., Shimizu, R., Oh, H.-S., and Collmer, A. 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.
4. Baltrus, D. A., Nishimura, M. T., Romanchuk, A., Chang, J. H., Mukhtar, M. S., Cherkis, K., Roach, J., Grant, S. R., Jones, C. D., and Dangl, J. L. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog. 7:e1002132. Published online.
5. Baltrus, D. A., Nishimura, M. T., Dougherty, K. M., Biswas, S., Mukhtar, M. S., Vicente, J., Holub, E. B., and Dangl, J. L. 2012. The molecular basis of host specialization in bean pathovars of Pseudomonas syringae. Mol. Plant-Microbe Interact. 25:877-888.
6. Baltrus, D. A., Dougherty, K., Beckstrom-Sternberg, S. M., Beckstrom- Sternberg, J. S., and Foster, J. T. 2013. Incongruence between MLSA and whole genome phylogenies: Pseudomonas syringae as a cautionary tale. Mol. Plant Pathol. 15:461-465.
7. Baltrus, D. A., Yourstone, S., Lind, A., Guilbaud, C., Sands, D. C., Jones, C. D., Morris, C. E., and Dangl, J. L. 2014. Draft genomes for a phylogenetically diverse suite of Pseudomonas syringae strains from multiple source populations. Genome Announce. 23:e01195-13. doi:10.1128/ genomeA.01195-13.
8. Bartoli, C., Berge, O., Monteil, C. L., Guilbaud, C., Balestra, G. M., Varvaro, L., Jones, C., Dangl, J. L., Sands, D. C., and Morris, C. E. 2014. The Pseudomonas viridiflava phylogroups in the P. syringae species complex are characterized by genetic variability and phenotypic plasticity of pathogenicity-related traits. Environ. Microbiol. doi:10.1111/1462-2920.12433. Published online.
9. Bender, C. L., Alarcón-Chaidez, F., and Gross, D. C. 1999. Pseudomonas syringae phytotoxins: Mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266-292.
10. Buetow, L., Flatau, G., Chiu, K., Boquet, P., and Ghosh, P. 2001. Structure of the Rho-Activating domain of Escherichia coli cytotoxic necrotizing factor 1. Nat. Struct. Biol. 8:584-588.
11. Chang, J. H., Urbach, J. M., Law, T. F., Arnold, L. W., Hu, A., Gombar, S., Grant, S. R., and Dangl, J. L. 2005. A high-throughput, near saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl. Acad. Sci. U.S.A. 102:2549-2554.
12. Chin, C.-S., Alexander, D. H., Marks, P., Klammer, A. A., Drake, J., Heiner, C., Clum, A., Copeland, A., Huddleston, J., Eichler, E. E., Turner, S. W., and Korlach, J. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10:563-569.
13. Chiu, J., March, P. E., Lee, R., and Tillett, D. 2004. Site-directed, Ligaseindependent mutagenesis (SLIM): A single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res. 32:e174.
14. Clarke, C. R., Cai, R., Studholme, D. J., Guttman, D. S., and Vinatzer, B. A. 2010. Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc locus are common leaf colonizers equipped with an atypical type III secretion system. Mol. Plant-Microbe Interact. 23:198-210.
15. Cui, H., Wang, Y., Xue, L., Chu, J., Yan, C., Fu, J., Chen, M., Innes, R. W., and Zhou, J.-M. 2010. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7:164-175.
16. Cunnac, S., Chakravarthy, S., Kvitko, B. H., Russell, A. B., Martin, G. B., and Collmer, A. 2011. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc. Natl. Acad. Sci. U.S.A. 108:2975-2980.
17. Feil, H., Feil, W. S., Chain, P., Larimer, F., DiBartolo, G., Copeland, A., Lykidis, A., Trong, S., Nolan, M., Goltsman, E., Thiel, J., Malfatti, S., Loper, J. E., Lapidus, A., Detter, J. C., Land, M., Richardson, P. M., Kyrpides, N. C., Ivanova, N., and Lindow, S. E. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 102:11064-11069.
18. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G., and Greenberg, J. T. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722-1726.
19. Henty-Ridilla, J. L., Shimono, M., Li, J., Chang, J. H., Day, B., and Staiger, C. J. 2013. The plant actin cytoskeleton responds to signals from microbe-Associated molecular patterns. PLoS Pathog. 9:e1003290. Published online.
20. Hirano, S., and Upper, C. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-A pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64:624.
21. Hwang, M. S. H., Morgan, R. L., Sarkar, S. F., Wang, P. W., and Guttman, D. S. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 71:5182-5191.
22. Jiang, S., Yao, J., Ma, K.-W., Zhou, H., Song, J., He, S. Y., and Ma, W. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog. 9:e1003715. Published online.
23. Kelley, L. A., and Sternberg, M. J. E. 2009. Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protocols 4:363-371.
24. Kobayashi, D. Y., Tamaki, S. J., and Keen, N. T. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. U.S.A. 86:157-161.
25. Kvitko, B. H., Park, D. H., Velásquez, A. C., Wei, C.-F., Russell, A. B., Martin, G. B., Schneider, D. J., and Collmer, A. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 5:e1000388. Published online.
26. Lee, A. H., Hurley, B., Felsensteiner, C., Yea, C., Ckurshumova, W., Bartetzko, V., Wang, P. W., Quach, V., Lewis, J. D., Liu, Y. C., Bornke, F., Angers, S., Wilde, A., Guttman, D. S., and Desveaux, D. 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLoS Pathog. 8:e1002523. Published online.
27. Lemonnier, M., Landraud, L., and Lemichez, E. 2007. Rho GTPase-Activating bacterial toxins: From bacterial virulence regulation to eukaryotic cell biology. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 31:515-534.
28. Lindeberg, M., Cunnac, S., and Collmer, A. 2012. Pseudomonas syringae type III effector repertoires: Last words in endless arguments. Trends Microbiol. 20:199-208.
29. Melotto, M., Underwood, W., Koczan, J., Nomura, K., and He, S. Y. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-980.
30. Morris, C. E., Sands, D. C., Vinatzer, B. A., Glaux, C., Guilbaud, C., Buffière, A., Yan, S., Dominguez, H., and Thompson, B. M. 2008. The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J. 2:321-334.
31. Mucha, E., Fricke, I., Schaefer, A. Wittinghofer, A., and Berken, A. 2011. Rho proteins of plants-Functional cycle and regulation of cytoskeletal dynamics. Eur. J. Cell Biol. 90:934-943.
32. Mucyn, T. S., Yourstone, S., Lind, A. L., Biswas, S., Nishimura, M. T., Baltrus, D. A., Cumbie, J. S., Chang, J. H., Jones, C. D., Dangl, J. L., and Grant, S. R. 2014. Variable suites of non-effector genes are coregulated in the type III secretion virulence regulons across the Pseudomonas syringae phylogeny. PLoS Pathog. 10:e1003807. doi:10.1371/ journal.ppat.1003807. Published online.
33. Nakamura, S., Mano, S., Tanaka, Y., Ohnishi, M., Nakamori, C., Araki, M., Niwa, T., Nishimura, M., Kaminaka, H., Nakagawa, T., Sato, Y., and Ishiguro, S. 2010. Gateway binary vectors with the bialaphos resistance gene, bar, as a selection marker for plant transformation. Biosci. Biotechnol. Biochem. 74:1315-1319.
34. O'Brien, H. E., Thakur, S., and Guttman, D. S. 2011. Evolution of plant pathogenesis in Pseudomonas syringae: A genomics perspective. Annu. Rev. Phytopathol. 49:269-289.
35. Quigley, N. B., and Gross, D. C. 1994. Syringomycin production among strains of Pseudomonas syringae pv. syringae: Conservation of the syrB and syrD genes and activation of phytotoxin production by plant signal molecules. Mol. Plant-Microbe Interact. 7:78-90.
36. Ramos, C., Matas, I. M., Bardaji, L., Aragón, I. M., and Murillo, J. 2012. Pseudomonas savastanoi pv. savastanoi: Some like it knot. Mol. Plant Pathol. 13:998-1009.
37. Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542.
38. Sarkar, S. F., and Guttman, D. S. 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl. Environ. Microbiol. 70:1999-2012.
39. Schellenberg, B., Ramel, C., and Dudler, R. 2010. Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol. Plant-Microbe Interact. 23:1287-1293.
40. Studholme, D. J. 2011. Application of high-throughput genome sequencing to intrapathovar variation in Pseudomonas syringae. Mol. Plant Pathol. 12:829-838.
41. Vinatzer, B. A., Teitzel, G. M., Lee, M.-W., Jelenska, J., Hotton, S., Fairfax, K., Jenrette, J., and Greenberg, J. T. 2006. The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Mol. Microbiol. 62:26-44.