Genomics-based exploration of virulence determinants and host-specific adaptations of pseudomonas syringae strains isolated from grasses

Pathogens

Volumn 3, Issue 1, 2014, Pages 121-148

  Dudnik, Alexey ^a   Dudler, Robert ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Genomics; Host pathogen interactions; Poaceae; Pseudomonas syringae

Indexed keywords

BACTERIOCIN; EXOPOLYSACCHARIDE; EXTRACHROMOSOMAL DNA; NONRIBOSOMAL PEPTIDE SYNTHETASE; PLANT TOXIN; POLYKETIDE SYNTHASE;

ADAPTATION; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; DEFENSE MECHANISM; GRASS; HOST PATHOGEN INTERACTION; NONHUMAN; PHYLOGENETIC TREE; PSEUDOMONAS SYRINGAE; QUORUM SENSING; TYPE VI SECRETION SYSTEM;

EID: 84906101221     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens3010121     Document Type: Article

References (141)

1. Bradbury, J.F. Pseudomonas syringae pv. syringae. In Guide to Plant Pathogenic Bacteria; CAB International Mycological Institute: Kew, England, 1986; pp. 175-177.
2. Gironde, S.; Manceau, C. Housekeeping gene sequencing and multilocus variable-number tandem-repeat analysis to identify subpopulations within Pseudomonas syringae pv. maculicola and Pseudomonas syringae pv. tomato that correlate with host specificity. Appl. Environ. Microbiol. 2012, 78, 3266-3279.
3. Martín-Sanz, A.; de la Vega, M.P.; Murillo, J.; Caminero, C. Strains of Pseudomonas syringae pv. syringae from pea are phylogenetically and pathogenically diverse. Phytopathology 2013, 103, 673-681.
4. Ramos, C.; Matas, I.M.; Bardaji, L.; Aragón, I.M.; Murillo, J. Pseudomonas savastanoi pv. savastanoi: some like it knot. Mol. Plant Pathol. 2012, 13, 998-1009.
5. Arnold, D.L.; Lovell, H.C.; Jackson, R.W.; Mansfield, J.W. Pseudomonas syringae pv. phaseolicola: from "has bean" to supermodel. Mol. Plant Pathol. 2011, 12, 617-627.
6. McCann, H.C.; Rikkerink, E.H.A.; Bertels, F.; Fiers, M.; Lu, A.; Rees-George, J.; Andersen, M.T.; Gleave, A.P.; Haubold, B.; Wohlers, M.W.; et al. Genomic Analysis of the Kiwifruit Pathogen Pseudomonas syringae pv. actinidiae Provides Insight into the Origins of an Emergent Plant Disease. PLoS Pathog. 2013, 9, e1003503.
7. Green, S.; Studholme, D.J.; Laue, B.E.; Dorati, F.; Lovell, H.; Arnold, D.; Cottrell, J.E.; Bridgett, S.; Blaxter, M.; Huitema, E. Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS One 2010, 5, e10224.
8. Qi, M.; Wang, D.; Bradley, C.A.; Zhao, Y. Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization-based comparative genomics with nine Pseudomonads. PLoS One 2011, 6, e16451.
9. Young, J.M. Taxonomy of Pseudomonas syringae. J. Plant Pathol. 2010, 92, S5-S14.
10. Sarkar, S.F.; Guttman, D.S. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl. Environ. Microbiol. 2004, 70, 1999-2012.
11. Hwang, M.S.H.; Morgan, R.L.; Sarkar, S.F.; Wang, P.W.; Guttman, D.S. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 2005, 71, 5182-5191.
12. Gardan, L.; Shafik, H.; Belouin, S.; Broch, R.; Grimont, F.; Grimont, P.A.D. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int. J. Syst. Bacteriol. 1999, 49, 469-478.
13. O'Brien, H.E.; Thakur, S.; Gong, Y.; Fung, P.; Zhang, J.; Yuan, L.; Wang, P.W.; Yong, C.; Scortichini, M.; Guttman, D.S. Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut. BMC Microbiol. 2012, 12, 141.
14. Lindeberg, M.; Cunnac, S.; Collmer, A. The evolution of Pseudomonas syringae host specificity and type III effector repertoires. Mol. Plant Pathol. 2009, 10, 767-775.
15. Rodríguez-Palenzuela, P.; Matas, I.M.; Murillo, J.; López-Solanilla, E.; Bardaji, L.; Pérez-Martínez, I.; Rodríguez-Moskera, M.E.; Penyalver, R.; López, M.M.; Quesada, J.M. Annotation and overview of the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 draft genome reveals the virulence gene complement of a tumour-inducing pathogen of woody hosts. Environ. Microbiol. 2010, 12, 1604-1620.
16. Haapalainen, M.; Mosorin, H.; Dorati, F.; Wu, R.-F.; Roine, E.; Taira, S.; Nissinen, R.; Mattinen, L.; Jackson, R.; Pirhonen, M. Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J. Bacteriol. 2012, 194, 4810-4822.
17. Lindeberg, M.; Cunnac, S.; Collmer, A. Pseudomonas syringae type III effector repertoires: Last words in endless arguments. Trends Microbiol. 2012, 20, 199-208.
18. Schellenberg, B.; Ramel, C.; Dudler, R. Pseudomonas syringae Virulence Factor Syringolin A Counteracts Stomatal Immunity by Proteasome Inhibition. Mol. Plant-Microbe Interact. 2010, 23, 1287-1293.
19. Bender, C.L.; Alarcón-Chaidez, F.; Gross, D.C. Pseudomonas syringae phytotoxins: Mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. MMBR 1999, 63, 266-292.
20. Denny, T.P. Involvement of bacterial polysaccharides in plant pathogenesis. Annu. Rev. Phytopathol. 1995, 33, 173-197.
21. Misas-Villamil, J.C.; Kolodziejek, I.; Crabill, E.; Kaschani, F.; Niessen, S.; Shindo, T.; Kaiser, M.; Alfano, J.R.; van der Hoorn, R.A.L. Pseudomonas syringae pv. syringae uses proteasome inhibitor syringolin A to colonize from wound infection sites. PLoS Pathog. 2013, 9, e1003281.
22. Yu, J.; Penaloza-Vazquez, A.; Chakrabarty, A.M.; Bender, C.L. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol. Microbiol. 1999, 33, 712-720.
23. Rodríguez-Moreno, L.; Barceló-Muñoz, A.; Ramos, C. In vitro analysis of the interaction of Pseudomonas savastanoi pvs. savastanoi and nerii with micropropagated olive plants. Phytopathology 2008, 98, 815-822.
24. Arrebola, E.; Cazorla, F.M.; Perez-García, A.; de Vicente, A. Chemical and metabolic aspects of antimetabolite toxins produced by Pseudomonas syringae pathovars. Toxins (Basel). 2011, 3, 1089-1110.
25. Galán, J.E.; Wolf-Watz, H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 2006, 444, 567-573.
26. Büttner, D. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol. Mol. Biol. Rev. 2012, 76, 262-310.
27. Jones, J.D.G.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323-329.
28. Cunnac, S.; Lindeberg, M.; Collmer, A. Pseudomonas syringae type III secretion system effectors: Repertoires in search of functions. Curr. Opin. Microbiol. 2009, 12, 53-60.
29. Munkvold, K.R.; Martin, M.E.; Bronstein, P.A.; Collmer, A. A survey of the Pseudomonas syringae pv. tomato DC3000 type III secretion system effector repertoire reveals several effectors that are deleterious when expressed in Saccharomyces cerevisiae. Mol. Plant-Microbe Interact. 2008, 21, 490-502.
30. Salomon, D.; Bosis, E.; Dar, D.; Nachman, I.; Sessa, G. Expression of Pseudomonas syringae type III effectors in yeast under stress conditions reveals that HopX1 attenuates activation of the high osmolarity glycerol MAP kinase pathway. Microbiology 2012, 158, 2859-2869.
31. Baltrus, D.A.; Nishimura, M.T.; Romanchuk, A.; Chang, J.H.; Mukhtar, M.S.; Cherkis, K.; Roach, J.; Grant, S.R.; Jones, C.D.; et al. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog. 2011, 7, e1002132.
32. Göhre, V.; Spallek, T.; Häweker, H.; Mersmann, S.; Mentzel, T.; Boller, T.; de Torres, M.; Mansfield, J.W.; Robatzek, S. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 2008, 18, 1824-1832.
33. Nicaise, V.; Joe, A.; Jeong, B.-R.; Korneli, C.; Boutrot, F.; Westedt, I.; Staiger, D.; Alfano, J.R.; Zipfel, C. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 2013, 32, 701-712.
34. Rodríguez-Herva, J.J.; González-Melendi, P.; Cuartas-Lanza, R.; Antúnez-Lamas, M.; Río-Alvarez, I.; Li, Z.; López-Torrejón, G.; Díaz, I.; del Pozo, J.C.; Chakravarthy, S.;. A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses. Cell. Microbiol. 2012, 14, 669-681.
35. Bhattacharjee, S.; Halane, M.K.; Kim, S.H.; Gassmann, W. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 2011, 334, 1405-1408.
36. Lee, A.H.-Y.; Hurley, B.; Felsensteiner, C.; Yea, C.; Ckurshumova, W.; Bartetzko, V.; Wang, P.W.; Quach, V.; Lewis, J.D.; Liu, Y.C.; et al. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLoS Pathog. 2012, 8, e1002523.
37. Jiang, S.; Yao, J.; Ma, K.-W.; Zhou, H.; Song, J.; He, S.Y.; Ma, W. Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors. PLoS Pathog. 2013, 9, e1003715.
38. Cunnac, S.; Chakravarthy, S.; Kvitko, B.H.; Russell, A.B.; Martin, G.B.; Collmer, A. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc. Natl. Acad. Sci. USA 2011, 108, 2975-2980.
39. Almeida, N.F.; Yan, S.; Lindeberg, M.; Studholme, D.J.; Schneider, D.J.; Condon, B.; Liu, H.; Viana, C.J.; Warren, A.; Evans, C.;. A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Mol. Plant Microbe. Interact. 2009, 22, 52-62.
40. 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. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 2003, 100, 10181-10186.
41. Wei, C.-F.; Kvitko, B.H.; Shimizu, R.; Crabill, E.; Alfano, J.R.; Lin, N.-C.; Martin, G.B.; Huang, H.-C.; Collmer, A. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J. 2007, 51, 32-46.
42. Feil, H.; Feil, W.S.; Chain, P.; Larimer, F.; DiBartolo, G.; Copeland, A.; Lykidis, A.; Trong, S.; Nolan, M.; Goltsman, E. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 2005, 102, 11064-11069.
43. Joardar, V.; Lindeberg, M.; Jackson, R.W.; Selengut, J.; Dodson, R.; Brinkac, L.M.; Daugherty, S.C.; Deboy, R.; Durkin, A.S.; Giglio, M.G.; Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 2005, 187, 6488-6498.
44. Dudnik, A.; Dudler, R. High-Quality Draft Genome Sequence of Pseudomonas syringae pv. Syringae Strain SM, Isolated from Wheat. Genome Announc. 2013, 1, e00610-e00613.
45. Dudnik, A.; Dudler, R. Non contiguous-finished genome sequence of Pseudomonas syringae pathovar syringae strain B64 isolated from wheat. Stand. Genomic Sci. 2013, 8, 420-429.
46. Gardiner, D.M.; Stiller, J.; Covarelli, L.; Lindeberg, M.; Shivas, R.G.; Manners, J.M. Genome Sequences of Pseudomonas spp. Isolated from Cereal Crops. Genome Announc. 2013, 1, e00209-e00213.
47. Reinhardt, J.A.; Baltrus, D.A.; Nishimura, M.T.; Jeck, W.R.; Jones, C.D.; Dangl, J.L. De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Res. 2009, 19, 294-305.
48. Liu, H.; Qiu, H.; Zhao, W.; Cui, Z.; Ibrahim, M.; Jin, G.; Li, B.; Zhu, B.; Xie, G.L. Genome sequence of the plant pathogen Pseudomonas syringae pv. panici LMG 2367. J. Bacteriol. 2012, 194, 5693-5694.
49. Sarris, P.F.; Trantas, E.A.; Baltrus, D.A.; Bull, C.T.; Wechter, W.P.; Yan, S.; Ververidis, F.; Almeida, N.F.; Jones, C.D.; Dangl, J.L. Comparative genomics of multiple strains of Pseudomonas cannabina pv. alisalensis, a potential model pathogen of both monocots and dicots. PLoS One 2013, 8, e59366.
50. Baltrus, D.A.; Dougherty, K.; Beckstrom-Sternberg, S.M.; Beckstrom-Sternberg, J.S.; Foster, J.T. Incongruence between multi-locus sequence analysis (MLSA) and whole-genome-based phylogenies: Pseudomonas syringae pathovar pisi as a cautionary tale. Mol. Plant Pathol. 2014, doi: 10.1111/mpp.12103.
51. Elasri, M.; Delorme, S.; Lemanceau, P.; Stewart, G.; Laue, B.; Glickmann, E.; Oger, P.M.; Dessaux, Y. Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp. Appl. Environ. Microbiol. 2001, 67, 1198-1209.
52. Marcelletti, S.; Ferrante, P.; Petriccione, M.; Firrao, G.; Scortichini, M. Pseudomonas syringae pv. actinidiae draft genomes comparison reveal strain-specific features involved in adaptation and virulence to Actinidia species. PLoS One 2011, 6, e27297.
53. Deng, W.-L.; Preston, G.; Collmer, A.; Chang, C.-J.; Huang, H.-C. Characterization of the hrpC and hrpRS operons of Pseudomonas syringae pathovars syringae, tomato, and glycinea and analysis of the ability of hrpF, hrpG, hrcC, hrpT, and hrpV mutants to elicit the hypersensitive response and disease in plants. J. Bacteriol. 1998, 180, 4523-4531.
54. Sarkar, S.F.; Gordon, J.S.; Martin, G.B.; Guttman, D.S. Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 2006, 174, 1041-1056.
55. Cintas, N.A.; Koike, S.T.; Bull, C.T. A New pathovar, Pseudomonas syringae pv. alisalensis pv. nov., proposed for the causal agent of bacterial blight of broccoli and broccoli raab. Plant Dis. 2002, 86, 992-998.
56. Ishiyama, Y.; Yamagishi, N.; Ogiso, H.; Fujinaga, M.; Takikawa, Y. Bacterial brown spot on Avena storigosa Schereb. caused by Pseudomonas syringae pv. alisalensis. J. Gen. Plant Pathol. 2013, 79, 155-157.
57. Gazi, A.D.; Sarris, P.F.; Fadouloglou, V.E.; Charova, S.N.; Mathioudakis, N.; Panopoulos, N.J.; Kokkinidis, M. Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains. BMC Microbiol. 2012, 12, 188.
58. Wang, Y.; Huang, H.; Sun, M.; Zhang, Q.; Guo, D. T3DB: An integrated database for bacterial type III secretion system. BMC Bioinform. 2012, 13, 66.
59. Cai, R.; Lewis, J.; Yan, S.; Liu, H.; Clarke, C.R.; Campanile, F.; Almeida, N.F.; Studholme, D.J.; Lindeberg, M.; Schneider, D.;. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog. 2011, 7, e1002130.
60. Murillo, J.; Bardaji, L.; Navarro de la Fuente, L.; Führer, M.E.; Aguilera, S.; Álvarez-Morales, A. Variation in conservation of the cluster for biosynthesis of the phytotoxin phaseolotoxin in Pseudomonas syringae suggests at least two events of horizontal acquisition. Res. Microbiol. 2011, 162, 253-261.
61. Arrebola, E.; Cazorla, F.M.; Codina, J.C.; Gutiérrez-Barranquero, J.A.; Pérez-García, A.; de Vicente, A. Contribution of mangotoxin to the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Int. Microbiol. 2009, 12, 87-95.
62. Groll, M.; Schellenberg, B.; Bachmann, A.S.; Archer, C.R.; Huber, R.; Powell, T.K.; Lindow, S.; Kaiser, M.; Dudler, R. A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature 2008, 452, 755-758.
63. Carrión, V.J.; Gutiérrez-Barranquero, J.A.; Arrebola, E.; Bardaji, L.; Codina, J.C.; de Vicente, A.; Cazorla, F.M.; Murillo, J. The mangotoxin biosynthetic operon (mbo) is specifically distributed within Pseudomonas syringae genomospecies 1 and was acquired only once during evolution. Appl. Environ. Microbiol. 2013, 79, 756-767.
64. Costacurta, A.; Vanderleyden, J. Synthesis of Phytohormones by Plant-Associated Bacteria. Crit. Rev. Microbiol. 2008, 21, 1-18.
65. Akiyoshi, D.E.; Regier, D.A.; Gordon, M.P. Cytokinin production by Agrobacterium and Pseudomonas spp. J. Bacteriol. 1987, 169, 4242-4248.
66. Weingart, H.; Völksch, B.; Ullrich, M.S. Comparison of Ethylene Production by Pseudomonas syringae and Ralstonia solanacearum. Phytopathology 1999, 89, 360-365.
67. Glickmann, E.; Gardan, L.; Jacquet, S.; Hussain, S.; Elasri, M.; Petit, A.; Dessaux, Y. Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol. Plant. Microbe. Interact. 1998, 11, 156-162.
68. Roberto, F.F.; Klee, H.; White, F.; Nordeen, R.; Kosuge, T. Expression and fine structure of the gene encoding N epsilon-(indole-3-acetyl)-L-lysine synthetase from Pseudomonas savastanoi. Proc. Natl. Acad. Sci. USA 1990, 87, 5797-5801.
69. Miller, M.B.; Bassler, B.L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 2001, 55, 165-199.
70. Nealson, K.H. Autoinduction of bacterial luciferase. Arch. Microbiol. 1977, 112, 73-79.
71. Von Bodman, S.B.; Bauer, W.D.; Coplin, D.L. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 2003, 41, 455-482.
72. Dumenyo, C.K.; Mukherjee, A.; Chun, W.; Chatterjee, A.K. Genetic and physiological evidence for the production of N-acyl homoserine lactones by Pseudomonas syringae pv. syringae and other fluorescent plant pathogenic Pseudomonas species. Eur. J. Plant Pathol. 1998, 104, 569-582.
73. BCCM/LMG bacteria catalogue-Strain details LMG2367. Available online: http://bccm.belspo.be/db/lmg_strain_details.php?NUM=2367 (accessed on 7 November 2013).
74. Venturi, V.; Fuqua, C. Chemical signaling between plants and plant-pathogenic bacteria. Annu. Rev. Phytopathol. 2013, 51, 17-37.
75. Schikora, A.; Schenk, S.T.; Stein, E.; Molitor, A.; Zuccaro, A.; Kogel, K.-H. N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol. 2011, 157, 1407-1418.
76. Brencic, A.; Winans, S.C. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 2005, 69, 155-194.
77. Subramoni, S.; Venturi, V. LuxR-family "solos": Bachelor sensors/regulators of signalling molecules. Microbiology 2009, 155, 1377-1385.
78. Subramoni, S.; Gonzalez, J.F.; Johnson, A.; Péchy-Tarr, M.; Rochat, L.; Paulsen, I.; Loper, J.E.; Keel, C.; Venturi, V. Bacterial subfamily of LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 2011, 77, 4579-4588.
79. Ferluga, S.; Venturi, V. OryR is a LuxR-family protein involved in interkingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice. J. Bacteriol. 2009, 191, 890-897.
80. González, J.F.; Myers, M.P.; Venturi, V. The inter-kingdom solo OryR regulator of Xanthomonas oryzae is important for motility. Mol. Plant Pathol. 2013, 14, 211-221.
81. Lu, S.-E.; Scholz-Schroeder, B.K.; Gross, D.C. Characterization of the salA, syrF, and syrG regulatory genes located at the right border of the syringomycin gene cluster of pseudomonas syringae pv. syringae. Mol. Plant-Microbe Interact. 2002, 15, 43-53.
82. Mo, Y.Y.; Gross, D.C. Plant signal molecules activate the syrB gene, which is required for syringomycin production by Pseudomonas syringae pv. syringae. J. Bacteriol. 1991, 173, 5784-5792.
83. Deisinger, P.J.; Hill, T.S.; English, J.C. Human exposure to naturally occurring hydroquinone. J. Toxicol. Environ. Health 1996, 47, 31-46.
84. Zakataeva, N.P.; Kutukova, E.A.; Gronskiy, S.V.; Troshin, P.V.; Livshits, V.A.; Aleshin, V.V. Export of metabolites by the proteins of the DMT and RhtB families and its possible role in intercellular communication. Microbiology 2006, 75, 438-448.
85. Degrassi, G.; Devescovi, G.; Solis, R.; Steindler, L.; Venturi, V. Oryza sativa rice plants contain molecules that activate different quorum-sensing N-acyl homoserine lactone biosensors and are sensitive to the specific AiiA lactonase. FEMS Microbiol. Lett. 2007, 269, 213-220.
86. Gao, M.; Teplitski, M.; Robinson, J.B.; Bauer, W.D. Production of Substances by Medicago truncatula that Affect Bacterial Quorum Sensing. Mol. Plant-Microbe Interact. 2003, 16, 827-834.
87. Osman, S.F.; Fett, W.F.; Fishman, M.L. Exopolysaccharides of the phytopathogen Pseudomonas syringae pv. glycinea. J. Bacteriol. 1986, 166, 66-71.
88. Franklin, M.J.; Nivens, D.E.; Weadge, J.T.; Howell, P.L. Biosynthesis of the Pseudomonas aeruginosa Extracellular Polysaccharides, Alginate, Pel, and Psl. Front. Microbiol. 2011, 2, 167.
89. Li, H.; Ullrich, M.S. Characterization and mutational analysis of three allelic lsc genes encoding levansucrase in Pseudomonas syringae. J. Bacteriol. 2001, 183, 3282-3292.
90. Penaloza-Vazquez, A.; Kidambi, S.; Chakrabarty, A.; Bender, C. Characterization of the alginate biosynthetic gene cluster in Pseudomonas syringae pv. syringae. J. Bacteriol. 1997, 179, 4464-4472.
91. Laue, H.; Schenk, A.; Li, H.; Lambertsen, L.; Neu, T.R.; Molin, S.; Ullrich, M.S. Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 2006, 152, 2909-2918.
92. Byrd, M.S.; Sadovskaya, I.; Vinogradov, E.; Lu, H.; Sprinkle, A.B.; Richardson, S.H.; Ma, L.; Ralston, B.; Parsek, M.R.; Anderson, E.M. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol. Microbiol. 2009, 73, 622-638.
93. Jackson, K.D.; Starkey, M.; Kremer, S.; Parsek, M.R.; Wozniak, D.J. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol. 2004, 186, 4466-4475.
94. Hockett, K.L.; Burch, A.Y.; Lindow, S.E. Thermo-regulation of genes mediating motility and plant interactions in Pseudomonas syringae. PLoS One 2013, 8, e59850.
95. Shrivastava, S.; Mande, S.S. Identification and functional characterization of gene components of Type VI Secretion system in bacterial genomes. PLoS One 2008, 3, e2955.
96. Kapitein, N.; Mogk, A. Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition. Curr. Opin. Microbiol. 2013, 16, 52-58.
97. Barret, M.; Egan, F.; Fargier, E.; Morrissey, J.P.; O'Gara, F. Genomic analysis of the type VI secretion systems in Pseudomonas spp.: Novel clusters and putative effectors uncovered. Microbiology 2011, 157, 1726-1739.
98. Hachani, A.; Lossi, N.S.; Hamilton, A.; Jones, C.; Bleves, S.; Albesa-Jové, D.; Filloux, A. Type VI secretion system in Pseudomonas aeruginosa: Secretion and multimerization of VgrG proteins. J. Biol. Chem. 2011, 286, 12317-12327.
99. Burtnick, M.N.; Brett, P.J.; Harding, S.V.; Ngugi, S.A.; Ribot, W.J.; Chantratita, N.; Scorpio, A.; Milne, T.S.; Dean, R.E.; Fritz, D.L.; The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect. Immun. 2011, 79, 1512-1525.
100. Sarris, P.F.; Skandalis, N.; Kokkinidis, M.; Panopoulos, N.J. In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. Mol. Plant Pathol. 2010, 11, 795-804.
101. Sarris, P.F.; Trantas, E.A.; Skandalis, N.; Tampakaki, A.P.; Kapanidou, M.; Kokkinidis, M.; Panopoulos, N.J. Phytobacterial type VI secretion system-Gene distribution, phylogeny, structure and biological functions. In InTech Plant Pathology; Cumagun, C.J.R., Ed.; InTech: Rijeca, Croatia, 2012; pp. 53-84.
102. Pukatzki, S.; Ma, A.T.; Revel, A.T.; Sturtevant, D.; Mekalanos, J.J. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. USA 2007, 104, 15508-15513.
103. Russell, A.B.; LeRoux, M.; Hathazi, K.; Agnello, D.M.; Ishikawa, T.; Wiggins, P.A.; Wai, S.N.; Mougous, J.D. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 2013, 496, 508-512.
104. Hood, R.D.; Singh, P.; Hsu, F.; Güvener, T.; Carl, M.A.; Trinidad, R.R.S.; Silverman, J.M.; Ohlson, B.B.; Hicks, K.G.; Plemel, R.L. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010, 7, 25-37.
105. Lindeberg, M.; Myers, C.R.; Collmer, A.; Schneider, D.J. Roadmap to new virulence determinants in Pseudomonas syringae: Insights from comparative genomics and genome organization. Mol. Plant. Microbe. Interact. 2008, 21, 685-700.
106. Greenberg, J.T.; Vinatzer, B.A. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 2003, 6, 20-28.
107. Swingle, B.; Bao, Z.; Markel, E.; Chambers, A.; Cartinhour, S. Recombineering using RecTE from Pseudomonas syringae. Appl. Environ. Microbiol. 2010, 76, 4960-4968.
108. Juhas, M.; van der Meer, J.R.; Gaillard, M.; Harding, R.M.; Hood, D.W.; Crook, D.W. Genomic islands: Tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol. Rev. 2009, 33, 376-393.
109. Gaillard, M.; Vallaeys, T.; Vorhölter, F.J.; Minoia, M.; Werlen, C.; Sentchilo, V.; Pühler, A.; van der Meer, J.R. The clc element of Pseudomonas sp. strain B13, a genomic island with various catabolic properties. J. Bacteriol. 2006, 188, 1999-2013.
110. Wozniak, R.A.F.; Waldor, M.K. Integrative and conjugative elements: Mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol. 2010, 8, 552-563.
111. Rodríguez-Blanco, A.; Lemos, M.L.; Osorio, C.R. Integrating conjugative elements as vectors of antibiotic, mercury, and quaternary ammonium compound resistance in marine aquaculture environments. Antimicrob. Agents Chemother. 2012, 56, 2619-2626.
112. Pitman, A.R.; Jackson, R.W.; Mansfield, J.W.; Kaitell, V.; Thwaites, R.; Arnold, D.L. Exposure to host resistance mechanisms drives evolution of bacterial virulence in plants. Curr. Biol. 2005, 15, 2230-2235.
113. Zhao, Y.; Ma, Z.; Sundin, G.W. Comparative genomic analysis of the pPT23A plasmid family of Pseudomonas syringae. J. Bacteriol. 2005, 187, 2113-2126.
114. Bender, C.; Palmer, D.; Peñaloza-Vázquez, A.; Rangaswamy, V.; Ullrich, M. Biosynthesis of coronatine, a thermoregulated phytotoxin produced by the phytopathogen Pseudomonas syringae. Arch. Microbiol. 1996, 166, 71-75.
115. Pérez-Martínez, I.; Zhao, Y.; Murillo, J.; Sundin, G.W.; Ramos, C. Global genomic analysis of Pseudomonas savastanoi pv. savastanoi plasmids. J. Bacteriol. 2008, 190, 625-635.
116. Juhas, M.; Crook, D.W.; Hood, D.W. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol. 2008, 10, 2377-2386.
117. Makarova, K.S.; Wolf, Y.I.; Koonin, E.V. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res. 2013, 41, 4360-4377.
118. Toussaint, A.; Prangishvili, D.; Molineux, I.; Fineran, P.C.; Charpentier, E. Memory of viral infections by CRISPR-Cas adaptive immune systems: Acquisition of new information. Virology 2012, 434, 202-209.
119. Haft, D.H.; Selengut, J.; Mongodin, E.F.; Nelson, K.E. A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol. 2005, 1, e60.
120. Makarova, K.S.; Wolf, Y.I.; van der Oost, J.; Koonin, E. V Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 2009, 4, 29.
121. Cotter, P.D.; Ross, R.P.; Hill, C. Bacteriocins-A viable alternative to antibiotics? Nat. Rev. Microbiol. 2013, 11, 95-105.
122. Hassan, M.; Kjos, M.; Nes, I.F.; Diep, D.B.; Lotfipour, F. Natural antimicrobial peptides from bacteria: Characteristics and potential applications to fight against antibiotic resistance. J. Appl. Microbiol. 2012, 113, 723-736.
123. Grinter, R.; Roszak, A.W.; Cogdell, R.J.; Milner, J.J.; Walker, D. The crystal structure of the lipid II-degrading bacteriocin syringacin M suggests unexpected evolutionary relationships between colicin M-like bacteriocins. J. Biol. Chem. 2012, 287, 38876-38888.
124. Nikolouli, K.; Mossialos, D. Bioactive compounds synthesized by non-ribosomal peptide synthetases and type-I polyketide synthases discovered through genome-mining and metagenomics. Biotechnol. Lett. 2012, 34, 1393-1403.
125. Ramel, C.; Tobler, M.; Meyer, M.; Bigler, L.; Ebert, M.-O.; Schellenberg, B.; Dudler, R. Biosynthesis of the proteasome inhibitor syringolin A: The ureido group joining two amino acids originates from bicarbonate. BMC Biochem. 2009, 10, 26.
126. Arrebola, E.; Carrión, V.J.; Cazorla, F.M.; Pérez-García, A.; Murillo, J.; de Vicente, A. Characterisation of the mgo operon in Pseudomonas syringae pv. syringae UMAF0158 that is required for mangotoxin production. BMC Microbiol. 2012, 12, 10.
127. Yu, X.; Lund, S.P.; Scott, R.A.; Greenwald, J.W.; Records, A.H.; Nettleton, D.; Lindow, S.E.; Gross, D.C.; Beattie, G.A. Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites. Proc. Natl. Acad. Sci. USA 2013, 110, E425-E434.
128. NCBI FTP Server. Available online: ftp://ftp.ncbi.nlm.nih.gov/genomes/ (accessed on 4 September 2013).
129. Aziz, R.K.; Bartels, D.; Best, A.A.; DeJongh, M.; Disz, T.; Edwards, R.A.; Formsma, K.; Gerdes, S.; Glass, E.M.; Kubal, M. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9, 75.
130. Seemann, T. Prokka: Prokaryotic Genome Annotation System. Available online: http://vicbioinformatics.com/ (Accessed on 10 September 2013).
131. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731-2739.
132. Zhao, Y.; Wu, J.; Yang, J.; Sun, S.; Xiao, J.; Yu, J. PGAP: Pan-genomes analysis pipeline. Bioinformatics 2012, 28, 416-418.
133. Carver, T.; Harris, S.R.; Berriman, M.; Parkhill, J.; McQuillan, J.A. Artemis: An integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 2012, 28, 464-469.
134. Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403-410.
135. Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T.L. BLAST+: Architecture and applications. BMC Bioinform. 2009, 10, 421.
136. Pseudomonas syringae Genome Resources Home Page. Available online: http://www.pseudomonas-syringae.org/ (accessed on 20 January 2014).
137. 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. Variable suites of non-effector genes are co-regulated in the type III secretion virulence regulon across the Pseudomonas syringae phylogeny. PLoS Pathog. 2014, 10, e1003807.
138. Markowitz, V.M.; Mavromatis, K.; Ivanova, N.N.; Chen, I.-M.A.; Chu, K.; Kyrpides, N.C. IMG ER: A system for microbial genome annotation expert review and curation. Bioinformatics 2009, 25, 2271-2278.
139. Marchler-Bauer, A.; Lu, S.; Anderson, J.B.; Chitsaz, F.; Derbyshire, M.K.; DeWeese-Scott, C.; Fong, J.H.; Geer, L.Y.; Geer, R.C.; Gonzales, N.R. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 2011, 39, D225-D229.
140. De Jong, A.; van Heel, A.J.; Kok, J.; Kuipers, O.P. BAGEL2: Mining for bacteriocins in genomic data. Nucleic Acids Res. 2010, 38, W647-W651.
141. Grissa, I.; Vergnaud, G.; Pourcel, C. CRISPRFinder: A web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007, 35, W52-W57.