Identification of novel virulence genes and metabolic pathways required for full fitness of Pseudomonas savastanoi pv. savastanoi in olive (Olea europaea) knots

New Phytologist

Volumn 196, Issue 4, 2012, Pages 1182-1196

  Matas, Isabel M ^a   Lambertsen, Lotte ^a   Rodríguez Moreno, Luis ^a   Ramos, Cayo ^a  

^a INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

Author keywords

Fitness; Metabolic pathway; Olive knot; Pseudomonas savastanoi; Pseudomonas syringae; Signature tagged mutagenesis; Virulence; Woody plant

Indexed keywords

BACTERIAL DISEASE; COLONIZATION; COMPARATIVE STUDY; FITNESS; GENOMICS; HERB; METABOLISM; MUTAGENICITY; PATHOGENICITY; SURVIVAL; SYMPTOM; VIRULENCE; WOODY PLANT;

ARTICLE; COMPUTER SIMULATION; CYTOLOGY; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MUTAGENESIS; MUTATION; OLIVE TREE; PATHOGENICITY; PLANT DISEASE; PSEUDOMONAS; VIRULENCE;

COMPUTER SIMULATION; HOST-PATHOGEN INTERACTIONS; METABOLIC NETWORKS AND PATHWAYS; MUTAGENESIS; MUTATION; OLEA; PLANT DISEASES; PSEUDOMONAS; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); OLEA EUROPAEA; PSEUDOMONAS; PSEUDOMONAS SAVASTANOI; PSEUDOMONAS SYRINGAE;

EID: 84868581223     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04357.x     Document Type: Article

References (76)

1. Agrios GN. 2005. Plant pathology. San Diego, CA, USA: Elsevier Academic Press.
2. Alfano JR, Collmer A. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8: 1683-1698.
3. Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, Condon B, Liu HJ, Viana CJ, Warren A, Evans C et al. 2009. 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. Molecular Plant-Microbe Interactions 22: 52-62.
4. Álvarez-Martínez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiology and Molecular Biology Reviews 73: 775-808.
5. Antonoaea R, Furst M, Nishiyama K, Muller M. 2008. The periplasmic chaperone PpiD interacts with secretory proteins exiting from the SecYEG translocon. Biochemistry 47: 5649-5656.
6. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55: 373-399.
7. Autret N, Charbit A. 2005. Lessons from signature-tagged mutagenesis on the infectious mechanisms of pathogenic bacteria. FEMS Microbiology Reviews 29: 703-717.
8. Backert S, Clyne M. 2011. Pathogenesis of Helicobacter pylori infection. Helicobacter 16: 19-25.
9. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, Cherkis K, Roach J, Grant SR, Jones CD, Dangl JL. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathogens 7: e1002132.
10. Bardaji L, Pérez-Martínez I, Rodríguez-Moreno L, Rodríguez-Palenzuela P, Sundin GW, Ramos C, Murillo J. 2011. Sequence and role in virulence of the three plasmid complement of the model tumor-inducing bacterium Pseudomonas savastanoi pv. savastanoi NCPPB 3335. PLoS ONE 6: e25705.
11. Bianconi I, Milani A, Cigana C, Paroni M, Levesque RC, Bertoni G, Bragonzi A. 2011. Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting airways chronic infection. PLoS Pathogens 7: e1001270.
12. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proceedings of the National Academy of Sciences, USA 100: 10181-10186.
13. Bullock WO, Fernandez JM, Short JM. 1987. Xl1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. BioTechniques 5: 376-378.
14. Cai R, Lewis J, Yan S, Liu H, Clarke CR, Campanile F, Almeida NF, Studholme DJ, Lindeberg M, Schneider D et al. 2011. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathogens 7: e1002130.
15. Cayuela JA, Rada M, Rios JJ, Albi T, Guinda A. 2006. Changes in phenolic composition induced by Pseudomonas savastanoi pv. savastanoi infection in olive tree: presence of large amounts of verbascoside in nodules of tuberculosis disease. Journal of Agriculture and Food Chemistry 54: 5363-5368.
16. Chen L, Li CM, Nester EW. 2000. Transferred DNA (T-DNA)-associated proteins of Agrobacterium tumefaciens are exported independently of virB. Proceedings of the National Academy of Sciences, USA 97: 7545-7550.
17. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annual Review of Microbiology 59: 451-485.
18. Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA. 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. Molecular Plant-Microbe Interactions 23: 198-210.
19. Cotter PA, Stibitz S. 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Current Opinion in Microbiology 10: 17-23.
20. Cunnac S, Lindeberg M, Collmer A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Current Opinion in Microbiology 12: 53-60.
21. Dam P, Olman V, Harris K, Su Z, Xu Y. 2007. Operon prediction using both genome-specific and general genomic information. Nucleic Acids Research 35: 288-298.
22. Ezraty B, Bos J, Barras F, Aussel L. 2005. Methionine sulfoxide reduction and assimilation in Escherichia coli: new role for the biotin sulfoxide reductase BisC. Journal of Bacteriology 187: 231-237.
23. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, Copeland A, Lykidis A, Trong S, Nolan M, Goltsman E et al. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proceedings of the National Academy of Sciences, USA 102: 11064-11069.
24. Frangipani E, Slaveykova VI, Reimmann C, Haas D. 2008. Adaptation of aerobically growing Pseudomonas aeruginosa to copper starvation. Journal of Bacteriology 190: 6706-6717.
25. García-Olmedo F, Rodríguez-Palenzuela P, Molina A, Alamillo JM, López-Solanilla E, Berrocal-Lobo M, Poza-Carrión C. 2001. Antibiotic activities of peptides, hydrogen peroxide and peroxynitrite in plant defence. FEBS Letters 498: 219-222.
26. Gardan L, Shafik H, Belouin S, Broch R, Grimont F, Grimont PAD. 1999. 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). International Journal of Systematic Bacteriology 49: 469-478.
27. Glass NL, Kosuge T. 1988. Role of indoleacetic acid-lysine synthetase in regulation of indoleacetic acid pool size and virulence of Pseudomonas syringae subsp. savastanoi. Journal of Bacteriology 170: 2367-2373.
28. Green S, Studholme DJ, Laue BE, Dorati F, Lovell H, Arnold D, Cottrell JE, Bridgett S, Blaxter M, Huitema E et al. 2010. Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS ONE 5: e10224.
29. Hagelueken G, Wiehlmann L, Adams TM, Kolmar H, Heinz DW, Tummler B, Schubert WD. 2007. Crystal structure of the electron transfer complex rubredoxin rubredoxin reductase of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, USA 104: 12276-12281.
30. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. Journal of Molecular Biology 166: 557-580.
31. Hensel M, Shea J, Gleeson C, Jones M, Dalton E, Holden D. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
32. Herrero M, de Lorenzo V, Timmis KN. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. Journal of Bacteriology 172: 6557-6567.
33. Hirano SS, Upper CD. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiology and Molecular Biology Reviews 64: 624-653.
34. Holden DW, Hensel M. 1998. Signature tagged mutagenesis. Methods in Microbiology 27: 359-370.
35. Hosni T, Moretti C, Devescovi G, Suárez-Moreno ZR, Fatmi MB, Guarnaccia C, Pongor S, Onofri A, Buonaurio R, Venturi V. 2011. Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME Journal 5: 1857-1870.
36. Iacobellis NS. 2001. Olive knot. In: Maloy OC, Murray TD, eds. Encyclopedia of plant pathology. New York, NY, USA: John Wiley & Sons, 714-715.
37. Iacobellis NS, Sisto A, Surico G, Evidente A, DiMaio E. 1994. Pathogenicity of Pseudomonas syringae subsp. savastanoi mutants defective in phytohormone production. Journal of Phytopathology 140: 238-248.
38. Jackson RW, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, Arnold DL, Gibbon MJ, Murillo J, Taylor JD, Vivian A. 1999. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proceedings of the National Academy of Sciences, USA 96: 10875-10880.
39. Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, Brinkac LM, Daugherty SC, DeBoy R, Durkin AS, Giglio MG et al. 2005. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. Journal of Bacteriology 187: 6488-6498.
40. de Jong MF, Tsolis RM. 2011. Brucellosis and type IV secretion. Future Microbiology 7: 47-58.
41. Kimbrough TG, Miller SI. 2002. Assembly of the type III secretion needle complex of Salmonella typhimurium. Microbes and Infection 4: 75-82.
42. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. Journal of Laboratory and Clinical Medicine 44: 301-307.
43. Laue H, Schenk A, Li H, Lambertsen L, Neu TR, Molin S, Ullrich MS. 2006. Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 152(Pt 10): 2909-2918.
44. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, Monack DM. 2006. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathogens 2: e11.
45. Lindeberg M, Myers CR, Collmer A, Schneider DJ. 2008. Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Molecular Plant-Microbe Interactions 21: 685-700.
46. Macho AP, Zumaquero A, Ortíz-Martín I, Beuzón CR. 2007. Competitive index in mixed infections: a sensitive and accurate assay for the genetic analysis of Pseudomonas syringae-plant interactions. Molecular Plant Pathology 8: 437-450.
47. Mansfield JW. 2009. From bacterial avirulence genes to effector functions via the hrp delivery system: an overview of 25 years of progress in our understanding of plant innate immunity. Molecular Plant Pathology 10: 721-734.
48. Mecsas J. 2002. Use of signature-tagged mutagenesis in pathogenesis studies. Current Opinion in Microbiology 5: 33-37.
49. Meyer JM, Abdallah MA. 1978. The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Journal of General Microbiology 107: 319-328.
50. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory.
51. Parvatiyar K, Alsabbagh EM, Ochsner UA, Stegemeyer MA, Smulian AG, Hwang SH, Jackson CR, McDermott TR, Hassett DJ. 2005. Global analysis of cellular factors and responses involved in Pseudomonas aeruginosa resistance to arsenite. Journal of Bacteriology 187: 4853-4864.
52. Patel PC, Goulhen F, Boothman C, Gault AG, Charnock JM, Kalia K, Lloyd JR. 2007. Arsenate detoxification in a Pseudomonad hypertolerant to arsenic. Archives of Microbiology 187: 171-183.
53. Penyalver R, García A, Ferrer A, Bertolini E, Quesada JM, Salcedo CI, Piquer J, Pérez-Panades J, Carbonell EA, Del Rio C et al. 2006. Factors affecting Pseudomonas savastanoi pv. savastanoi plant inoculations and their use for evaluation of Olive cultivar susceptibility. Phytopathology 96: 313-319.
54. Pérez-Martínez I, Rodríguez-Moreno L, Lambertsen L, Matas IM, Murillo J, Tegli S, Jiménez AJ, Ramos C. 2010. Fate of a Pseudomonas savastanoi pv. savastanoi type III secretion system mutant in olive plants (Olea europaea L.). Applied and Environment Microbiology 76: 3611-3619.
55. Pérez-Martínez I, Rodríguez-Moreno L, Matas IM, Ramos C. 2007. Strain selection and improvement of gene transfer for genetic manipulation of Pseudomonas savastanoi isolated from olive knots. Research in Microbiology 158: 60-69.
56. Pobigaylo N, Szymczak S, Nattkemper TW, Becker A. 2008. Identification of genes relevant to symbiosis and competitiveness in Sinorhizobium meliloti using signature-tagged mutants. Molecular Plant-Microbe Interactions 21: 219-231.
57. Pobigaylo N, Wetter D, Szymczak S, Schiller U, Kurtz S, Meyer F, Nattkemper TW, Becker A. 2006. Construction of a large signature-tagged mini-Tn5 transposon library and its application to mutagenesis of Sinorhizobium meliloti. Applied and Environment Microbiology 72: 4329-4337.
58. Powell GK, Morris RO. 1986. Nucleotide sequence and expression of a Pseudomonas savastanoi cytokinin biosynthetic gene: homology with Agrobacterium tumefaciens tmr and tzs loci. Nucleic Acids Research 14: 2555-2565.
59. Qi M, Wang D, Bradley CA, Zhao Y. 2011. Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization-based comparative genomics with nine pseudomonads. PLoS ONE 6: e16451.
60. Quesada JM, Penyalver R, Pérez-Panadés J, Salcedo CI, Carbonell EA, López MM. 2010. Comparison of chemical treatments for reducing epiphytic Pseudomonas savastanoi pv. savastanoi populations and for improving subsequent control of olive knot disease. Crop Protection 29: 1413-1420.
61. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, Lau GW, Mahajan-Miklos S, Plotnikova J, Tan MW, Tsongalis J et al. 2000. Plants and animals share functionally common bacterial virulence factors. Proceedings of the National Academy of Sciences, USA 97: 8815-8821.
62. Reinhardt JA, Baltrus DA, Nishimura MT, Jeck WR, Jones CD, Dangl JL. 2009. De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Research 19: 294-305.
63. Rico A, Preston GM. 2008. Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Molecular Plant-Microbe Interactions 21: 269-282.
64. Rodríguez-Moreno L, Barceló-Muñoz A, Ramos C. 2008. In vitro analysis of the interaction of Pseudomonas savastanoi pvs. savastanoi and nerii with micropropagated olive plants. Phytopathology 98: 815-822.
65. Rodríguez-Moreno L, Jiménez AJ, Ramos C. 2009. Endopathogenic lifestyle of Pseudomonas savastanoi pv. savastanoi in olive knots. Microbial Biotechnology 2: 476-488.
66. Rodríguez-Palenzuela P, Matas IM, Murillo J, López-Solanilla E, Bardaji L, Pérez-Martínez I, Rodríguez-Moskera ME, Penyalver R, López MM, Quesada JM et al. 2010. 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. Environmental Microbiology 12: 1604-1620.
67. Saenz HL, Dehio C. 2005. Signature-tagged mutagenesis: technical advances in a negative selection method for virulence gene identification. Current Opinion in Microbiology 8: 612-619.
68. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
69. Schroder G, Schuelein R, Quebatte M, Dehio C. 2011. Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae. Proceedings of the National Academy of Sciences, USA 108: 14643-14648.
70. Shimoda Y, Mitsui H, Kamimatsuse H, Minamisawa K, Nishiyama E, Ohtsubo Y, Nagata Y, Tsuda M, Shinpo S, Watanabe A et al. 2008. Construction of signature-tagged mutant library in Mesorhizobium loti as a powerful tool for functional genomics. DNA Research 15: 297-308.
71. Simon LD, Randolph B, Irwin N, Binkowski G. 1983. Stabilization of proteins by a bacteriophage T4 gene cloned in Escherichia coli. Proceedings of the National Academy of Sciences, USA 80: 2059-2062.
72. Sisto A, Cipriani MG, Morea M. 2004. Knot formation caused by Pseudomonas syringae subsp. savastanoi on olive plants is hrp-dependent. Phytopathology 94: 484-489.
73. Studholme DJ, Ibanez SG, MacLean D, Dangl JL, Chang JH, Rathjen JP. 2009. A draft genome sequence and functional screen reveals the repertoire of type III secreted proteins of Pseudomonas syringae pv. tabaci 11528. BMC Genomics 10: 395.
74. Surico G, Iacobellis NS, Sisto A. 1985. Studies on the role of indole-3-acetic acid and cytokinins in the formation of knots on olive and oleander plants by Pseudomonas syringae pv. savastanoi. Physiological Plant Pathology 26: 309-320.
75. Wang L, Beer SV. 2006. Application of signature-tagged mutagenesis to the study of virulence of Erwinia amylovora. FEMS Microbiology Letters 265: 164-171.
76. Yu J, Penaloza-Vazquez A, Chakrabarty AM, Bender CL. 1999. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Molecular Microbiology 33: 712-720.