Pathogenicity and infection strategies of the fire blight pathogen Erwinia amylovora in Rosaceae: State of the art

Microbiology (United Kingdom)

Volumn 159, Issue PART 5, 2013, Pages 823-832

  Vrancken, K ^a   Holtappels, M ^a   Schoofs, H ^b   Deckers, T ^b   Valcke, R ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b PC Fruit Research Station   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; PATTERN RECOGNITION RECEPTOR; PHLORETIN; PHYTOALEXIN; PHYTOHORMONE; REACTIVE OXYGEN METABOLITE;

BACTERIAL GENE; BACTERIAL VIRULENCE; CONCENTRATION (PARAMETERS); ERWINIA AMYLOVORA; FIRE BLIGHT; GENE INTERACTION; GENOTYPE; MOLECULAR SIZE; NONHUMAN; PATHOGENICITY; PHOTOSYNTHESIS; PLANT IMMUNITY; PLANT PATHOGEN INTERACTION; PRIORITY JOURNAL; QUORUM SENSING; RESPIRATORY BURST; REVIEW; ROSACEAE; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM;

BACTERIA (MICROORGANISMS); ERWINIA AMYLOVORA; ROSACEAE;

EID: 84876936228     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.064881-0     Document Type: Review

References (149)

1. Abramovitch, R. B. & Martin, G. B. (2004). Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7, 356-364.
2. Agati, G. & Tattini, M. (2010). Multiple functional roles of flavonoids in photoprotection. New Phytol 186, 786-793.
3. Ahuja, I., Kissen, R. & Bones, A. M. (2012). Phytoalexins in defense against pathogens. Trends Plant Sci 17, 73-90.
4. Al-Karablieh, N., Weingart, H. & Ullrich, M. S. (2009). The outer membrane protein TolC is required for phytoalexin resistance and virulence of the fire blight pathogen Erwinia amylovora. Microb Biotechnol 2, 465-475.
5. Alfano, J. R. & Collmer, A. (2004). Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42, 385-414.
6. Ardi, R., Kobiler, I., Jacoby, B., Keen, N. T. & Prusky, D. (1998). Involvement of epicatechin biosynthesis in the activation of the mechanism of resistance of avocado fruits to Colletotrichum gloeosporioides. Physiol Mol Plant Pathol 53, 269-285.
7. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez- Gomez, L., Boller, T., Ausubel, F. M. & Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983.
8. Baker, C. J. & Orlandi, E. W. (1995). Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33, 299-321.
9. Baker, C. J., Orlandi, E. W. & Mock, N. M. (1993). Harpin, an elicitor of the hypersensitive response in tobacco caused by Erwinia amylovora, elicits active oxygen production in suspension cells. Plant Physiol 102, 1341-1344.
10. Baldo, A., Norelli, J. L., Farrell, R. E., Jr, Bassett, C. L., Aldwinckle, H. S. & Malnoy, M. (2010). Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus x domestica) with Erwinia amylovora. BMC Plant Biol 10, 1.
11. Barnard, A. M. L. & Salmond, G. P. C. (2007). Quorum sensing in Erwinia species. Anal Bioanal Chem 387, 415-423.
12. Belkhadir, Y., Subramaniam, R. & Dangl, J. L. (2004). Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7, 391-399.
13. Bellemann, P. & Geider, K. (1992). Localization of transposon insertions in pathogenicity mutants of Erwinia amylovora and their biochemical characterization. J Gen Microbiol 138, 931-940.
14. Bent, A. F. & Mackey, D. (2007). Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45, 399-436.
15. Block, A., Li, G. Y., Fu, Z. Q. & Alfano, J. R. (2008). Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11, 396-403.
16. Bocsanczy, A. M., Nissinen, R. M., Oh, C. S. & Beer, S. V. (2008). HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol Plant Pathol 9, 425-434.
17. Bonasera, J. M., Kim, J. F. & Beer, S. V. (2006a). PR genes of apple: identification and expression in response to elicitors and inoculation with Erwinia amylovora. BMC Plant Biol 6, 23.
18. Bonasera, J. M., Meng, X., Beer, S. V., Owens, T. & Kim, W. S. (2006b). Interaction of DspE/A, a pathogenicity/avirulence protein of Erwinia amylovora, with pre-ferredoxin from apple and its relationship to photosynthetic efficiency. Acta Hortic 704, 473-477.
19. Boureau, T., ElMaarouf-Bouteau, H., Garnier, A., Brisset, M. N., Perino, C., Pucheu, I. & Barny, M. A. (2006). DspA/E, a type III effector essential for Erwinia amylovora pathogenicity and growth in planta, induces cell death in host apple and nonhost tobacco plants. Mol Plant Microbe Interact 19, 16-24.
20. Bugert, P. & Geider, K. (1997). Characterization of the amsI gene product as a low molecular weight acid phosphatase controlling exopolysaccharide synthesis of Erwinia amylovora. FEBS Lett 400, 252-256.
21. Burse, A., Weingart, H. & Ullrich, M. S. (2004). The phytoalexin- inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora. Mol Plant Microbe Interact 17, 43-54.
22. Buttner, D. & Bonas, U. (2006). Who comes first? How plant pathogenic bacteria orchestrate type III secretion. Curr Opin Microbiol 9, 193-200.
23. Buttner, D. & He, S. Y. (2009). Type III protein secretion in plant pathogenic bacteria. Plant Physiol 150, 1656-1664.
24. Chang, X. L. & Nick, P. (2012). Defence signalling triggered by Flg22 and Harpin is integrated into a different stilbene output in Vitis cells. PLoS ONE 7, e40446.
25. Chisholm, S. T., Coaker, G., Day, B. & Staskawicz, B. J. (2006). Host- microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814.
26. Chizzali, C. & Beerhues, L. (2012). Phytoalexins of the Pyrinae. Biphenyls and dibenzofurans. Beilstein J Org Chem 8, 613-620.
27. Chizzali, C., Gaid, M. M., Belkheir, A. K., Hansch, R., Richter, K., Flachowsky, H., Peil, A., Hanke, M. V., Liu, B. Y. & Beerhues, L. (2012). Differential expression of biphenyl synthase gene family members in fire-blight-infected apple 'Holsteiner Cox'. Plant Physiol 158, 864-875.
28. Chizzali, C., Khalil, M. N. A., Beuerle, T., Schuehly, W., Richter, K., Flachowsky, H., Peil, A., Hanke, M. V., Liu, B. Y. & Beerhues, L. (2012). Formation of biphenyl and dibenzofuran phytoalexins in the transition zones of fire blight-infected stems of Malus domestica cv. 'Holsteiner Cox' and Pyrus communis cv. 'Conference'. Phytochemistry 77, 179-185.
29. Cornelis, G. R. & Van Gijsegem, F. (2000). Assembly and function of type III secretory systems. Annu Rev Microbiol 54, 735-774.
30. Dai, G. H., Nicole, M., Andary, C., Martinez, C., Bresson, E., Boher, B., Daniel, J. F. & Geiger, J. P. (1996). Flavonoids accumulate in cell walls, middle lamellae and callose-rich papillae during an incompatible interaction between Xanthomonas campestris pv malvacearum and cotton. Physiol Mol Plant Pathol 49, 285-306.
31. Davey, M. E. & O'toole, G. A. (2000). Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64, 847-867.
32. de Bernonville, T. D., Gaucher, M., Guyot, S., Durel, C. E., Dat, J. F. & Brisset, M. N. (2011). The constitutive phenolic composition of two Malus x domestica genotypes is not responsible for their contrasted susceptibilities to fire blight. Environ Exp Bot 74, 65-73.
33. de Bernonville, T. D., Gaucher, M., Flors, V., Gaillard, S., Paulin, J. P., Dat, J. F. & Brisset, M. N. (2012). T3SS-dependent differential modulations of the jasmonic acid pathway in susceptible and resistant genotypes of Malus spp. challenged with Erwinia amylovora. Plant Sci 188-189, 1-9.
34. Deckers, T. & Schoofs, H. (2008). Status of the pear production in Europe. Acta Hortic 800, 95-105.
35. Dellagi, A., Brisset, M. N., Paulin, J. P. & Expert, D. (1998). Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol Plant Microbe Interact 11, 734-742.
36. Denny, T. P. (1995). Involvement of bacterial polysaccharides in plant pathogenesis. Annu Rev Phytopathol 33, 173-197.
37. Desikan, R., Reynolds, A., Hancock, J. T. & Neill, S. J. (1998). Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochem J 330, 115-120.
38. Dow, M., Newman, M. A. & von Roepenack, E. (2000). The induction and modulation of plant defense responses by bacterial lipopolysac- charides. Annu Rev Phytopathol 38, 241-261.
39. Eastgate, J. A. (2000). Erwinia amylovora: the molecular basis of fireblight disease. Mol Plant Pathol 1, 325-329.
40. Expert, D. (1999). Withholding and exchanging iron: Interactions between Erwinia spp. and their plant hosts. Annu Rev Phytopathol 37, 307-334.
41. Faize, M., Brisset, M. N., Paulin, J. P. & Tharaud, M. (1999). Secretion and regulation Hrp mutants of Erwinia amylovora trigger different responses in apple. FEMS Microbiol Lett 171, 173-178.
42. Feucht, W., Treutter, D., Santosbuelga, C. & Christ, E. (1996). Catechin as a radical scavenger in paraquat-treated Prunus avium. Journal of Applied Botany-Angewandte Botanik 70, 119-123.
43. Fischer, T. C., Gosch, C., Pfeiffer, J., Halbwirth, H., Halle, C., Stich, K. & Forkmann, G. (2007). Flavonoid genes of pear (Pyrus communis). Trees-Structure and Function 21, 521-529.
44. Flachowsky, H., Halbwirth, H., Treutter, D., Richter, K., Hanke, M. V., Szankowski, I., Gosch, C., Stich, K. & Fischer, T. C. (2012). Silencing of flavanone-3-hydroxylase in apple (Malus x domestica Borkh.) leads to accumulation of flavanones, but not to reduced fire blight susceptibility. Plant Physiol Biochem 51, 18-25.
45. Foyer, C. H. & Noctor, G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875.
46. Fraga, C. G. & Oteiza, P. I. (2011). Dietary flavonoids: Role of - epicatechin and related procyanidins in cell signaling. Free Radic Biol Med 51, 813-823.
47. Friedman, M. (2007). Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res 51, 116-134.
48. Galan, J. E. & Wolf-Watz, H. (2006). Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573.
49. Gander, S. & Gilbert, P. (1997). The development of a small-scale biofilm model suitable for studying the effects ofantibiotics on biofilms of Gram-negative bacteria. J Antimicrob Chemother 40, 329-334.
50. Gaudriault, S., Paulin, J. P. & Barny, M. A. (2002). The DspB/F protein of Erwinia amylovora is a type III secretion chaperone ensuring efficient intrabacterial production of the Hrp-secreted DspA/E pathogenicity factor. Mol Plant Pathol 3, 313-320.
51. Geier, G. & Geider, K. (1993). Characterization and influence on virulence of the levansucrase gene from the fireblight pathogen Erwinia amylovora. Physiol Mol Plant Pathol 42, 387-404.
52. Gerber, I. B., Zeidler, D., Durner, J. & Dubery, I. A. (2004). Early perception responses of Nicotiana tabacum cells in response to lipopolysaccharides from Burkholderia cepacia. Planta 218, 647-657.
53. Gould, K. S. (2004). Nature's Swiss army knife: The diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 2004, 314-320.
54. Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M. & Dangl, J. L. (2006). Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60, 425-449.
55. Gunen, Y., Misirli, A. & Gulcan, R. (2005). Leaf phenolic content of pear cultivars resistant or susceptible to fire blight. Sci Hortic (Amsterdam) 105, 213-221.
56. Halbwirth, H., Fischer, T. C., Roemmelt, S., Spinelli, F., Schlangen, K., Peterek, S., Sabatini, E., Messina, C., Speakman, J. B. & other authors (2003). Induction of antimicrobial 3-deoxyflavonoids in pome fruit trees controls fire blight. Z Naturforsch C 58, 765-770.
57. He, S. Y., Nomura, K. & Whittam, T. S. (2004). Type III protein secretion mechanism in mammalian and plant pathogens. Biochim Biophys Acta 1694, 181-206.
58. He, P., Shan, L. & Sheen, J. (2007). Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant- microbe interactions. Cell Microbiol 9, 1385-1396.
59. Hernandez, I., Alegre, L., Van Breusegem, F. & Munne-Bosch, S. How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14, 125-132.
60. Heyens, K. & Valcke, R. (2006). Fluorescence imaging of the infection pattern of apple leaves with Erwinia amylovora. Acta Hortic 704, 69-74.
61. Heyens, K., Valcke, R., Dumont, D., Robben, J. & Noben, J. P. (2006). Differential expression of proteins in apple following inoculation with Erwinia amylovoria. Acta Hortic 704, 489-494.
62. Hildebrand, M., Aldridge, P. & Geider, K. (2006). Characterization of hns genes from Erwinia amylovora. Mol Genet Genomics 275, 310-319.
63. Hueck, C. J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62, 379-433.
64. Huttner, C., Beuerle, T., Scharnhop, H., Ernst, L. & Beerhues, L. Differential effect of elicitors on biphenyl and dibenzofuran formation in Sorbus aucuparia cell cultures. J Agric Food Chem 58, 11977-11984.
65. Jensen, P. J., Halbrendt, N., Fazio, G., Makalowska, I., Altman, N., Praul, C., Maximova, S. N., Ngugi, H. K., Crassweller, R. M. & other authors (2012). Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. BMC Genomics 13, 9.
66. Jin, Q. L., Hu, W. Q., Brown, I., McGhee, G., Hart, P., Jones, A. L. & He, S.Y. (2001). Visualization of secreted Hrp and Avr proteins along the Hrp pilus during type III secretion in Erwinia amylovora and Pseudomonas syringae. Mol Microbiol 40, 1129-1139.
67. Jones, J. D. G. & Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329.
68. Kim, J. F. & Beer, S. V. (1998). HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class. J Bacteriol 180, 5203-5210.
69. Koczan, J. M., McGrath, M. J., Zhao, Y. F. & Sundin, G. W. (2009). Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 99, 1237-1244.
70. Koczan, J. M., Lenneman, B. R., McGrath, M. J. & Sundin, G. W. Cell surface attachment structures contribute to biofilm formation and xylem colonization by Erwinia amylovora. Appl Environ Microbiol 77, 7031-7039.
71. Krieger-Liszkay, A. (2005). Singlet oxygen production in photosynthesis. J Exp Bot 56, 337-346.
72. Kunkel, B. N., Bent, A. F., Dahlbeck, D., Innes, R. W. & Staskawicz, B. J. (1993). RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5, 865-875.
73. Lahaye, T. & Bonas, U. (2001). Molecular secrets of bacterial type III effector proteins. Trends Plant Sci 6, 479-485.
74. Langlotz, C., Schollmeyer, M., Coplin, D. L., Nimtz, M. & Geider, K. Biosynthesis of the repeating units of the exopolysaccharides amylovoran from Erwinia amylovora and stewartan from Pantoea stewartii. Physiol Mol Plant Pathol 75, 163-169.
75. Livaja, M., Zeidler, D., von Rad, U. & Durner, J. (2008). Transcriptional responses of Arabidopsis thaliana to the bacteria- derived PAMPs, harpin and lipopolysaccharide. Immunobiology 213, 161-171.
76. Llop, P., Cabrefiga, J., Smits, T. H. M., Dreo, T., Barbe, S., Pulawska, J., Bultreys, A., Blom, J., Duffy, B. & other authors (2011). Erwinia amylovora novel plasmid pEI70: complete sequence, biogeography, and role in aggressiveness in the fire blight phytopathogen. PLoS ONE e28651.
77. Llop, P., Barbe, S. & Lopez, M. M. (2012). Functions and origin of plasmids in Erwinia species that are pathogenic to or epiphytically associated with pome fruit trees. Trees-Structure and Function 26, 31-46.
78. Loquet, A., Sgourakis, N. G., Gupta, R., Giller, K., Riedel, D., Goosmann, C., Griesinger, C., Kolbe, M., Baker, D. & other authors. Atomic model of the type III secretion system needle. Nature 486, 276-279.
79. Loureiro, A., Nicole, M. R., Varzea, V., Moncada, P., Bertrand, B. & Silva, M. C. (2012). Coffee resistance to Colletotrichum kahawae is associated with lignification, accumulation of phenols and cell death at infection sites. Physiol Mol Plant Pathol 77, 23-32.
80. Maes, M., Orye, K., Bobev, S., Devreese, B., Van Beeumen, J., De Bruyn, A., Busson, R., Herdewijn, P., Morreel, K. & Messens, E. Influence of amylovoran production on virulence of Erwinia amylovora and a different amylovoran structure in E. amylovora isolates from Rubus. Eur J Plant Pathol 107, 839-844.
81. Malnoy, M., Jin, Q., Borejsza-Wysocka, E. E., He, S. Y. & Aldwinckle, H. S. (2007). Overexpression of the apple MpNPR1 gene confers increased disease resistance in Malus x domestica. Mol Plant Microbe Interact 20, 1568-1580.
82. Malnoy, M., Martens, S., Norelli, J. L., Barny, M. A., Sundin, G. W., Smits, T. H. M. & Duffy, B. (2012). Fire blight: applied genomic insights of the pathogen and host. Annu Rev Phytopathol 50, 475-494.
83. Mansfield, J. W. (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. Mol Plant Pathol 10, 721-734.
84. Martin, G. B., Bogdanove, A. J. & Sessa, G. (2003). Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54, 23-61.
85. Mayer, M., Oberhuber, C., Loncaric, I., Heissenberger, B., Keck, M., Scheiner, O. & Hoffmann-Sommergruber, K. (2011). Fireblight (Erwinia amylovora) affects Mal d 1-related allergenicity in apple. Eur J Plant Pathol 131, 1-7.
86. McCann, H. C. & Guttman, D. S. (2008). Evolution of the type III secretion system and its effectors in plant-microbe interactions. New Phytol 177, 33-47.
87. McDowell, J. M. & Simon, S. A. (2006). Recent insights into R gene evolution. Mol Plant Pathol 7, 437-448.
88. McDowell, J. M. & Simon, S. A. (2008). Molecular diversity at the plant-pathogen interface. Dev Comp Immunol 32, 736-744.
89. McGhee, G. C. & Jones, A. L. (2000). Complete nucleotide sequence of ubiquitous plasmid pEA29 from Erwinia amylovora strain Ea88: gene organization and intraspecies variation. Appl Environ Microbiol 66, 4897-4907.
90. McNally, R. R., Toth, I. K., Cock, P. J. A., Pritchard, L., Hedley, P. E., Morris, J. A., Zhao, Y. F. & Sundin, G. W. (2012). Genetic characterization of the HrpL regulon of the fire blight pathogen Erwinia amylovora reveals novel virulence factors. Mol Plant Pathol 13, 160-173.
91. Meng, X. D., Bonasera, J. M., Kim, J. F., Nissinen, R. M. & Beer, S. V. (2006). Apple proteins that interact with DspA/E, a pathogenicity effector of Erwinia amylovora, the fire blight pathogen. Mol Plant Microbe Interact 19, 53-61.
92. Meyer, A., Pühler, A. & Niehaus, K. (2001). The lipopolysaccharides of the phytopathogen Xanthomonas campestris pv. campestris induce an oxidative burst reaction in cell cultures of Nicotiana tabacum. Planta 213, 214-222.
93. Milcevicova, R., Gosch, C., Halbwirth, H., Stich, K., Hanke, M. V., Peil, A., Flachowsky, H., Rozhon, W., Jonak, C. & other authors (2010). Erwinia amylovora-induced defense mechanisms of two apple species that differ in susceptibility to fire blight. Plant Sci 179, 60-67.
94. Mohammadi, M. (2010). Enhanced colonization and pathogenicity of Erwinia amylovora strains transformed with the near-ubiquitous pEA29 plasmid on pear and apple. Plant Pathol 59, 252-261.
95. Molina, L., Rezzonico, F., Defago, G. & Duffy, B. (2005). Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J Bacteriol 187, 3206-3213.
96. Mudgett, M. B. (2005). New insights to the function of phytopatho- genic bacterial type III effectors in plants. Annu Rev Plant Biol 56, 509-531.
97. Newman, M. A., von Roepenack-Lahaye, E., Parr, A., Daniels, M. J. & Dow, J. M. (2002). Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant J 29, 487-495.
98. Nicaise, V., Roux, M. & Zipfel, C. (2009). Recent advances in PAMP- triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150, 1638-1647.
99. Nimtz, M., Mort, A., Domke, T., Wray, V., Zhang, Y. X., Qiu, F., Coplin, D. & Geider, K. (1996). Structure of amylovoran, the capsular exopolysaccharide from the fire blight pathogen Erwinia amylovora. Carbohydr Res 287, 59-76.
100. Nissinen, R. M., Ytterberg, A. J., Bogdanove, A. J., Van Wijk, K. J. & Beer, S. V. (2007). Analyses of the secretomes of Erwinia amylovora and selected hrp mutants reveal novel type III secreted proteins and an effect of HrpJ on extracellular harpin levels. Mol Plant Pathol 8, 55-67.
101. Oh, C. S. & Beer, S. V. (2005). Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol Lett 253, 185-192.
102. Oh, C. S., Kim, J. F. & Beer, S. V. (2005). The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infection. Mol Plant Pathol 6, 125-138.
103. Oh, C. S., Martin, G. B. & Beer, S. V. (2007). DspA/E, a type III effector of Erwinia amylovora, is required for early rapid growth in Nicotiana benthamiana and causes NbSGT1-dependent cell death. Mol Plant Pathol 8, 255-265.
104. Oh, C. S., Carpenter, S. C., Hayes, M. L. & Beer, S. (2010 Secretion and translocation signals and DspB/F-binding domains in the type III effector DspA/E of Erwinia amylovora. Microbiology 156, 1211-1220.
105. Ordax, M., Marco-Noales, E., Lopez, M. M. & Biosca, E. G. (2010). Exopolysaccharides favor the survival of Erwinia amylovora under copper stress through different strategies. Res Microbiol 161, 549-555.
106. Pester, D., Milcevicova, R., Schaffer, J., Wilhelm, E. & Blümel, S. Erwinia amylovora expresses fast and simultaneously hrp/dsp virulence genes during flower infection on apple trees. PLoS ONE 7, e325-e383.
107. Pfeiffer, J., Kuhnel, C., Brandt, J., Duy, D., Punyasiri, P. A. N., Forkmann, G. & Fischer, T. C. (2006). Biosynthesis of flavan 3-ols by leucoanthocyanidin 4-reductases and anthocyanidin reductases in leaves of grape (Vitis vinifera L.), apple (Malus x domestica Borkh.) and other crops. Plant Physiol Biochem 44, 323-334.
108. Pontais, I., Treutter, D., Paulin, J. P. & Brisset, M. N. (2008). Erwinia amylovora modifies phenolic profiles of susceptible and resistant apple through its type III secretion system. Physiol Plant 132, 262-271.
109. Ramey, B. E., Koutsoudis, M., von Bodman, S. B. & Fuqua, C. (2004). Biofilm formation in plant-microbe associations. Curr Opin Microbiol 602-609.
110. Reboutier, D., Frankart, C., Briand, J., Biligui, B., Laroche, S., Rona, J. P., Barny, M. A. & Bouteau, F. (2007). The HrpNea harpin from Erwinia amylovora triggers differential responses on the nonhost Arabidopsis thaliana cells and on the host apple cells. Mol Plant Microbe Interact 20, 94-100.
111. Rezzonico, F. & Duffy, B. (2008). Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 8, 154.
112. Robert-Seilaniantz, A., Navarro, L., Bari, R. & Jones, J. D. (2007). Pathological hormone imbalances. Curr Opin Plant Biol 10, 372-379.
113. Ronald, P. C., Salmeron, J. M., Carland, F. M. & Staskawicz, B. J. (1992). The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J Bacteriol 174, 1604-1611.
114. Sarowar, S., Zhao, Y. F., Soria-Guerra, R. E., Ali, S., Zheng, D. M., Wang, D. P. & Korban, S. S. (2011). Expression profiles of differentially regulated genes during the early stages of apple flower infection with Erwinia amylovora. J Exp Bot 62, 4851-4861.
115. Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W. & Davies, D. G. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184, 1140-1154.
116. Schollmeyer, M., Langlotz, C., Huber, A., Coplin, D. L. & Geider, K. Variations in the molecular masses of the capsular exopolysaccharides amylovoran, pyrifolan and stewartan. Int J Biol Macromol 50, 518-522.
117. Schraidt, O. & Marlovits, T. C. (2011). Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331, 1192-1195.
118. Segonzac, C. & Zipfel, C. (2011). Activation of plant pattern- recognition receptors by bacteria. Curr Opin Microbiol 14, 54-61.
119. Sels, J., Mathys, J., De Coninck, B. M. A., Cammue, B. P. A. & De Bolle, M. F. C. (2008). Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem 46, 941-950.
120. Singh, D. K., Maximova, S. N., Jensen, P. J., Lehman, B. L., Ngugi, H. K. & McNellis, T. W. (2010). FIBRILLIN4 is required for plastoglobule development and stress resistance in apple and Arabidopsis. Plant Physiol 154, 1281-1293.
121. Sinn, J. P., Oh, C. S., Jensen, P. J., Carpenter, S. C. D., Beer, S. V. & McNellis, T. W. (2008). The C-terminal half of the HrpN virulence protein of the fire blight pathogen Erwinia amylovora is essential for its secretion and for its virulence and avirulence activities. Mol Plant Microbe Interact 21, 1387-1397.
122. Sklodowska, M., Gajewska, E., Kuzniak, E., Wielanek, M., Mikicinski, A. & Sobiczewski, P. (2011). Antioxidant profile and polyphenol oxidase activities in apple leaves after Erwinia amylovora infection and pretreatment with a benzothiadiazole-type resistance inducer (BTH). J Phytopathol 159, 495-504.
123. Smits, T. H. M. & Duffy, B. (2011). Genomics of iron acquisition in the plant pathogen Erwinia amylovora: insights in the biosynthetic pathway of the siderophore desferrioxamine E. Arch Microbiol 193, 693-699.
124. Smits, T. H. M., Rezzonico, F., Kamber, T., Blom, J., Goesmann, A., Frey, J. E. & Duffy, B. (2010). Complete genome sequence of the fire blight pathogen Erwinia amylovora CFBP 1430 and comparison to other Erwinia spp. Mol Plant Microbe Interact 23, 384-393.
125. Soylu, S. (2006). Accumulation of cell-wall bound phenolic compounds and phytoalexin in Arabidopsis thaliana leaves following inoculation with pathovars of Pseudomonas syringae. Plant Sci 170, 942-952.
126. Spinelli, F., Speakman, J. B., Rademacher, W., Halbwirth, H., Stich, K. & Costa, G. (2005). Luteoforol, a flavan-4-ol, is induced in pome fruits by prohexadione-calcium and shows phytoalexin-like properties against Erwinia amylovora and other plant pathogens. Eur J Plant Pathol 112, 133-142.
127. Spinelli, F., Costa, G., Rondelli, E., Busi, S., Vanneste, J. L., Rodriguez, E. M. T. & other authors (2011). Emission of volatiles during the pathogenic interaction between Erwinia amylovora and Malus domestica. Acta Hortic 896, 55-63.
128. Tai, T. H., Dahlbeck, D., Clark, E. T., Gajiwala, P., Pasion, R., Whalen, M. C., Stall, R. E. & Staskawicz, B. J. (1999). Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 96, 14153-14158.
129. Takeuchi, K., Taguchi, F., Inagaki, Y., Toyoda, K., Shiraishi, T. & Ichinose, Y. (2003). Flagellin glycosylation island in Pseudomonas syringae pv. glycinea and its role in host specificity. J Bacteriol 185, 6658-6665.
130. Torres, M. A., Jones, J. D. G. & Dangl, J. L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiol 141, 373-378.
131. Treutter, D. (2001). Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul 34, 71-89.
132. Treutter, D. (2005). Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol (Stuttg) 7, 581-591.
133. Treutter, D. (2010). Managing phenol contents in crop plants by phytochemical farming and breeding-visions and constraints. Int J Mol Sci 11, 807-857.
134. Triplett, L. R., Melotto, M. & Sundin, G. W. (2009). Functional analysis of the N terminus of the Erwinia amylovora secreted effector DspA/E reveals features required for secretion, translocation, and binding to the chaperone DspB/F. Mol Plant Microbe Interact 22, 1282-1292.
135. Triplett, L. R., Wedemeyer, W. J. & Sundin, G. W. (2010). Homology- based modeling of the Erwinia amylovora type III secretion chaperone DspF used to identify amino acids required for virulence and interaction with the effector DspE. Res Microbiol 161, 613-618.
136. Tsiamis, G., Mansfield, J. W., Hockenhull, R., Jackson, R. W., Sesma, A., Athanassopoulos, E., Bennett, M. A., Stevens, C., Vivian, A. & other authors (2000). Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseo- licola, the cause of bean halo-blight disease. EMBO J 19, 3204-3214.
137. Van Loon, L. C. & Van Strien, E. A. (1999). The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55, 85-97.
138. Venisse, J. S., Gullner, G. & Brisset, M. N. (2001). Evidence for the involvement of an oxidative stress in the initiation of infection of pear by Erwinia amylovora. Plant Physiol 125, 2164-2172.
139. Venisse, J. S., Malnoy, M., Faize, M., Paulin, J. P. & Brisset, M. N. Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. Mol Plant Microbe Interact 15, 1204-1212.
140. Venisse, J. S., Barny, M. A., Paulin, J. P. & Brisset, M. N. (2003). Involvement of three pathogenicity factors of Erwinia amylovora in the oxidative stress associated with compatible interaction in pear. FEBS Lett 537, 198-202.
141. Viljevac, M., Dugalic, K., Stolfa, I., Dermic, E., Cvjetkovic, B., Sudar, R., Kovacevic, J., Cesar, V., Lepedus, H. & other authors (2009). Biochemical basis of apple leaf resistance to Erwinia amylovora infection. Food Technol Biotechnol 47, 281-287.
142. Vrancken, K., Schoofs, H., Deckers, T. & Valcke, R. (2012). Real time qPCR expression analysis of some stress related genes in leaf tissue of Pyrus communis cv. Conference after infection with Erwinia amylovora. Trees Structure and Function 26, 67-73.
143. Wang, D. P., Korban, S. S. & Zhao, Y. F. (2009). The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora. Mol Plant Pathol 10, 277-290.
144. Wei, Z. M., Laby, R. J., Zumoff, C. H., Bauer, D. W., He, S. Y., Collmer, A. & Beer, S. V. (1992). Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257, 85-88.
145. White, F. F., Yang, B. & Johnson, L. B. (2000). Prospects for understanding avirulence gene function. Curr Opin Plant Biol 3, 291-298.
146. Williams, R. J., Spencer, J. P. E. & Rice-Evans, C. (2004). Flavonoids: antioxidants or signalling molecules? Free Radic Biol Med 36, 838-849.
147. Wojtaszek, P. (1997). Oxidative burst: an early plant response to pathogen infection. Biochem J 322, 681-692.
148. Zhang, Y. X., Bak, D. D., Heid, H. & Geider, K. (1999). Molecular characterization of a protease secreted by Erwinia amylovora. J Mol Biol 289, 1239-1251.
149. Zhao, Y. F., Wang, D. P., Nakka, S., Sundin, G. W. & Korban, S. S. (2009). Systems level analysis of two-component signal transduction systems in Erwinia amylovora: role in virulence, regulation of amylovoran biosynthesis and swarming motility. BMC Genomics 10, 245.