1887

Abstract

Plants are host to a large amount of pathogenic bacteria. Fire blight, caused by the bacterium , is an important disease in . Pathogenicity of is greatly influenced by the production of exopolysaccharides, such as amylovoran, and the use of the type III secretion system, which enables bacteria to penetrate host tissue and cause disease. When infection takes place, plants have to rely on the ability of each cell to recognize the pathogen and the signals emanating from the infection site in order to generate several defence mechanisms. These mechanisms consist of physical barriers and the production of antimicrobial components, both in a preformed and an inducible manner. Inducible defence responses are activated upon the recognition of elicitor molecules by plant cell receptors, either derived from invading micro-organisms or from pathogen-induced degradation of plant tissue. This recognition event triggers a signal transduction cascade, leading to a range of defence responses [reactive oxygen species (ROS), plant hormones, secondary metabolites, …] and redeployment of cellular energy in a fast, efficient and multiresponsive manner, which prevents further pathogen ingress. This review highlights the research that has been performed during recent years regarding this specific plant–pathogen interaction between and , with a special emphasis on the pathogenicity and the infection strategy of and the possible defence mechanisms of the plant against this disease.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.064881-0
2013-05-01
2020-01-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/5/823.html?itemId=/content/journal/micro/10.1099/mic.0.064881-0&mimeType=html&fmt=ahah

References

  1. Abramovitch R. B., Martin G. B.. ( 2004;). Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol7:356–364 [CrossRef][PubMed]
    [Google Scholar]
  2. Agati G., Tattini M.. ( 2010;). Multiple functional roles of flavonoids in photoprotection. New Phytol186:786–793 [CrossRef][PubMed]
    [Google Scholar]
  3. Ahuja I., Kissen R., Bones A. M.. ( 2012;). Phytoalexins in defense against pathogens. Trends Plant Sci17:73–90 [CrossRef][PubMed]
    [Google Scholar]
  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 Biotechnol2:465–475 [CrossRef][PubMed]
    [Google Scholar]
  5. Alfano J. R., Collmer A.. ( 2004;). Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol42:385–414 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol53:269–285 [CrossRef]
    [Google Scholar]
  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. Nature415:977–983 [CrossRef][PubMed]
    [Google Scholar]
  8. Baker C. J., Orlandi E. W.. ( 1995;). Active oxygen in plant pathogenesis. Annu Rev Phytopathol33:299–321 [CrossRef][PubMed]
    [Google Scholar]
  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 Physiol102:1341–1344[PubMed]
    [Google Scholar]
  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 × domestica) with Erwinia amylovora . BMC Plant Biol10:1 [CrossRef][PubMed]
    [Google Scholar]
  11. Barnard A. M. L., Salmond G. P. C.. ( 2007;). Quorum sensing in Erwinia species. Anal Bioanal Chem387:415–423 [CrossRef][PubMed]
    [Google Scholar]
  12. Belkhadir Y., Subramaniam R., Dangl J. L.. ( 2004;). Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol7:391–399 [CrossRef][PubMed]
    [Google Scholar]
  13. Bellemann P., Geider K.. ( 1992;). Localization of transposon insertions in pathogenicity mutants of Erwinia amylovora and their biochemical characterization. J Gen Microbiol138:931–940[PubMed][CrossRef]
    [Google Scholar]
  14. Bent A. F., Mackey D.. ( 2007;). Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol45:399–436 [CrossRef][PubMed]
    [Google Scholar]
  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 Biol11:396–403 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol9:425–434 [CrossRef][PubMed]
    [Google Scholar]
  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 Biol6:23 [CrossRef][PubMed]
    [Google Scholar]
  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 Hortic704:473–477
    [Google Scholar]
  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 Interact19:16–24 [CrossRef][PubMed]
    [Google Scholar]
  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 Lett400:252–256 [CrossRef][PubMed]
    [Google Scholar]
  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 Interact17:43–54 [CrossRef][PubMed]
    [Google Scholar]
  22. Büttner D., Bonas U.. ( 2006;). Who comes first? How plant pathogenic bacteria orchestrate type III secretion. Curr Opin Microbiol9:193–200 [CrossRef][PubMed]
    [Google Scholar]
  23. Büttner D., He S. Y.. ( 2009;). Type III protein secretion in plant pathogenic bacteria. Plant Physiol150:1656–1664 [CrossRef][PubMed]
    [Google Scholar]
  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 ONE7:e40446 [CrossRef][PubMed]
    [Google Scholar]
  25. Chisholm S. T., Coaker G., Day B., Staskawicz B. J.. ( 2006;). Host–microbe interactions: shaping the evolution of the plant immune response. Cell124:803–814 [CrossRef][PubMed]
    [Google Scholar]
  26. Chizzali C., Beerhues L.. ( 2012;). Phytoalexins of the Pyrinae: Biphenyls and dibenzofurans. Beilstein J Org Chem8:613–620 [CrossRef][PubMed]
    [Google Scholar]
  27. Chizzali C., Gaid M. M., Belkheir A. K., Hänsch R., Richter K., Flachowsky H., Peil A., Hanke M. V., Liu B. Y., Beerhues L.. ( 2012a;). Differential expression of biphenyl synthase gene family members in fire-blight-infected apple ‘Holsteiner Cox’. Plant Physiol158:864–875 [CrossRef][PubMed]
    [Google Scholar]
  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.. ( 2012b;). 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’. Phytochemistry77:179–185 [CrossRef][PubMed]
    [Google Scholar]
  29. Cornelis G. R., Van Gijsegem F.. ( 2000;). Assembly and function of type III secretory systems. Annu Rev Microbiol54:735–774 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol49:285–306 [CrossRef]
    [Google Scholar]
  31. Davey M. E., O’toole G. A.. ( 2000;). Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev64:847–867 [CrossRef][PubMed]
    [Google Scholar]
  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 × domestica genotypes is not responsible for their contrasted susceptibilities to fire blight. Environ Exp Bot74:65–73 [CrossRef]
    [Google Scholar]
  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 Sci188-189:1–9 [CrossRef][PubMed]
    [Google Scholar]
  34. Deckers T., Schoofs H.. ( 2008;). Status of the pear production in Europe. Acta Hortic800:95–105
    [Google Scholar]
  35. Dellagi A., Brisset M. N., Paulin J. P., Expert D.. ( 1998;). Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol Plant Microbe Interact11:734–742 [CrossRef][PubMed]
    [Google Scholar]
  36. Denny T. P.. ( 1995;). Involvement of bacterial polysaccharides in plant pathogenesis. Annu Rev Phytopathol33:173–197 [CrossRef][PubMed]
    [Google Scholar]
  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 J330:115–120[PubMed]
    [Google Scholar]
  38. Dow M., Newman M. A., von Roepenack E.. ( 2000;). The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu Rev Phytopathol38:241–261 [CrossRef][PubMed]
    [Google Scholar]
  39. Eastgate J. A.. ( 2000;). Erwinia amylovora: the molecular basis of fireblight disease. Mol Plant Pathol1:325–329 [CrossRef][PubMed]
    [Google Scholar]
  40. Expert D.. ( 1999;). Withholding and exchanging iron: Interactions between Erwinia spp. and their plant hosts. Annu Rev Phytopathol37:307–334 [CrossRef][PubMed]
    [Google Scholar]
  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 Lett171:173–178 [CrossRef]
    [Google Scholar]
  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 Botanik70:119–123
    [Google Scholar]
  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 Function21:521–529 [CrossRef]
    [Google Scholar]
  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 × domestica Borkh.) leads to accumulation of flavanones, but not to reduced fire blight susceptibility. Plant Physiol Biochem51:18–25 [CrossRef][PubMed]
    [Google Scholar]
  45. Foyer C. H., Noctor G.. ( 2005;). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell17:1866–1875 [CrossRef][PubMed]
    [Google Scholar]
  46. Fraga C. G., Oteiza P. I.. ( 2011;). Dietary flavonoids: Role of (−)-epicatechin and related procyanidins in cell signaling. Free Radic Biol Med51:813–823 [CrossRef][PubMed]
    [Google Scholar]
  47. Friedman M.. ( 2007;). Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res51:116–134 [CrossRef][PubMed]
    [Google Scholar]
  48. Galán J. E., Wolf-Watz H.. ( 2006;). Protein delivery into eukaryotic cells by type III secretion machines. Nature444:567–573 [CrossRef][PubMed]
    [Google Scholar]
  49. Gander S., Gilbert P.. ( 1997;). The development of a small-scale biofilm model suitable for studying the effects of antibiotics on biofilms of Gram-negative bacteria. J Antimicrob Chemother40:329–334 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol3:313–320 [CrossRef][PubMed]
    [Google Scholar]
  51. Geier G., Geider K.. ( 1993;). Characterization and influence on virulence of the levansucrase gene from the fireblight pathogen Erwinia amylovora . Physiol Mol Plant Pathol42:387–404 [CrossRef]
    [Google Scholar]
  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 . Planta218:647–657 [CrossRef][PubMed]
    [Google Scholar]
  53. Gould K. S.. ( 2004;). Nature’s Swiss army knife: The diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol2004:314–320 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol60:425–449 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  56. Halbwirth H., Fischer T. C., Roemmelt S., Spinelli F., Schlangen K., Peterek S., Sabatini E., Messina C., Speakman J. B. et al. ( 2003;). Induction of antimicrobial 3-deoxyflavonoids in pome fruit trees controls fire blight. Z Naturforsch C58:765–770[PubMed][CrossRef]
    [Google Scholar]
  57. He S. Y., Nomura K., Whittam T. S.. ( 2004;). Type III protein secretion mechanism in mammalian and plant pathogens. Biochim Biophys Acta1694:181–206 [CrossRef][PubMed]
    [Google Scholar]
  58. He P., Shan L., Sheen J.. ( 2007;). Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant–microbe interactions. Cell Microbiol9:1385–1396 [CrossRef][PubMed]
    [Google Scholar]
  59. Hernández I., Alegre L., Van Breusegem F., Munné-Bosch S.. ( 2009;). How relevant are flavonoids as antioxidants in plants?. Trends Plant Sci14:125–132 [CrossRef][PubMed]
    [Google Scholar]
  60. Heyens K., Valcke R.. ( 2006;). Fluorescence imaging of the infection pattern of apple leaves with Erwinia amylovora . Acta Hortic704:69–74
    [Google Scholar]
  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 Hortic704:489–494
    [Google Scholar]
  62. Hildebrand M., Aldridge P., Geider K.. ( 2006;). Characterization of hns genes from Erwinia amylovora . Mol Genet Genomics275:310–319 [CrossRef][PubMed]
    [Google Scholar]
  63. Hueck C. J.. ( 1998;). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev62:379–433[PubMed]
    [Google Scholar]
  64. Hüttner C., Beuerle T., Scharnhop H., Ernst L., Beerhues L.. ( 2010;). Differential effect of elicitors on biphenyl and dibenzofuran formation in Sorbus aucuparia cell cultures. J Agric Food Chem58:11977–11984 [CrossRef][PubMed]
    [Google Scholar]
  65. Jensen P. J., Halbrendt N., Fazio G., Makalowska I., Altman N., Praul C., Maximova S. N., Ngugi H. K., Crassweller R. M. et al. ( 2012;). Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. BMC Genomics13:9 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol40:1129–1139 [CrossRef][PubMed]
    [Google Scholar]
  67. Jones J. D. G., Dangl J. L.. ( 2006;). The plant immune system. Nature444:323–329 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol180:5203–5210[PubMed]
    [Google Scholar]
  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. Phytopathology99:1237–1244 [CrossRef][PubMed]
    [Google Scholar]
  70. Koczan J. M., Lenneman B. R., McGrath M. J., Sundin G. W.. ( 2011;). Cell surface attachment structures contribute to biofilm formation and xylem colonization by Erwinia amylovora . Appl Environ Microbiol77:7031–7039 [CrossRef][PubMed]
    [Google Scholar]
  71. Krieger-Liszkay A.. ( 2005;). Singlet oxygen production in photosynthesis. J Exp Bot56:337–346 [CrossRef][PubMed]
    [Google Scholar]
  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 Cell5:865–875[PubMed][CrossRef]
    [Google Scholar]
  73. Lahaye T., Bonas U.. ( 2001;). Molecular secrets of bacterial type III effector proteins. Trends Plant Sci6:479–485 [CrossRef][PubMed]
    [Google Scholar]
  74. Langlotz C., Schollmeyer M., Coplin D. L., Nimtz M., Geider K.. ( 2011;). Biosynthesis of the repeating units of the exopolysaccharides amylovoran from Erwinia amylovora and stewartan from Pantoea stewartii . Physiol Mol Plant Pathol75:163–169 [CrossRef]
    [Google Scholar]
  75. Livaja M., Zeidler D., von Rad U., Durner J.. ( 2008;). Transcriptional responses of Arabidopsis thaliana to the bacteria-derived PAMPs, harpin and lipopolysaccharide. Immunobiology213:161–171 [CrossRef][PubMed]
    [Google Scholar]
  76. Llop P., Cabrefiga J., Smits T. H. M., Dreo T., Barbé S., Pulawska J., Bultreys A., Blom J., Duffy B. et al. ( 2011;). Erwinia amylovora novel plasmid pEI70: complete sequence, biogeography, and role in aggressiveness in the fire blight phytopathogen. PLoS ONE6:e28651 [CrossRef][PubMed]
    [Google Scholar]
  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 Function26:31–46 [CrossRef]
    [Google Scholar]
  78. Loquet A., Sgourakis N. G., Gupta R., Giller K., Riedel D., Goosmann C., Griesinger C., Kolbe M., Baker D. et al. ( 2012;). Atomic model of the type III secretion system needle. Nature486:276–279[PubMed]
    [Google Scholar]
  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 Pathol77:23–32 [CrossRef]
    [Google Scholar]
  80. Maes M., Orye K., Bobev S., Devreese B., Van Beeumen J., De Bruyn A., Busson R., Herdewijn P., Morreel K., Messens E.. ( 2001;). Influence of amylovoran production on virulence of Erwinia amylovora and a different amylovoran structure in E. amylovora isolates from Rubus . Eur J Plant Pathol107:839–844 [CrossRef]
    [Google Scholar]
  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 × domestica . Mol Plant Microbe Interact20:1568–1580 [CrossRef][PubMed]
    [Google Scholar]
  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 Phytopathol50:475–494 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol10:721–734 [CrossRef][PubMed]
    [Google Scholar]
  84. Martin G. B., Bogdanove A. J., Sessa G.. ( 2003;). Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol54:23–61 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol131:1–7 [CrossRef]
    [Google Scholar]
  86. McCann H. C., Guttman D. S.. ( 2008;). Evolution of the type III secretion system and its effectors in plant-microbe interactions. New Phytol177:33–47 [CrossRef][PubMed]
    [Google Scholar]
  87. McDowell J. M., Simon S. A.. ( 2006;). Recent insights into R gene evolution. Mol Plant Pathol7:437–448 [CrossRef][PubMed]
    [Google Scholar]
  88. McDowell J. M., Simon S. A.. ( 2008;). Molecular diversity at the plant–pathogen interface. Dev Comp Immunol32:736–744 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol66:4897–4907 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol13:160–173 [CrossRef][PubMed]
    [Google Scholar]
  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 Interact19:53–61 [CrossRef][PubMed]
    [Google Scholar]
  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 . Planta213:214–222 [CrossRef][PubMed]
    [Google Scholar]
  93. Milcevicova R., Gosch C., Halbwirth H., Stich K., Hanke M. V., Peil A., Flachowsky H., Rozhon W., Jonak C. et al. ( 2010;). Erwinia amylovora-induced defense mechanisms of two apple species that differ in susceptibility to fire blight. Plant Sci179:60–67 [CrossRef]
    [Google Scholar]
  94. Mohammadi M.. ( 2010;). Enhanced colonization and pathogenicity of Erwinia amylovora strains transformed with the near-ubiquitous pEA29 plasmid on pear and apple. Plant Pathol59:252–261 [CrossRef]
    [Google Scholar]
  95. Molina L., Rezzonico F., Défago G., Duffy B.. ( 2005;). Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J Bacteriol187:3206–3213 [CrossRef][PubMed]
    [Google Scholar]
  96. Mudgett M. B.. ( 2005;). New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol56:509–531 [CrossRef][PubMed]
    [Google Scholar]
  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 J29:487–495 [CrossRef][PubMed]
    [Google Scholar]
  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 Physiol150:1638–1647 [CrossRef][PubMed]
    [Google Scholar]
  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 Res287:59–76 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol8:55–67 [CrossRef][PubMed]
    [Google Scholar]
  101. Oh C. S., Beer S. V.. ( 2005;). Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol Lett253:185–192 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol6:125–138 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol8:255–265 [CrossRef][PubMed]
    [Google Scholar]
  104. Oh C. S., Carpenter S. C., Hayes M. L., Beer S. V.. ( 2010;). Secretion and translocation signals and DspB/F-binding domains in the type III effector DspA/E of Erwinia amylovora . Microbiology156:1211–1220 [CrossRef][PubMed]
    [Google Scholar]
  105. Ordax M., Marco-Noales E., López M. M., Biosca E. G.. ( 2010;). Exopolysaccharides favor the survival of Erwinia amylovora under copper stress through different strategies. Res Microbiol161:549–555 [CrossRef][PubMed]
    [Google Scholar]
  106. Pester D., Milčevičová R., Schaffer J., Wilhelm E., Blümel S.. ( 2012;). Erwinia amylovora expresses fast and simultaneously hrp/dsp virulence genes during flower infection on apple trees. PLoS ONE7:e32583 [CrossRef][PubMed]
    [Google Scholar]
  107. Pfeiffer J., Kühnel 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 × domestica Borkh.) and other crops. Plant Physiol Biochem44:323–334 [CrossRef][PubMed]
    [Google Scholar]
  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 Plant132:262–271 [CrossRef][PubMed]
    [Google Scholar]
  109. Ramey B. E., Koutsoudis M., von Bodman S. B., Fuqua C.. ( 2004;). Biofilm formation in plant–microbe associations. Curr Opin Microbiol7:602–609 [CrossRef][PubMed]
    [Google Scholar]
  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 Interact20:94–100 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol8:154 [CrossRef][PubMed]
    [Google Scholar]
  112. Robert-Seilaniantz A., Navarro L., Bari R., Jones J. D.. ( 2007;). Pathological hormone imbalances. Curr Opin Plant Biol10:372–379 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol174:1604–1611[PubMed]
    [Google Scholar]
  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 Bot62:4851–4861 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol184:1140–1154 [CrossRef][PubMed]
    [Google Scholar]
  116. Schollmeyer M., Langlotz C., Huber A., Coplin D. L., Geider K.. ( 2012;). Variations in the molecular masses of the capsular exopolysaccharides amylovoran, pyrifolan and stewartan. Int J Biol Macromol50:518–522 [CrossRef][PubMed]
    [Google Scholar]
  117. Schraidt O., Marlovits T. C.. ( 2011;). Three-dimensional model of Salmonella’s needle complex at subnanometer resolution. Science331:1192–1195 [CrossRef][PubMed]
    [Google Scholar]
  118. Segonzac C., Zipfel C.. ( 2011;). Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol14:54–61 [CrossRef][PubMed]
    [Google Scholar]
  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 Biochem46:941–950 [CrossRef][PubMed]
    [Google Scholar]
  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 Physiol154:1281–1293 [CrossRef][PubMed]
    [Google Scholar]
  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 Interact21:1387–1397 [CrossRef][PubMed]
    [Google Scholar]
  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 Phytopathol159:495–504 [CrossRef]
    [Google Scholar]
  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 Microbiol193:693–699 [CrossRef][PubMed]
    [Google Scholar]
  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 Interact23:384–393 [CrossRef][PubMed]
    [Google Scholar]
  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 Sci170:942–952 [CrossRef]
    [Google Scholar]
  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 Pathol112:133–142 [CrossRef]
    [Google Scholar]
  127. Spinelli F., Costa G., Rondelli E., Busi S., Vanneste J. L., Rodriguez E. M. T. et al. ( 2011;). Emission of volatiles during the pathogenic interaction between Erwinia amylovora and Malus domestica . Acta Hortic896:55–63
    [Google Scholar]
  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 U S A96:14153–14158 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol185:6658–6665 [CrossRef][PubMed]
    [Google Scholar]
  130. Torres M. A., Jones J. D. G., Dangl J. L.. ( 2006;). Reactive oxygen species signaling in response to pathogens. Plant Physiol141:373–378 [CrossRef][PubMed]
    [Google Scholar]
  131. Treutter D.. ( 2001;). Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul34:71–89 [CrossRef]
    [Google Scholar]
  132. Treutter D.. ( 2005;). Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol (Stuttg) 7:581–591 [CrossRef][PubMed]
    [Google Scholar]
  133. Treutter D.. ( 2010;). Managing phenol contents in crop plants by phytochemical farming and breeding-visions and constraints. Int J Mol Sci11:807–857 [CrossRef][PubMed]
    [Google Scholar]
  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 Interact22:1282–1292 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol161:613–618 [CrossRef][PubMed]
    [Google Scholar]
  136. Tsiamis G., Mansfield J. W., Hockenhull R., Jackson R. W., Sesma A., Athanassopoulos E., Bennett M. A., Stevens C., Vivian A. et al. ( 2000;). Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J19:3204–3214 [CrossRef][PubMed]
    [Google Scholar]
  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 Pathol55:85–97 [CrossRef]
    [Google Scholar]
  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 Physiol125:2164–2172 [CrossRef][PubMed]
    [Google Scholar]
  139. Venisse J. S., Malnoy M., Faize M., Paulin J. P., Brisset M. N.. ( 2002;). Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora . Mol Plant Microbe Interact15:1204–1212 [CrossRef][PubMed]
    [Google Scholar]
  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 Lett537:198–202 [CrossRef][PubMed]
    [Google Scholar]
  141. Viljevac M., Dugalic K., Stolfa I., Dermic E., Cvjetkovic B., Sudar R., Kovacevic J., Cesar V., Lepedus H. et al. ( 2009;). Biochemical basis of apple leaf resistance to Erwinia amylovora infection. Food Technol Biotechnol47:281–287
    [Google Scholar]
  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. Conférence after infection with Erwinia amylovora. Trees Structure and Function26:67–73 [CrossRef]
    [Google Scholar]
  143. Wang D. P., Korban S. S., Zhao Y. F.. ( 2009;). The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora . Mol Plant Pathol10:277–290 [CrossRef][PubMed]
    [Google Scholar]
  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 . Science257:85–88 [CrossRef][PubMed]
    [Google Scholar]
  145. White F. F., Yang B., Johnson L. B.. ( 2000;). Prospects for understanding avirulence gene function. Curr Opin Plant Biol3:291–298 [CrossRef][PubMed]
    [Google Scholar]
  146. Williams R. J., Spencer J. P. E., Rice-Evans C.. ( 2004;). Flavonoids: antioxidants or signalling molecules?. Free Radic Biol Med36:838–849 [CrossRef][PubMed]
    [Google Scholar]
  147. Wojtaszek P.. ( 1997;). Oxidative burst: an early plant response to pathogen infection. Biochem J322:681–692[PubMed]
    [Google Scholar]
  148. Zhang Y. X., Bak D. D., Heid H., Geider K.. ( 1999;). Molecular characterization of a protease secreted by Erwinia amylovora . J Mol Biol289:1239–1251 [CrossRef][PubMed]
    [Google Scholar]
  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 Genomics10:245 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.064881-0
Loading
/content/journal/micro/10.1099/mic.0.064881-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error