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

Molecular Plant-Microbe Interactions

Volumn 21, Issue 11, 2008, Pages 1387-1397

  Sinn, Judith P ^a   Oh, Chang Sik ^b,c   Jensen, Philip J ^a   Carpenter, Sara C D ^b   Beer, Steven V ^b   McNellis, Timothy W ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

DspA E; HrpJ; HrpW; Hypersensitive response

Indexed keywords

BACTERIAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ERWINIA AMYLOVORA; GENETICS; IMMUNOBLOTTING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; SEQUENCE HOMOLOGY; TOBACCO; VIRULENCE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ERWINIA AMYLOVORA; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; PLANT DISEASES; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO; VIRULENCE;

BACTERIA (MICROORGANISMS); ERWINIA AMYLOVORA; MALUS X DOMESTICA; NICOTIANA TABACUM; PYRUS;

EID: 55549100619     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-21-11-1387     Document Type: Article

References (55)

1. Anderson, D. M., and Schneewind, O. 1997. A mRNA Signal for the Type III Secretion of Yop Proteins by Yersinia enterocolitica. Science 278:1140-1143.
2. Arthur, J. C. 1885. Proof that bacteria are the direct cause of the disease in trees known as pear blight. Am. Assoc. Adv. Sci. Proc. 34:294-298.
3. + and hypersensitive responses in tobacco. Plant Physiol. 92:215-221.
4. Ech: An elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol. Plant-Microbe Interact. 8:484-491.
5. Bereswill, S., Jock, S., Bellemann, P., and Geider, K. 1998. Identification of Erwinia amylovora by growth morphology on agar containing copper sulfate and by capsule staining with lectin. Plant Dis. 82:158-164.
6. Blume, B., Nurnberger, T., Nass, N., and Scheel, D. 2000. Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425-1440.
7. Bocsanczy, A. M., Nissinen, R. M., Oh, C.-S., and Beer, S. V. 2008. HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol. Plant Pathol. 9:425-434.
8. Bogdanove, A. J., Wei, Z. M., Zhao, L. P., and Beer, S. V. 1996. Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopN of Yersinia spp. J. Bacteriol. 178:1720-1730.
9. Bogdanove, A. J., Kim, J. F., Wei, Z. M., Kolchinsky, P., Charkowski, A. O., Conlin, A. K., Collmer, A., and Beer, S. V. 1998. Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato. Proc. Natl. Acad. Sci. U.S.A. 95:1325-1330.
10. Bogs, J., Bruchmuller, I., Erbar, C., and Geider, K. 1998. Colonization of host plants by the fire blight pathogen Erwinia amylovora marked with genes for bioluminescence and fluorescence. Phytopathology 88:416-421.
11. Burrill, T. J. 1880. Anthrax of fruit trees; or the so-called fire blight of pear, and twig blight of apple trees. Am. Assoc. Adv. Sci. Proc. 29:583-597.
12. Chandra, S., and Low, P. S. 1997. Measurement of Ca2+ fluxes during elicitation of the oxidative burst in aequorin-transformed tobacco cells. J. Biol. Chem. 272:28274-28280.
13. de Capdeville, G., Wilson, C. L., Beer, S. V., and Aist, J. R. 2002. Alternative disease control agents induce resistance to blue mold in harvested 'Red Delicious' apple fruit. Phytopathology 92:900-908.
14. de Capdeville, G., Beer, S. V., Watkins, C. B., Wilson, C. L., Tedeschi, L. O., and Aist, J. R. 2003. Pre- and post-harvest harpin treatments of apples induce resistance to blue mold. Plant Dis. 87:39-44.
15. Denning, W. 1794. On the decay of apple trees. Trans. Soc. Promotion Agric. Arts Manufact. Inst. State N. Y. 1:219-222.
16. Desikan, R., Hancock, J. T., Coffey, M. J., and Neill, S. J. 1996. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS (Fed. Eur. Biochem. Soc.) Lett. 382:213-217.
17. Dong, H. S., Delaney, T. P., Bauer, D. W., and Beer, S. V. 1999. Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J. 20:207-215.
18. Dong, H. P., Peng, J. L., Bao, Z. L., Meng, X. D., Bonasera, J. M., Chen, G. Y., Beer, S. V., and Dong, H. S. 2004. Downstream divergence of the ethylene signaling pathway for harpin-stimulated Arabidopsis growth and insect defense. Plant Physiol. 136:3628-3638.
19. Dong, H. P., Yu, H. Q., Bao, Z. L., Guo, X. J., Peng, J. L., Yao, Z., Chen, G. Y., Qu, S. P., and Dong, H. S. 2005. The ABI2-dependent abscisic acid signalling controls HrpN-induced drought tolerance in Arabidopsis. Planta 221:313-327.
20. El-Maarouf, H., Barny, M. A., Rona, J. P., and Bouteau, F. 2001. Harpin, a hypersensitive response elicitor from Erwinia amylovora, regulates ion channel activities in Arabidopsis thaliana suspension cells. FEBS (Fed. Eur. Biochem. Soc.) Lett. 497:82-84.
21. Galan, J. E., and Wolf-Watz, H. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567-573.
22. Gaudriault, S., Malandrin, L., Paulin, J. P., and Barny, M. A. 1997. DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol. Microbiol. 26:1057-1069.
23. Gaudriault, S., Brisset, M. N., and Barny, M. A. 1998. HrpW of Erwinia amylovora, a new Hrp-secreted protein. FEBS (Fed. Eur. Biochem. Soc.) Lett. 428:224-228.
24. Ham, J. H., Bauer, D. W., Fouts, D. E., and Collmer, A. 1998. A cloned Erwinia chrysanthemi Hrp (type III protein secretion) system functions in Escherichia coli to deliver Pseudomonas syringae Avr signals to plant cells and to secrete Avr proteins in culture. Proc. Natl. Acad. Sci. U.S.A. 95:10206-10211.
25. He, S. Y., Bauer, D. W., Collmer, A., and Beer, S. V. 1994. Hypersensitive response elicited by Erwinia amylovora harpin requires active plant metabolism. Mol. Plant-Microbe Interact. 7:289-292.
26. Huynh, T. V., Dahlbeck, D., and Staskawicz, B. J. 1989. Bacterial blight of soybean - regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-1377.
27. Jensen, P. J., Rytter, J., Detwiler, E. A., Travis, J. W., and McNellis, T. W. 2003. Rootstock effects on gene expression patterns in apple tree scions. Plant Mol. Biol. 53:493-511.
28. Jock, S., and Geider, K. 2004. Molecular differentiation of Erwinia amylovora strains from North America and of two Asian pear pathogens by analyses of PFGE patterns and hrpN genes. Environ. Microbiol. 6:480-490.
29. Journet, L., Hughes, K. T., and Cornelis, G. R. 2005. Type III secretion: A secretory pathway serving both motility and virulence (review). Mol. Membrane Biol. 22:41-50.
30. Kaniga, K., Delor, I., and Cornelis, G. R. 1991. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: Inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137-141.
31. Kim, J. F., and 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.
32. Kim, J. F., Wei, Z. M., and Beer, S. V. 1997. The hrpA and hrpC operons of Erwinia amylovora encode components of a type III pathway that secretes harpin. J. Bacteriol. 179:1690-1697.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227:680-685.
34. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
35. Mudgett, M. B. 2005. New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu. Rev. Plant Biol. 56:509-531.
36. Nissinen, R. M., Ytterberg, A. J., Bogdanove, A. J., Van Wijk, K. J., and 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.
37. Oh, C. S., and Beer, S. V. 2005. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 253:185-192.
38. Oh, C. S., Kim, J. F., and 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.
39. Peng, J. L., Dong, H. S., Dong, H. P., Delaney, T. P., Bonasera, J. M., and Beer, S. V. 2003. Harpin-elicited hypersensitive cell death and pathogen resistance require the NDR1 and EDS1 genes. Physiol. Mol. Plant Pathol. 62:317-326.
40. Perino, C., Gaudriault, S., Vian, B., and Barny, M. A. 1999. Visualization of harpin secretion in planta during infection of apple seedlings by Erwinia amylovora. Cell. Microbiol. 1:131-141.
41. Pike, S. M., Adam, A. L., Pu, X. A., Hoyos, M. E., Laby, R., Beer, S. V., and Novacky, A. 1998. Effects of Erwinia amylovora harpin on tobacco leaf cell membranes are related to leaf necrosis and electrolyte leakage and distinct from perturbations caused by inoculated E. amylovora. Physiol. Mol. Plant Pathol. 53:39-60.
42. Popham, P. L., Pike, S. M., and Novacky, A. 1995. The effect of harpin from Erwinia amylovora on the plasmalemma of suspension-cultured tobacco cells. Physiol. Mol. Plant Pathol. 47:39-50.
43. Sambrook, J., and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
44. Schesser, K., Frithz-Lindsten, E., and Wolf-Watz, H. 1996. Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J. Bacteriol. 178:7227-7233.
45. Shrestha, R., Park, D. H., Cho, J. M., Cho, S., Wilson, C., Hwang, I., Hur, J. H., and Lim, C. K. 2008. Genetic organization of the hrp genes cluster in Erwinia pyrifoliae and characterization of HR active domains in HrpN(Ep) protein by mutational analysis. Mol. Cells 25:30-42.
46. Sobiczewski, P., Deckers, T., and Pulawska, J. 1997. Fire Blight (Erwinia amylovora): Some Aspects of Epidemiology and Control. Research Institute of Pomology and Floriculture, Skierniewice, Poland.
47. Sory, M., Boland, A., Lambermont, I., and Cornelis, G. R. 1995. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl. Acad. Sci. U.S.A. 92:11998-12002.
48. Tabor, S., and Richardson, C. C. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. U.S.A. 82:1074-1078.
49. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. 1997. The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
50. van der Zwet, T., and Keil, H. L. 1979. Fire blight: A bacterial disease of rosaceous plants. In: Agriculture Handbook 510. United States Department of Agriculture, Washington, D.C.
51. Venisse, J. S., Barny, M. A., Paulin, J. P., and Brisset, M. N. 2003. Involvement of three pathogenicity factors of Erwinia amylovora in the oxidative stress associated with compatible interaction in pear. FEBS (Fed. Eur. Biochem. Soc.) Lett. 537:198-202.
52. Wei, Z. M., Laby, R. J., Zumoff, C. H., Bauer, D. W., He, S. Y., Collmer, A., and Beer, S. V. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85-88.
53. Xie, Z. X., and Chen, Z. X. 2000. Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells. Mol. Plant-Microbe Interact. 13:183-190.
54. Yang, B., Shiping, T., Jie, Z., and Yonghong, G. 2005. Harpin induces local and systemic resistance against Trichothecium roseum in harvested Hami melons. Postharvest Biol. Technol. 38:183-187.
55. Zhao, Y. F., He, S. Y., and Sundin, G. W. 2006. The Erwinia amylovora avrRpt2(EA) gene contributes to virulence on pear and AvrRpt2(EA) is recognized by Arabidopsis RPS2 when expressed in Pseudomonas syringae. Mol. Plant-Microbe Interact. 19:644-654.