The bacterial effector DspA/E is toxic in Arabidopsis thaliana and is required for multiplication and survival of fire blight pathogen

Molecular Plant Pathology

Volumn 14, Issue 5, 2013, Pages 506-517

  Degrave, Alexandre ^a,b,c   Moreau, Manon ^a,b,c   Launay, Alban ^a,b,c   Barny, Marie Anne ^a,b,c   Brisset, Marie Noëlle ^d   Patrit, Oriane ^a,b,c   Taconnat, Ludivine ^e   Vedel, Regine ^a,b,c   Fagard, Mathilde ^a,b,c,f  

^a UMR217   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c AGROPARISTECH   (France)

^d UNIVERSITÉ D'ANGERS   (France)

^e INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^f CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; CALLOSE; ELECTROLYTE; GLUCAN; SALICYLIC ACID;

ARABIDOPSIS; ARTICLE; CELL DEATH; CYTOLOGY; DNA MICROARRAY; ERWINIA AMYLOVORA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MUTATION; NUCLEOLUS; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT LEAF; PLANT ROOT; PROTEIN SYNTHESIS; PSEUDOMONAS SYRINGAE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; CELL DEATH; CELL NUCLEOLUS; ELECTROLYTES; ERWINIA AMYLOVORA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCANS; MICROBIAL VIABILITY; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN BIOSYNTHESIS; PSEUDOMONAS SYRINGAE; SALICYLIC ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ERWINIA AMYLOVORA;

EID: 84877037858     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12022     Document Type: Article

References (40)

1. Alfano, J.R. (2009) Roadmap for future research on plant pathogen effectors. Mol. Plant Pathol. 10, 805-813.
2. Badel, J.L., Shimizu, R., Oh, H.S. and Collmer, A. (2006) A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol. Plant-Microbe Interact. 19, 99-111.
3. Barny, M.A., Guinebretiere, M.H., Marcais, B., Coissac, E., Paulin, J.P. and Laurent, J. (1990) Cloning of a large gene cluster involved in Erwinia amylovora CFBP1430 virulence. Mol. Microbiol. 4, 777-786.
4. Billing (1983) Fire blight. J. R. Hortic. Soc. 55, 206-210.
5. Block, A. and Alfano, J.R. (2011) Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr. Opin. Microbiol. 14, 39-46.
6. Block, A., Li, G.Y., Fu, Z.Q. and Alfano, J.R. (2008) Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11, 396-403.
7. Boch, J. and Bonas, U. (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48, 419-436.
8. Bocsanczy, A., Nissinen, R., Oh, C. and Beer, S. (2008) HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol. Plant Pathol. 9, 425-434.
9. Bogdanove, A., Bauer, D. and Beer, S. (1998) Erwinia amylovora secretes DspE, a pathogenicity factor and functional AvrE homolog, through the hrp (type III secretion) pathway. J. Bacteriol. 180, 2244-2247.
10. Boureau, T., ElMaarouf-Bouteau, H., Garnier, A., Brisset, M., Perino, C., Pucheu, I. and Barny, M. (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.
11. Boureau, T., Siamer, S., Perino, C., Gaubert, S., Patrit, O., Degrave, A., Fagard, M., Chevreau, E. and Barny, M.A. (2011) The HrpN effector of Erwinia amylovora, which is involved in type III translocation, contributes directly or indirectly to callose elicitation on apple leaves. Mol. Plant-Microbe Interact. 24, 577-584.
12. Chen, L.Q., Hou, B.H., Lalonde, S., Takanaga, H., Hartung, M.L., Qu, X.Q., Guo, W.J., Kim, J.G., Underwood, W., Chaudhuri, B., Chermak, D., Antony, G., White, F.F., Somerville, S.C., Mudgett, M.B. and Frommer, W.B. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature, 468, 527-532.
13. Chen, Z., Agnew, J., Cohen, J., He, P., Shan, L., Sheen, J. and Kunkel, B. (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. USA, 104, 20131-20136.
14. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
15. Crowe, M., Serizet, C., Thareau, V., Aubourg, S., Rouzé, P., Hilson, P., Beynon, J., Weisbeek, P., van Hummelen, P., Reymond, P., Paz-Ares, J., Nietfeld, W. and Trick, M. (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res. 31, 156-158.
16. DebRoy, S., Thilmony, R., Kwack, Y., Nomura, K. and He, S. (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc. Natl. Acad. Sci. USA, 101, 9927-9932.
17. Degrave, A., Fagard, M., Perino, C., Brisset, M.N., Gaubert, S., Laroche, S., Patrit, O. and Barny, M.A. (2008) Erwinia amylovora type three-secreted proteins trigger cell death and defense responses in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21, 1076-1086.
18. Fagard, M., Dellagi, A., Roux, C., Perino, C., Rigault, M., Boucher, V., Shevchik, V.E. and Expert, D. (2007) Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi. Mol. Plant-Microbe Interact. 20, 794-805.
19. Fontana, M.F., Banga, S., Barry, K.C., Shen, X., Tan, Y., Luo, Z.Q. and Vance, R.E. (2011) Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. Plos Pathog. 7, e1001289.
20. 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.
21. Grant, S.R., Fisher, E.J., Chang, J.H., Mole, B.M. and Dangl, J.L. (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60, 425-449.
22. Ham, J.H., Majerczak, D.R., Arroyo-Rodriguez, A.S., Mackey, D.M. and Coplin, D.L. (2006) WtsE, an AvrE-family effector protein from Pantoea stewartii subsp stewartii, causes disease-associated cell death in corn and requires a chaperone protein for stability. Mol. Plant-Microbe Interact. 19, 1092-1102.
23. Ham, J., Majerczak, D., Ewert, S., Sreerekha, M., Mackey, D. and Coplin, D. (2008) WtsE, an AvrE-family type III effector protein of Pantoea stewartii subsp. stewartii, causes cell death in non-host plants. Mol. Plant Pathol. 9, 633-643.
24. Ham, J., Majerczak, D., Nomura, K., Mecey, C., Uribe, F., He, S., Mackey, D. and Coplin, D. (2009) Multiple activities of the plant pathogen type III effector proteins WtsE and AvrE require WxxxE motifs. Mol. Plant-Microbe Interact. 22, 703-712.
25. Hilson, P., Allemeersch, J., Altmann, T., Aubourg, S., Avon, A., Beynon, J., Bhalerao, R., Bitton, F., Caboche, M., Cannoot, B., Chardakov, V., Cognet-Holliger, C., Colot, V., Crowe, M., Darimont, C., Durinck, S., Eickhoff, H., de Longevialle, A., Farmer, E., Grant, M., Kuiper, M., Lehrach, H., Léon, C., Leyva, A., Lundeberg, J., Lurin, C., Moreau, Y., Nietfeld, W., Paz-Ares, J., Reymond, P., Rouzé, P., Sandberg, G., Segura, M., Serizet, C., Tabrett, A., Taconnat, L., Thareau, V., Van Hummelen, P., Vercruysse, S., Vuylsteke, M., Weingartner, M., Weisbeek, P., Wirta, V., Wittink, F., Zabeau, M. and Small, I. (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res. 14, 2176-2189.
26. Kim, H.S., Thammarat, P., Lommel, S.A., Hogan, C.S. and Charkowski, A.O. (2011) Pectobacterium carotovorum elicits plant cell death with DspE/F but the P. carotovorum DspE does not suppress callose or induce expression of plant genes early in plant-microbe interactions. Mol. Plant-Microbe Interact. 24, 773-786.
27. Kvitko, B.H., Park, D.H., Velasquez, A.C., Wei, C.F., Russell, A.B., Martin, G.B., Schneider, D.J. and Collmer, A. (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 5, e1000388.
28. Lam, Y.W., Trinkle-Mulcahy, L. and Lamond, A.I. (2005) The nucleolus. J. Cell Sci. 118, 1335-1337.
29. Lawton, K., Weymann, K., Friedrich, L., Vernooij, B., Uknes, S. and Ryals, J. (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol. Plant-Microbe Interact. 8, 863-870.
30. Lorrain, S., Vailleau, F., Balaque, C. and Roby, D. (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263-271.
31. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B. and Ton, J. (2011) Callose deposition: a multifaceted plant defense response. Mol. Plant-Microbe Interact. 24, 183-193.
32. Meng, P., Raynaud, C., Tcherkez, G., Blanchet, S., Massoud, K., Domenichini, S., Henry, Y., Soubigou-Taconnat, L., Lelarge-Trouverie, C., Saindrenan, P., Renou, J. and Bergounioux, C. (2009) Crosstalks between myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS ONE 4, e7364.
33. Moreau, M., Degrave, A., Vedel, R., Bitton, F., Patrit, O., Renou, J.P., Barny, M.A. and Fagard, M. (2012) EDS1 contributes to nonhost resistance of Arabidopsis thaliana against Erwinia amylovora. Mol. Plant-Microbe Interact. 25, 421-430.
34. 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.
35. Oh, C.S., Martin, G.B. and 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.
36. Pester, D., Milčevičová, R., Schaffer, J., Wilhelm, E. and Blümel, S. (2012) Erwinia amylovora expresses fast and simultaneously hrp/dsp virulence genes during flower infection on apple trees. PLoS ONE 7, e32583.
37. Ren, X., Liu, F., Bao, Z., Zhang, C., Wu, X., Chen, L., Liu, R. and Dong, H. (2008) Root growth of Arabidopsis thaliana is regulated by ethylene and abscisic acid signaling interaction in response to HrpN(Ea), a Bacterial Protein of Harpin Group. Plant Mol. Biol. Rep. 26, 225-240.
38. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Güldener, U., Mannhaupt, G., Münsterkötter, M. and Mewes, H. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32, 5539-5545.
39. Venisse, J., Malnoy, M., Faize, M., Paulin, J. and Brisset, M. (2002) Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. Mol. Plant-Microbe Interact. 15, 1204-1212.
40. Zuo, J., Niu, Q.W. and Chua, N.H. (2000) Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265-273.