The Pseudomonas syringae type III effector AvrRpt2 functions downstream or independently of SA to promote virulence on Arabidopsis thaliana

Plant Journal

Volumn 37, Issue 4, 2004, Pages 494-504

  Chen, Zhongying ^a   Kloek, Andrew P ^a,e   Cuzick, Alayne ^b,f   Moeder, Wolfgang ^c   Tang, Dingzhong ^d   Innes, Roger W ^d   Klessig, Daniel F ^c   McDowell, John M ^b   Kunkel, Barbara N ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b Fralin Life Science Institute   (United States)

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

^d INDIANA UNIVERSITY   (United States)

^e Divergence Inc   (United States)

^f HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Arabidopsis; AvrRpt2; NahG; Pseudomonas syringae; Salicylic acid; Virulence

Indexed keywords

BIODEGRADATION; ENZYMES; GENES; VIRUSES;

INFECTIONS; TRANSGENIC PLANTS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; AVRRPT2 PROTEIN, PSEUDOMONAS SYRINGAE; BACTERIAL PROTEIN; MIXED FUNCTION OXIDASE; PATHOGENESIS RELATED PROTEINS, PLANT; PATHOGENESIS-RELATED PROTEINS, PLANT; RPM1 PROTEIN, ARABIDOPSIS; RPS2 PROTEIN, ARABIDOPSIS; SALICYLATE 1 MONOOXYGENASE; SALICYLATE 1-MONOOXYGENASE; SALICYLIC ACID; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; FUNGUS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PERONOSPORA; PLANT DISEASE; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; VIRULENCE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; FUNGI; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; IMMUNITY, NATURAL; MIXED FUNCTION OXYGENASES; MUTATION; PERONOSPORA; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS SYRINGAE; SALICYLIC ACID; SIGNAL TRANSDUCTION; VIRULENCE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ERYSIPHE; FUNGI; GOLOVINOMYCES CICHORACEARUM; HYALOPERONOSPORA PARASITICA; LYCOPERSICON ESCULENTUM; PERONOSPORA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; TEREBRANTIA;

EID: 1342290780     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2003.01984.x     Document Type: Article

References (58)

1. Abramovitch, R.B., Kim, Y.J., Chen, S., Dickman, M.B. and Martin, G.B. (2003) Pseudomonastype III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60-69.
2. Adam, L. and Somerville, S.C. (1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9, 341-356.
3. Alfano, J.R. and Collmer, A. (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell, 8, 1683-1698.
4. Axtell, M.J. and Staskawicz, B.J. (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell, 112, 369-377.
5. Axtell, M.J., Chisholm, S.T., Dahlbeck, D. and Staskawicz, B.J. (2003) Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol. Microbiol. 49, 1537-1546.
6. Boch, J., Verbsky, M.L., Roberstson, T.L., Larkin, J.C. and Kunkel, B.N. (1998) Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5. Mol. Plant Microbe Interact. 11, 1196-1206.
7. Boch, J., Joardar, V., Gao, L., Robertson, T.L., Lim, M. and Kunkel, B.N. (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol. Microbiol. 44, 73-88.
8. Bonas, U. and Lahaye, T. (2002) Plant disease resistance triggered by pathogen-derived molecules: refined models of specific recognition. Curr. Opin. Microbiol. 5, 44-50.
9. Bowling, S.A., Guo, A., Hui, C., Gordon, A.S., Klessig, D.F. and Dong, X. (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845-1857.
10. Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell, 9, 1573-1584.
11. Cao, H., Bowling, S.A., Gordon, A.S. and Dong, X. (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 6, 1583-1592.
12. Chang, J.H., Rathjen, J.P., Bernal, A.J., Staskawicz, B.J. and Michelmore, R.W. (2000) avrPto enhances growth and necrosis caused by Pseudomonas syringae pv. tomato in tomato lines lacking either Pto or Prf. Mol. Plant Microbe Interact. 13, 568-571.
13. Chen, Z., Kloek, A.P., Boch, J., Katagiri, F. and Kunkel, B.N. (2000) The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol. Plant Microbe Interact. 13, 1312-1321.
14. Clarke, J.D., Liu, Y., Klessig, D. and Dong, X. (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell, 10, 557-569.
15. 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.
16. Cornelis, G.R. and Van Gijsegem, F. (2000) Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54, 735-774.
17. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
18. Delaney, T.P., Uknes, S., Vernooij, B. et al. (1994) A central role for salicylic acid in plant disease resistance. Science, 266, 1247-1250.
19. Dong, X., Mindrinos, M., Davis, K.R. and Ausubel, F.M. (1991) Induction of Arabidopsis thaliana defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell, 3, 61-72.
20. Fouts, D.E., Abramovitch, R.B., Alfano, J.R. et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. USA, 99, 2275-2280.
21. Frye, C.A., Tang, D. and Innes, R.W. (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA, 98, 373-378.
22. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement for salicylic acid for the induction of systemic acquired resistance. Science, 261, 754-756.
23. Galan, J.E. and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science, 284, 1322-1328.
24. Gomez-Gomez, L. and Boller, T. (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7, 251-256.
25. Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Stattler, A., Innes, R.W. and Dangl, J.L. (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science, 269, 843-846.
26. Greenberg, J.T. and Vinatzer, B.A. (2003) Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6, 20-28.
27. Greenberg, J.T., Silverman, F.P. and Liang, H. (2000) Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics, 156, 341-350.
28. Guttman, D.S. and Greenberg, J.T. (2001) Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol. Plant Microbe Interact. 14, 145-155.
29. Guttman, D.S., Vinatzer, B.A., Sarkar, S.F., Ranall, M.V., Kettler, G. and Greenberg, J.T. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science, 295, 1722-1726.
30. Hauck, P., Thilmony, R. and He, S.Y. (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA, 100, 8577-8582.
31. Holub, E.B. and Beynon, J.L. (1997) Symbiology of mouse ear cress (Arabidopsis thaliana) and oomycetes. Adv. Bot. Res. 24, 228-273.
32. Kim, H.S. and Delaney, T.P. (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell, 14, 1469-1482.
33. Kunkel, B.N., Bent, A.F., Dahlbeck, D., Innes, R.W. and 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.
34. Lawton, K.A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., Staub, T. and Ryals, J. (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10, 71-82.
35. Lindgren, P.B., Peet, R.C. and Panopoulos, N.J. (1986) Gene cluster of Pseudomonas syringae pv. 'phaseolicola' controls pathogenicity of bean plants and hypersensitivity on nonhost plants. J. Bacteriol. 168, 512-522.
36. Mackey, D., Holt, B.F., Wiig, A. and Dangl, J.L. (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell, 108, 743-754.
37. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R. and Dangl, J.L. (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112, 379-389.
38. McDowell, J.M., Cuzick, A., Can, C., Beynon, J., Dangl, J.L. and Holub, E.B. (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J. 22, 523-529.
39. Nawrath, C. and Metraux, J. (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell, 11, 1393-1404.
40. Neff, M.M., Neff, J.D., Chory, J. and Pepper, A.E. (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J. 14, 387-392.
41. Niepold, F., Anderson, D. and Mills, D. (1985) Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. Proc. Natl. Acad. Sci. USA, 82, 406-410.
42. Nimchuk, Z., Rohmer, L., Chang, J.H. and Dangl, J.L. (2001) Knowing the dancer from the dance: R-gene products and their interactions with other proteins from host and pathogen. Curr. Opin. Plant Biol. 4, 288-294.
43. Rairdan, G.J., Donofrio, N.M. and Delaney, T.P. (2001) Salicylic acid and NIM1/NPR7-independent gene induction by incompatible Peronospora parasitica in Arabidopsis. Mol. Plant Microbe Interact. 14, 1235-1246.
44. Ritter, C. and Dangl, J.L. (1996) Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell, 8, 251-257.
45. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H. and Hunt, M.D. (1996) Systemic acquired resistance. Plant Cell, 8, 1809-1819.
46. Shan, L., He, P., Zhou, J. and Tang, X. (2000) A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. Mol. Plant Microbe Interact. 13, 592-598.
47. Shapiro, A.D. and Zhang, C. (2001) The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis. Plant Physiol. 127, 1089-1101.
48. Tang, D. and Innes, R.W. (2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J. 32, 975-983.
49. Tsiamis, G., Mansfield, J.W., Hockenhull, R. et al. (2000) Cultivar-specific avirulence and virulence functions assigned to avrPphF. Pseudomonas syringae pv. phaseolicola, the cause of bean haloblight disease. EMBO J. 19, 3204-3214.
50. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E. and Ryals, J. (1992) Acquired resistance in Arabidopsis. Plant Cell, 4, 645-656.
51. Varet, A., Parker, J., Tornero, P., Nass, N., Nurnberger, T., Dangl, J.L., Scheel, D. and Lee, J. (2002) NHL25 and NHL3, two NDR1/HIN1-1ike genes in Arabidopsis thaliana with potential role(s) in plant defense. Mol. Plant Microbe Interact. 15, 608-616.
52. Whalen, M., Innes, R., Bent, A. and Staskawicz, B. (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis thaliana and a bacterial gene determining avirulence on both Arabidopsis and soybean. Plant Cell, 3, 49-59.
53. White, R.F. (1979) Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology, 99, 401-412.
54. Wildermuth, M.C., Dewdney, J., Wu, G. and Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature, 414, 562-565.
55. Yamada, T. (1993) The role of auxin in plant-disease development. Annu. Rev. Phytopathol. 31, 253-273.
56. Yu, G.L., Katagiri, F. and Ausubel, F.M. (1993) Arabidopsis mutations at the RPS2 locus result in loss of resistance to Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Mol. Plant Microbe Interact. 6, 434-443.
57. Yu, I., Parker, J. and Bent, A.F. (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl. Acad. Sci. USA, 95, 7819-7824.
58. Zwiesler-Vollick, J., Plovanich-Jones, A., Nomura, K., Bandyopadhyay, S., Joardar, V., Kunkel, B.N. and He, S.Y. (2002) Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45, 1207-1218.