Genetic and molecular requirements for function of the Pto/Prf effector recognition complex in tomato and Nicotiana benthamiana

Plant Journal

Volumn 51, Issue 6, 2007, Pages 978-990

  Balmuth, Alexi ^a   Rathjen, John P ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

Author keywords

avrPto; avrPtoB; N. benthamiana; Prf; Pto; Tomato

Indexed keywords

GENOMIC PROMOTER; PHENOTYPES;

BACTERIA; MOLECULAR STRUCTURE; PLANTS (BOTANY); PROTEINS;

GENETIC ENGINEERING;

AVRPTO PROTEIN, PSEUDOMONAS SYRINGAE; BACTERIAL PROTEIN; PRF PROTEIN, LYCOPERSICON ESCULENTUM; PROTEIN SERINE THREONINE KINASE; PTO PROTEIN, LYCOPERSICON; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PHENOTYPE; PHYSIOLOGY; PROMOTER REGION; PSEUDOMONAS SYRINGAE; TOBACCO; TOMATO; TRANSGENIC PLANT;

BACTERIAL PROTEINS; IMMUNITY, NATURAL; LYCOPERSICON ESCULENTUM; PHENOTYPE; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; PSEUDOMONAS SYRINGAE; TOBACCO;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; NICOTIANA BENTHAMIANA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; SOLANUM;

EID: 34548489408     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03199.x     Document Type: Article

References (37)

1. Abramovitch, R.B., Kim, Y.-J., Chen, S., Dickman, M.B. Martin, G.B. (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60 69.
2. Abramovitch, R.B., Janjusevic, R., Stebbins, C.E. Martin, G.B. (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc. Natl Acad. Sci. USA, 103, 2851 2856.
3. Ade, J., DeYoung, B.J., Golstein, C. Innes, R.W. (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc. Natl Acad. Sci. USA, 104, 2531 2536.
4. Andriotis, V.M. Rathjen, J.P. (2006) The Pto kinase of tomato, which regulates plant immunity, is repressed by its myristoylated N terminus. J. Biol. Chem. 281, 26578 26586.
5. Carland, F. Staskawicz, B. (1993) Genetic characterization of the Pto locus of tomato: semi-dominance and cosegregation of resistance to Pseudomonas syringae pathovar tomato and sensitivity to the insecticide Fenthion. Mol. Gen. Genet. 239, 17 27.
6. Chang, J.H., Rathjen, J.P., Bernal, A.J., Staskawicz, B.J. 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.
7. Chang, J.H., Tai, Y.S., Bernal, A.J., Lavelle, D.T., Staskawicz, B.J. Michelmore, R.W. (2002) Functional analyses of the Pto resistance gene family in tomato and the identification of a minor resistance determinant in a susceptible haplotype. Mol. Plant Microbe Interact. 15, 281 291.
8. Day, B., Dahlbeck, D., Huang, J., Chisholm, S.T., Li, D. Staskawicz, B.J. (2005) Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell, 17, 1292 1305.
9. German, M.A., Kandel-Kfir, M., Swarzberg, D., Matsevitz, T. Granot, D. (2003) A rapid method for the analysis of zygosity in transgenic plants. Plant Sci. 164, 183 187.
10. Hann, D.R. Rathjen, J.P. (2007) Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J. 49, 607 618.
11. He, P., Shan, L., Lin, N.C., Martin, G.B., Kemmerling, B., Nurnberger, T. Sheen, J. (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell, 125, 563 575.
12. Janjusevic, R., Abramovitch, R.B., Martin, G.B. Stebbins, C.E. (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science, 311, 222 226.
13. Jones, J.D. Dangl, J.L. (2006) The plant immune system. Nature, 444, 323 329.
14. Keen, N.T., Tamaki, S., Kobayashi, D. Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene, 70, 191 197.
15. Kim, Y.J., Lin, N.C. Martin, G.B. (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell, 109, 589 598.
16. Leipe, D., Koonin, E. Aravind, L. (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J. Mol. Biol. 343, 1 28.
17. Li, J., Shan, L., Zhou, J. Tang, X. (2002) Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol. Plant Microbe Interact. 15, 654 661.
18. Loh, Y.T., Zhou, J. Martin, G.B. (1998) The myristylation motif of Pto is not required for disease resistance. Mol. Plant Microbe Interact. 11, 572 576.
19. Lu, R., Malcuit, I., Moffett, P., Ruiz, M.T., Peart, J., Wu, A.-J., Rathjen, J.P., Bendahmane, A., Day, L. Baulcombe, D.C. (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 22, 5690 5699.
20. McCormick, S., Niedermeyer, J., Fry, J., Barnason, A., Horsch, R. Fraley, R. (1986) Leaf disk transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens. Plant Cell Rep. 5, 81 84.
21. Mucyn, T.S., Clemente, A., Andriotis, V.M., Balmuth, A.L., Oldroyd, G.E., Staskawicz, B.J. Rathjen, J.P. (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell, 18, 2792 2806.
22. Oldroyd, G.E.D. Staskawicz, B.J. (1998) Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA, 95, 10300 10305.
23. Pedley, K.F. Martin, G.B. (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41, 215 243.
24. Rathjen, J.P., Chang, J.H., Staskawicz, B.J. Michelmore, R.W. (1999) Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of avrPto. EMBO J. 18, 3232 3240.
25. Rommens, C.M.T., Salmeron, J.M., Oldroyd, G.E.D. Staskawicz, B.J. (1995) Intergeneric transfer and functional expression of the tomato disease resistance gene Pto. Plant Cell, 7, 1537 1544.
26. 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.
27. Salmeron, J.M. Staskawicz, B.J. (1993) Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato. Mol. Gen. Genet. 239, 6 16.
28. Salmeron, J.M., Barker, S.J., Carland, F.M., Mehta, A.Y. Staskawicz, B.J. (1994) Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell, 6, 511 520.
29. Shan, L., Thara, V.K., Martin, G.B., Zhou, J.-M. Tang, X. (2000a) The Pseudomonas AvrPto protein is differentially recognised by tomato and tobacco and is localised to the plant plasma membrane. Plant Cell, 12, 2323 2337.
30. Shan, L.B., He, P., Zhou, J.M. Tang, X.Y. (2000b) A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. Mol. Plant Microbe Interact. 13, 592 598.
31. Tang, X., Xie, M., Kim, Y.J., Zhou, J., Klessig, D.F. Martin, G.B. (1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell, 11, 15 30.
32. Thilmony, R.L., Chen, Z., Bressan, R.A. Martin, G.B. (1995) Expression of the tomato Pto gene in tobacco enhances resistance to Pseudomonas syringae pv tabaci expressing avrPto. Plant Cell, 7, 1529 1536.
33. Tobias, C.M., Oldroyd, G.E.D., Chang, J.H. Staskawicz, B.J. (1999) Plants expressing the Pto disease resistance gene confer resistance to recombinant PVX containing the avirulence gene AvrPto. Plant J. 17, 41 50.
34. de Torres, M., Mansfield, J.W., Grabov, N., Brown, I.R., Ammouneh, H., Tsiamis, G., Forsyth, A., Robatzek, S., Grant, M. Boch, J. (2006) Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant J. 47, 368 382.
35. de Vries, J.S., Andriotis, V.M.E., Wu, A.-J. Rathjen, J.P. (2006) Tomato Pto encodes a functional N-myristoylation motif that is required for signal transduction in Nicotiana benthamiana. Plant J. 45, 31 45.
36. Wu, A.-J., Andriotis, V.M.E., Durrant, M.C. Rathjen, J.P. (2004) A patch of surface-exposed residues mediates negative regulation of immune signaling by tomato Pto kinase. Plant Cell, 16, 2809 2821.
37. Xiao, F., Lu, M., Li, J., Zhao, T., Yi, S.Y., Thara, V.K., Tang, X. Zhou, J.-M. (2003) Pto mutants differentially activate Prf-dependent, avrPto-independent resistance and gene-for-gene resistance. Plant Physiol. 131, 1239 1249.