Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: Convergence of resistance gene, elicitor, wound, and salicylate responses

Plant Cell

Volumn 11, Issue 2, 1999, Pages 273-287

  Romeis, Tina ^a   Piedras, Pedro ^a   Zhang, Shuqun ^b   Klessig, Daniel F ^b   Hirt, Heribert ^c   Jones, Jonathan D G ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b RUTGERS UNIVERSITY   (United States)

^c Vienna Biocenter   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0033078703     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.11.2.273     Document Type: Article

References (71)

1. Ádám, A.L., Pike, S., Hoyos, M.E., Stone, J.M., Walker, J.C., and Novacky, A. (1997). Rapid and transient activation of a myelin basic protein kinase in tobacco leaves treated with harpin from Erwinia amylovora. Plant Physiol. 115, 853-861.
2. Bögre, L., Ligterink, W., Heberle-Bors, E., and Hirt, H. (1996). Mechanosensors in plants. Nature 383, 489-490.
3. Bögre, L., Ligterink, W., Meskiene, I., Barker, P.J., Heberle-Bors, E., Huskisson, N.S., and Hirt, H. (1997). Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell 9, 75-83.
4. Chandra, S., and Low, P.S. (1995). Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells. Proc. Natl. Acad. Sci. USA 92, 4120-4123.
5. Church, G.M., and Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. USA 81, 1991-1995.
6. Cohen, P. (1997). The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol. 7, 353-361.
7. Dean, C., van den Elzen, P., Tamaki, S., Dunsmuir, P., and Bedbrook, J. (1985). Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multi-gene family. EMBO J. 4, 3055-3061.
8. Després, C., Subramaniam, R., Matton, D.P., and Brisson, N. (1995). The activation of the potato PR-10a gene requires the phosphorylation of the nuclear factor PBF-1. Plant Cell 7, 589-598.
9. De Wit, P.J.G.M. (1997). Pathogen avirulence and plant resistance: A key role for recognition. Trends Plant Sci. 2, 452-458.
10. De Wit, P.J.G.M., and Spikman, G. (1982). Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiol. Plant Pathol. 21, 1-11.
11. Dietrich, A., Mayer, J.E., and Hahlbrock, K. (1990). Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. J. Biol. Chem. 265, 6360-6368.
12. Dröge-Laser, W., Kaiser, A., Lindsay, W.P., Halkier, B.A., Loake, G.J., Doerner, P., Dixon, R.A., and Lamb, C. (1997). Rapid stimulation of a soybean protein-serine kinase which phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J. 16, 726-738.
13. Ellis, J., and Jones, D. (1998). Structure and function of proteins controlling strain-specific pathogen resistance in plants. Curr. Opin. Plant Sci. 1, 288-293.
14. Felix, G., Grosskopf, D.G., Regenass, M., and Boller, T. (1991). Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc. Natl. Acad. Sci. USA 88, 8831-8834.
15. 33P] phosphate. Proc. Natl. Acad. Sci. USA 91, 952-956.
16. Flor, H.H. (1971). Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275-296.
17. Gotoh, Y., Nishida, E., Yamashita, T., Hoshi, M., Kawakami, M., and Sakai, H. (1990). Microtubule-associated protein (MAP) kinase activated by nerve growth factor and epidermal growth factor in PC12 cells. Eur. J. Biochem. 193, 661-669.
18. Groom, Q.J., Torres, M.A., Fordham-Skelton, A.P., Hammond-Kosack, K.E., Robinson, N.J., and Jones, J.D.G. (1996). rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J. 10, 515-522.
19. Grosskopf, D.G., Felix, G., and Boller, T. (1990). K-252a inhibits the response of tomato cells to fungal elicitors in vivo and their microsomal protein kinase in vitro. FEBS Lett. 275, 177-180.
20. Hammond-Kosack, K.E., and Jones, J.D.G. (1997). Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 575-607.
21. Hammond-Kosack, K.E., Harrison, K., and Jones, J.D.G. (1994). Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9. Proc. Natl. Acad. Sci. USA 91, 10445-10449.
22. Hammond-Kosack, K.E., Tang, S., Harrison, K., and Jones, J.D.G. (1998). The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product Avr9. Plant Cell 10, 1251-1266.
23. 2 and NADPH oxidase. Biochem. J. 326, 867-876.
24. Herskowitz, I. (1995). MAP kinase pathways in yeast: For mating and more. Cell 80, 187-197.
25. Hirt, H. (1997). Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci. 2, 11-15.
26. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA 94, 4800-4805.
27. Jonak, C., Páy, A., Bögre, L., Hirt, H., and Heberle-Bors, E. (1993). The plant homologue of MAP kinase is expressed in a cell cycle-dependent and organ-specific manner. Plant J. 3, 611-617.
28. Jonak, C., Kiegerl, S., Ligterink, W., Barker, P.J., Huskisson, N.S., and Hirt, H. (1996). Stress signaling in plants: A mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. USA 93, 11274-11279.
29. Jones, D.A., Thomas, C.M., Hammond-Kosack, K.E., Balint-Kurti, P.J., and Jones, J.D.G. (1994). Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266, 789-793.
30. 2+ binding motifs. Plant Cell 10, 255-266.
31. Lamb, C., and Dixon, R.A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
32. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
33. Ligterink, W., Kroj, T., zur Nieden, U., Hirt, H., and Scheel, D. (1997). Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276, 2054-2057.
34. 2 is phosphorylated and activated by MAP kinase. Cell 72, 269-278.
35. Mackintosh, C., Lyon, G.D., and Mackintosh, R.W. (1994). Protein phosphatase inhibitors activate anti-fungal defense responses of soybean cotyledons and cell cultures. Plant J. 5, 137-147.
36. Madhani, H.D., and Fink, G.R. (1998). The riddle of MAP kinase signaling specificity. Trends Genet. 14, 151-155.
37. Madhani, H.D., Styles, C.A., and Fink, G.R. (1997). MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91, 673-689.
38. Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D., and Tanksley, S.D. (1993). Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262, 1432-1436.
39. Mizoguchi, T., Hayashida, N., Yamaguchi-Shinozaki, K., Kamada, H., and Shinozaki, K. (1995). Two genes that encode ribosomal-protein S6 kinase homologs are induced by cold or salinity stress in Arabidopsis thaliana. FEBS Lett. 358, 199-204.
40. Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., Yamaguchi-Shinozaki, K., Matsumota, K., and Shinozaki, K. (1996). A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93, 765-769.
41. Mizoguchi, T., Ichimura, K., and Shinozaki, K. (1997). Environmental stress response in plants: The role of mitogen-activated protein kinases. Trends Biotechnol. 15, 15-19.
42. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
43. Nishida, E., and Gotoh, Y. (1993). The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci. 18, 128-131.
44. Nishina, H., Fischer, K.D., Radvanyi, L., Shahinian, A., Hakem, R., Rubie, E.A., Bernstein, A., Mak, T.W., Woodgett, J.R., and Penninger, J.M. (1997). Stress-signaling kinase Sek1 protects thymocytes from apoptosis mediated by CD95 and CD3. Nature 385, 350-353.
45. Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K., and Scheel, D. (1994). High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78, 449-460.
46. Piedras, P., Hammond-Kosack, K.E., Harrison, K., and Jones J.D.G. (1998). Rapid, Cf-9 and Avr9-dependent, production of active oxygen species in tobacco suspension cultures. Mol. Plant-Microbe Interact. 11, 1155-1166.
47. Raingeaud, J., Whitmarsh, A.J., Barrett, T., Derijard, B., and Davis, R.J. (1996). MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol. 16, 1247-1255.
48. Rushton, P.J., and Somssich, I.E. (1998). Transcriptional control of plant genes responsive to pathogens. Curr. Opin. Plant Biol. 1, 311-315.
49. Scheel, D. (1998). Resistance response physiology and signal transduction. Curr. Opin. Plant Biol. 1, 305-310.
50. 2+ and protein-kinase activity. Planta 187, 136-141.
51. Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavalle, D.T., Michelmore, R.W., and Staskawicz, B.J. (1996). Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274, 2063-2065.
52. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., and Ohashi, Y. (1995). Tobacco MAP kinase: A possible mediator in wound signal transduction pathways. Science 270, 1988-1992.
53. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A., and Lamb, C. (1997). Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261-270.
54. Somssich, I.E. (1997). MAP kinases and plant defence. Trends Plant Sci. 2, 406-408.
55. Song, W.-Y., Wang, G.-L., Chen, L.-L., Kim, H.-S., Pi, L.-Y., Holsten, T., Gardner, J., Wang, B., Zhai, W.-X., Zhu, L.-H., Fauquet, C., and Ronald, P. (1995). A receptor kinase-like protein encoded by the rice disease resistance gene Xa21. Science 270, 1804-1806.
56. Staskawicz, B.J., Ausubel, F.M., Baker, B.J., Ellis, J.G., and Jones, J.D.G. (1995). Molecular genetics of plant disease resistance. Science 268, 661-667.
57. Stratman, J.W., and Ryan, C.A. (1997). Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc. Natl. Acad. Sci. USA 94, 11085-11089.
58. Subramaniam, R., Després, C., and Brisson, N. (1997). A functional homolog of mammalian protein kinase C participates in the elicitor-induced defense response in potato. Plant Cell 9, 653-664.
59. Suzuki, K., and Shinshi, H. (1995). Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with a fungal elicitor. Plant Cell 7, 639-647.
60. Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y., and Martin, G.M. (1996). Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274, 2060-2063.
61. phox). Plant J. 14, 365-370.
62. Umemoto, N., Kakitani, M., Iwamatsu, A., Yoshikawa, N., Yamaoka, N., and Ishida, I. (1997). The structure and function of a soybean β-glucan-elicitor-binding protein. Proc. Natl. Acad. Sci. USA 94, 1029-1034.
63. Usami, S., Banno, H., Ito, Y., Nishihama, R., and Machida, Y. (1995). Cutting activates a 46-kilodalton protein kinase in plants. Proc. Natl. Acad. Sci. USA 92, 8660-8664.
64. Van den Ackerveken, G.F.J.M., Van Kan, J.A.L., and De Wit, P.J.G.M. (1992). Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J. 2, 359-366.
65. Van den Ackerveken, G.F.J.M., Vossen, P., and De Wit, P.J.G.M. (1993). The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol. 103, 91-96.
66. Viard, M.-P., Martin, F., Pugin, A., Ricci, P., and Blein, J.-P. (1994). Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein. Plant Physiol. 104, 1245-1249.
67. Yang, Y., Shah, J., and Klessig, D.F. (1997). Signal perception and transduction in plant defense responses. Genes Dev. 11, 1621-1639.
68. Zhang, S., and Klessig, D.F. (1997). Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9, 809-824.
69. Zhang, S., and Klessig, D.F. (1998a). N resistance gene-mediated de novo synthesis and activation of a tobacco MAP kinase by TMV infection. Proc. Natl. Acad. Sci. USA 95, 7433-7438.
70. Zhang, S., and Klessig, D.F. (1998b). The tobacco wounding-activated MAP kinase is encoded by SIPK. Proc. Natl. Acad. Sci. USA 95, 7225-7230.
71. Zhang, S., Du, H., and Klessig, D.F. (1998). Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10, 435-449.