Two MARK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato

Plant Journal

Volumn 36, Issue 6, 2003, Pages 905-917

  Ekengren, Sophia K ^a   Liu, Yule ^b   Schiff, Michael ^b   Dinesh Kumar, S P ^b   Martin, Gregory B ^a,c  

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

^b YALE UNIVERSITY   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

Plant immunity; Pseudomonas syringae; Pto kinase

Indexed keywords

BACTERIA; BIODIVERSITY; DISEASE CONTROL; ENZYME KINETICS; GROWTH KINETICS; PROTEINS; VIRUSES;

TRANSDUCTION PATHWAYS;

PLANTS (BOTANY);

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

PRIMER DNA; PROTEIN SERINE THREONINE KINASE; PTO PROTEIN, LYCOPERSICON; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ARTICLE; GENE SILENCING; GENETICS; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION;

BASE SEQUENCE; DNA PRIMERS; GENE SILENCING; IMMUNITY, NATURAL; MAP KINASE SIGNALING SYSTEM; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PSEUDOMONAS SYRINGAE; TRANSCRIPTION FACTORS;

EID: 0346687514     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01944.x     Document Type: Article

References (83)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R-gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA, 95, 10306-10311.
2. Agrawal, G.K., Iwahashi, H. and Rakwal, R. (2003) Rice MAPKs. Biochem. Biophys. Res. Commun. 302, 171-180.
3. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977-983.
4. Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K. and Schulze-Lefert, P. (2002) The RAR1 interactor SGT1, an essential component of R-gene-triggered disease resistance. Science, 295, 2073-2076.
5. Baulcombe, D.C. (1999) Fast forward genetics based on virus-induced gene silencing. Curr. Opin. Plant Biol. 2, 109-113.
6. Baulcombe, D.C. (2002) RNA silencing. Curr. Biol. 12, R82-R84.
7. Bittner-Eddy, P.D. and Beynon, J.L. (2001 ) The Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid. Mol. Plant-Microbe Interact. 14, 416-421.
8. Bogdanove, A.J. (2002) Protein-protein interactions in pathogen recognition by plants. Plant Mol. Biol. 50, 981-989.
9. Bogdanove, A.J. and Martin, G.B. (2000) AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc. Natl. Acad. Sci. USA, 97, 8836-8840.
10. Calderini, O., Glab, N., Bergounioux, C., Heberle-Bors, E. and Wilson, C. (2001) A novel tobacco mitogen-activated protein (MAP) kinase kinase, NtMEK1, activates the cell cycle regulated p43Ntf6 MAP kinase. J. Biol. Chem. 276, 18139-18145.
11. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell, 88, 57-63.
12. Century, K.S. and Staskawicz, B.J. (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science, 278, 1963-1965.
13. Chandra, S., Martin, G.B. and Low, P.S. (1996) The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Proc. Natl. Acad. Sci. USA, 93, 13393-13397.
14. Chang, L. and Karin, M. (2001) Mammalian MAP kinase signaling cascades. Nature, 410, 37-40.
15. Chen, W., Provart, N.J., Glazebrook, J. et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell, 14, 559-574.
16. Dangl, J.L. and Jones, J.D.G. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
17. Davis, R. (2000) Signal transduction by the JNK group of MAP kinases. Cell, 103, 239-252.
18. Despres, C., DeLong, C., Glaze, S., Liu, E. and Fobert, P.R. (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell, 12, 279-290.
19. Despres, C., Chubak, C., Rochon, A., Clark, R., Bethune, T., Desveaux, D. and Fobert, P.R. (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell, 15, 2181-2191.
20. Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D. (2000) cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell, 12, 963-977.
21. Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
22. Fan, W.H. and Dong, X. (2002) In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell, 14, 1377-1389.
23. Feys, B.J. and Parker, J.E. (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449-455.
24. Feys, B.J.F., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 6, 751-759.
25. Gu, Y.-Q., Yang, C., Thara, V.K., Zhou, J. and Martin, G.B, (2000) Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell, 12, 771-785.
26. Gu, Y.-Q., Wildermuth, M.C., Chakravarthy, S., Loh, Y.-T., Yang, C., He, X., Han, Y. and Martin, G.B. (2002) Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell, 14, 817-831.
27. Hammond-Kosack, K. and Jones, J.D.G. (2000) Response to plant pathogens. In Biochemistry and Molecular Biology of Plants (Buchanan, B., Gruissem, D. and Jones, R., eds). Rockville, MD: American Society of Plant Physiologists, pp. 1102-1156.
28. He, P., Warren, R.F., Zhao, T., Shan, L., Tang, X. and Zhou, J.M. (2001) Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 12, 1453-1457.
29. Israel, A. (2003) Signal transduction: a regulator branches out. Nature, 423, 596-598.
30. Jackson, A.L., Bartz, S.R., Schelter, J., Kobayashi, S.V., Burchard, J., Mao, M., Li, B., Cavet, G. and Linsley, P.S. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21, 635-637.
31. Jia, Y. and Martin, G.B. (1999) Rapid transcript accumulation of pathogenesis-related genes during an incompatible interaction in bacterial speck disease-resistant tomato plants. Plant Mol. Biol. 40, 455-465.
32. Jin, H., Axtell, M.J., Dahlbeck, D., Ekwenna, O., Zhang, S., Staskawicz, B. and Baker, B. (2002) NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. Dev. Cell, 3, 291-297.
33. Jin, H., Liu, Y., Yang, K.-Y., Baker, B. and Zhang, S. (2003) Function of a mitogen-activated protein kinase pathway in N-gene mediated resistance in tobacco. Plant J. 33, 719-731.
34. Johnson, C., Boden, E. and Arias, J. (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell, 15, 1846-1858.
35. Kachroo, P., Yoshioka, K., Shah, J., Dooner, H.K. and Klessig, D.F. (2000) Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell, 12, 677-690.
36. Kim, H.S. and Delaney, T.P. (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/ NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J. 32, 151-163.
37. Kim, Y.J., Lin, N.C. and Martin, G.B. (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell, 109, 589-598.
38. Kumigai, M.H., Donson, J., della-Cioppa, G., Harvey, D., Hanley, K. and Grill, L.K. (1995) Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc. Natl. Acad. Sci. USA, 92, 1679-1683.
39. Kunkel, B.N. and Brooks, D.M. (2002) Cross-talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325-331.
40. Lamb, C. and Dixon, R.A. (1997) The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
41. Liu, Y., Schiff, M. and Dinesh-Kumar, S.P. (2002a) Virus-induced gene silencing in tomato. Plant J. 31, 777-786.
42. Liu, Y., Schiff, M., Marathe, R. and Dinesh-Kumar, S.P. (2002b) Tobacco Rar1, EDS1 and NPR1/NIM1-like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30, 415-429.
43. Liu, Y., Schiff, M., Serino, G., Deng, X.-W. and Dinesh-Kumar, S.P. (2002c) Role of SCF ubiquitin-ligase and the COP9 signalosome in the N-gene-mediated resistance response to tobacco mosaic virus. Plant Cell, 14, 1483-1496.
44. 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.
45. Martin, G.B., Bogdanove, A.J. and Sessa, G. (2003) Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54, 23-61.
46. McDowell, J.M. and Dangl, J.L. (2000) Signal transduction in the plant immune response. Trends Biochem. Sci. 25, 79-82.
47. McDowell, J.M., Cuzick, A., Can, C., Beynon, J.L., 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.
48. Mysore, K.S., Crasta, O.R., Tuori, R.P., Folkerts, O., Swirsky, P.B. and Martin, G.B. (2002) Comprehensive transcript profiling of Pto-and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J. 32, 299-315.
49. Niggewegg, R., Thurow, C., Kegler, C. and Gatz, C. (2000a) Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid-and auxin-inducible expression of as-1-containing target promoters. J. Biol. Chem. 275, 19897-19905.
50. Niggewegg, R., Thurow, C., Weigel, R., Pfitzner, U. and Gate, C. (2000b) Tobacco TGA factors differ with respect to interaction with NPR1, activation potential and DNA-binding properties. Plant Mol. Biol. 42, 775-788.
51. Ohme-Takagi, M., Suzuki, K. and Shinshi, H. (2000) Regulation of ethylene-induced transcription of defense genes. Plant Cell Physiol. 41, 1187-1192.
52. Peart, J.R., Cook, G., Feys, B.J., Parker, J.E. and Baulcombe, D.C. (2002a) An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. Plant J. 29, 569-579.
53. Peart, J.R., Lu, R., Sadanandom, A. et al. (2002b) Ubiquitin ligase-associated protein SGT1 is required for host and non-host disease resistance in plants. Proc. Natl. Acad. Sci. USA, 99, 10865-10869.
54. Pedley, K.P. and Martin, G.B. (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease. Annu. Rev. Phytopathol. 41, 215-243.
55. Rairdan, G.J. and Delaney, T.P. (2002) Role of salicylic acid and Nim1/NPR1 in race-specific resistance in Arabidopsis. Genetics, 161, 803-811.
56. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D. (1999) Rapid avr-9-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, 11, 273-288.
57. Romeis, T., Ludwig, A.A., Martin, R. and Jones, J.D. (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20, 5556-5567.
58. Ronald, P.C., Salmeron, J.M., Carland, F.M. and 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.
59. Ryals, J., Weymann, K., Lawton, K. et al. (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IkB. Plant Cell, 9, 425-439.
60. Salmeron, J.M., Oldroyd, G.E.D., Rommens, C.M.T., Scofield, S.R., Kim, H.-S., Lavelle, D.T., Dahlbeck, D. and Staskawicz, B.J. (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell, 86, 123-133.
61. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA, 97, 11655-11660.
62. Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavelle, 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.
63. 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.
64. Shen, Q.H., Zhou, F., Bieri, S., Haizel, T., Shirasu, K. and Schulze-Lefert, P. (2003) Recognition specificity and RAR1/SGT1 dependence in barley Mla disease-resistance genes to the powdery mildew fungus. Plant Cell, 15, 732-744.
65. Shirasu, K. and Schulze-Lefert, P. (2003) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci. 8, 252-258.
66. Shirasu, K., Lahaye, T., Tan, M.W., Zhou, F., Azevedo, C. and Schulze-Lefert, P. (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell, 99, 355-366.
67. Soyano, T., Nishihama, R., Morikiyo, K., Ishikawa, M. and Machida, Y. (2003) NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MARK cascade and is required for plant cytokinesis. Genes Dev. 17, 1055-1067.
68. Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y. and Martin, G.B. (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science, 274, 2060-2063.
69. Thara, V.K., Tang, X., Gu, Y.Q., Martin, G.B. and Zhou, J.M. (1999) Pseudomonas syringae pv. tomato induces the expression of tomato EREBP-like genes Pti4 and Pti5 independent of ethylene, salicylate and jasmonate. Plant J. 20, 475-483.
70. Thomas, C.L., Jones, L., Baulcombe, D.C. and Maule, A.J. (2001) Size constraints for targeting post-transcriptional gene silencing and for RNA-directed methylation in Nicotiana benthamiana using potato virus X vector. Plant J. 25, 417-425.
71. Thomma, B., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A. and Broekaert, W.F. (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA, 95, 15107-15111.
72. Tör, M., Yemm, A. and Holub, E. (2003) The role of proteolysis in R-gene-mediated defence in plants. Mol. Plant Pathol. 4, 287-296.
73. Widmann, C., Gibson, S., Jarpe, M.B. and Johnson, G.L. (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180.
74. Wu, K., Tian, L., Hollingworth, J., Brown, D.C. and Miki, B. (2002) Functional analysis of tomato Pti4 in Arabidopsis. Plant Physiol. 128, 30-37.
75. Xu, L.H., Liu, F.Q., Lechner, E., Genschik, P., Crosby, W.L., Ma, H., Peng, W., Huang, D.F. and Xie, D.X. (2002) The SCF (COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell, 14, 1919-1935.
76. Zhang, S. and Klessig, D.F. (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell, 9, 809-824.
77. Zhang, S. and Klessig, D.F. (1998) Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl. Acad. Sci. USA, 95, 7433-7438.
78. Zhang, S. and Klessig, D.F. (2001) MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520-527.
79. Zhang, Y.L., Fan, W.H., Kinkema, M., Li, X. and Dong, X. (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. USA, 96, 6523-6528.
80. Zhou, J.-M., Loh, Y.-T., Bressan, R.A. and Martin, G.B. (1995) The tomato gene Pti1 encodes a serine-threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell, 83, 925-935.
81. Zhou, J., Tang, X. and Martin, G.B. (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J. 16, 3207-3218.
82. Zhou, J., Tang, X., Frederick, R. and Martin, G. (1998) Pathogen recognition and signal transduction by the Pto kinase. J. Plant Sci. Res. 111, 353-356.
83. Zhou, J.-M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J. and Klessig, D.F. (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant-Microbe Interact. 13, 191-202.