The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants

Plant Journal

Volumn 49, Issue 5, 2007, Pages 899-909

  Seo, Shigemi ^a,b   Katou, Shinpei ^a,b   Seto, Hideharu ^c   Gomi, Kenji ^a,b   Ohashi, Yuko ^a,b  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b Basic Research Activities for Innovative Biosciences   (Japan)

^c RIKEN   (Japan)

Author keywords

Jasmonic acid; Mitogen activated protein kinase; Salicylic acid; Wound signal transduction

Indexed keywords

JASMONIC ACID; MITOGEN-ACTIVATED PROTEIN KINASE; WOUND SIGNAL TRANSDUCTION;

BIOSYNTHESIS; CARBOXYLIC ACIDS; PLANTS (BOTANY); RNA; TOBACCO;

ENZYMES;

CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; GLUCOSIDE; JASMONIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; SALICYLIC ACID DERIVATIVE; SALICYLIC ACID GLUCOSIDE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TOBACCO; TRANSGENIC PLANT;

CYCLOPENTANES; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSIDES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SALICYLIC ACIDS; TOBACCO;

BIOSYNTHESIS; CARBOXYLIC ACIDS; GENES; PLANTS;

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

EID: 33847110282     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.03003.x     Document Type: Article

References (63)

1. Baldwin, I.T., Zhang, Z.-P., Diab, N., Ohnmeiss, T.E., McCloud, E.S., Lynds, G.Y. and Schmelz, E.A. (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta, 201, 397-404.
2. 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.
3. Bostock, R.M. and Stermer, B.A. (1989) Perspectives on wound healing in resistance to pathogens. Annu. Rev. Plant Physiol. 27, 343-371.
4. Bowles, D.J. (1990) Defence-related proteins in higher plants. Annu. Rev. Biochem. 59, 873-907.
5. Brederode, F.T., Linthorst, H.J.M. and Bol, J.F. (1991) Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol. Biol. 17, 1117-1125.
6. de Bruxelles, G.L. and Roberts, M.R. (2001) Signals regulating multiple responses to wounding and herbivores. Crit. Rev. Plant Sci. 20, 487-521.
7. Conconi, A., Miquel, M., Browse, J.A. and Ryan, C.A. (1996) Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant Physiol. 111, 797-803.
8. Creelman, R.A. and Mullet, J.E. (1997) Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 355-381.
9. Creelman, R.A., Tierney, M.L. and Mullet, J.E. (1992) Jasmonic acid/ methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc. Natl Acad. Sci. USA, 89, 4938-4941.
10. Farmer, E.E. and Ryan, C.A. (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell, 4, 129-134.
11. Farmer, E.E., Weber, H. and Vollenweider, S. (1998) Fatty acid signaling in Arabidopsis. Planta, 206, 167-174.
12. Gomi, K., Ogawa, D., Katou, S. et al. (2005) A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol. 46, 1902-1914.
13. Holley, S.R., Yalamanchili, R.D., Moura, D.S., Ryan, C.A. and Stratmann, J.W. (2003) Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol. 132, 1728-1738.
14. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science, 227, 1229-1231.
15. Howe, G.A. (2004) Jasmonates as signals in the wound response. J. Plant Growth Regul. 23, 223-237.
16. Huang, X., Stettmaier, K., Michel, C., Hutzler, P., Mueller, M.J. and Durner, J. (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Plant Cell, 218, 938-946.
17. Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T. and Shinozaki, K. (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24, 1-13.
18. Jefferson, R.A., Burgess, S.M. and Hirsh, D. (1986) β-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc. Natl Acad. Sci. USA, 83, 8447-8451.
19. Kanzaki, H., Saitoh, H., Ito, A., Fujisawa, S., Kamoun, S., Katou, S., Yoshioka, H. and Terauchi, R. (2003) Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4, 383-391.
20. Kariola, T., Brader, G., Li, J. and Palva, E.T. (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell, 17, 282-294.
21. Katou, S., Karita, E., Yamakawa, H., Seo, S., Mitsuhara, I., Kuchitsu, K. and Ohashi, Y. (2005a) Catalytic activation of the plant MAPK phosphatase NtMKP1 by its physiological substrate salicylic acid-induced protein kinase, but not by calmodulins. J. Biol. Chem. 280, 39569-39581.
22. Katou, S., Yoshioka, H., Kawakita, K., Rowland, O., Jones, J.D.G., Mori, H. and Doke, N. (2005b) Involvement of PPS3 phosphorylated by elicitor-responsive mitogen-activated protein kinases in the regulation of plant cell death. Plant Physiol. 139, 1914-1926.
23. Kim, C.Y., Liu, Y., Thorne, E.T., Yang, H., Fukushige, H., Gassmann, W., Hildebrand, D., Sharp, R.E. and Zhang, S. (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell, 15, 2707-2718.
24. Lee, D.-E., Lee, I.-J., Han, O., Baik, M.-G., Han, S.-S. and Back, K. (2004) Pathogen resistance of transgenic rice plants expressing mitogen-activated protein kinase 1, MK1, from Capsicum annuum. Mol. Cells, 17, 81-85.
25. Linthorst, H.J.B., Melchers, L.S., Mayer, A., van Roekel, J.S.C., Cornelissen, B.J.C. and Bol J.F. (1990) Analysis of gene families encoding acidic and basic β-1,3-glucanases of tobacco. Proc. Natl Acad. Sci. USA, 87, 8756-8760.
26. Liu, Y. and Zhang, S. (2004) Phosphorylation of 1-aminocyclopropane- 1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell, 16, 3386-3399.
27. Malamy, J., Carr, J.P., Klessig, D.F. and Raskin, I. (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250, 1002-1004.
28. MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301-308.
29. Menke, F.L.H., Parchmann, S., Mueller, M.J., Kijine, J.W. and Memelink, J. (1999) Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthaus roseus. Plant Physiol. 119, 1289-1296.
30. Menke, F.L.H., van Pelt, J.A., Pieterse, C.M.J. and Klessig, D.F. (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell, 16, 897-907.
31. Mitsuhara, I., Ugaki, M., Hirochika, H. et al. (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 37, 49-59.
32. Mur, L.A.J., Kenton, P., Atzorn, R., Miersch, O. and Wasternack, C. (2006) The outcome of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140, 249-262.
33. Nakagami, H., Pitzschke, A. and Hirt, H. (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10, 339-346.
34. Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N. and Ohashi, Y. (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39, 500-507.
35. Nojiri, H., Yamane, H., Seto, H., Yamaguchi, I., Murofushi, N., Yoshihara, T. and Shibaoka, H. (1992) Qualitative and quantitative analysis of endogenous jasmonic acid in bulbing and non-bulbing onion plants. Plant Cell Physiol. 33, 1225-1231.
36. O'Donnell, P.J., Calvert, C., Atzon, R., Wasternack, C., Leyser, H.M.O. and Bowles, D.J. (1996) Ethylene as a signal mediating the wound response of tomato plants. Science, 274, 1914-1917.
37. Ohtsubo, N., Mitsuhara, I., Koga, M., Seo, S. and Ohashi, Y. (1999) Ethylene promotes the necrotic lesion formation and basic PR gene expression in TMV-infected tobacco. Plant Cell Physiol. 40, 808-817.
38. Pauw, B. and Memelink, J. (2005) Jasmonate-responsive gene expression. J. Plant Growth Regul. 23, 200-210.
39. Petersen, M., Brodersen, P., Naested, H. et al. (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell, 103, 1111-1120.
40. Ren, D., Yang, K.-Y., Li, G.-J., Liu, Y. and Zhang, S. (2006) Activation of Ntf4, a tobacco mitogen-activated protein kinase, during plant defense response and its involvement in hypersensitive response-like cell death. Plant Physiol. 141, 1482-1493.
41. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D.G. (1999) 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, 11, 273-287.
42. Ryan, C.A. (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 289, 425-449.
43. Ryan, C.A. (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta, 1477, 112-121.
44. Samuel, M.A., Hall, H., Krzymowska, M., Drzewiecka, K., Hennig, J. and Ellis, B.E. (2005) SIPK signaling controls multiple components of harpin-induced cell death in tobacco. Plant J. 42, 406-416.
45. Sano, H., Seo, S., Koizumi, N., Niki, T., Iwamura, H. and Ohashi, Y. (1996) Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant Cell Physiol. 37, 762-769.
46. Schaller, F., Schaller, A. and Stintzi, A. (2005) Biosynthesis and metabolism of jasmonates. J. Plant Growth Regul. 23, 179-199.
47. 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.
48. Seo, S., Sano, H. and Ohashi, Y. (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell, 11, 289-298.
49. Seo, S., Seto, H., Koshino, H., Yoshida, S. and Ohashi, Y. (2003) A diterpene as an endogenous signal for the activation of defense responses to infection with tobacco mosaic virus and wounding in tobacco. Plant Cell, 15, 863-873.
50. Spoel, S.H., Koornneef, A., Claessens, S.M.C. et al. (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell, 15, 760-770.
51. Stenzel, I., Hause, B., Miersch, O., Kruz, T., Maucher, H., Weichert, H., Ziegler, J., Feussner, I. and Wasternack, C. (2003) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol. Biol. 51, 895-911.
52. Stratmann, 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.
53. Takabatake, R., Shigemi, S., Ito, N., Gotoh, Y., Mitsuhara, I. and Ohashi, Y. (2006) Involvement of wound-induced receptor-like protein kinase in the wound signal transduction in tobacco plant. Plant J. 47, 249-257.
54. Voronin, V., Aionesei, T., Limmongkon, A. et al. (2004) The MAP kinase kinase NtMEK2 is involved in tobacco pollen germination. FEBS Lett. 560, 86-90.
55. Walling, L.L. (2000) The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195-216.
56. Wasternack, C., Stenzel, I., Hause, B., Hause, G., Kutter, C., Maucher, H., Neumerkel, J., Feussner, I. and Miersch, O. (2006) The wound response in tomato - role of jasmonic acid. J. Plant Physiol. 163, 297-306.
57. Weber, H., Vick, B.A. and Farmer, E.F. (1997) Dinor-oxo- phytodienoic acid: a new hexadecanoid signal in the jasmonate family. Proc. Natl Acad. Sci. USA, 94, 10473-10478.
58. 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.
59. Xiong, L. and Yang, Y. (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell, 15, 745-759.
60. Yamakawa, H., Katou, S., Seo, S., Mitsuhara, I., Kamada, H. and Ohashi, Y. (2004) Plant mitogen-activated protein kinase phosphatase interacts with calmodulins. J. Biol. Chem. 279, 928-936.
61. Zhang, S. and Klessig, D.F. (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell, 9, 809-824.
62. Zhang, S. and Klessig, D.F. (1998a) The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl Acad. Sci. USA, 95, 7225-7230.
63. Zhang, S. and Klessig, D.F. (1998b) 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.