Silencing of WIPK and SIPK mitogen-activated protein kinases reduces tobacco mosaic virus accumulation but permits systemic viral movement in tobacco possessing the N resistance gene

Molecular Plant-Microbe Interactions

Volumn 23, Issue 8, 2010, Pages 1032-1041

  Kobayashi, Michie ^a   Seo, Shigeml ^a   Hirai, Katsuyuki ^a,b   Yamamoto Katou, Ayako ^a   Katou, Shinpel ^a,d   Seto, Hideharu ^c   Meshi, Tetsuo ^a   Mitsuhara, Ichiro ^a   Ohashi, Yuko ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c RIKEN   (Japan)

^d SHINSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE;

ARTICLE; ENZYMOLOGY; GENE SILENCING; GENETICS; INNATE IMMUNITY; KINETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); NECROSIS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; TEMPERATURE; THERMODYNAMICS; TOBACCO; TOBACCO MOSAIC VIRUS; TRANSGENIC PLANT; VIROLOGY;

GENE SILENCING; IMMUNITY, INNATE; KINETICS; MITOGEN-ACTIVATED PROTEIN KINASES; MOVEMENT; NECROSIS; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; TEMPERATURE; THERMODYNAMICS; TOBACCO; TOBACCO MOSAIC VIRUS;

NICOTIANA TABACUM; TOBACCO MOSAIC VIRUS;

EID: 77955220030     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-23-8-1032     Document Type: Article

References (52)

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. Beckers, G. J. M., Jasklewicz, M., Liu, Y., Underwood, W. R., He, S. Y., Zhang, S., and Conrath, U. 2009. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsls thaliana. Plant Cell 21:944-953.
3. Brader, G., Djamei, A., Teige, M., Paiva, E. T., and Hirt, H. 2007. The MAP kinase kinase MKK2 affects disease resistance in Arabidopsis. Mol. Plant-Microbe Interact. 20:589-596.
4. 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.
5. Chivasa, S., Murphy, A. M., Naylor, M., and Carr, J. P. 1997. Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism.. Plant Cell 9:547-557.
6. Dangl, J. L., and Jones, J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-833.
7. de Laat, A. M. M., and von Loon, L. C. 1982. Regulation, of ethylene biosynthesis in virus-infected tobacco leaves. II. Time course of levels of intermediates and in vivo conversion rates. Plant Physiol. 69:240-254.
8. del Pozo, O., Pedley, K. F., and Martin, G. B. 2004. MAPKKKa is a positive regulator of cell death associated with both plant immunity and disease. EMBO (Eur. Mol. Biol. Organ.) J. 23:3072-3082.
9. Dhondt, S., Geoffroy, P., Stelmach, B. A., Legrand, M., and Heiz, T. 2000. Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J. 23:431-440.
10. Dinesh-Kumar, S. P., and Baker, B. J. 2000. Alternatively spliced N resis-tance gene transcripts: Their possible role in tobacco mosaic virus resistance. Proc. Natl. Acad. Sci. U.S.A. 97:1908-1913.
11. Ditt, R. F., Nester, E. W., and Comai, L. 2001. Plant gene expression, response to Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. U.S.A. 98:10954-10959.
12. Ekengren, S. K., Liu, Y., Schiff, M., Dinesh-Kumar, S. P., and Martin, G. B. 2003. Two MAPK cascades, NPR, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36:905-917.
13. Erickson, F. L., Holzberg, S., Calderon-Urrea, A., Handley, V., Axtell, M., Corr, C., and Baker, B. 1999. The helicase domain of the TMV replicase proteins induces the Af-mediated defence response in tobacco. Plant J. 18:67-75.
14. Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296.
15. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Ukness, S., Ward, E., Kessmann, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754756.
16. Hammond-Kosack, K. E., and Jones, J. D. G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791.
17. Heitz, T., Bergey, D. R., and Ryan, C. A. 1997. A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemln, and methyl jasmonate. Plant Physiol. 114:10851093.
18. Hirai, K., Kubota, K., Mochizuki, T., Tsuda, S., and Meshi, T. 2008. Antiviral RNA silencing is restricted to the marginal region of the dark green tissue in the mosaic leaves of Tomato mosaic vires-infected tobacco plants. J. Virol. 82:3250-3260.
19. Holmes, F. O. 1938. Inheritance of resistance to tobacco-mosaic disease in tobacco. Phytopathology 28:553-561.
20. 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.
21. Jin, H., Liu, Y., Yang, K.-Y., Kim, C. Y., Baker, B., and Zhang, S. 2003. Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J. 33:719-73.1.
22. Kandoth, P. K., Ranf, S., Pancholi, S. S., Jayanty, S., Walla, M. D., Miller, W., Howe, G. A., Lincoln, D. E., and Stratmann, J. W. 2007. Tomato MAPK LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proc. Natl. Acad. Sci. U.S.A. 104:12205-12210.
23. Kenton, P., Mur, L. A. J., Wasternack, C., and Draper, J. 1999. (-)-Jasmonic acid accumulation, in tobacco hypersensitive response lesions. Mol. PlantMicrobe Interact. 12:74-78.
24. Kim, C. Y., Liu, Y., Thome, 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.
25. Li, Q., Xie, Q.-G, Smith-Becker, J., Navarre, D. A., and Kaloshian, I. 2006. Mi-l-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19:655-664.
26. Liu, Y., and Zhang, S. 2004. Phosphorylation of 1-aminocyclopropane- lcarboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386-3399.
27. Liu, Y., Schiff, M., and Dinesh-Kumar, S. P. 2004. Involvement of MEK1. MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J. 38:800-809.
28. 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.
29. MAPK Group. 2002. Mitogen-activated protein kinase cascades in plants: Anew nomenclature. Trends Plant Sci. 7:301-308.
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. Nakagami, H., Pitzschke, A., and Hirt, H. 2005. Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10:339-346.
32. 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.
33. 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.
34. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H. B., Lacy, M., Austin, M. J., Parker, J. E., Sharma, S. B., Klessig, D. F., Martienssen, R., Mattsson, O., Jensen, A. B., and Mundy, J. 2000. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111-1120.
35. 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.
36. 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.
37. Schaller, A., and Stintzi, A. 2009. Enzymes in jasmonate biosynthesis-structure, function, regulation. Phytochemistry 70:1532-1538.
38. 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.
39. 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.
40. Seo, S., Seto, H., Yamakawa, H., and Ohashi, Y. 2001. Transient accumulation of jasmonic acid during the synchronized hypersensitive cell death in tobacco mosaic virus-infected tobacco leaves. Mol. Plant-Microbe Interact. 14:261-264.
41. Seo, S., Katou, S., Seto, H., Gomi, K., and Ohashi, Y. 2007. The mitogenactivated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J. 49:899-909.
42. Sharma, P. C., Ito, A., Shimizu, T., Terauchi, R., Kamoun, S., and Saitoh, H. 2003. Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF-induced hypersensitive response (HR) in Nicotiana benthamiana. Mol. Gen. Genomics 269:583-591.
43. Stenzel, I., Hause, B., Miersch, O., Kruz, T., Maucher., H., Weichert, H., Ziegler., J., Feussner, I., and Wasternack, C. 2003. Jasmonate biosynthesis and the aliene oxide cyclase family of Arabidopsis thallana. Plant Mol. Biol. 51:895-911.
44. Stulemeijer, I. J. E., Stratmann, J. W., and Joosten, M. H. A. J. 2007. Tomato mitogen-activated protein kinases LeMPK1, LeMPK2, and LeMPK3 are activated during the Cf-4/Avr4-induced hypersensitive response and have distinct phosphorylation specificities. Plant Physiol. 144:1481-1494.
45. Takabatake, R., Ando, Y., Seo, S., Katou, S., Tsuda, S., Ohashi, Y., and Mitsuhara, I. 2007. MAP kinases function downstream of HSP90 and upstream, of mitochondria in TMV resistance gene N-mediated hypersensitive cell death. Plant Cell Physiol. 48:498-510.
46. Whitham, S., Dinesh-Kumar, S. P., Choi, D., Hehl, R., Corr, C., and Baker, B. 1994. The product of the tobacco mosaic virus resistance gene N: Similarity to Toll and the Interleukin-1 receptor. Cell 78:1101-1115.
47. Widmann, C., Gibson, S., Jarpe, M., B., and Johnson, G. L. 1999. Mitogenactivated protein kinase: Conservation of a three-kinase module from yeast to human. Physiol. Rev. 79:143-180.
48. Wu, J., Hettenhausen, C., Meldau, S., and Baldwin, I. 2007. Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuate. Plant Cell 19:1096-1122.
49. 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.
50. Yang, K.-Y., Liu, Y., and Zhang, S. 2001. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. U.S.A. 98:741-746.
51. Yuan, B., Shen, X., Li, X., Xu, C., and Wang, S. 2007. Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta 226:953-960.
52. 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. U.S.A. 95:7433-7438.