The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Functions of MAPK Cascade Pathways in Plant Defense Signaling

  • Cheong, Yong-Hwa (Department of Bio-Environmental Science, Sunchon National University) ;
  • Kim, Min-Chul (Department of Agronomy and Division of Applied Life Science, Gyeongsang National University)
  • Received : 2010.01.15
  • Accepted : 2010.04.08
  • Published : 2010.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Protein phosphorylation is one of the major mechanisms for controlling many cellular processes in all living organisms. Mitogen-activated protein kinase (MAPK) cascades are known to transducer extracellular stimuli to several cellular processes, including cell division, differentiation as well as responses to various stresses. In plants, several studies have revealed that MAPK cascade pathways play an important role in responses against biotic and abiotic stresses, including wounding, pathogen infection, temperature, drought, salinity and plant hormones. It is also known that MAPK cascades-mediated signaling is an essential process in the resistance step to pathogens by regulating the activity of transcription factors. Here, the insights into the functions of MAPK cascade pathways in plant defense response signaling from Arabidopsis, tobacco and rice are described.

Keywords

References

  1. Agrawal, G. K., Iwahashi, H. and Rakwal, R. 2003. Rice MAPKs. Biochem. Biophys. Res. Commun. 302: 171-180. https://doi.org/10.1016/S0006-291X(03)00174-8
  2. Ahlfors, R., Macioszek, V., Rudd, J., Brosche, M., Schlichting, R., Scheel, D. and Kangasjarvi, J. 2004. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J. 40:512-522. https://doi.org/10.1111/j.1365-313X.2004.02229.x
  3. Andreasson, E., Jenkins, T., Brodersen, P., Thorgrimsen, S., Petersen, N. H., Zhu, S., Qiu, J. L., Micheelsen, P., Rocher, A., Petersen, M., Newman, M. A., Bjorn-Nielsen, H., Hirt, H., Somssich, I., Mattsson, O. and Mundy, J. 2005. The MAP Kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 24:2579-2589. https://doi.org/10.1038/sj.emboj.7600737
  4. Apel, K. and Hirt, H. 2004. Reactive oxygen species: metabolism oxidative stress and signal transduction. Annu. Rev. Plant Biol. 55:373-399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
  5. 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 signaling cascade in Arabidopsis innate immunity. Nature 415:977-983. https://doi.org/10.1038/415977a
  6. Brodersen, P., Petersen, M., Bjorn-Nielsen, H., Zhu, S., Newman, M. A., Shokat, K. M., Rietz, S., Parker, J. and Mundy, J. 2006. Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47:532-546. https://doi.org/10.1111/j.1365-313X.2006.02806.x
  7. Chang, L. and Karin, M. 2001. Mammalian MAP kinase signaling cascades. Nature 410:37-40. https://doi.org/10.1038/35065000
  8. Cheong, Y. H., Moon, B. C., Kim, J. K., Kim, C. Y., Kim, M. C., Kim, I. H., Park, C. Y., Kim, J. C., Park, B. O., Koo, S. C., Yoon, H. W., Chung ,W. S., Lim, C. O., Lee, S. Y. and Cho, M. J. 2003. BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol. 132:1961-1972. https://doi.org/10.1104/pp.103.023176
  9. Cho, K., Agrawal, G. K., Jwa, N. S., Kubo, A. and Rakwal, R. 2009. Rice OsSIPK and its orthologs: a central master switch for stress responses. Biochem. Biophys. Res. Commun. 379: 649-653. https://doi.org/10.1016/j.bbrc.2008.12.107
  10. Colcombet, J. and Hirt, H. 2008. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem. J. 413:217-226. https://doi.org/10.1042/BJ20080625
  11. Dangl, J. L. and Jones, J. D. 2001. Plant pathogens and integrated defense responses to infection. Nature 411:826-833. https://doi.org/10.1038/35081161
  12. Djamei, A., Pitzschke, A., Nakagami, H., Rajh, I. and Hirt, H. 2007. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318:453-456. https://doi.org/10.1126/science.1148110
  13. Fiil, B. K., Petersen, K., Petersen, M. and Mundy, J. 2009. Gene regulation by MAP kinase cascades. Curr. Opin. Plant Biol. 12:615-621. https://doi.org/10.1016/j.pbi.2009.07.017
  14. Frye, C. A., Tang, D. and Innes, R. W. 2001. From the cover: negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA 98:373-378. https://doi.org/10.1073/pnas.011405198
  15. Fu, S. F., Chou, W. C., Huang, D. D. and Huang, H. J. 2002. Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stress. Plant Cell Physiol. 43:958-963. https://doi.org/10.1093/pcp/pcf111
  16. Hamel, L. P., Nicole, M. C., Sritubtim. S., Morency, M. J., Ellis, M., Ehlting, J., Beaudoin, N., Barbazuk, B., Klessig, D., Lee, J., Martin, G., Mundy, J., Ohashi. Y., Scheel, D., Sheen, J., Xing, T., Zhang, S., Seguin, A. and Ellis, B. E. 2006. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci. 11:192-198. https://doi.org/10.1016/j.tplants.2006.02.007
  17. Hanks, S. K., Quinn, A. M. and Hunter, T. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52. https://doi.org/10.1126/science.3291115
  18. He, C., Fong, S. H., Yang, D. and Wang, G. L. 1999. BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice. Mol. Plant-Microbe Interact. 12:1064-1073. https://doi.org/10.1094/MPMI.1999.12.12.1064
  19. Ichimura, K., Casais, C., Peck, S. C., Shinozaki, K. and Shirasu, K. 2006. MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J. Biol. Chem. 281:36969-36976. https://doi.org/10.1074/jbc.M605319200
  20. 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. 24:655-665. https://doi.org/10.1046/j.1365-313x.2000.00913.x
  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. 33:719-731. https://doi.org/10.1046/j.1365-313X.2003.01664.x
  22. Jonak, C., Okresz, L., Bogre, L. and Hirt, H. 2002. Complexity, cross talk and integration of plant MAP kinase signaling. Curr. Opin. Plant Biol. 5:415-424. https://doi.org/10.1016/S1369-5266(02)00285-6
  23. Kieber, J. J., Rothenberg, M., Roman, G., Feldmann, K. A. and Ecker, J. R. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinase. Cell 72:427-441. https://doi.org/10.1016/0092-8674(93)90119-B
  24. Kiegerl, S., Cardinale, F., Siligan, C., Gross, A., Baudouin, E., Liwosz, A., Eklof, S., Till, S., Bogre, L., Hirt, H. and Meskiene, I, 2000. SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell 12:2247-2258. https://doi.org/10.1105/tpc.12.11.2247
  25. Kim, C.Y. and Zhang, S. 2004. Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J. 38:142-151. https://doi.org/10.1111/j.1365-313X.2004.02033.x
  26. Koo, S. C., Moo, B. C., Kim, J. K., Kim, C. Y., Sung, S. J., Kim, M. C., Cho, M. J. and Cheong, Y. H. 2009. OsBWMK1 mediates SA-dependent defense responses by activating the transcription factor OsWRKY33. Biochem. Biophys. Res. Commun. 387:365-370. https://doi.org/10.1016/j.bbrc.2009.07.026
  27. Kumar, D. and Klessig, D. F. 2000. Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol. Plant-Microbe Interact. 13:347-351. https://doi.org/10.1094/MPMI.2000.13.3.347
  28. Lieberherr, D., Thao, N. P., Nakashima, A., Umemura, K., Kawasaki, T. and Shimamoto, K. 2005. A sphingolipid elicitor-inducible mitogenactivated protein kinase is regulated by the small GTPase OsRac1 and heterotrimeric G-protein in rice. Plant Physiol. 138:1644-1652. https://doi.org/10.1104/pp.104.057414
  29. Liu, Y. and Zhang, S. 2004. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ET biosynthesis in Arabidopsis. Plant Cell 16:3386-3399. https://doi.org/10.1105/tpc.104.026609
  30. MAPK Group. 2002. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7:301-308. https://doi.org/10.1016/S1360-1385(02)02302-6
  31. Menke, F. L .H., Kang, H., Chen, Z., Park, J. M., Kumar, D. and Klessig, D. F. 2005. Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HRlike cell death in tobacco. Mol. Plant-Microbe Interact. 18: 1027-1034. https://doi.org/10.1094/MPMI-18-1027
  32. Menke, F. L., van Pelt, J. A., Pieterse, C. M. and Klessig, D. F. 2004. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16: 897-907. https://doi.org/10.1105/tpc.015552
  33. Meszaros, T., Helfer, A., Hatzimasoura, E., Magyar, Z., Serazetdinova, L., Rios, G., Bardoczy, V., Teige, M., Koncz, C., Peck, S. and Bogre, L. 2006. The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J. 48:485-498. https://doi.org/10.1111/j.1365-313X.2006.02888.x
  34. Miao, Y., Laun, T. M., Smykowski, A. and Zentgraf, U. 2007. Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol. Biol. 65:63-76. https://doi.org/10.1007/s11103-007-9198-z
  35. Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., Yamaguchi-Shinozaki, K., Matsumoto, 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. https://doi.org/10.1073/pnas.93.2.765
  36. Nakagami, H., Kiegerl, S. and Hirt, H. 2004. OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J. Biol. Chem. 279:26959-26966. https://doi.org/10.1074/jbc.M312662200
  37. Nakagami, H., Soukupova, H., Schikora, A., Zarsky, V. and Hirt, H. 2006. A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281:38697-38704. https://doi.org/10.1074/jbc.M605293200
  38. Nishihama, R., Ishikawa, M., Araki, S., Soyano, T., Asada, T. and Machida, Y. 2001. The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev. 15:352-363. https://doi.org/10.1101/gad.863701
  39. 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. https://doi.org/10.1016/S0092-8674(00)00213-0
  40. Pitzschke, A., Schikora, A. and Hirt, H. 2009. MAPK cascade signalling networks in plant defense. Curr. Opin. Plant Biol. 12:421-426. https://doi.org/10.1016/j.pbi.2009.06.008
  41. Qiu, J. L., Fiil, B. K., Petersen, K., Nielsen, H. B., Botanga, C. J., Thorgrimsen, S., Palma, K., Suarez-Rodriguez, M. C., Sandbech-Clausen, S., Lichota, J., Brodersen, P., Grasser, K. D., Mattsson, O., Glazebrook, J., Mundy, J. and Petersen, M. 2008. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27:2214-2221. https://doi.org/10.1038/emboj.2008.147
  42. Quimby, B. B., Wilson, C. A. and Corbett, A. H. 2000. The interaction between Ran and NTF2 is required for cell cycle progression. Mol. Biol. Cell 11:2617-2629.
  43. Ren, D., Liu, Y., Yang, K. Y., Han, L., Mao, G., Glazebrook, J. and Zhang, S. 2008. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. USA 105:5638-5643. https://doi.org/10.1073/pnas.0711301105
  44. Ren, D., Yang, H. and Zhang, S. 2002. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem. 277:559-565. https://doi.org/10.1074/jbc.M109495200
  45. Reyna, N. S. and Yang, Y. 2006. Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol. Plant-Microbe. Interact. 19:530-540. https://doi.org/10.1094/MPMI-19-0530
  46. Samuel, M. A. and Ellis, B. E. 2002. Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell 14:2059-2069. https://doi.org/10.1105/tpc.002337
  47. Samuel, M. A., Miles. G. P. and Ellis. B. E. 2000. Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J. 22: 367-376. https://doi.org/10.1046/j.1365-313x.2000.00741.x
  48. Schaffer, R., Landgraf, J., Accerbi, M., Simon, V., Larson, M. and Wisman, E. 2001. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13:113-123. https://doi.org/10.1105/tpc.13.1.113
  49. Schoenbeck, M. A., Samac, D. A., Fedorova, M., Gregerson, R. G., Gantt, J. S. and Vance, C. P. 1999. The alfalfa (Medicago sativa) TDY1 gene encodes a mitogen-activated protein kinase homolog. Mol. Plant-Microbe Interact. 12:882-893. https://doi.org/10.1094/MPMI.1999.12.10.882
  50. 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. https://doi.org/10.1126/science.270.5244.1988
  51. Song, D., Chen, J., Song, F. and Zheng, Z. 2006. A novel rice MAPK gene, OsBIMK2, is involved in disease-resistance responses. Plant Biol. 8:587-596. https://doi.org/10.1055/s-2006-924149
  52. Suarez-Rodriguez, M. C., Adams-Phillips, L., Liu, Y., Wang, H., Su, S. H., Jester, P. J., Zhang, S., Bent, A. F. and Krysan, P. J. 2007. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol. 143:661-669. https://doi.org/10.1104/pp.106.091389
  53. Takahashi, Y., Uehara, Y., Berberich, T., Ito, A., Saitoh, H., Miyazaki, A., Terauchi, R. and Kusano, T. 2004. A subset of hypersensitive response marker genes, including HSR203J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J. 40:586-595. https://doi.org/10.1111/j.1365-313X.2004.02234.x
  54. Tang, D. and Innes, R. W. 2002. Overexpression of a kinasedeficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J. 32:975-983. https://doi.org/10.1046/j.1365-313X.2002.01482.x
  55. Teige, M., Scheikl, E., Eulgem, T., Doczi, R., Ichimura, K., Shinozaki, K., Dangl, J. L. and Hirt, H. 2004. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell 15:141-152. https://doi.org/10.1016/j.molcel.2004.06.023
  56. Xiong, L. and Yang, Y. 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acidinducible mitogen-activated protein kinase. Plant Cell 15:745-759. https://doi.org/10.1105/tpc.008714
  57. Xu. J., Li, Y., Wang, Y., Liu, H., Lei, L., Yang, H., Liu, G. and Ren, D. 2008. Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J. Biol. Chem. 283:26996-27006. https://doi.org/10.1074/jbc.M801392200
  58. Yang, K. Y., Liu, Y. and Zhang, S. 2001. Activation of a mitogenactivated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98:741-746. https://doi.org/10.1073/pnas.98.2.741
  59. Yap, Y., Kodama, Y., Waller, F., Chung, K. M., Ueda, H., Nakamura, K., Oldsen, M., Yoda, H., Yamaguchi, Y. and Sano, H. 2005. Activation of a novel transcription factor through phosphorylation by WIPK, a wound-induced mitogen-activated protein kinase in tobacco plants. Plant Physiol. 139:127-137. https://doi.org/10.1104/pp.105.065656
  60. Yoshioka, H., Numata, N., Nakajima, K., Katou, S., Kawakita, K., Rowland, O., Jones, J. D. G. and Doke, N. 2003. Nicotiana benthamiana $gp^{91phox}$ homologs NbrbohA and NbrbohB participate in $H_2O_2$ accumulation and resistance to Phytophthora infestans. Plant Cell 15:706-718. https://doi.org/10.1105/tpc.008680
  61. Yuan, B., Shen, X., Li, X., Xu, C. and Wang, S. 2007. Mitogenactivated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta 226:953-960. https://doi.org/10.1007/s00425-007-0541-z
  62. Zhang, S. and Klessig, D. F. 1997. Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9:809-824. https://doi.org/10.1105/tpc.9.5.809
  63. 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. https://doi.org/10.1073/pnas.95.13.7433
  64. Zhang, S. and Klessig, D. F. 2001. MAPK cascades in plant defense signaling. Trends Plant Sci. 6:520-527. https://doi.org/10.1016/S1360-1385(01)02103-3
  65. Zhang, S. and Liu, Y. 2001. Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell 13:1877-1889. https://doi.org/10.1105/tpc.13.8.1877
  66. Zhang, S., Liu, Y. and Klessig, D. F. 2000. Multiple levels of tobacco WIPK activation during the induction of cell death by fungal elicitins. Plant J. 23:339-347. https://doi.org/10.1046/j.1365-313x.2000.00780.x
  67. Zwerger, K. and Hirt, H. 2001. Recent advances in plant MAP kinase signalling. Biol. Chem. 382:1123-1131. https://doi.org/10.1515/BC.2001.142

Cited by

  1. Involvement of the OsMKK4-OsMPK1 Cascade and its Downstream Transcription Factor OsWRKY53 in the Wounding Response in Rice vol.30, pp.2, 2014, https://doi.org/10.5423/PPJ.OA.10.2013.0106
  2. Protein–protein interactions in plant mitogen-activated protein kinase cascades vol.67, pp.3, 2016, https://doi.org/10.1093/jxb/erv508
  3. Signaling pathway in development of Camellia oleifera nurse seedling grafting union vol.31, pp.5, 2017, https://doi.org/10.1007/s00468-017-1568-9
  4. Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress vol.84, pp.3, 2018, https://doi.org/10.1007/s10725-017-0354-4
  5. ) Roots by Illumina- and Single-Molecule Real-Time-Based RNA Sequencing pp.1557-7430, 2018, https://doi.org/10.1089/dna.2018.4352
  6. Expressing OsMPK4 Impairs Plant Growth but Enhances the Resistance of Rice to the Striped Stem Borer Chilo suppressalis vol.19, pp.4, 2018, https://doi.org/10.3390/ijms19041182