MAP kinase cascades in Arabidopsis innate immunity

Frontiers in Plant Science

Volumn 3, Issue JUL, 2012, Pages

  Rasmussen, Magnus W ^a   Roux, Milena ^a   Petersen, Morten ^a   Mundy, John ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Calcium signaling; Hypersensitive response; MAP kinase cascade; MAP kinase substrates; Pathogen effectors; Pattern recognition receptors; Reactive oxygen species; Resistance proteins

Indexed keywords

EID: 84888429609     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00169     Document Type: Review

References (51)

1. 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., Bjørn 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.
2. 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.
3. Bethke, G., Pecher, P., Eschen-Lippold, L., Tsuda, K., Katagiri, F., Glazebrook, J., Scheel, D., and Lee, J. (2012). Activation of the Arabidopsis thaliana mitogen-activated protein kinase MPK11 by the flagellin-derived elicitor peptide, flg22. Mol. Plant Microbe Interact. 25, 471-480.
4. Brodersen, P., Petersen, M., Nielsen, H. B., Zhu, S., Newman, M., 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.
5. Cui, H., Wang, Y., Xue, L., Chu, J., Yan, C., Fu, J., Chen, M., Innes, R. W., and Zhou, J.-M. (2010). Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7, 164-175.
6. del Pozo, O., Pedley, K. F., and Martin, G. B. (2004). MAPKKK[alpha] is a positive regulator of cell death associated with both plant immunity and disease. EMBO J. 23, 3072-3082.
7. Djamei, A., Pitzschke, A., Nakagami, H., Rajh, I., and Hirt, H. (2007). trojan horse strategy in Agrobacteriumtransformation: abusing MAPK defense signaling. Science 318, 453-456.
8. Dóczi, R., Brader, G., Pettkó-Szandtner, A., Rajh, I., Djamei, A., Pitzschke, A., Teige, M., and Hirt, H. (2007). TheArabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19, 3266-3279.
9. Feilner, T., Hultschig, C., Lee, J., Meyer, S., Immink, R. G. H., Koenig, A., Possling, A., Seitz, H., Beveridge, A., Scheel, D., Cahill, D. J., Lehrach, H., Kreutzberger, J., and Kersten, B. (2005). High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol. Cell. Proteomics 4, 1558-1568.
10. Felix, G., Duran, J. D., Volko, S., and Boller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276.
11. Fiil, B. K., Petersen, K., Petersen, M., and Mundy, J. (2009). Gene regulation by MAP kinase cascades. Curr. Opin. Plant Biol. 12, 615-621.
12. Forzani, C., Carreri, A., de la Fuente van Bentem, S., Lecourieux, D., Lecourieux, F., and Hirt, H. (2011). TheArabidopsis protein kinase Pto-interacting 1-4 is a common target of the oxidative signal-inducible 1 and mitogen-activated protein kinases. FEBS J. 278, 1126-1136.
13. Frei dit Frey, N., Mbengue, M., Kwaaitaal, M., Nitsch, L., Altenbach, D., Haweker, H., Lozano-Duran, R., Njo, M. F., Beeckman, T., Huettel, B., Borst, J. W., Panstruga, R., and Robatzek, S. (2012). Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. Plant Physiol. 159, 798-809.
14. Frye, C. A., Tang, D., and Innes, R. W. (2001). Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 373-378.
15. Gao, M., Liu, J., Bi, D., Zhang, Z., Cheng, F., Chen, S., and Zhang, Y. (2008). MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190-1198.
16. Gimenez-Ibanez, S., and Rathjen, J. P. (2010). The case for the defense: plants versus Pseudomonas syringae. Microbes Infect. 12, 428-437.
17. Gómez-Gómez, L., and Boller, T. (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011.
18. Ichimura, K., Shinozaki, K., Tena, G., Sheen, J., Henry, Y., Champion, A., Kreis, M., Zhang, S., Hirt, H., Wilson, C., Heberle-Bors, E., Ellis, B. E., Morris, P. C., Innes, R. W., Ecker, J. R., Scheel, D., Klessig, D. F., Machida, Y., Mundy, J., Ohashi, Y., and Walker, J. C. (2002). Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301-308.
19. Komis, G., Illés, P., Beck, M., and Šamaj, J. (2011). Microtubules and mitogen-activated protein kinase signalling. Curr. Opin. Plant Biol. 14, 650-657.
20. Kwaaitaal, M., Huisman, R., Maintz, J., Reinstädler, A., and Panstruga, R. (2011). Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem. J. 440, 355-365.
21. Lee, K., Song, E. H., Kim, H. S., Yoo, J. H., Han, H. J., Jung, M. S., Lee, S. M., Kim, K. E., Kim, M. C., Cho, M. J., and Chung, W. S. (2008). Regulation of MAPK phosphatase 1 (AtMKP1) by calmodulin in Arabidopsis. J. Biol. Chem.283, 23581-23588.
22. Ma, W., Qi, Z., Smigel, A., Walker, R. K., Verma, R., and Berkowitz, G. A. (2009). Ca2+, cAMP, and transduction of non-self perception during plant immune responses. Proc. Natl. Acad. Sci. U.S.A. 106, 20995-21000.
23. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., and Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639-1653.
24. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H., and Shibuya, N. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 19613-19618.
25. Parisy, V., Poinssot, B., Owsianowski, L., Buchala, A., Glazebrook, J., and Mauch, F. (2007). Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J. 49, 159-172.
26. Petersen, K., Qiu, J.-L., Lütje, J., Fiil, B. K., Hansen, S., Mundy, J., and Petersen, M. (2010). Arabidopsis MKS1 is involved in basal immunity and requires an intact N-terminal domain for proper function. PLoS ONE 5, e14364. doi: 10.1371/journal.pone.0014364
27. 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.
28. Popescu, S. C., Popescu, G. V., Bachan, S., Zhang, Z., Gerstein, M., Snyder, M., and Dinesh-Kumar, S. P. (2009). MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23, 80-92.
29. 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. (2008a). Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27, 2214-2221.
30. Qiu, J.-L., Zhou, L., Yun, B.-W., Nielsen, H. B., Fiil, B. K., Petersen, K., MacKinlay, J., Loake, G. J., Mundy, J., and Morris, P. C. (2008b). Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 148, 212-222.
31. 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. U.S.A. 105, 5638-5643.
32. Rentel, M. C., Lecourieux, D., Ouaked, F., Usher, S. L., Petersen, L., Okamoto, H., Knight, H., Peck, S. C., Grierson, C. S., Hirt, H., and Knight, M. R. (2004). OXI1 kinase is necessary for oxidative burst-mediated signalling inArabidopsis. Nature 427, 858-861.
33. 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.
34. Rodriguez, M. C., Petersen, M., and Mundy, J. (2010). Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621-649.
35. Roux, M., Schwessinger, B., Albrecht, C., Chinchilla, D., Jones, A., Holton, N., Malinovsky, F. G., Tör, M., De Vries, S., and Zipfel, C. (2011). The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23, 2440-2455.
36. Schwessinger, B., Roux, M., Kadota, Y., Ntoukakis, V., Sklenar, J., Jones, A., and Zipfel, C. (2011). Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046. doi: 10.1371/journal.pgen.1002046
37. Takahashi, F., Mizoguchi, T., Yoshida, R., Ichimura, K., and Shinozaki, K. (2011). Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol. Cell 41, 649-660.
38. Ulm, R., Ichimura, K., Mizoguchi, T., Peck, S. C., Zhu, T., Wang, X., Shinozaki, K., and Paszkowski, J. (2002). Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J. 21, 6483-6493.
39. Van Der Biezen, E. A., and Jones, J. D. G. (1998). Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454-456.
40. Wang, H., Ngwenyama, N., Liu, Y., Walker, J. C., and Zhang, S. (2007). Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19, 63-73.
41. Wurzinger, B., Mair, A., Pfister, B., and Teige, M. (2011). Cross-talk of calcium-dependent protein kinase and MAP kinase signaling. Plant Signal. Behav. 6, 8-12.
42. 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.
43. Yoo, S.-D., Cho, Y.-H., Tena, G., Xiong, Y., and Sheen, J. (2008). Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451, 789-795.
44. Zhang, J., Shao, F., Li, Y., Cui, H., Chen, L., Li, H., Zou, Y., Long, C., Lan, L., Chai, J., Chen, S., Tang, X., and Zhou, J. M. (2007a). A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1, 175-185.
45. Zhang, X., Dai, Y., Xiong, Y., DeFraia, C., Li, J., Dong, X., and Mou, Z. (2007b). Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J. 52, 1066-1079.
46. Zhang, Z., Wu, Y., Gao, M., Zhang, J., Kong, Q., Liu, Y., Ba, H., Zhou, J., and Zhang, Y. (2012). Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11, 253-263.
47. Zheng, Z., Qamar, S. A., Chen, Z., and Mengiste, T. (2006). Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 48, 592-605.
48. Zhou, N., Tootle, T. L., and Glazebrook, J. (1999). Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11, 2419-2428.
49. Zhu, X., Caplan, J., Mamillapalli, P., Czymmek, K., and Dinesh-Kumar, S. P. (2010). Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. EMBO J. 29, 1007-1018.
50. Zipfel, C. (2008). Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20, 10-16.
51. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D. G., Boller, T., and Felix, G. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760.