The Plant Pathology Journal

한국식물병리학회 (The Korean Society of Plant Pathology)
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Ser360 and Ser364 in the Kinase Domain of Tomato SIMAPKKKα are Critical for Programmed Cell Death Associated with Plant Immunity

  • Hwang, In Sun (Department of Horticultural Biotechnology, Kyung Hee University) ;
  • Brady, Jen (Boyce Thompson Institute for Plant Research) ;
  • Martin, Gregory B. (Boyce Thompson Institute for Plant Research) ;
  • Oh, Chang-Sik (Department of Horticultural Biotechnology, Kyung Hee University)
  • 투고 : 2016.11.20
  • 심사 : 2017.01.22
  • 발행 : 2017.04.01
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초록

$SIMAPKKK{\alpha}$, a tomato (Solanum lycopersicum) mitogen-activated protein kinase kinase kinase, is a positive regulator of Pto-mediated effector-triggered immunity, which elicits programmed cell death (PCD) in plants. In this study, we examined whether putative phosphorylation sites in the conserved activation segment of the $SIMAPKKK{\alpha}$ kinase domain are critical for eliciting PCD. Three amino acids, $threonine^{353}$, $serine^{360}$ ($Ser^{360}$), or $serine^{364}$ ($Ser^{364}$), in the conserved activation segment of $SIMAPKKK{\alpha}$ kinase domain were substituted to alanine (T353A, S360A, or S364A), and these variants were transiently expressed in tomato and Nicotiana benthamiana plants. Two alanine substitutions, S360A and S364A, completely abolished $SIMAPKKK{\alpha}$ PCD-eliciting activity in both plants, while T353A substitution did not affect its PCD-eliciting activity. $SIMAPKKK{\alpha}$ wild type and variant proteins accumulated to similar levels in plant leaves. However, $SIMAPKKK{\alpha}$ protein with the largest size was missed when either S360A or S364A substitutions were expressed, whereas proteins with the smaller masses were more accumulated than those of full-length of $SIMAPKKK{\alpha}$ and T353A. These results suggest that phosphorylation of $SIMAPKKK{\alpha}$ at $Ser^{360}$ and $Ser^{364}$ is critical for PCD elicitation in plants.

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참고문헌

  1. 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. https://doi.org/10.1038/415977a
  2. 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
  3. Coll, N. S., Epple, P. and Dangl, J. L. 2011. Programmed cell death in the plant immune system. Cell Death Differ. 18: 1247-1256. https://doi.org/10.1038/cdd.2011.37
  4. del Pozo, O., Pedley, K. F. and Martin, G. B. 2004. MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO J. 23:3072-3082. https://doi.org/10.1038/sj.emboj.7600283
  5. Eulgem, T. 2005. Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 10:71-78.
  6. Group, M. 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
  7. Hashimoto, M., Komatsu, K., Maejima, K., Okano, Y., Shiraishi, T., Ishikawa, K., Takinami, Y., Yamaji, Y. and Namba, S. 2012. Identification of three MAPKKKs forming a linear signaling pathway leading to programmed cell death in Nicotiana benthamiana. BMC Plant Biol. 12:103. https://doi.org/10.1186/1471-2229-12-103
  8. He, P., Shan, L., Lin, N. C., Martin, G. B., Kemmerling, B., Nurnberger, T. and Sheen, J. 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563-575. https://doi.org/10.1016/j.cell.2006.02.047
  9. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. and Pease, L. R. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. https://doi.org/10.1016/0378-1119(89)90358-2
  10. 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. https://doi.org/10.1016/S1534-5807(02)00205-8
  11. Jonak, C., Okresz, L., Bogre, L. and Hirt, H. 2002. Complexity, cross talk and integration of plant MAP kinase signalling. Curr. Opin. Plant Biol. 5:415-424. https://doi.org/10.1016/S1369-5266(02)00285-6
  12. Jones, J. D. and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  13. Katagiri, F. 2004. A global view of defense gene expression regulation: a highly interconnected signaling network. Curr. Opin. Plant Biol. 7:506-511. https://doi.org/10.1016/j.pbi.2004.07.013
  14. 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. https://doi.org/10.1016/S0092-8674(02)00743-2
  15. Kong, F., Wang, J., Cheng, L., Liu, S., Wu, J., Peng, Z. and Lu, G. 2012. Genome-wide analysis of the mitogen-activated protein kinase gene family in Solanum lycopersicum. Gene 499:108-120. https://doi.org/10.1016/j.gene.2012.01.048
  16. Li, X., Zhang, Y., Huang, L., Ouyang, Z., Hong, Y., Zhang, H., Li, D. and Song, F. 2014. Tomato SlMKK2 and SlMKK4 contribute to disease resistance against Botrytis cinerea. BMC Plant Biol. 14:166. https://doi.org/10.1186/1471-2229-14-166
  17. Lin, N. C. and Martin, G. B. 2007. Pto- and Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Mol. Plant-Microbe Interact. 20:806-815. https://doi.org/10.1094/MPMI-20-7-0806
  18. Melech-Bonfil, S. and Sessa, G. 2010. Tomato MAPKKK${\varepsilon}$ is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J. 64:379-391. https://doi.org/10.1111/j.1365-313X.2010.04333.x
  19. Melech-Bonfil, S. and Sessa, G. 2011. The SlMKK2 and SlMPK2 genes play a role in tomato disease resistance to Xanthomonas campestris pv. vesicatoria. Plant Signal. Behav. 6:154-156. https://doi.org/10.4161/psb.6.1.14311
  20. Mishra, N. S., Tuteja, R. and Tuteja, N. 2006. Signaling through MAP kinase networks in plants. Arch. Biochem. Biophys. 452:55-68. https://doi.org/10.1016/j.abb.2006.05.001
  21. Oh, C. S. and Martin, G. B. 2011. Tomato 14-3-3 protein TFT7 interacts with a MAP kinase kinase to regulate immunity-associated programmed cell death mediated by diverse disease resistance proteins. J. Biol. Chem. 286:14129-14136. https://doi.org/10.1074/jbc.M111.225086
  22. Oh, C. S., Hwang, J., Choi, M. S., Kang, B. C. and Martin, G. B. 2013. Two leucines in the N-terminal MAPK-docking site of tomato SlMKK2 are critical for interaction with a downstream MAPK to elicit programmed cell death associated with plant immunity. FEBS Lett. 587:1460-1465. https://doi.org/10.1016/j.febslet.2013.03.033
  23. Oh, C. S., Pedley, K. F. and Martin, G. B. 2010. Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK${\alpha}$. Plant Cell 22:260-272. https://doi.org/10.1105/tpc.109.070664
  24. Pedley, K. F. and Martin, G. B. 2004. Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J. Biol. Chem. 279:49229-49235. https://doi.org/10.1074/jbc.M410323200
  25. Salmeron, J. M., Oldroyd, G. E., Rommens, C. M., 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. https://doi.org/10.1016/S0092-8674(00)80083-5
  26. Wu, J., Wang, J., Pan, C., Guan, X., Wang, Y., Liu, S., He, Y., Chen, J., Chen, L. and Lu, G. 2014. Genome-wide identification of MAPKK and MAPKKK gene families in tomato and transcriptional profiling analysis during development and stress response. PLoS One 9:e103032. https://doi.org/10.1371/journal.pone.0103032
  27. Zipfel, C. 2008. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20:10-16. https://doi.org/10.1016/j.coi.2007.11.003
  28. Zuo, J., Niu, Q. W. and Chua, N. H. 2000. An estrogen receptorbased transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24:265-273. https://doi.org/10.1046/j.1365-313x.2000.00868.x