DOI QR코드

DOI QR Code

Mitogen-Activated Protein Kinase Kinase 3 Is Required for Regulation during Dark-Light Transition

  • Lee, Horim (Department of Pre-PharmMed, College of Natural Sciences, Duksung Women's University)
  • Received : 2015.03.03
  • Accepted : 2015.04.06
  • Published : 2015.07.31

Abstract

Plant growth and development are coordinately orchestrated by environmental cues and phytohormones. Light acts as a key environmental factor for fundamental plant growth and physiology through photosensory phytochromes and underlying molecular mechanisms. Although phytochromes are known to possess serine/threonine protein kinase activities, whether they trigger a signal transduction pathway via an intracellular protein kinase network remains unknown. In analyses of mitogen-activated protein kinase kinase (MAPKK, also called MKK) mutants, the mkk3 mutant has shown both a hypersensitive response in plant hormone gibberellin (GA) and a less sensitive response in red light signaling. Surprisingly, light-induced MAPK activation in wild-type (WT) seedlings and constitutive MAPK phosphorylation in dark-grown mkk3 mutant seedlings have also been found, respectively. Therefore, this study suggests that MKK3 acts in negative regulation in darkness and in light-induced MAPK activation during dark-light transition.

Keywords

References

  1. Alabadi, D., Gil, J., Blazquez, M.A., and Garcia-Martinez, J.L. (2004). Gibberellins repress photomorphogenesis in darkness. Plant Physiol. 134, 1050-1057. https://doi.org/10.1104/pp.103.035451
  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. https://doi.org/10.1038/415977a
  3. Bu, Q., Zhu, L., Dennis, M.D., Yu, L., Lu, S.X., Person, M.D., Tobin, E.M., Browning, K.S., and Huq, E. (2011). Phosphorylation by CK2 enhances the rapid light-induced degradation of phytochrome interacting factor 1 in Arabidopsis. J. Biol. Chem. 286, 12066-12074. https://doi.org/10.1074/jbc.M110.186882
  4. Carvalho, S.D., and Folta, K.M. (2014). Sequential light programs shape kale (Brassica napus) sprout appearance and alter metabolic and nutrient content. Hort. Res. 1, 8. https://doi.org/10.1038/hortres.2014.8
  5. Chen, M., and Chory, J. (2011). Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21, 664-671. https://doi.org/10.1016/j.tcb.2011.07.002
  6. Dai, Y., Wang, H., Li, B., Huang, J., Liu, J., Liu, X., Zhou, Y., Mou, Z., and Li, J. (2006). Increased expression of MAPK kinase kinase7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 18, 308-320. https://doi.org/10.1105/tpc.105.037846
  7. de Lucas, M., Jean-Michel, D., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480-484. https://doi.org/10.1038/nature06520
  8. Doczi, R., Brader, G., Pettko-Szandtner, A., Rajh, I., Djamei, A., Pitzschke, A., Teige, M., and Hirt, H. (2007). The Arabidopsis 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. https://doi.org/10.1105/tpc.106.050039
  9. Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., Chen, L., Yu, L., Iglesias-Pedraz, J.M., Kircher, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475-479. https://doi.org/10.1038/nature06448
  10. 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. https://doi.org/10.1038/cr.2008.300
  11. Hamel, L.P., Nicole, M.C., Sritubtim, S., Morency, M.J., Ellis, M., Ehlting, J., Beaudoin, N., Barbazuk, B., Klessig, D., Lee, J., et al. (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
  12. Ichimura, K., Shinozaki, K., Tena, G., Sheen, J., Henry, Y., Champion, A., Kreis, M., Zhang, S., Hirt, H., Wilson, C., et al. (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
  13. Jang, I.C., Yang, J.Y., Seo, H.S., and Chua, N.H. (2005). HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev. 19, 593-602. https://doi.org/10.1101/gad.1247205
  14. Lampard, G.R., Lukowitz, W., Ellis, B.E., and Bergmann, D.C. (2009). Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21, 3506-3517. https://doi.org/10.1105/tpc.109.070110
  15. Lampard, G.R., Wengier, D.L., and Bergmann, D.C. (2014). Manipulation of mitogen-activated protein kinase kinase signaling in the Arabidopsis stomatal lineage reveals motifs that contribute to protein localization and signaling specificity. Plant Cell 26, 3358-3371. https://doi.org/10.1105/tpc.114.127415
  16. Leivar, P., and Quail, P.H. (2010). PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19-28.
  17. Matsuoka, D., Nanmori, T., Sato, K.I., Fukami, Y., Kikkawa, U., and Yasuda, T. (2002). Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant J. 29, 637-647. https://doi.org/10.1046/j.0960-7412.2001.01246.x
  18. Melikant, B., Giuliani, C., Halbmayer-Watzina, S., Limmongkon, A., Heberle-Bors, E., and Wilson, C. (2004). The Arabidopsis thaliana MEK AtMKK6 activates the MAP kinase AtMPK13. FEBS Lett. 576, 5-8. https://doi.org/10.1016/j.febslet.2004.08.051
  19. Molas, M.L., Kiss, J.Z., and Correll, M.J. (2006). Gene profiling of the red light signaling pathways in roots. J. Exp. Bot. 57, 3217-3229. https://doi.org/10.1093/jxb/erl086
  20. Oh, E., Zhu, J.Y., and Wang, Z.Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802-809. https://doi.org/10.1038/ncb2545
  21. Park, H.J., Ding, L., Dai, M., Lin, R., and Wang, H. (2008). Multisite phosphorylation of Arabidopsis HFR1 by casein kinase II and plausible role in regulating its degradation rate. J. Biol. Chem. 283, 23264-23273. https://doi.org/10.1074/jbc.M801720200
  22. Pitzschke, A., Djamei, A., Bitton, F., and Hirt, H. (2009). A major role of the MEKK1-MKK1/MKK2-MPK4 pathway in ROS signalling. Mol. Plant 2, 120-137. https://doi.org/10.1093/mp/ssn079
  23. Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M., and Chory, J. (1993). Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147-157. https://doi.org/10.1105/tpc.5.2.147
  24. Sajio, Y., Sullivan, J.A., Wang, H., Yang, J., Shen, Y., Rubio, V., Ma, L., Hoecker, U., and Deng, X.W. (2003). The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev. 17, 2642-2647. https://doi.org/10.1101/gad.1122903
  25. Seo, H.S., Yang, J.Y., Ishikawa, M., Bolle, C., Ballestros, M.L., and Chua, N.H. (2003). LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423, 995-999. https://doi.org/10.1038/nature01696
  26. Sethi, V., Raghuram, B., Sinha, A.K., and Chattopadhyay, S. (2014). A mitogen-activated protein kinase cascade module, MKK3-MPK6 and MYC2, is involved in blue light-mediated seedling development in Arabidopsis. Plant Cell 26, 3343-3357. https://doi.org/10.1105/tpc.114.128702
  27. Sharma, S.K., and Carew, T.J. (2002). Inclusion of phosphatase inhibitors during western blotting enhances signal detection with phospho-specific antibodies. Anal. Biochem. 307, 187-189. https://doi.org/10.1016/S0003-2697(02)00008-8
  28. Soyano, T., Nishihama, R., Morikiyo, K., Ishikawa, M., and Machida, Y. (2003). NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev. 17, 1055-1067. https://doi.org/10.1101/gad.1071103
  29. Takahashi, F., Yoshida, R., Ichimura, K., Mizoguchi, T., Seo, S., Yonezawa, M., Maruyama, K., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2007). The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19, 805-818. https://doi.org/10.1105/tpc.106.046581
  30. 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
  31. 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 kinase in Arabidopsis. Plant Cell 19, 63-73. https://doi.org/10.1105/tpc.106.048298
  32. Wang, H., Liu, Y., Bruffett, K., Lee, J., Hause, G., Walker, J.C., and Zhang, S. (2008). Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development. Plant Cell 20, 602-613. https://doi.org/10.1105/tpc.108.058032
  33. Yang, J., Lin, R., Sullivan, J., Hoecker, U., Liu, B., Xu, L., Deng, X.W., and Wang, H. (2005). Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 17, 804-821. https://doi.org/10.1105/tpc.104.030205
  34. Yoo, S.D., Cho, Y.H., Tena, G., Xiong, Y., and Sheen, J. (2008). Dual control of nuclear EIN3 by bifurcate MAPK cascades in $C_2H_2$ signalling. Nature 451, 789-795. https://doi.org/10.1038/nature06543
  35. 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

Cited by

  1. The CottonMitogen-Activated Protein Kinase Kinase 3Functions in Drought Tolerance by Regulating Stomatal Responses and Root Growth vol.57, pp.8, 2016, https://doi.org/10.1093/pcp/pcw090
  2. Convergence of Multiple MAP3Ks on MKK3 Identifies a Set of Novel Stress MAPK Modules vol.07, 2016, https://doi.org/10.3389/fpls.2016.01941
  3. An Arabidopsis kinase cascade influences auxin-responsive cell expansion vol.92, pp.1, 2017, https://doi.org/10.1111/tpj.13635
  4. The Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase 20 (MKKK20) Acts Upstream of MKK3 and MPK18 in Two Separate Signaling Pathways Involved in Root Microtubule Functions vol.8, 2017, https://doi.org/10.3389/fpls.2017.01352
  5. Mitogen-Activated Protein Kinase Cascades in Plant Hormone Signaling vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.01387
  6. Comparative analysis of plant MKK gene family reveals novel expansion mechanism of the members and sheds new light on functional conservation vol.19, pp.1, 2018, https://doi.org/10.1186/s12864-018-4793-8
  7. Apple MPK4 mediates phosphorylation of MYB1 to enhance light‐induced anthocyanin accumulation vol.106, pp.6, 2015, https://doi.org/10.1111/tpj.15267