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The Shaker Type Potassium Channel, GORK, Regulates Abscisic Acid Signaling in Arabidopsis

  • Lim, Chae Woo (Department of Life Science (BK21 Program), Chung-Ang University) ;
  • Kim, Sang Hee (Division of Applied Life Science (BK 21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Choi, Hyong Woo (Department of Plant Medicals, Andong National University) ;
  • Luan, Sheng (Department of Plant and Microbial Biology, University of California) ;
  • Lee, Sung Chul (Department of Life Science (BK21 Program), Chung-Ang University)
  • Received : 2019.07.18
  • Accepted : 2019.08.28
  • Published : 2019.12.01

Abstract

Evolution of adaptive mechanisms to abiotic stress is essential for plant growth and development. Plants adapt to stress conditions by activating the abscisic acid (ABA) signaling pathway. It has been suggested that the ABA receptor, clade A protein phosphatase, SnRK2 type kinase, and SLAC1 anion channel are important components of the ABA signaling pathway. In this study, we report that the shaker type potassium (K+) channel, GORK, modulates plant responses to ABA and abiotic stresses. Our results indicate that the full length of PP2CA is needed to interact with the GORK C-terminal region. We identified a loss of function allele in gork that displayed ABA-hyposensitive phenotype. gork and pp2ca mutants showed opposite responses to ABA in seed germination and seedling growth. Additionally, gork mutant was tolerant to the NaCl and mannitol treatments, whereas pp2ca mutant was sensitive to the NaCl and mannitol treatments. Thus, our results indicate that GORK enhances the sensitivity to ABA and negatively regulates the mechanisms involved in high salinity and osmotic stresses via PP2CA-mediated signals.

Keywords

References

  1. Baek, W., Lim, C. W. and Lee, S. C. 2018. A DEAD-box RNA helicase, RH8, is critical for regulation of ABA signalling and the drought stress response via inhibition of PP2CA activity. Plant Cell Environ. 41:1593-1604. https://doi.org/10.1111/pce.13200
  2. Corratge-Faillie, C., Ronzier, E., Sanchez, F., Prado, K., Kim, J.-H., Lanciano, S., Leonhardt, N., Lacombe, B. and Xiong, T. C. 2017. The Arabidopsis guard cell outward potassium channel GORK is regulated by CPK33. FEBS Lett. 591:1982-1992. https://doi.org/10.1002/1873-3468.12687
  3. Dreyer, I. and Blatt, M. R. 2009. What makes a gate? The ins and outs of Kv-like $K^+$ channels in plants. Trends Plant Sci. 14:383-390. https://doi.org/10.1016/j.tplants.2009.04.001
  4. Fuchs, S., Grill, E., Meskiene, I. and Schweighofer, A. 2013. Type 2C protein phosphatases in plants. FEBS J. 280:681-693. https://doi.org/10.1111/j.1742-4658.2012.08670.x
  5. Golldack, D., Li, C., Mohan, H. and Probst, N. 2014. Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front. Plant Sci. 5:151. https://doi.org/10.3389/fpls.2014.00151
  6. Hedrich, R. 2012. Ion channels in plants. Physiol. Rev. 92:1777-1811. https://doi.org/10.1152/physrev.00038.2011
  7. Hosy, E., Vavasseur, A., Mouline, K., Dreyer, I., Gaymard, F., Poree, F., Boucherez, J., Lebaudy, A., Bouchez, D., Very, A.-A., Simonneau, T., Thibaud, J.-B. and Sentenac, H. 2003. The Arabidopsis outward $K^+$ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl. Acad. Sci. U. S. A. 100:5549-5554. https://doi.org/10.1073/pnas.0733970100
  8. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168. https://doi.org/10.1128/jb.153.1.163-168.1983
  9. Lebaudy, A., Pascaud, F., Very, A.-A., Alcon, C., Dreyer, I., Thibaud, J.-B. and Lacombe, B. 2010. Preferential KAT1-KAT2 heteromerization determines inward $K^+$ current properties in Arabidopsis guard cells. J. Biol. Chem. 285:6265-6274. https://doi.org/10.1074/jbc.M109.068445
  10. Lee, S. C., Lan, W., Buchanan, B. B. and Luan, S. 2009. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl. Acad. Sci. U. S. A. 106:21419-21424. https://doi.org/10.1073/pnas.0910601106
  11. Lee, S. C., Lan, W.-Z., Kim, B.-G., Li, L., Cheong, Y. H., Pandey, G. K., Lu, G., Buchanan, B. B. and Luan, S. 2007. A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc. Natl. Acad. Sci. U. S. A. 104:15959-15964. https://doi.org/10.1073/pnas.0707912104
  12. Lee, S. C., Lim, C. W., Lan, W., He, K. and Luan, S. 2013. ABA signaling in guard cells entails a dynamic protein-protein interaction relay from the PYL-RCAR family receptors to ion channels. Mol. Plant 6:528-538. https://doi.org/10.1093/mp/sss078
  13. Lee, S. C. and Luan, S. 2012. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 35:53-60. https://doi.org/10.1111/j.1365-3040.2011.02426.x
  14. Lefoulon, C., Boeglin, M., Moreau, B., Very, A.-A., Szponarski, W., Dauzat, M., Michard, E., Gaillard, I. and Cherel, I. 2016. The Arabidopsis AtPP2CA protein phosphatase inhibits the GORK $K^+$ efflux channel and exerts a dominant suppressive effect on phosphomimetic-activating mutations. J. Biol. Chem. 291:6521-6533. https://doi.org/10.1074/jbc.M115.711309
  15. Lemtiri-Chlieh, F. and MacRobbie, E. A.1994. Role of calcium in the modulation of Vicia guard cell potassium channels by abscisic acid: a patch-clamp study. J. Membr. Biol. 137:99-107. https://doi.org/10.1007/BF00233479
  16. Lim, C. W., Baek, W., Jung, J., Kim, J.-H. and Lee, S. C. 2015a. Function of ABA in stomatal defense against biotic and drought stresses. Int. J. Mol. Sci. 16:15251-15270. https://doi.org/10.3390/ijms160715251
  17. Lim, C. W., Hwang, B. K. and Lee, S. C. 2015b. Functional roles of the pepper RING finger protein gene, CaRING1, in abscisic acid signaling and dehydration tolerance. Plant Mol. Biol. 89:143-156. https://doi.org/10.1007/s11103-015-0359-1
  18. Lim, C. W. and Lee, S. C. 2016. Pepper protein phosphatase type 2C, CaADIP1 and its interacting partner CaRLP1 antagonistically regulate ABA signalling and drought response. Plant Cell Environ. 39:1559-1575. https://doi.org/10.1111/pce.12721
  19. Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A. and Grill, E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064-1068. https://doi.org/10.1126/science.1172408
  20. Negi, J., Matsuda, O., Nagasawa, T., Oba, Y., Takahashi, H., Kawai-Yamada, M., Uchimiya, H., Hashimoto, M. and Iba, K. 2008. $CO_2$ regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483-486. https://doi.org/10.1038/nature06720
  21. Nieves-Cordones, M., Chavanieu, A., Jeanguenin, L., Alcon, C., Szponarski, W., Estaran, S., Cherel, I., Zimmermann, S., Sentenac, H. and Gaillard, I. 2014. Distinct amino acids in the C-linker domain of the Arabidopsis $K^+$ channel KAT2 determine its subcellular localization and activity at the plasma membrane. Plant Physiol. 164:1415-1429. https://doi.org/10.1104/pp.113.229757
  22. Osakabe, Y., Osakabe, K., Shinozaki, K. and Tran, L.-S. P. 2014. Response of plants to water stress. Front. Plant Sci. 5:86.
  23. Park, S.-Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.-F. F., Alfred, S. E., Bonetta, D., Finkelstein, R., Provart, N. J., Desveaux, D., Rodriguez, P. L., McCourt, P., Zhu, J.-K., Schroeder, J. I., Volkman, B. F. and Cutler, S. R. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068-1071. https://doi.org/10.1126/science.1173041
  24. Pilot, G., Pratelli, R., Gaymard, F., Meyer, Y. and Sentenac, H. 2003. Five-group distribution of the Shaker-like $K^+$ channel family in higher plants. J. Mol. Evol. 56:418-434. https://doi.org/10.1007/s00239-002-2413-2
  25. Sah, S. K., Reddy, K. R. and Li, J. 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7:571.
  26. Schroeder, J. I. and Hagiwara, S. 1989. Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427-430. https://doi.org/10.1038/338427a0
  27. Schroeder, J. I., Kwak, J. M. and Allen, G. J. 2001. Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327-330. https://doi.org/10.1038/35066500
  28. Schroeder, J. I., Raschke, K. and Neher, E. 1987. Voltage dependence of $K^+$ channels in guard-cell protoplasts. Proc. Natl. Acad. Sci. U. S. A. 84:4108-4112. https://doi.org/10.1073/pnas.84.12.4108
  29. Sirichandra, C., Wasilewska, A., Vlad, F., Valon, C. and Leung, J. 2009. The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J. Exp. Bot. 60:1439-1463. https://doi.org/10.1093/jxb/ern340
  30. Szostkiewicz, I., Richter, K., Kepka, M., Demmel, S., Ma, Y., Korte, A., Assaad, F. F., Christmann, A. and Grill, E. 2010. Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J. 61:25-35. https://doi.org/10.1111/j.1365-313X.2009.04025.x
  31. Vahisalu, T., Kollist, H., Wang, Y.-F., Nishimura, N., Chan, W.-Y., Valerio, G., Lamminmaki, A., Brosche, M., Moldau, H., Desikan, R., Schroeder, J. I. and Kangasjarvi, J. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487-491. https://doi.org/10.1038/nature06608
  32. Waadt, R., Schmidt, L. K., Lohse, M., Hashimoto, K., Bock, R. and Kudla, J. 2008. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56:505-516. https://doi.org/10.1111/j.1365-313X.2008.03612.x