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Arabidopsis PYL8 Plays an Important Role for ABA Signaling and Drought Stress Responses

  • Lim, Chae Woo (Department of Life Sciences, Chung-Ang University) ;
  • Baek, Woonhee (Department of Life Sciences, Chung-Ang University) ;
  • Han, Sang-Wook (Department of Integrative Plant Science, Chung-Ang University) ;
  • Lee, Sung Chul (Department of Life Sciences, Chung-Ang University)
  • Received : 2013.07.22
  • Accepted : 2013.08.26
  • Published : 2013.12.01

Abstract

Plants are frequently exposed to numerous environmental stresses such as dehydration and high salinity, and have developed elaborate mechanisms to counteract the deleterious effects of stress. The phytohormone abscisic acid (ABA) plays a critical role as an integrator of plant responses to water-limited condition to activate ABA signal transduction pathway. Although perception of ABA has been suggested to be important, the function of each ABA receptor remains elusive in dehydration condition. Here, we show that ABA receptor, pyrabactin resistance-like protein 8 (PYL8), functions in dehydration conditions. Transgenic plants overexpressing PYL8 exhibited hypersensitive phenotype to ABA in seed germination, seedling growth and establishment. We found that hypersensitivity to ABA of transgenic plants results in high degrees of stomatal closure in response to ABA leading to low transpiration rates and ultimately more vulnerable to drought than the wild-type plants. In addition, high expression of ABA maker genes also contributes to altered drought tolerance phenotype. Overall, this work emphasizes the importance of ABA signaling by ABA receptor in stomata during defense response to drought stress.

Keywords

References

  1. Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. 2003. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63-78. https://doi.org/10.1105/tpc.006130
  2. Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Peirats-Llobet, M., Pizzio, G. A., Fernandez, M. A., De Winne, N., De Jaeger, G., Dietrich, D., Bennett, M. J. and Rodriguez, P. L. 2013. PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol. 161:931-941. https://doi.org/10.1104/pp.112.208678
  3. Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Rodrigues, A., Pizzio, G. A. and Rodriguez, P. L. 2012. Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiol. 158:970-980. https://doi.org/10.1104/pp.111.188623
  4. Cheong, Y. H., Pandey, G. K., Grant, J. J., Batistic, O., Li, L., Kim, B. G., Lee, S. C., Kudla, J. and Luan, S. 2007. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 52:223-239. https://doi.org/10.1111/j.1365-313X.2007.03236.x
  5. Christmann, A. and Grill, E. 2009. Are GTGs ABA's biggest fans? Cell 136:21-23. https://doi.org/10.1016/j.cell.2008.12.033
  6. Christmann, A., Weiler, E. W., Steudle, E. and Grill, E. 2007. A hydraulic signal in root-to-shoot signalling of water shortage. Plant J. 52:167-174. https://doi.org/10.1111/j.1365-313X.2007.03234.x
  7. Clough, S. J. and Bent, A. F. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
  8. Finkelstein, R. R., Gampala, S. S. and Rock, C. D. 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell 14 Suppl:S15-45. https://doi.org/10.1105/tpc.010441
  9. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S. Y., Cutler, S. R., Sheen. J., Rodriguez, P. L. and Zhu, J. K. 2009. In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660-664. https://doi.org/10.1038/nature08599
  10. Fujii, H., Verslues, P. E. and Zhu, J. K. 2007. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485-494. https://doi.org/10.1105/tpc.106.048538
  11. Fujii, H. and Zhu, J. K. 2009. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl. Acad. Sci. USA 106:8380-8385. https://doi.org/10.1073/pnas.0903144106
  12. Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K., Kobayashi, M., Nakasone, S., Yamada, K., Ito, T., Shinozaki, K. and Yamaguchi-Shinozaki, K. 2009. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50:2123-2132. https://doi.org/10.1093/pcp/pcp147
  13. Geiger, D., Scherzer, S., Mumm, P., Stange, A., Marten, I., Bauer, H., Ache, P., Matschi, S., Liese, A., Al-Rasheid, K. A., Romeis, T. and Hedrich, R. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl. Acad. Sci. U S A 106:21425-21430. https://doi.org/10.1073/pnas.0912021106
  14. Gonzalez-Guzman, M., Pizzio, G. A., Antoni, R., Vera-Sirera, F., Merilo, E., Bassel, G. W., Fernandez, M. A., Holdsworth, M. J., Perez-Amador, M. A., Kollist, H. and Rodriguez, P. L. 2012. Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24:2483-2496. https://doi.org/10.1105/tpc.112.098574
  15. Gosti, F., Beaudoin, N., Serizet, C., Webb, A. A., Vartanian, N. and Giraudat, J. 1999 ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897-1910. https://doi.org/10.1105/tpc.11.10.1897
  16. Karimi, M., Inze, D. and Depicker, A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7:193-195. https://doi.org/10.1016/S1360-1385(02)02251-3
  17. Lang, V. and Palva, E. T. 1992. The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 20:951-962. https://doi.org/10.1007/BF00027165
  18. Lee, S. C. and Hwang, B. K. 2009. Functional roles of the pepper antimicrobial protein gene, CaAMP1, in abscisic acid signaling, and salt and drought tolerance in Arabidopsis. Planta 229:383-391. https://doi.org/10.1007/s00425-008-0837-7
  19. Lee, S. C., Hwang, I. S., Choi, H. W. and Hwang, B. K. 2008. Identification and functional expression of the novel pepper antimicrobial protein, CaAMP1 enhances broad-spectrum disease resistance in transgenic Arabidopsis. Plant Physiol. 148:1004-1020. https://doi.org/10.1104/pp.108.123836
  20. 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. USA 106:21419-21424. https://doi.org/10.1073/pnas.0910601106
  21. 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
  22. 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
  23. Li, H., Jiang, H., Bu, Q., Zhao, Q., Sun, J., Xie, Q. and Li, C. 2011. The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response. Plant Physiol. 156:550-563. https://doi.org/10.1104/pp.111.176214
  24. Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  25. 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.
  26. Merlot, S., Gosti, F., Guerrier, D., Vavasseur, A. and Giraudat, J. 2001. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 25:295-303. https://doi.org/10.1046/j.1365-313x.2001.00965.x
  27. Mustilli, A. C., Merlot, S., Vavasseur, A., Fenzi, F. and Giraudat, J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089-3099. https://doi.org/10.1105/tpc.007906
  28. Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., Maruyama, K., Yoshida, T., Ishiyama, K., Kobayashi, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. 2009. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 50:1345-1363. https://doi.org/10.1093/pcp/pcp083
  29. Nishimura, N., Yoshida, T., Murayama, M., Asami, T., Shinozaki, K. and Hirayama, T. 2004. Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. Plant Cell Physiol. 45:1485-1499. https://doi.org/10.1093/pcp/pch171
  30. Park, S. Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T. 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.
  31. Radauer, C., Lackner, P. and Breiteneder, H. 2008. The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol. Biol. 8:286. https://doi.org/10.1186/1471-2148-8-286
  32. Robert-Seilaniantz, A., Navarro, L., Bari, R. and Jones, J. D. 2007. Pathological hormone imbalances. Curr. Opin. Plant Biol. 10:372-379. https://doi.org/10.1016/j.pbi.2007.06.003
  33. Saavedra. X., Modrego, A. Rodriguex, D., Gonzalez-Garcia, M. P., Sanz, L., Nicolas, G. and Lorenzo, O. 2010. The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signaling in seeds and stress. Plant Physiol. 152:133-150. https://doi.org/10.1104/pp.109.146381
  34. Saez, A., Apostolova, N., Gonzalez-Guzman, M., Gonzalez-Garcia, M. P., Nicolas, C., Lorenzo, O. and Rodriguez, P. L. 2004. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J. 37:354-369. https://doi.org/10.1046/j.1365-313X.2003.01966.x
  35. Santiago, J., Rodrigues, A., Saez, A., Rubio, S., Antoni, R., Dupeux, F., Park, S. Y., Marquez, J. A., Cutler, S. R. and Rodriguez, P. L. 2009. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 60:575-588. https://doi.org/10.1111/j.1365-313X.2009.03981.x
  36. Schweighofer, A., Hirt, H. and Meskiene, I. 2004. Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci. 9:236−243. https://doi.org/10.1016/j.tplants.2004.03.007
  37. Shen, Y. Y., Wang, X. F., Wu, F. Q., Du, S. Y., Cao, Z., Shang, Y., Wang, X. L., Peng, C. C., Yu, X. C., Zhu, S. Y., Fan, R. C., Xu, Y. H. and Zhang, D. P. 2006. The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823-826. https://doi.org/10.1038/nature05176
  38. 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
  39. Ton, J, Flors, V. and Mauch-Mani, B. 2009. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14: 310-317. https://doi.org/10.1016/j.tplants.2009.03.006
  40. Umezawa, T., Sugiyama, N., Mizoguchi, M., Hayashi, S., Myouga, F., Yamaguchi-Shinozaki, K., Ishihama, Y., Hirayama, T. and Shinozaki, K. 2009. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. USA 106:17588-17593. https://doi.org/10.1073/pnas.0907095106
  41. Vlad, F., Rubio, S., Rodrigues, A., Sirichandra, C., Belin, C., Robert, N., Leung, J., Rodriguez, P. L., Lauriere, C. and Merlot, S. 2009. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21:3170-3184. https://doi.org/10.1105/tpc.109.069179
  42. Wasilewska, A., Vlad, F., Sirichandra, C., Redko, Y., Jammes, F., Valon, C., Frey, N. F. d. and Leung, J. 2008. An update on abscisic acid signaling in plants and more. Mol. Plant 1:198-217. https://doi.org/10.1093/mp/ssm022
  43. Yang, Y., Costa, A., Leonhardt, N., Siegel, R. S. and Schroeder, J. I. 2008. Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4:6. https://doi.org/10.1186/1746-4811-4-6

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