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http://dx.doi.org/10.14348/molcells.2019.0173

Arabidopsis Raf-Like Kinase Raf10 Is a Regulatory Component of Core ABA Signaling  

Nguyen, Quy Thi Cam (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Lee, Sun-ji (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Choi, Seo-wha (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Na, Yeon-ju (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Song, Mi-ran (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Hoang, Quyen Thi Ngoc (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Sim, Seo Young (Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST))
Kim, Min-Sik (Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST))
Kim, Jeong-Il (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Soh, Moon-Soo (Department of Molecular Biology, Sejong University)
Kim, Soo Young (Department of Biotechnology and Kumho Life Science Laboratory, College of Agriculture and Life Sciences, Chonnam National University)
Abstract
Abscisic acid (ABA) is a phytohormone essential for seed development and seedling growth under unfavorable environmental conditions. The signaling pathway leading to ABA response has been established, but relatively little is known about the functional regulation of the constituent signaling components. Here, we present several lines of evidence that Arabidopsis Raf-like kinase Raf10 modulates the core ABA signaling downstream of signal perception step. In particular, Raf10 phosphorylates subclass III SnRK2s (SnRK2.2, SnRK2.3, and SnRK2.6), which are key positive regulators, and our study focused on SnRK2.3 indicates that Raf10 enhances its kinase activity and may facilitate its release from negative regulators. Raf10 also phosphorylates transcription factors (ABI5, ABF2, and ABI3) critical for ABA-regulted gene expression. Furthermore, Raf10 was found to be essential for the in vivo functions of SnRK2s and ABI5. Collectively, our data demonstrate that Raf10 is a novel regulatory component of core ABA signaling.
Keywords
ABI5; abscisic acid; phytohormone; Raf10; signaling; SnRK2s;
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1 Kim, S.Y., Ma, J., Perret, P., Li, Z., and Thomas, T.L. (2002). Arabidopsis ABI5 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol. 130, 688-697.   DOI
2 Yoshida, T., Fujita, Y., Maruyama, K., Mogami, J., Todaka, D., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2015a). Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 38, 35-49.   DOI
3 Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABREdependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672-685.   DOI
4 Kobayashi, Y., Murata, M., Minami, H., Yamamoto, S., Kagaya, Y., Hobo, T., Yamamoto, A., and Hattori, T. (2005). Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J. 44, 939-949.   DOI
5 Kuhn, J.M., Boisson-Dernier, A., Dizon, M.B., Maktabi, M.H., and Schroeder, J.I. (2006). The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 140, 127-139.   DOI
6 Lee, S.J., Cho, D.I., Kang, J.Y., and Kim, S.Y. (2009). An ARIA-interacting AP2 domain protein is a novel component of ABA signaling. Mol. Cells 27, 409-416.   DOI
7 Lee, S.J., Lee, M.H., Kim, J.I., and Kim, S.Y. (2015). Arabidopsis putative MAP kinase kinase kinases Raf10 and Raf11 are positive regulators of seed dormancy and ABA response. Plant Cell Physiol. 56, 84-97.   DOI
8 Lopez-Molina, L. and Chua, N.H. (2000). A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol. 41, 541-547.   DOI
9 Lopez-Molina, L., Mongrand, S., and Chua, N.H. (2001). A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 98, 4782-4787.   DOI
10 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.   DOI
11 Ng, L.M., Soon, F.F., Zhou, X.E., West, G.M., Kovach, A., Suino-Powell, K.M., Chalmers, M.J., Li, J., Yong, E.L., Zhu, J.K., et al. (2011). Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc. Natl. Acad. Sci. U. S. A. 108, 21259-21264.   DOI
12 Yoshida, T., Mogami, J., and Yamaguchi-Shinozaki, K. (2015b). Omics approaches toward defining the comprehensive abscisic acid signaling network in plants. Plant Cell Physiol. 56, 1043-1052.   DOI
13 Yoshida, T., Nishimura, N., Kitahata, N., Kuromori, T., Ito, T., Asami, T., Shinozaki, K., and Hirayama, T. (2006b). ABA-Hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol. 140, 115-126.   DOI
14 Zhou, Q., Hare, P.D., Yang, S.W., Zeidler, M., Huang, L.F., and Chua, N.H. (2005). FHL is required for full phytochrome A signaling and shares overlapping functions with FHY1. Plant J. 43, 356-370.   DOI
15 Moglich, A., Ayers, R.A., and Moffat, K. (2009). Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17, 1282-1294.   DOI
16 Munemasa, S., Hauser, F., Park, J., Waadt, R., Brandt, B., and Schroeder, J.I. (2015). Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr. Opin. Plant Biol. 28, 154-162.   DOI
17 Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., Maruyama, K., Yoshida, T., Ishiyama, K., Kobayashi, M., et al. (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.   DOI
18 Nambara, E. and Marion-Poll, A. (2005). Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 56, 165-185.   DOI
19 Nishimura, N., Sarkeshik, A., Nito, K., Park, S.Y., Wang, A., Carvalho, P.C., Lee, S., Caddell, D.F., Cutler, S.R., Chory, J., et al. (2010). PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 61, 290-299.   DOI
20 Park, J., Lee, N., Kim, W., Lim, S., and Choi, G. (2011). ABI3 and PIL5 collaboratively activate the expression of SOMNUS by directly binding to its promoter in imbibed Arabidopsis seeds. Plant Cell 23, 1404-1415.   DOI
21 Park, S.Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.F., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071.   DOI
22 Boudsocq, M., Droillard, M.J., Barbier-Brygoo, H., and Lauriere, C. (2007). Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol. Biol. 63, 491-503.   DOI
23 Choi, S.W., Lee, S.B., Na, Y.J., Jeung, S.G., and Kim, S.Y. (2017). Arabidopsis MAP3K16 and other salt-inducible MAP3Ks regulate ABA response redundantly. Mol. Cells 40, 230-242.   DOI
24 Assmann, S.M., Snyder, J.A., and Lee, Y.R.J. (2000). ABA-deficient (aba1) and ABA-insensitive (abi1-1, abi2-1) mutants of Arabidopsis have a wildtype stomatal response to humidity. Plant Cell Environ. 23, 387-395.   DOI
25 Belin, C., de Franco, P.O., Bourbousse, C., Chaignepain, S., Schmitter, J.M., Vavasseur, A., Giraudat, J., Barbier-Brygoo, H., and Thomine, S. (2006). Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol. 141, 1316-1327.   DOI
26 Bensmihen, S., Rippa, S., Lambert, G., Jublot, D., Pautot, V., Granier, F., Giraudat, J., and Parcy, F. (2002). The homologous ABI5 and EEL transcription factors function antagonistically to Fine-tune gene expression during late embryogenesis. Plant Cell 14, 1391-1403.   DOI
27 Bentsink, L. and Koornneef, M. (2008). Seed dormancy and germination. Arab. Book 6, e0119.   DOI
28 Cai, Z.Y., Liu, J.J., Wang, H.J., Yang, C.J., Chen, Y.X., Li, Y.C., Pan, S.J., Dong, R., Tang, G.L., Barajas-Lopez, J.D., et al. (2014). GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 111, 9651-9656.   DOI
29 Santiago, J., Dupeux, F., Betz, K., Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Marquez, J.A., and Rodriguez, P.L. (2012). Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci. 182, 3-11.   DOI
30 Raghavendra, A.S., Gonugunta, V.K., Christmann, A., and Grill, E. (2010). ABA perception and signalling. Trends Plant Sci. 15, 395-401.   DOI
31 Saruhashi, M., Ghosh, T.K., Arai, K., Ishizaki, Y., Hagiwara, K., Komatsu, K., Shiwa, Y., Izumikawa, K., Yoshikawa, H., Umezawa, T., et al. (2015). Plant Raf-like kinase integrates abscisic acid and hyperosmotic stress signaling upstream of SNF1-related protein kinase2. Proc. Natl. Acad. Sci. U. S. A. 112, E6388-E6396.   DOI
32 Schweighofer, A., Hirt, H., and Meskiene, I. (2004). Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci. 9, 236-243.   DOI
33 Singh, A., Pandey, A., Srivastava, A.K., Tran, L.S., and Pandey, G.K. (2016). Plant protein phosphatases 2C: from genomic diversity to functional multiplicity and importance in stress management. Crit. Rev. Biotechnol. 36, 1023-1035.   DOI
34 Sirichandra, C., Davanture, M., Turk, B.E., Zivy, M., Valot, B., Leung, J., and Merlot, S. (2010). The Arabidopsis ABA-Activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS One 5, e13935.   DOI
35 Soon, F.F., Ng, L.M., Zhou, X.E., West, G.M., Kovach, A., Tan, M.H., Suino-Powell, K.M., He, Y., Xu, Y., Chalmers, M.J., et al. (2012). Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335, 85-88.   DOI
36 Takahashi, F., Kuromori, T., Sato, H., and Shinozaki, K. (2018a). Regulatory gene networks in drought stress responses and resistance in plants. Adv. Exp. Med. Biol. 1081, 189-214.   DOI
37 Finkelstein, R. (2013). Abscisic Acid synthesis and response. Arab. Book 11, e0166.   DOI
38 Choi, H., Hong, J., Ha, J., Kang, J., and Kim, S.Y. (2000). ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275, 1723-1730.   DOI
39 Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R. (2010). Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.   DOI
40 Duttweiler, H.M. (1996). A highly sensitive and non-lethal betagalactosidase plate assay for yeast. Trends Genet. 12, 340-341.   DOI
41 Fujii, H., Verslues, P.E., and Zhu, J.K. (2011). Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc. Natl. Acad. Sci. U. S. A. 108, 1717-1722.   DOI
42 Finkelstein, R.R. and Lynch, T.J. (2000). The arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12, 599-609.   DOI
43 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.   DOI
44 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.   DOI
45 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. U. S. A. 106, 8380-8385.   DOI
46 Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2000). Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. U. S. A. 97, 11632-11637.   DOI
47 Takahashi, F., Suzuki, T., Osakabe, Y., Betsuyaku, S., Kondo, Y., Dohmae, N., Fukuda, H., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2018b). A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556, 235-238.   DOI
48 Tian, W., Hou, C., Ren, Z., Pan, Y., Jia, J., Zhang, H., Bai, F., Zhang, P., Zhu, H., He, Y., et al. (2015). A molecular pathway for CO(2) response in Arabidopsis guard cells. Nat. Commun. 6, 6057.   DOI
49 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 acidactivated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 106, 17588-17593.   DOI
50 Vilela, B., Najar, E., Lumbreras, V., Leung, J., and Pages, M. (2015). Casein kinase 2 negatively regulates abscisic acid-activated SnRK2s in the core abscisic acid-signaling module. Mol. Plant 8, 709-721.   DOI
51 Guthrie, C. and Fink, G.R. (1991). Guide to yeast genetics and molecular biology. Methods Enzymol. 194, 1-863.
52 Fujita, Y., Fujita, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2011). ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 124, 509-525.   DOI
53 Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K., et al. (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.   DOI
54 Fujita, Y., Yoshida, T., and Yamaguchi-Shinozaki, K. (2013). Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol. Plant. 147, 15-27.   DOI
55 Vlad, F., Droillard, M.J., Valot, B., Khafif, M., Rodrigues, A., Brault, M., Zivy, M., Rodriguez, P.L., Merlot, S., and Lauriere, C. (2010). Phosphosite mapping, genetic and in planta activation studies reveal key aspects of the different phosphorylation mechanisms involved in activation of SnRK2s. Plant J. 63, 778-790.   DOI
56 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.   DOI
57 Furihata, T., Maruyama, K., Fujita, Y., Umezawa, T., Yoshida, R., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006). Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl. Acad. Sci. U. S. A. 103, 1988-1993.   DOI
58 Giraudat, J., Hauge, B.M., Valon, C., Smalle, J., Parcy, F., and Goodman, H.M. (1992). Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4, 1251-1261.   DOI
59 Holdsworth, M.J., Bentsink, L., and Soppe, W.J. (2008). Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol. 179, 33-54.   DOI
60 Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956.   DOI
61 Walter, M., Chaban, C., Schutze, K., Batistic, O., Weckermann, K., Nake, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., et al. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438.   DOI
62 Wang, P.C., Xue, L., Batelli, G., Lee, S., Hou, Y.J., Van Oosten, M.J., Zhang, H.M., Tao, W.A., and Zhu, J.K. (2013). Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc. Natl. Acad. Sci. U. S. A. 110, 11205-11210.   DOI
63 Kim, S.Y. (2006). The role of ABF family bZIP class transcription factors in stress response. Physiol. Plant. 126, 519-527.   DOI
64 Ichimura, K., Shinozaki, K., Tena, G., Sheen, J., Henry, Y., Champion, A., Kreis, M., Zhang, S.Q., Hirt, H., Wilson, C., et al. (2002). Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301-308.   DOI
65 Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 20, 3901-3907.   DOI
66 Kanno, Y., Jikumaru, Y., Hanada, A., Nambara, E., Abrams, S.R., Kamiya, Y., and Seo, M. (2010). Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol. 51, 1988-2001.   DOI
67 Kim, S.Y., Chung, H.J., and Thomas, T.L. (1997). Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryospecification elements in the Dc3 promoter using a modified yeast onehybrid system. Plant J. 11, 1237-1251.   DOI
68 Xiong, L.M., Schumaker, K.S., and Zhu, J.K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell 14, S165-S183.   DOI
69 Witte, C.P., Noel, L.D., Gielbert, J., Parker, J.E., and Romeis, T. (2004). Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol. Biol. 55, 135-147.   DOI
70 Wooten, M.W. (2002). In-gel kinase assay as a method to identify kinase substrates. Sci. STKE 2002, pl15.
71 Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.   DOI
72 Yoshida, R., Umezawa, T., Mizoguchi, T., Takahashi, S., Takahashi, F., and Shinozaki, K. (2006a). The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J. Biol. Chem. 281, 5310-5318.   DOI