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SCAB1 coordinates sequential Ca2+ and ABA signals during osmotic stress induced stomatal closure in Arabidopsis

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Abstract

Hyperosmotic stress caused by drought is a detrimental threat to plant growth and agricultural productivity due to limited water availability. Stomata are gateways of transpiration and gas exchange, the swift adjustment of stomatal aperture has a strong influence on plant drought resistance. Despite intensive investigations of stomatal closure during drought stress in past decades, little is known about how sequential signals are integrated during complete processes. Here, we discovered that the rapid Ca2+ signaling and subsequent abscisic acid (ABA) signaling contribute to the kinetics of both F-actin reorganizations and stomatal closure in Arabidopsis thaliana, while STOMATAL CLOSURE-RELATED ACTIN BINDING PROTEIN1 (SCAB1) is the molecular switch for this entire process. During the early stage of osmotic shock responses, swift elevated calcium signaling promotes SCAB1 phosphorylation through calcium sensors CALCIUM DEPENDENT PROTEIN KINASE3 (CPK3) and CPK6. The phosphorylation restrained the microfilament binding affinity of SCAB1, which bring about the F-actin disassembly and stomatal closure initiation. As the osmotic stress signal continued, both the kinase activity of CPK3 and the phosphorylation level of SCAB1 attenuated significantly. We further found that ABA signaling is indispensable for these attenuations, which presumably contributed to the actin filament reassembly process as well as completion of stomatal closure. Notably, the dynamic changes of SCAB1 phosphorylation status are crucial for the kinetics of stomatal closure. Taken together, our results support a model in which SCAB1 works as a molecular switch, and directs the microfilament rearrangement through integrating the sequentially generated Ca2+ and ABA signals during osmotic stress induced stomatal closure.

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References

  • Brandt, B., Brodsky, D.E., Xue, S., Negi, J., Iba, K., Kangasjärvi, J., Ghassemian, M., Stephan, A.B., Hu, H., and Schroeder, J.I. (2012). Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109, 10593–10598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt, B., Munemasa, S., Wang, C., Nguyen, D., Yong, T., Yang, P.G., Poretsky, E., Belknap, T.F., Waadt, R., Alemán, F., et al. (2015). Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4, e03599.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R., Tang, X., and Zhou, J.M. (2008). Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146, 323–324.

    Article  Google Scholar 

  • Chen, K., Gao, J., Sun, S., Zhang, Z., Yu, B., Li, J., Xie, C., Li, G., Wang, P., Song, C.P., et al. (2020a). BONZAI proteins control global osmotic stress responses in plants. Curr Biol 30, 4815–4825.e4.

    Article  CAS  PubMed  Google Scholar 

  • Chen, K., Li, G., Bressan, R.A., Song, C., Zhu, J., and Zhao, Y. (2020b). Abscisic acid dynamics, signaling, and functions in plants. JIPB 62, 25–54.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Q., Hu, T., Li, X., Song, C.P., Zhu, J.K., Chen, L., and Zhao, Y. (2022). Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought. Nat Plants 8, 68–77.

    Article  CAS  PubMed  Google Scholar 

  • Choi, W.G., Toyota, M., Kim, S.H., Hilleary, R., and Gilroy, S. (2014). Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111, 6497–6502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Vries, J., Stanton, A., Archibald, J.M., and Gould, S.B. (2016). Streptophyte terrestrialization in light of plastid evolution. Trends Plant Sci 21, 467–476.

    Article  CAS  PubMed  Google Scholar 

  • Dietrich, D., Pang, L., Kobayashi, A., Fozard, J.A., Boudolf, V., Bhosale, R., Antoni, R., Nguyen, T., Hiratsuka, S., Fujii, N., et al. (2017). Root hydrotropism is controlled via a cortex-specific growth mechanism. Nat Plants 3, 17057.

    Article  CAS  PubMed  Google Scholar 

  • Dong, C.H., Xia, G.X., Hong, Y., Ramachandran, S., Kost, B., and Chua, N.H. (2001). ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13, 1333–1346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Entzian, C., and Schubert, T. (2016). Studying small molecule-aptamer interactions using MicroScale Thermophoresis (MST). Methods 97, 27–34.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Y., Gu, Y., Zheng, Z., Wasteneys, G., and Yang, Z. (2005). Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120, 687–700.

    Article  CAS  PubMed  Google Scholar 

  • Fujii, H., and Zhu, J.K. (2012). Osmotic stress signaling via protein kinases. Cell Mol Life Sci 69, 3165–3173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, X.Q., Chen, J., Wei, P.C., Ren, F., Chen, J., and Wang, X.C. (2008). Array and distribution of actin filaments in guard cells contribute to the determination of stomatal aperture. Plant Cell Rep 27, 1655–1665.

    Article  CAS  PubMed  Google Scholar 

  • Gao, X., Wang, X., Ren, F., Chen, J., and Wang, X. (2009). Dynamics of vacuoles and actin filaments in guard cells and their roles in stomatal movement. Plant Cell Environ 32, 1108–1116.

    Article  CAS  PubMed  Google Scholar 

  • Geiger, D., Maierhofer, T., AL-Rasheid, K.A.S., Scherzer, S., Mumm, P., Liese, A., Ache, P., Wellmann, C., Marten, I., Grill, E., et al. (2011). Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4, ra32.

    Article  PubMed  Google Scholar 

  • Geiger, D., Scherzer, S., Mumm, P., Marten, I., Ache, P., Matschi, S., Liese, A., Wellmann, C., Al-Rasheid, K.A.S., Grill, E., et al. (2010). Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107, 8023–8028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geiger, D., Scherzer, S., Mumm, P., Stange, A., Marten, I., Bauer, H., Ache, P., Matschi, S., Liese, A., Al-Rasheid, K.A.S., et al. (2009). Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106, 21425–21430.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong, Z., Xiong, L., Shi, H., Yang, S., Herrera-Estrella, L.R., Xu, G., Chao, D.Y., Li, J., Wang, P.Y., Qin, F., et al. (2020). Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63, 635–674.

    Article  PubMed  Google Scholar 

  • Gu, Y., Li, G., Wang, P., Guo, Y., and Li, J. (2022). A simple and precise method (Y2H-in-frame-seq) improves yeast two-hybrid screening with cDNA libraries. J Genet Genomics 49, 595–598.

    Article  PubMed  Google Scholar 

  • Gupta, A., Rico-Medina, A., and Caño-Delgado, A.I. (2020). The physiology of plant responses to drought. Science 368, 266–269.

    Article  CAS  PubMed  Google Scholar 

  • Hagihara, T., Mano, H., Miura, T., Hasebe, M., and Toyota, M. (2022). Calcium-mediated rapid movements defend against herbivorous insects in Mimosa pudica. Nat Commun 13, 6412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henty-Ridilla, J.L., Li, J., Day, B., and Staiger, C.J. (2014). ACTIN DEPOLYMERIZING FACTOR4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell 26, 340–352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hetherington, A.M., and Woodward, F.I. (2003). The role of stomata in sensing and driving environmental change. Nature 424, 901–908.

    Article  CAS  PubMed  Google Scholar 

  • Higaki, T., Kutsuna, N., Sano, T., Kondo, N., and Hasezawa, S. (2010). Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61, 156–165.

    Article  CAS  PubMed  Google Scholar 

  • Hua, D., Wang, C., He, J., Liao, H., Duan, Y., Zhu, Z., Guo, Y., Chen, Z., and Gong, Z. (2012). A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24, 2546–2561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, S., Blanchoin, L., Kovar, D.R., and Staiger, C.J. (2003). Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J Biol Chem 278, 44832–44842.

    Article  CAS  PubMed  Google Scholar 

  • Huang, S., Robinson, R.C., Gao, L.Y., Matsumoto, T., Brunet, A., Blanchoin, L., and Staiger, C.J. (2005). Arabidopsis VILLIN1 generates actin filament cables that are resistant to depolymerization. Plant Cell 17, 486–501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, S., Waadt, R., Nuhkat, M., Kollist, H., Hedrich, R., and Roelfsema, M.R.G. (2019). Calcium signals in guard cells enhance the efficiency by which abscisic acid triggers stomatal closure. New Phytol 224, 177–187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang, J.U., and Lee, Y. (2001). Abscisic acid-induced actin reorganization in guard cells of dayflower is mediated by cytosolic calcium levels and by protein kinase and protein phosphatase activities. Plant Physiol 125, 2120–2128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imes, D., Mumm, P., Böhm, J., Al-Rasheid, K.A.S., Marten, I., Geiger, D., and Hedrich, R. (2013). Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. Plant J 74, 372–382.

    Article  CAS  PubMed  Google Scholar 

  • Jalakas, P., Takahashi, Y., Waadt, R., Schroeder, J.I., and Merilo, E. (2021). Molecular mechanisms of stomatal closure in response to rising vapour pressure deficit. New Phytol 232, 468–475.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, Y., Wang, J., Xie, Y., Chen, N., and Huang, S. (2017). ADF10 shapes the overall organization of apical actin filaments by promoting their turnover and ordering in pollen tubes. J Cell Sci 130, 3988–4001.

    CAS  PubMed  Google Scholar 

  • Juenger, T.E., and Verslues, P.E. (2023). Time for a drought experiment: Do you know your plants’ water status? Plant Cell 35, 10–23.

    Article  PubMed  Google Scholar 

  • Kim, T.H., Böhmer, M., Hu, H., Nishimura, N., and Schroeder, J.I. (2010). Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61, 561–591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, T.H., Hauser, F., Ha, T., Xue, S., Böhmer, M., Nishimura, N., Munemasa, S., Hubbard, K., Peine, N., Lee, B., et al. (2011). Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr Biol 21, 990–997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knight, H., Trewavas, A.J., and Knight, M.R. (1997). Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12, 1067–1078.

    Article  CAS  PubMed  Google Scholar 

  • Kudla, J., Batistič, O., and Hashimoto, K. (2010). Calcium signals: the lead currency of plant information processing. Plant Cell 22, 541–563.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M., Kummer, U., Parniske, M., Romeis, T., and Schumacher, K. (2018). Advances and current challenges in calcium signaling. New Phytol 218, 414–431.

    Article  PubMed  Google Scholar 

  • Lang, Z.B., and Zuo, J.R. (2015). Say “NO” to ABA signaling in guard cells by S-nitrosylation of OST1. Sci China Life Sci 58, 313–314.

    Article  PubMed  Google Scholar 

  • Leung, J., Bouvier-Durand, M., Morris, P.C., Guerrier, D., Chefdor, F., and Giraudat, J. (1994). Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264, 1448–1452.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Blanchoin, L., and Staiger, C.J. (2015). Signaling to actin stochastic dynamics. Annu Rev Plant Biol 66, 415–440.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Wang, X.Q., Watson, M.B., and Assmann, S.M. (2000). Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287, 300–303.

    Article  CAS  PubMed  Google Scholar 

  • Li, X., Diao, M., Zhang, Y., Chen, G., Huang, S., and Chen, N. (2019). Guard cell microfilament analyzer facilitates the analysis of the organization and dynamics of actin filaments in Arabidopsis guard cells. Int J Mol Sci 20, 2753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, X., Li, J., Wang, W., Chen, N., Ma, T., Xi, Y., Zhang, X., Lin, H., Bai, Y., Huang, S., et al. (2014). ARP2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis. Plant Cell Environ 37, 1548–1560.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Wang, Y., Tan, S., Li, Z., Yuan, Z., Glanc, M., Domjan, D., Wang, K., Xuan, W., Guo, Y., et al. (2020). Root growth adaptation is mediated by PYLs ABA receptor-PP2A protein phosphatase complex. Adv Sci 7, 1901455.

    Article  CAS  Google Scholar 

  • Li, Z., Takahashi, Y., Scavo, A., Brandt, B., Nguyen, D., Rieu, P., and Schroeder, J.I. (2018). Abscisic acid-induced degradation of Arabidopsis guanine nucleotide exchange factor requires calcium-dependent protein kinases. Proc Natl Acad Sci USA 115, E4522–E4531.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lian, N., Wang, X., Jing, Y., and Lin, J. (2021). Regulation of cytoskeleton-associated protein activities: Linking cellular signals to plant cytoskeletal function. JIPB 63, 241–250.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Z., Hou, S., Rodrigues, O., Wang, P., Luo, D., Munemasa, S., Lei, J., Liu, J., Ortiz-Morea, F.A., Wang, X., et al. (2022). Phytocytokine signalling reopens stomata in plant immunity and water loss. Nature 605, 332–339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, Y.J., Li, P., Shimono, M., Corrion, A., Higaki, T., He, S.Y., and Day, B. (2020). Arabidopsis calcium-dependent protein kinase 3 regulates actin cytoskeleton organization and immunity. Nat Commun 11, 6234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, L., Ye, J., Yang, Y., Lin, H., Yue, L., Luo, J., Long, Y., Fu, H., Liu, X., Zhang, Y., et al. (2019). The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-Dependent calcium signature under salt stress. Dev Cell 48, 697–709.e5.

    Article  CAS  PubMed  Google Scholar 

  • Mehlmer, N., Parvin, N., Hurst, C.H., Knight, M.R., Teige, M., and Vothknecht, U.C. (2012). A toolset of aequorin expression vectors for in planta studies of subcellular calcium concentrations in Arabidopsis thaliana. J Exp Bot 63, 1751–1761.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, K., Leube, M.P., and Grill, E. (1994). A protein phosphatase 2C Involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 1452–1455.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, S., Mumm, P., Imes, D., Endler, A., Weder, B., Al-Rasheid, K.A.S., Geiger, D., Marten, I., Martinoia, E., and Hedrich, R. (2010). AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63, 1054–1062.

    Article  CAS  PubMed  Google Scholar 

  • Mori, I.C., Murata, Y., Yang, Y., Munemasa, S., Wang, Y.F., Andreoli, S., Tiriac, H., Alonso, J.M., Harper, J.F., Ecker, J.R., et al. (2006). CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 4, e327.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan, Z., Zhao, Y., Zheng, Y., Liu, J., Jiang, X., and Guo, Y. (2012). A high-throughput method for screening Arabidopsis mutants with disordered abiotic stress-induced calcium signal. J Genet Genomics 39, 225–235.

    Article  CAS  PubMed  Google Scholar 

  • Pardee, J.D., and Spudich, J.A. (1982). Purification of muscle actin. Methods Enzymo 85 Pt B, 164–181.

    Article  CAS  Google Scholar 

  • Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M., and Schroeder, J.I. (1997). Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9, 409–423.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quan, R., Lin, H., Mendoza, I., Zhang, Y., Cao, W., Yang, Y., Shang, M., Chen, S., Pardo, J.M., and Guo, Y. (2007). SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19, 1415–1431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rentel, M.C., and Knight, M.R. (2004). Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135, 1471–1479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronzier, E., Corratgé-Faillie, C., Sanchez, F., Prado, K., Brière, C., Leonhardt, N., Thibaud, J.B., and Xiong, T.C. (2014). CPK13, a noncanonical Ca2+-dependent protein kinase, specifically inhibits KAT2 and KAT1 shaker K+ channels and reduces stomatal opening. Plant Physiol 166, 314–326.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruberti, C., Feitosa-Araujo, E., Xu, Z., Wagner, S., Grenzi, M., Darwish, E., Lichtenauer, S., Fuchs, P., Parmagnani, A.S., Balcerowicz, D., et al. (2022). MCU proteins dominate in vivo mitochondrial Ca2+ uptake in Arabidopsis roots. Plant Cell 34, 4428–4452.

    Article  PubMed  PubMed Central  Google Scholar 

  • Saito, S., and Uozumi, N. (2019). Guard cell membrane anion transport systems and their regulatory components: an elaborate mechanism controlling stress-induced stomatal closure. Plants 8, 9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato, A., Sato, Y., Fukao, Y., Fujiwara, M., Umezawa, T., Shinozaki, K., Hibi, T., Taniguchi, M., Miyake, H., Goto, D.B., et al. (2009). Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem J 424, 439–448.

    Article  CAS  PubMed  Google Scholar 

  • Schulze, S., Dubeaux, G., Ceciliato, P.H.O., Munemasa, S., Nuhkat, M., Yarmolinsky, D., Aguilar, J., Diaz, R., Azoulay-Shemer, T., Steinhorst, L., et al. (2021). A role for calcium-dependent protein kinases in differential CO2- and ABA-controlled stomatal closing and low CO2-induced stomatal opening in Arabidopsis. New Phytol 229, 2765–2779.

    Article  CAS  PubMed  Google Scholar 

  • Schweiger, R., and Schwenkert, S. (2014). Protein-protein interactions visualized by bimolecular fluorescence complementation in tobacco protoplasts and leaves. J Vis Exp 9, 51327.

    Google Scholar 

  • Shi, Y., Liu, X., Zhao, S., and Guo, Y. (2022). The PYR-PP2C-CKL2 module regulates ABA-mediated actin reorganization during stomatal closure. New Phytol 233, 2168–2184.

    Article  CAS  PubMed  Google Scholar 

  • Shkolnik, D., Nuriel, R., Bonza, M.C., Costa, A., and Fromm, H. (2018). MIZ1 regulates ECA1 to generate a slow, long-distance phloem-transmitted Ca2+ signal essential for root water tracking in Arabidopsis. Proc Natl Acad Sci USA 115, 8031–8036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spector, I., Shochet, N.R., Kashman, Y., and Groweiss, A. (1983). Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219, 493–495.

    Article  CAS  PubMed  Google Scholar 

  • Stephan, A.B., Kunz, H.H., Yang, E., and Schroeder, J.I. (2016). Rapid hyperosmotic-induced Ca2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters. Proc Natl Acad Sci USA 113, E5242–5249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sussmilch, F.C., Schultz, J., Hedrich, R., and Roelfsema, M.R.G. (2019). Acquiring control: the evolution of stomatal signalling pathways. Trends Plant Sci 24, 342–351.

    Article  CAS  PubMed  Google Scholar 

  • Tan, Y.Q., Yang, Y., Shen, X., Zhu, M., Shen, J., Zhang, W., Hu, H., and Wang, Y.F. (2023). Multiple cyclic nucleotide-gated channels function as ABA-activated Ca2+ channels required for ABA-induced stomatal closure in Arabidopsis. Plant Cell 35, 239–259.

    Article  PubMed  Google Scholar 

  • Tardieu, F., Simonneau, T., and Muller, B. (2018). The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annu Rev Plant Biol 69, 733–759.

    Article  CAS  PubMed  Google Scholar 

  • Teardo, E., Carraretto, L., Moscatiello, R., Cortese, E., Vicario, M., Festa, M., Maso, L., De Bortoli, S., Calì, T., Vothknecht, U.C., et al. (2019). A chloroplast-localized mitochondrial calcium uniporter transduces osmotic stress in Arabidopsis. Nat Plants 5, 581–588.

    Article  CAS  PubMed  Google Scholar 

  • van Kleeff, P.J.M., Gao, J., Mol, S., Zwart, N., Zhang, H., Li, K.W., and de Boer, A.H. (2018). The Arabidopsis GORK K+-channel is phosphorylated by calcium-dependent protein kinase 21 (CPK21), which in turn is activated by 14–3-3 proteins. Plant Physiol Biochem 125, 219–231.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wang, P., Zhao, Y., Li, Z., Hsu, C.C., Liu, X., Fu, L., Hou, Y.J., Du, Y., Xie, S., Zhang, C., et al. (2018). Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol Cell 69, 100–112.e6.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y.F., Munemasa, S., Nishimura, N., Ren, H.M., Robert, N., Han, M., Puzõrjova, I., Kollist, H., Lee, S., Mori, I., et al. (2013). Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. Plant Physiol 163, 578–590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Z., Zhang, Y., Liu, Y., Fu, D., You, Z., Huang, P., Gao, H., Zhang, Z., and Wang, C. (2023). Calcium-dependent protein kinases CPK21 and CPK23 phosphorylate and activate the iron-regulated transporter IRT1 to regulate iron deficiency in Arabidopsis. Sci China Life Sci 66, 2646–2662.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Y., Zhao, S., Tian, H., He, Y., Xiong, W., Guo, L., and Wu, Y. (2013). CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells. J Exp Bot 64, 3327–3338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie, X., Wang, Y., Williamson, L., Holroyd, G.H., Tagliavia, C., Murchie, E., Theobald, J., Knight, M.R., Davies, W.J., Leyser, H.M.O., et al. (2006). The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr Biol 16, 882–887.

    Article  CAS  PubMed  Google Scholar 

  • Xu, Z., Liu, H., Meng, Y., Yin, J., Ren, H., Li, M.H., Yang, S., Tang, S., Jiang, Y., and Jiang, L. (2023). Nitrogen addition and mowing alter drought resistance and recovery of grassland communities. Sci China Life Sci 66, 1682–1692.

    Article  CAS  PubMed  Google Scholar 

  • Yang, W., Kong, Z., Omo-Ikerodah, E., Xu, W., Li, Q., and Xue, Y. (2008). Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). J Genet Genomics 35, 531–S2.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y., Zhao, Y., Zheng, W., Zhao, Y., Zhao, S., Wang, Q., Bai, L., Zhang, T., Huang, S., Song, C., et al. (2022). Phosphatidylinositol 3-phosphate regulates SCAB1-mediated F-actin reorganization during stomatal closure in Arabidopsis. Plant Cell 34, 477–494.

    Article  PubMed  Google Scholar 

  • Yip Delormel, T., and Boudsocq, M. (2019). Properties and functions of calcium-dependent protein kinases and their relatives in Arabidopsis thaliana. New Phytol 224, 585–604.

    Article  CAS  PubMed  Google Scholar 

  • Yuan, F., Yang, H., Xue, Y., Kong, D., Ye, R., Li, C., Zhang, J., Theprungsirikul, L., Shrift, T., Krichilsky, B., et al. (2014). OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371.

    Article  CAS  PubMed  Google Scholar 

  • Zeevaart, J.A.D. (1980). Changes in the levels of abscisic acid and its metabolites in excised leaf blades of Xanthium strumarium during and after water stress. Plant Physiol 66, 672–678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Liu, D., Yang, B., Liu, W.Z., Mu, B., Song, H., Chen, B., Li, Y., Ren, D., Deng, H., et al. (2020). Arabidopsis CPK6 positively regulates ABA signaling and drought tolerance through phosphorylating ABA-responsive element-binding factors. J Exp Bot 71, 188–203.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, W., Zhao, Y., Guo, Y., and Ye, K. (2012). Plant actin-binding protein SCAB1 is dimeric actin cross-linker with atypical pleckstrin homology domain. J Biol Chem 287, 11981–11990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X., Man, Y., Zhuang, X., Shen, J., Zhang, Y., Cui, Y., Yu, M., Xing, J., Wang, G., Lian, N., et al. (2021). Plant multiscale networks: charting plant connectivity by multi-level analysis and imaging techniques. Sci China Life Sci 64, 1392–1422.

    Article  PubMed  Google Scholar 

  • Zhao, C., Wang, Y., Chan, K.X., Marchant, D.B., Franks, P.J., Randall, D., Tee, E.E., Chen, G., Ramesh, S., Phua, S.Y., et al. (2019). Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land. Proc Natl Acad Sci USA 116, 5015–5020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, S., Jiang, Y., Zhao, Y., Huang, S., Yuan, M., Zhao, Y., and Guo, Y. (2016a). CASEIN KINASE1-LIKE PROTEIN2 regulates actin filament stability and stomatal closure via phosphorylation of actin depolymerizing factor. Plant Cell 28, 1422–1439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, S.S., Zhao, Y.X., and Guo, Y. (2015). 14–3-3 λ protein interacts with ADF1 to regulate actin cytoskeleton dynamics in Arabidopsis. Sci China Life Sci 58, 1142–1150.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Y., Chan, Z., Gao, J., Xing, L., Cao, M., Yu, C., Hu, Y., You, J., Shi, H., Zhu, Y., et al. (2016b). ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci USA 113, 1949–1954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, Y., Xing, L., Wang, X., Hou, Y.J., Gao, J., Wang, P., Duan, C.G., Zhu, X., and Zhu, J.K. (2014). The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Sci Signal 7, ra53.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, Y., Zhao, S., Mao, T., Qu, X., Cao, W., Zhang, L., Zhang, W., He, L., Li, S., Ren, S., et al. (2011). The plant-specific actin binding protein SCAB1 stabilizes actin filaments and regulates stomatal movement in Arabidopsis. Plant Cell 23, 2314–2330.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu, J.K. (2016). Abiotic stress signaling and responses in plants. Cell 167, 313–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, S.Y., Yu, X.C., Wang, X.J., Zhao, R., Li, Y., Fan, R.C., Shang, Y., Du, S.Y., Wang, X.F., Wu, F.Q., et al. (2007). Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19, 3019–3036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgement

This work was supported by the National Natural Science Foundation of China (31921001). We thank Professor Yi Wang at China Agricultural University, China, for providing cpk3-1, cpk3-2, cpk6-4 seeds. We thank Professor Cun Wang at Northwest A&F University, China, for providing cpk6-1 seeds. We thank Professor Yang Zhao at Chinese Academy of Sciences, China, for providing RAB18pro:GFP seeds.

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  1. State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural University, Beijing, 100193, China

    Tianren Zhang, Li Bai & Yan Guo

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  1. Tianren Zhang
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  2. Li Bai
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Correspondence to Yan Guo.

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Zhang, T., Bai, L. & Guo, Y. SCAB1 coordinates sequential Ca2+ and ABA signals during osmotic stress induced stomatal closure in Arabidopsis. Sci. China Life Sci. 67, 1–18 (2024). https://doi.org/10.1007/s11427-023-2480-4

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  • DOI: https://doi.org/10.1007/s11427-023-2480-4

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