8 Circadian Regulation of Ca2+ Signalling
Annual Plant Reviews book series, Volume 21: Endogenous Plant Rhythms
Michael J. Gardner,
Antony N. Dodd,
Carlos T. Hotta,
Dale Sanders,
Alex A. R. Webb,
Michael J. Gardner
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorAntony N. Dodd
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorCarlos T. Hotta
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorDale Sanders
The Plant Laboratory, Biology Department, P.O. Box No 373, York, YO10 5YW UK
Search for more papers by this authorAlex A. R. Webb
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorMichael J. Gardner,
Antony N. Dodd,
Carlos T. Hotta,
Dale Sanders,
Alex A. R. Webb,
Michael J. Gardner
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorAntony N. Dodd
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorCarlos T. Hotta
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorDale Sanders
The Plant Laboratory, Biology Department, P.O. Box No 373, York, YO10 5YW UK
Search for more papers by this authorAlex A. R. Webb
Department of Plant Sciences, University of Cambridge, Downing Site, Downing Street, Cambridge, CB2 3EA UK
Search for more papers by this authorFirst published: 19 April 2018
This article was originally published in 2005 in Endogenous Plant Rhythms, Volume 21 (ISBN 9781405123761) of the Annual Plant Reviews book series, this volume edited by Anthony J W Hall and Harriet McWatterss. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
The sections in this article are
- Introduction
- Ca2+ Signalling is Ubiquitous and Versatile
- The Cellular Basis of Circadian Oscillations of Plant [Ca2+ ]cyt
- The Cellular Basis of Circadian Oscillations of [Ca2+ ]cyt in Mammals
- A Comparison of the Circadian Regulation of Ca2+ Homeostasis in Both SCN and Plant Cells
- Molecular Regulation of Circadian Ca2+ Signalling in Plants
- Physiological Targets for Circadian Oscillations of [Ca2+ ]cyt
- Conclusions and Future Prospects
- Acknowledgements
- Abbreviations
References
- Agostino, P.V., Ferreyra, G.A., Murad, A.D., Watanabe, Y. & Golombek, D.A. (2004) Diurnal, circadian and photic regulation of calcium/calmodulin-dependent kinase II and neuronal nitric oxide synthase in the hamster suprachiasmatic nuclei. Neurochem. Int., 44, 61–69.
- Allen, G.J., Chu, S.P., Harrington, C.L., Schumacher, K., Hoffman, T., Tang, Y.Y., Grill, E. & Schroeder, J.I. (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature, 411, 1053–1057.
- Allen, G.J., Chu, S.P., Schumacher, K., Shimazaki, C.T., Vafeados, D., Kemper, A., Hawke, S.D., Tallman, G., Tsien, R.Y., Harper, J.F., Chory, J. & Schroeder, J.I. (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science, 289, 2338–2342.
- Chan, C.W., Schorrak, L.M., Smith Jr, R.K., Bent, A.F. & Sussman, M.R. (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol., 132, 728–731.
- Colwell, C.S. (2000) Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur. J. Neuroscience, 12, 571–576.
- Dodd, A.N., Parkinson, K. & Webb, A.A.R. (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phyt., 162, 63–70.
- Dodd, A.N., Love, J. & Webb, A.A.R. (2005) The plant clock shows its metal: circadian regulation of cytosolic free Ca2+ . Trends Plant. Sci. 10, 15–21.
- Evans, N.H., McAinsh, M.R. & Hetherington A.M. et al. (2001) Calcium oscillations in higher plants. Current Curr. Op. Plant Biol., 4, 415–420.
-
Fricker, M.D., Plieth, C., Knight, H., Blancaflor, E., Knight, M.R., White, N.S. & Gilroy, S. (1999) Fluorescence and luminescence techniques to probe ion activities in living plant cells. In: Fluorescent and Luminescent Probes for Biological Activity
second edition (ed W.T. Mason). Academic Press, San Diego.
10.1016/B978-012447836-7/50044-0 Google Scholar
- Friedman, H., Goldschmidt E.E., Spiegelstein, H. & Halevy, A.H. et al. (1992) A rhythm in the flowering response of photoperiodically-induced Pharbitis nil to agents affecting cytosolic calcium and pH. Physiol. Plant, 85, 57–60.
- Garcia-Mata, C., Gay, R., Sokolovski, S., Hills, A., Lamattina, L. & Blatt, M.R. (2003) Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signalling pathways. PNAS Proc. Natl. Acad. Sci. USA, 100, 11116–11121.
- Geisler, M., Frangne, N., Gomes, E., Martinoia, E. & Palmgren, M.G. (2000) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol., 124, 1814–1827.
- Gilroy, S., Read, N.D. & Trewavas, A.J. (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature, 346, 769–771.
- Golombek, D.A. & Ralph, M.R. (1994) KN-62, an inhibitor of Ca2+/calmodulin kinase II, attenuates circadian responses to light. Neuroreport, 5, 1638–1640.
- Golombek, D.A. & Ralph, M.R. (1995) Circadian responses to light: the calmodulin connection. Neurosci Lett., 192, 101–104.
- Golombek, D.A., Agostino, P.V., Plano, S.A. & Ferreyra, G.A. (2004) Signalling in the mammalian circadian clock: the NO/cGMP pathway. Neurochem Int., 45, 929–936.
- Gómez, L.A. & Simón, E. (1995) Circadian rhythm of Robinia pseudoacacia leaflet movement: Role of calcium and phytochrome. Photochem. Photobiol., 61, 210–215.
- Han, S., Tang, R., Anderson, L.K., Woerner, T.E. & Pei Z-M. (2003) A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature, 425, 196–200.
- Hannibal, J. (2002) Neurotransmitters of the retino-hypothalamic tract. Cell and Tissue Res., 309, 73–88.
- Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.S., Han, B., Zhu, T., Wang, X., Kreps, J.A. & Kay, S.A. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science, 290, 2110–2113.
- Harmer, S.L., Panda, S. & Kay, S.A. (2001) Molecular basis of circadian rhythms. Ann. Rev. Cell Dev. Biol., 17, 215–253.
- He, Y., Tang, R-H., Hao, Y., Stevens, R.D., Cook, C.W., Ahn, S.M., Jing, L., Yang, Z., Chen, L., Guo, F., Fiorani, F., Jackson, R.B., Crawford, N.M. & Pei, Z-M. (2004) Nitric oxide represses the Arabidopsis floral transition. Science, 305, 1968–1971.
- Hetherington, A.M., Gray, J.E., Leckie, C.P., McAinsh, M.R., Ng, C., Pical, C., Priestley, A.J., Staxén, I. & Webb, A.A.R. (1998) The control of specificity in guard cell signal transduction. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 353, 1489–1494.
- Hetherington, A.M. & Brownlee, C. (2004) The generation of Ca2+ signals in plants. Ann. Rev. Plant Biol., 55, 401–427.
- Hirschi, K.D. (1999) Expression of Arabidopsis CAX1 in tobacco: Altered calcium homeostasis and increased stress sensitivity. Plant Cell, 11, 2113–2122.
- Hirschi, K. (2001) Vacuolar H+/Ca2+ transport: Who's directing the traffic? Trends Plant Sci., 6, 100–104.
- Hirschi, K.D. (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol., 136, 2438–2442.
- Holdaway-Clark, T.L. & Hepler, P.K. (2003) Control of pollen tube growth: the role of ion gradients and fluxes. New Phytol., 159, 539–563.
- Honma, S. & Honma, K. (2003) The biological clock: Ca2+ links the pendulum to the hands. Trends Neurosci., 26, 650–653.
- Ikeda, M. (2003) Response to Honma and Honma: Do circadian rhythms in cytosolic Ca2+ modulate autonomous gene transcription cycles in the SCN? Trends Neurosci., 26, 654.
- Ikeda, M. (2004) Calcium dynamics and circadian rhythms in suprachiasmatic nucleus neurons. The Neuroscintist, 10, 315–324.
- Ikeda, M., Sugiyama, T., Wallace, C.S., Gompf, H.S., Yoshioka, T., Miyawaki, A. & Allen, C.N. (2003) Circadian dynamics of circadian and nuclear Ca2+ in single suprachiasmatic nucleus neurones. Neuron, 38, 253–263.
- Ivanova, T.N. & Iuvone, P.M. (2003) Circadian rhythm and photic control of cAMP level in chick retinal cell cultures: a mechanism for coupling the circadian oscillator to the melatonin-synthesizing enzyme, arylalkylamine N-acetyltransferase, in photoreceptor cells. Brain Res., 991, 96–103.
- Jaworski, K., Szmidt-Jaworska, A., Tretyn, A. & Kopcewicz, J. (2003) Biochemical evidence for a calcium-dependent protein kinase from Pharbitis nil and its involvement in photoperiodic flower induction. Phytochemistry, 62, 1047–1055.
- Johnson, C.H., Knight, M.R., Kondo, T., Masson, P., Sedbook, J., Haley, A. & Trewavas, A. (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science, 269, 1863–1865.
- Jung, J.Y., Kim, Y.W., Kwak, J.M., Hwang, J.U., Young, J., Schroeder, J.I., Hwang, I. & Lee, Y. (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell, 14, 2399–2412.
- Kim, K.N., Cheong, Y.H., Gupta, R. & Luan, S. (2000) Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol., 124, 1844–1853.
- Klüsener, B., Young, J.J., Murata, Y., Allen, G.J., Mori, I.C., Hugouvieux, V. & Schroeder, J.I. (2002) Convergence of calcium signalling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol., 130, 2152–2163.
- Ko, G.Y., Ko, M.L. & Dryer, S.E. (2004) Circadian regulation of cGMP-gated channels of vertebrate cone photoreceptors: Role of cAMP and Ras. J. Neurosci., 24, 1296–1304.
- Kudla, J., Xu, Q., Harter, K., Gruissem, W. & Luan, S. (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA, 96, 4718–4723.
- Lamotte, O., Gould, K., Lecourieux, D., Sequeira-Legrand, A., Lebrun-Garcia, A., Durner, J., Pugin, A. & Wendehenne, D. (2004) Analysis of nitric oxide signalling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiology Physiol., 135, 516–529.
- Leckie, C.P., McAinsh, M.R., Allen G.J., Sanders, D. & Hetherington, A.M. (1998) Abscisic acid-mediated stomatal closure mediated by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA, 95, 15837–15842.
- Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D. & Hetherington, A M. (1998) Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA, 95, 15837–15842.
- Lee, J.Y., Yoo, B.C. & Harmon, A.C. (1998) Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. Biochemistry, 37, 6801–6809.
- Lemtiri-Chlieh, F. & Berkowitz, G.A. (2004) Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J. Biol. Chem., 279, 35306–35312.
- Leng, Q., Mercier, R.W., Yao, W.Z. & Berkowitz, G.A. (1999) Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol., 121, 753–761.
- Leng, Q., Mercier, R.W., Hua, B-G., Fromm, H. & Berkowitz, G.A. (2002) Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol., 128, 400–410.
- Love, J., Dodd, A.N. & Webb, A.A.R. (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell, 16, 956–966.
- McAinsh, M.R., Webb, A.A.R., Taylor, J.E. & Hetherington, A.M. (1995) Stimulus-induced oscillations in guard cell cytoplasmic free calcium. Plant Cell, 7, 1207–1219.
- McAinsh, M.R. & Hetherington, A.M. (1998). Encoding specificity in Ca2+ signalling systems. Trends Plant Sci., 3, 32–36.
- Mills, C.E. 1999–2004. Bioluminescence of Aequorea, a hydromedusa. Electronic internet document available at http://faculty.washington.edu/cemills/Aequorea.html. Published by the author, web page established June 1999, last updated 2004.
- Morot-Gaudry-Talarmain, Y., Rockel, P., Moureaux, T., Quillere, I., Leydecker, M.T., Kaiser, W.M. & Morot-Gaudry, J.F. (2002) Nitrite accumulation and nitric oxide emission in relation to cellular signalling in nitrite reductase antisense tobacco. Planta, 215, 708–715.
- Navazio, L., Mariani, P. & Sanders, D. (2001) Mobilization of Ca2+ by cyclic ADP-ribose from endoplasmic reticulum of cauliflower florets. Plant Physiol., 125, 2129–21238.
- Ng, C.K.Y., Carr, K., McAinsh, M.R., Powell, B. & Hetherington, A.M. (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature, 410, 596–599.
- Pandey, S. & Assmann, S.M. (2004) The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signalling. Plant Cell, 16, 1616–1632.
- Park, D., Lee, S., Jun, K., Hong, Y.M., Kim, D.Y., Kim, Y.I. & Shin, H.S. (2003) Translation of clock rhythmicity into neural firing in the suprachiasmatic nucleus requires mGluR-PLCβ4 signalling. Nature Neurosci., 6, 571–576.
- Pennartz, C.M.A., de Jeu, M.T.G., Bos, N.P.A., Schaap, J. & Geurtsen, A.M.S. (2002) Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature, 416, 286–290.
- Roberts, D.M. & Harmon, A.C. (1992) Calcium modulated protein targets of intracellular calcium signals in higher plants. Ann. Rev. Plant. Physiol. Plant Mol. Biol., 43, 375–414.
- Sai, J. & Johnson, C.H. (1999) Different circadian oscillators control Ca2+ fluxes and Lhcb gene expression. Proc. Natl. Acad. Sci. USA, 96, 11659–11663.
- Sai, J.Q. & Johnson, C.H. (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell, 14, 1279–1291.
- Sánchez, J-P, Duque, P. & Chua, N-H. (2004) ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. Plant J., 38, 381–395.
- Sanders, D., Pelloux, J., Brownlee, C & Harper, J.F. (2002) Calcium at the crossroads of signalling. Plant Cell, 14, S401–S417.
- Schaffer, R., Landgraf, J., Accerbi, M., Simon, V., Larson, M. & Wisman E. (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell, 13, 113–123.
- Shacklock, P.S., Read, N.D. & Trewavas, A.J. (1992) Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature, 358, 753–755.
- Staxèn, I., Pical, C., Montogomery, L.T., Gray, J.E., Hetherington, A.M. & McAinsh, M.R. (1999) Abscisic acid induces oscillations in guard cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc. Natl. Acad. Sci. USA, 96, 1779–1784.
- Stoelzle, S., Kagawa, T., Wada, M., Hedrich, R. & Dietrich, P. (2003) Blue light activates calciumpermeable channels in Arabidopsis mesophyll cells via the phototropin signalling pathway. Proc. Natl. Acad. Sci. USA, 100, 1456–1461.
- Sugiyama, T., Yoshioka, T. & Ikeda M. (2004) mPer2 antisense oligonucleotides inhibit mPer2 expression but not circadian rhythms of physiological activity in cultured suprachiasmatic nucleus neurones. Biochem. Biophys. Res. Comm., 323, 479–483.
- Tischkau, S.A., Mitchell J.W., Pace, L.A., Barnes, J.W., Barnes, J.A. & Gillette, M.U. (2004) Protein kinase G Type II is required for night-to-day progression of the mammalian circadian clock. Neuron, 43, 539–549.
- Volotovski, I.D., Sokolovsky, S.G., Molchan, O.V. & Knight, M.R. (1998) Second messengers mediate increases in cytosolic calcium in tobacco protoplasts. Plant Physiol., 117, 1023–1030.
- Webb, A.A.R. (2003) The physiology of circadian rhythms in plants. New Phytologist, 160, 281–303.
- Webb, A.A.R., Larman, M.G., Montgomery, L.T., Taylor, J.E. & Hetherington, A.M. (2001) The role of calcium in ABA-induced gene expression and stomatal movements. Plant Journal, 26, 351–362.
- Wood, N.T., Haley, A., Viry-Moussaïd, M., Johnson, C.H., van der Luit, A.H. & Trewavas, A.J. (2001) The calcium rhythms of different cell types oscillate with different circadian phases. Plant Physiol., 125, 787–796.
- Wu, L., Niemeyer, B., Colley, N., Socolich, M. & Zucker C.S. (1995) Regulation of PLC-mediated signalling in vivo by CDP-diacylglycerol synthase. Nature, 373, 216–222.
- Yang, Y., Cheng, P., Zhi, G. & Liu, Y. (2001) Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J. Biol. Chem., 276, 41064–41072.
- Zielinski, R.E. (1998) Calmodulin and calmodulin-binding proteins in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol., 49, 697–725.
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