Abstract
Plant development and reproduction depend on a precise recognition of environmental conditions and the integration of this information with endogenous metabolic and developmental cues. Calcium ions have been firmly established as ubiquitous second messengers functioning in these processes. Calcium signal deciphering and signal-response coupling often involve calcium-binding proteins as responders or relays in this information flow. Here we review the calcineurin B-like protein (CBL) calcium sensor/CBL-interacting protein kinase (CIPK) network as a newly emerging signaling system mediating a complex array of environmental stimuli. We focus particularly on the mechanisms generating signaling specificity. Moreover, we emphasize the functional implications that are emerging from the analyses of CBL and CIPK loss-of-function mutants.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- CBL:
-
Calcineurin B-like protein
- CDPK:
-
Calcium-dependent protein kinase
- CIPK:
-
CBL-interacting protein kinase
- MAPK:
-
Mitogen-activated protein kinase
References
Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063
Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470
Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057
Barabasi AL, Oltvai ZN (2004) Network biology: understanding the cells functional organization. Nat Rev Genet 5:101–113
Bijlmakers MJ, Marsh M (2003) The on-off story of protein palmitoylation. Trends Cell Biol 13:32–42
Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5:241–246
Burgoyne RD, Weiss JL (2001) The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J 353:1–12
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845
Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415–420
Farazi TA, Waksman G, Gordon JI (2001) The biology and enzymology of protein N-myristoylation. J Biol Chem 276:39501–39504
Gilroy S, Trewavas A (2001) Signal processing and transduction in plant cells: the end of the beginning? Nat Rev Mol Cell Biol 2:307–314
Gong D, Gong Z, Guo Y, Chen X, Zhu JK (2002a) Biochemical and functional characterization of PKS11, a novel Arabidopsis protein kinase. J Biol Chem 277:28340–28350
Gong D, Gong Z, Guo Y, Zhu JK (2002b) Expression, activation, and biochemical properties of a novel Arabidopsis protein kinase. Plant Physiol 129:225–234
Gong D, Guo Y, Jagendorf AT, Zhu JK (2002c) Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance. Plant Physiol 130:256–264
Gong D, Zhang C, Chen X, Gong Z, Zhu JK (2002d) Constitutive activation and transgenic evaluation of the function of an Arabidopsis PKS protein kinase. J Biol Chem 277:42088–42096
Guo Y, Halfter U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383–1400
Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740
Harper JF (2001) Dissecting calcium oscillators in plant cells. Trends Plant Sci 6:395–397
Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Physiol Plant Mol Biol 55:263–288
Hetherington AM, Brownlee C (2004) the generation of Ca2+ signals in plants. Annu Rev Plant Physiol Plant Mol Biol 55:401–427
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680
Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678
Kim KN, Cheong YH, Gupta R, Luan S (2000) Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol 124:1844–1853
Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423
Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267
Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134:43–58
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
Lewit-Bentley A, Rety S (2000) EF-hand calcium-binding proteins. Curr Opin Struct Biol 10:637–643
Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945
Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734
Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123
Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell [Suppl] 14:389–400
McAinsh MR, Hetherington AM (1998) Encoding specificity in Ca2+ signaling systems. Trends Plant Sci 3:32–36
McCarty DR, Chory J (2000) Conservation and innovation in plant signaling pathways. Cell 103:201–209
Nagae M, Nozawa A, Koizumi N, Sano H, Hashimoto H, Sato M, Shimizu T (2003) The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana. J Biol Chem 278:42240–42246
Nozawa A, Koizumi N, Sano H (2001) An Arabidopsis SNF1-related protein kinase, AtSR1, interacts with a calcium-binding protein, AtCBL2, of which transcripts respond to light. Plant Cell Physiol 42:976–981
Ohba H, Steward N, Kawasaki S, Berberich T, Ikeda Y, Koizumi N, Kusano T, Sano H (2000) Diverse response of rice and maize genes encoding homologs of WPK4, an SNF1-related protein kinase from wheat, to light, nutrients, low temperature and cytokinins. Mol Gen Genet 263:359–366
Ohta M, Guo Y, Halfter U, Zhu JK (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100:11771–11776
Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D‘Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor Calcineurin B-Like 9 modulates ABA sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441
Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99:9061–9066
Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556–5567
Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell [Suppl] 14:401–417
Scrase-Field SA, Knight MR (2003) Calcium: just a chemical switch? Curr Opin Plant Biol 6:500–506
Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405
Snedden W, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304
Trewavas A (2002) Mindless mastery. Nature 415:841
Vranova E, Atichartpongkul S, Villarroel R, Van Montagu M, Inze D, Van Camp W (2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc Natl Acad Sci USA 99:10870–10875
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell [Suppl] 14:165–183
Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512
Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191
Acknowledgements
Research in the authors laboratory is supported by grants from the Deutsche Forschungsgemeinschaft to J.K. We thank Dr. Ralph Bock for stimulating discussions during the preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Batistic, O., Kudla, J. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219, 915–924 (2004). https://doi.org/10.1007/s00425-004-1333-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-004-1333-3