Skip to main content
Log in

Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network

  • Review
  • Published:
Planta Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Barabasi AL, Oltvai ZN (2004) Network biology: understanding the cells functional organization. Nat Rev Genet 5:101–113

    Article  CAS  PubMed  Google Scholar 

  • Bijlmakers MJ, Marsh M (2003) The on-off story of protein palmitoylation. Trends Cell Biol 13:32–42

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5:241–246

    Google Scholar 

  • Burgoyne RD, Weiss JL (2001) The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J 353:1–12

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415–420

    Article  CAS  PubMed  Google Scholar 

  • Farazi TA, Waksman G, Gordon JI (2001) The biology and enzymology of protein N-myristoylation. J Biol Chem 276:39501–39504

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Harper JF (2001) Dissecting calcium oscillators in plant cells. Trends Plant Sci 6:395–397

    Google Scholar 

  • Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Physiol Plant Mol Biol 55:263–288

    Article  CAS  Google Scholar 

  • Hetherington AM, Brownlee C (2004) the generation of Ca2+ signals in plants. Annu Rev Plant Physiol Plant Mol Biol 55:401–427

    Article  CAS  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Lewit-Bentley A, Rety S (2000) EF-hand calcium-binding proteins. Curr Opin Struct Biol 10:637–643

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • McCarty DR, Chory J (2000) Conservation and innovation in plant signaling pathways. Cell 103:201–209

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Snedden W, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304

    Article  Google Scholar 

  • Trewavas A (2002) Mindless mastery. Nature 415:841

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Jörg Kudla.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1333-3

Keywords

Navigation