Calcium Signalling in Plants


Ca2+ is an important signal transduction molecule that has been shown to regulate responses to a large number of environmental stimuli in plants and control many developmental processes. These stimuli induce the formation of Ca2+ signals within a cell, which are generated through the action of Ca2+ release and uptake from and into internal cellular stores or the apoplast by the activity of Ca2+ channels, pumps and exchangers. These signals take the form of elevations of Ca2+ with specific spatio‐temporal characteristics which are thought to denote the initial stimulus and mediate an appropriate cellular response. Information is therefore hypothesised to be encoded in these signals, which are decoded and relayed to downstream gene expression regulators and protein kinases via an array of Ca2+‐binding sensor proteins.

Key Concepts:

  • Calcium signals allow plants to specifically sense and respond to environmental stimuli.

  • Calcium signals are generated through the coordinated action of calcium influx channels and calcium efflux transporters.

  • A large network of calcium‐binding proteins act as calcium sensors and relay calcium signals to downstream effector proteins.

Keywords: Arabidopsis; calcium; calcium transport; calmodulin; protein kinases; signal transduction; transcription factors

Figure 1.

Schematic highlighting the key steps in Ca2+ signalling pathways. Stimuli such as pathogen elicitors, ABA, H2O2 and cold, show specific cytosolic Ca2+ signatures after influx of Ca2+. Ca2+ binds to sensors such as calmodulin (CaM), CaM‐like proteins (CML), calcium‐dependent protein kinases (CDPK), and calcineurin B‐like proteins (CBL) (which forms a complex with Ca2+‐independent protein kinase (CIPK)). Ca2+ sensors activate transcription factors (TF) and other proteins either by direct binding or through phosphorylation (P). TFs bind DNA and cause up‐ or down‐regulation of gene expression. CAMTA, CaM‐binding transcription activator; CBP60, CaM‐binding protein; TGA, basic leucine zipper (bZIP) transcription factor; MYB, plant homologue of animal myeloblastosis TFs; WRKY, TF with conserved domain containing these amino acids.

Figure 2.

The distribution of Ca2+ transporters within a typical plant cell. Plants possess Ca2+‐permeable influx channels (blue rectangles), as well as vacuolar Ca2+/H+ exchangers (green cylinder) and Ca2+ pumps (red ovals) for extruding Ca2+. All named proteins are from Arabidopsis thaliana. ACA, autoinhibited Ca2+‐ATPase; CAX, Ca2+/H+ exchanger; CNGC, cyclic nucleotide gated channel; DACC, depolarisation‐activated Ca2+ channel; ECA, ER‐type Ca2+‐ATPase; GLR, glutamate receptor‐like channel; HACC, hyperpolarisation‐activated Ca2+ channel; IP3R‐like, inositol‐1,4,5‐trisphosphate receptor‐like channel; MCC, mechanosensitive Ca2+ channel; NAADPR, nicotinic acid adenine dinucleotide phosphate receptor channel; RyR‐like, cyclic ADP‐ribose‐activated ryanodine receptor‐like channel; TPC, two‐pore channel, a slow‐activating vacuolar (SV) Ca2+ channel; VVCC, vacuolar voltage‐gated Ca2+ channel. Courtesy of Dr. James Connorton.

Figure 3.

Putative pathways for pathogen‐mediated, Ca2+‐dependent activation of plant defence responses. Binding of an elicitor (AtPep) to a receptor (AtPepR1) activates adenylyl cyclase (AC) and/or guanylyl cyclase (GC), which generate cAMP or cGMP, respectively. Increase in cAMP and cGMP concentration activates cyclic nucleotide gated channels (CNGC), which causes influx of Ca2+ into the cytosol. Ca2+ binding to calmodulin (CaM) and calcium‐dependent protein kinases (CDPK) indirectly activates the hypersensitive response (HR), defence‐related gene expression and increased salicylic acid (SA) production. CaM activates NO synthase, producing NO which acts in conjunction with H2O2 generated from CDPK‐activated NADPH oxidase in order to stimulateHR and gene expression. CaM binding to transcription factors (TF) (e.g. CAMTA, WRKY and CBP60) activates gene expression, while CDPK may phosphorylate TFs which can then bind to DNA (dashed arrows). Red line depicts inhibition of CNGC activity by Ca2+/CaM.



Ali R, Ma W, Lemtiri‐Chlieh F et al. (2007) Death don't have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel2 and innate immunity. Plant Cell 19: 1081–1095.

Ali R, Zielinski RE and Berkowitz GA (2006) Expression of plant cyclic nucleotide‐gated cation channels in yeast. Journal of Experimental Botany 57: 125–138.

Allen GJ, Chu SP, Schumacher K et al. (2000) Alteration of stimulus‐specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289: 2338–2342.

Anil VS, Rajkumar P, Kumar P and Mathew MK (2008) A plant Ca2+ pump, ACA2, relieves salt hypersensitivity in yeast. Modulation of cytosolic calcium signature and activation of adaptive Na+ homeostasis. Journal of Biological Chemistry 283: 3497–3506.

Boursiac Y, Lee SM, Romanowsky SM et al. (2010) Disruption of the vacuolar calcium‐ATPases in Arabidopsis results in the activation of a salicylic acid‐dependent programmed cell death pathway. Plant Physiology 154: 1158–1171.

Catalá R, Santos E, Alonso JM et al. (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold‐acclimation response in Arabidopsis. Plant Cell 15: 2940–2951.

Cheng NH, Pittman JK, Barkla BJ et al. (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15: 347–364.

Cheng NH, Pittman JK, Shigaki T et al. (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiology 138: 2048–2060.

Clough SJ, Fengler KA, Yu IC et al. (2000) The Arabidopsis dnd1 ‘defense, no death’ gene encodes a mutated cyclic nucleotide‐gated ion channel. Proceedings of the National Academy of Sciences of the USA 97: 9323–9328.

Conn SJ, Gilliham M, Athman A et al. (2011) Cell‐specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. Plant Cell 23: 240–257.

DeFalco TA, Bender KW and Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochemical Journal 425: 27–40.

Dodd AN, Gardner MJ, Hotta CT et al. (2007) The Arabidopsis circadian clock incorporates a cADPR‐based feedback loop. Science 318: 1789–1792.

Doherty CJ, Van Buskirk HA, Myers SJ and Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold‐regulated gene expression and freezing tolerance. Plant Cell 21: 972–984.

Du L, Ali GS, Simons KA et al. (2009) Ca2+/calmodulin regulates salicylic‐acid‐mediated plant immunity. Nature 457: 1154–1158.

Foreman J, Demidchik V, Bothwell JHF et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442–446.

Frietsch S, Wang YF, Sladek C et al. (2007) A cyclic nucleotide‐gated channel is essential for polarized tip growth of pollen. Proceedings of the National Academy of Sciences of the USA 104: 14531–14536.

Galon Y, Nave R, Boyce JM et al. (2008) Calmodulin‐binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Letters 582: 943–948.

Geiger D, Scherzer S, Mumm P et al. (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proceedings of the National Academy of Sciences of the USA 107: 8023–8028.

Gong DM, Guo Y, Schumaker KS and Zhu JK (2004) The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis. Plant Physiology 134: 919–926.

Harper JE, Breton G and Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annual Review of Plant Biology 55: 263–288.

Hayashi T, Banba M, Shimoda Y et al. (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant Journal 63: 141–154.

Hedrich R and Marten I (2011) TPC1 – SV channels gain shape. Molecular Plant 4: 428–441.

Hwang I, Sze H and Harper JF (2000) A calcium‐dependent protein kinase can inhibit a calmodulin‐stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proceedings of the National Academy of Sciences of the USA 97: 6224–6229.

Kim BG, Waadt R, Cheong YH et al. (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant Journal 52: 473–484.

Kim KC, Fan B and Chen Z (2006) Pathogen‐induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiology 142: 1180–1192.

Kim KN, Cheong YH, Gupta R and Luan S (2000) Interaction specificity of Arabidopsis calcineurin B‐like calcium sensors and their target kinases. Plant Physiology 124: 1844–1853.

Kosuta S, Hazledine S, Sun J et al. (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proceedings of the National Academy of Sciences of the USA 105: 9823–9828.

Kugler A, Kohler B, Palme K et al. (2009) Salt‐dependent regulation of a CNG channel subfamily in Arabidopsis. BMC Plant Biology 9: 140.

Kwak JM, Mori IC, Pei ZM et al. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS‐dependent ABA signaling in Arabidopsis. EMBO Journal 22: 2623–2633.

Laohavisit A, Mortimer JC, Demidchik V et al. (2009) Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+‐permeable conductance. Plant Cell 21: 479–493.

Ma W and Berkowitz GA (2011) Ca2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytologist 190: 566–572.

Ma W, Qi Z, Smigel A et al. (2009) Ca2+, cAMP, and transduction of non‐self perception during plant immune responses. Proceedings of the National Academy of Sciences of the USA 106: 20995–21000.

Magnan F, Ranty B, Charpenteau M et al. (2008) Mutations in AtCML9, a calmodulin‐like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant Journal 56: 575–589.

McAinsh MR, Brownlee C and Hetherington AM (1992) Visualising changes in cytosolic‐free Ca2+ during the response of stomatal guard cells to abscisic acid. Plant Cell 4: 1113–1122.

McAinsh MR and Hetherington AM (1998) Encoding specificity in Ca2+ signalling systems. Trends in Plant Science 3: 32–36.

McAinsh MR and Pittman JK (2009) Shaping the calcium signature. New Phytologist 181: 275–294.

McAinsh MR, Webb AAR, Taylor JE and Hetherington AM (1995) Stimulus‐induced oscillations in guard cell cytosolic‐free calcium. Plant Cell 7: 1207–1219.

McCormack E, Tsai YC and Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends in Plant Science 10: 383–389.

Meyerhoff O, Muller K, Roelfsema MR et al. (2005) AtGLR3.4, a glutamate receptor channel‐like gene is sensitive to touch and cold. Planta 222: 418–427.

Mori IC, Murata Y, Yang YZ et al. (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S‐type anion‐ and Ca2+‐permeable channels and stomatal closure. PLoS Biology 4: 1749–1762.

Oldroyd GED and Downie JM (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59: 519–546.

Park CY, Lee JH, Yoo JH et al. (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Letters 579: 1545–1550.

Peiter E, Maathuis FJM, Mills LN et al. (2005) The vacuolar Ca2+‐activated channel TPC1 regulates germination and stomatal movement. Nature 434: 404–408.

Qi Z, Stephens NR and Spalding EP (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiology 142: 963–971.

Qudeimat E, Faltusz AMC, Wheeler G et al. (2008) A PIIB‐type Ca2+‐ATPase is essential for stress adaptation in Physcomitrella patens. Proceedings of the National Academy of Sciences of the USA 105: 19555–19560.

Reddy ASN, Ali GS, Celesnik H and Day IS (2011) Coping with stresses: roles of calcium‐ and calcium/calmodulin‐regulated gene expression. Plant Cell 23: 2010–2032.

Weinl S and Kudla J (2009) The CBL–CIPK Ca2+‐decoding signaling network: function and perspectives. New Phytologist 184: 517–528.

Whalley HJ, Sargeant AW, Steele JFC et al. (2011) Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis. Plant Cell 23: 4079–4095.

White PJ (2009) Depolarization‐activated calcium channels shape the calcium signatures induced by low‐temperature stress. New Phytologist 183: 7–8.

Yamanaka T, Nakagawa Y, Mori K et al. (2010) MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis thaliana. Plant Physiology 152: 1284–1296.

Zhu X, Caplan J, Mamillapalli P et al. (2010) Function of endoplasmic reticulum calcium ATPase in innate immunity‐mediated programmed cell death. EMBO Journal 29: 1007–1018.

Further Reading

Dodd AN, Kudla J and Sanders D (2010) The language of calcium signaling. Annual Review of Plant Biology 61: 593–620.

Hashimoto K and Kudla J (2011) Calcium decoding mechanisms in plants. Biochimie 93: 2054–2059.

Kim MC, Chung WS, Yun DJ and Cho MJ (2009) Calcium and calmodulin‐mediated regulation of gene expression in plants. Molecular Plant 2: 13–21.

Kim TH, Bohmer M, Hu HH et al. (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annual Review of Plant Biology 61: 561–591.

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

Manohar M, Shigaki T and Hirschi KD (2011) Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biology 13: 561–569.

Peiter E (2011) The plant vacuole: emitter and receiver of calcium signals. Cell Calcium 50: 120–128.

Pittman JK (2011) Vacuolar Ca2+ uptake. Cell Calcium 50: 139–146.

Pittman JK, Bonza MC and De Michelis MI (2011) Ca2+ pumps and Ca2+ antiporters in plant development. In: Geisler M and Venema K (eds) Transporters and Pumps in Plant Signaling, pp. 133–161. Heidelberg, Germany: Springer.

Roelfsema MRG and Hedrich R (2010) Making sense out of Ca2+ signals: their role in regulating stomatal movements. Plant Cell and Environment 33: 305–321.

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How to Cite close
Bickerton, Peter D, and Pittman, Jon K(May 2012) Calcium Signalling in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0023722]