Calcium in plant cells

  • V. V. Schwartau Institute of Plant Physiology and Genetics of NAS of Ukraine
  • P. A. Virych Institute of Plant Physiology and Genetics of NAS of Ukraine
  • T. I. Makoveychuk Institute of Plant Physiology and Genetics of NAS of Ukraine
  • A. Y. Artemenko ESC “Institute of Biology” of Taras Shevchenkо Kyiv National University
Keywords: calcium, plants, signal system, homeostasis


The paper gives the review on the role of calcium in many physiological processes of plant organisms, including growth and development, protection from pathogenic influences, response to changing environmental factors, and many other aspects of plant physiology. Initial intake of calcium ions is carried out by Ca2+-channels of plasma membrane and they are further transported by the xylem owing to auxins’ attractive ability. The level of intake and selectivity of calcium transport to ove-ground parts of the plant is controlled by a symplast. Ca2+enters to the cytoplasm of endoderm cells through calcium channels on the cortical side of Kaspary bands, and is redistributed inside the stele by the symplast, with the use of Ca2+-АТPases and Ca2+/Н+-antiports. Owing to regulated expression and activity of these calcium transporters, calclum can be selectively delivered to the xylem. Important role in supporting calcium homeostasis is given to the vacuole which is the largest depo of calcium. Regulated quantity of calcium movement through the tonoplast is provided by a number of potential-, ligand-gated active transporters and channels, like Ca2+-ATPase and Ca2+/H+ exchanger. They are actively involved in the inactivation of the calcium signal by pumping Ca2+ to the depo of cells. Calcium ATPases are high affinity pumps that efficiently transfer calcium ions against the concentration gradient in their presence in the solution in nanomolar concentrations. Calcium exchangers are low affinity, high capacity Ca2+ transporters that are effectively transporting calcium after raising its concentration in the cell cytosol through the use of protons gradients. Maintaining constant concentration and participation in the response to stimuli of different types also involves EPR, plastids, mitochondria, and cell wall. Calcium binding proteins contain several conserved sequences that provide sensitivity to changes in the concentration of Ca2+ and when you connect ion conformationally rearranged, thus passing the signal through the chain of intermediaries. The most important function of calcium is its participation in many cell signaling pathways. Channels, pumps, gene expression, synthesis of alkaloids, protective molecules, NO etc. respond to changes in [Ca2+]cyt, while transductors are represented by a number of proteins. The universality of calcium is evident in the study in connection with other signaling systems, such as NO, which is involved in the immune response and is able to control the feedback activity of protein activators channels, producing nitric oxide. Simulation of calcium responses can determine the impact of key level and their regulation, and also depends on the type of stimulus and the effector protein that specifically causes certain changes. Using spatiotemporal modeling, scientists showed that the key components for the formation of Ca2+ bursts are the internal and external surfaces of the nucleus membrane. The research was aimed at understanding of the mechanisms of influence of Ca2+-binding components on Ca2+ oscillations. The simulation suggests the existence of a calcium depot EPR with conjugated lumen of the nucleus which releases its contents to nucleoplasm. With these assumptions, the mathematical model was created and confirmed experimentally. It describes the oscillation of nuclear calcium in root hairs of Medicago truncatula at symbiotic relationship of plants and fungi (rhizobia). Calcium oscillations are present in symbiotic relationships of the cortical layer of plant root cells. Before penetration of bacteria into the cells, slow oscillations of Ca2+ are observed, but with their penetration into the cells the oscillation frequency increases. These processes take place by changing buffer characteristics of the cytoplasm caused by signals from microbes, such as Nod-factor available after penetration of bacteria through the cell wall. Thus, the basic known molecular mechanisms for regulation of calcium homeostasis in plant cells are reviewed. Data presented in the paper is important for understanding the role of calcium in the ions’ homeostasis and can be used for developing high-performance technologies of crops nutrition. 


Banba, M., Gutjahr, C., Miyao, A., Hirochika, H., Paszkowsk, U., Kouchi, H., Imaizumi-Anraku, H., 2008. Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol. 49(11), 1659–1671.

Batistic, O., Waadt, R., Steinhorst, L., Held, K., Kudla, J., 2010. CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J. 61(2), 211–222.

Boller, T., Felix, G., 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant. Biol. 60, 379–406.

Bonaventure, G., Gfeller, A., Rodrigues, V., Armand, F., Farmer, E., 2007. The fou2 gain-of-function allele and the wild-type allele of Two Pore Channel 1 contribute to different extents or by different mechanisms to defense gene expression in Arabidopsis. Plant Cell Physiol. 48(12), 1775–1789.

Bou Daher, F., Geitmann, A., 2011. Actin is involved in pollen tube tropism through redefining the spatial targeting of secretory vesicles Traffic 12, 1537–1551. >> doi: 10.1111/j.1600-0854.2011.01256.x.

Bradley, J., Reisert, J., Frings, S., 2005. Regulation of cyclic nucleotide-gated channels. Curr. Opin. Neurobiol. 15, 343–349.

Brini, M., Crafoli, E., 2009. Calcium pumps in heart and disease. Physiol. Rev. 89(4), 1341–1378.

Capoen W., Sun, J., Wysham, D., Otegui, M.S., Venkateshwaran, M., Hirsch, S., Miwa, H., Downie, J.A., Morris, R.J., Ané, J.M., Oldroyd, G.E., 2011. Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl. Acad. Sci. USA 108(34), 14348–14353.

Cardenas, L., Lovy-Wheeler, A., Kunkel, J., Hepler, P., 2008. Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol. 146, 1611–1621.

Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E., Parniske, M., 2008. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20(12), 3467–3479.

Chen, C., Fan, C., Gao, M., Zhu, H., 2009. Antiquity and function of CASTOR and POLLUX, the twin ion channel-encoding genes key to the evolution of root symbioses in plants. Plant Physiol. 149, 306–317.

Chen, J., Xue, B., Xia, X., & Yin, W., 2013. A novel calcium-dependent protein kinase gene from Populus euphratica, confers both drought and cold stress tolerance. Biochem. Biophys. Res. Commun. 441(3), 630–636.

Chen, L., Ren, F., Zhou, L., 2012. The Brassica napus calcineurin B-like 1-CBL-interacting protein kinase 6 component is involved in the plant response to abiotic stress and ABA sig-nalling. J. Exp. Bot. 63(17), 6211–6222.

Cheng, N.-H., Pittman, J.K., Shigaki, T., Lachmansingh, J., LeClere, S., Lahner, B., Salt, D.E., Hirschi, K.D., 2005. Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol. 138, 2048–2060.

Dadacz-Narloch, B., Beyhl, D., Larisch, C., Lopez-Sanjurjo, E.J., Reski, R., Kuchitsu, K., Mueller, T.D., Becker, D., Schönknecht, G., Hedrich, R., 2011. A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. Plant Cell. 23, 2696–2707.

Day, S., Reddy, S., Ali, S., Reddy, A., 2002. Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol. 10(3), 1–24.

Demidchik, V., Shabala, S., Coutts, K., Tester, M., Davies, J., 2003. Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J. Cell Sci. 116, 81–88.

Ding, J., Richard, B., 1993. Mechanosensory calcium-selective cation channels in epidermal calls. Plant J. 3, 83–110.

Dobney, S., Chiasson, D., Lam, P., Smith, S., Snedden, W., 2009. The calmodulin-related calcium sensor CML42 plays a role in trichome branching. J. Biol. Chem. 46, 31647–31657.

Dubiella, U., Seybold, H., Durian, G., Komander, E., Lassig, R., 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. USA. 110(21), 8744-8449.

Edmond, C., Shigaki, T., Ewert, S., 2009. Comparative analysis of CAX2-like cation transporters indicates functional and regulatory diversity. Biochem. J. 418, 145–154.

Edwards, A., Heckmann, A.B., Yousafzai, F., Duc, G., Downie, J.A., 2007. Structural implications of mutations in the pea SYM8 symbiosis gene, the DMI1 ortholog, encoding a predicted ion channel. Mol. Plant Microbe Interact. 20, 1183–1191.

Falcke, M., 2004. Reading the patterns in living cells: The physics of Ca2+signaling. Adv. Phys. 53, 255–440.

Franklin-Tong, V., Drobak, B., Allan, A., Watkins, P., Trewavas, A., 1996. Growth of pollen tubes of Papaver rhoeas is regulated by a slow-moving calcium wave propagated by inositol 1,4,5-trisphosphate. Plant Cell 8, 1305–1321.

Galva, C., Virgin, G., Helms, J., Gatto, C., 2013. ATP protects against FITC labeling of Solanum lycopersicon and Arabidopsis thaliana Ca2+-ATPase ATP binding domains. Plant Physiol. Biochem. 71, 261–267.

Garcia-Mata, C., Gay, R., Sokolovski, S., Hills, A., Lamattina, L., Blatt, M., 2003. Nitric oxide regulates K+ and Cl– channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. USA 100, 11116–11121.

Ge, L., Xie, C., Tian, H., Russell, S., 2009. Distribution of calcium in the stigma and style of tobacco during pollen germination and tube elongation. Sex. Plant Reprod. 22, 87–96.

Gobert, A., Isayenkov, S., Voelker, C., Czempinski, K., Maathuis, F., 2007. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc. Natl. Acad. Sci. USA 104, 10726–10731.

Granqvist, E., Wysham, D., Hazledine, S., Kozlowski, W., Sun, J., Charpentier, M., Martins, T.V., Haleux, P., Tsaneva-Atanasova, K., Downie, J.A., Oldroyd, G.E.D., Morris, R.J., 2012. Buffering capacity explains signal variation in symbiotic calcium oscillations. Plant Physiol. 160, 2300–2310.

Grant, M., Brown, I., Adams, S., Knight, M., Ainslie, A., Mansfield, J., 2000. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 23, 441–450.

Groth, M., Takeda, N., Perry, J., Uchida, H., Drlxl, S., Brachmann, A., Sato, S., Tabata, S., Kawaguchi, M., Wang, T.L., Parniske, M., 2010. NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509–2526.

Hamamoto, S., Marui, J., Matsuoka, K., 2008. Characterization of a tobacco TPK-type K+ channel as a novel tonoplast K+ channel using yeast tonoplasts. J. Biol. Chem. 283, 1911–1920.

Harada, A., Shimazak, K., 2007. Phototropins and blue light-dependent calcium signaling in higher plants. Photochem. Photobiol. 83, 102–111.

Harada, A., Sakai, T., Okada, K., 2003. phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc. Natl. Acad. Sci. USA 100, 8583–8588.

Harada, A., Takemiya, A., Inoue, S., Sakai, T., Shimazaki, K., 2013. Role of RPT2 in leaf positioning and flattening and a possible inhibition of phot2 signaling by phot1. Plant Cell Physiol. 54, 36–47.

Hayashi, T., Banba, M., Shimoda, Y., Kouchi, H., Hayashi, M., Imaizumi-Anraku, H., 2010. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J. 63, 141–154.

He, L., Yang, X., Wang, L., 2013. Molecular cloning and functional characterization of a novel cotton CBL-interacting protein kinase gene (GhCIPK6) reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Biochem. Biophys. Res. Commun. 435(2), 209–215.

Held, K., Pascaud, F., Eckert, C., Gajdanowicz, P., Hashimoto, K., Corratgq-Faillie, C., Offenborn, J.N., Lacombe, B., Dreyer, I., Thibaud, J.B., Kudla, J., 2011. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res. 21, 1116–1130.

Helling, D., Possart, A., Cottier, S., Klahre, U., Kost, B., 2006. Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18, 3519–3534.

Hen, X., Gu, Z., Xin, D., Hao, L., Liu, C., Huang, J., Ma, B., Zhang, H., 2011. CIdentification and characterization of putative CIPK genes in maiz. J. Genet. Genomics. 38(2), 77–87.

Hepler, P., Winship, L., 2010. Calcium at the cell wall-cytoplast interface. J. Integr. Plant Biol. 52, 147–160.

Hepler, P., Kunkel, J., Rounds, C., Winship, L., 2012. Calcium entry into pollen tubes. Trends Plant Sci. 17, 32–38.

Hettenhausen, C., Baldwin, I., Wu, J. (2013). Nicotiana attenuata MPK4 suppresses a novel jasmonic acid (JA) signaling-independent defense pathway against the specialist insect Manduca sexta, but is not required for the resistance to the generalist Spodoptera littoralis. New Phytol. 199(3), 787–799.

Hettenhausen, C., Yang, D., Baldwin, I., Wu, J., 2012. Calcium-dependent protein kinases, CDPK4 and CDPK5, affect early steps of jasmonic acid biosynthesis in Nicotiana attenuata. Plant Signal Behav. 8(1), e22784.

Hirschi, K., Korenkov, V., Wilganowski, N., Wagner, G., 2000. Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol. 124, 125–133.

Holdaway-Clarke, T., Feijу, J., Hackett, G., Kunkel, J., Hepler, P., 1997. Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9, 1999–2010.

Hua, D., Wang, C., He, J., Liao, H., Duan, Y., Zhu, Z., Guo, Y., Chen, Z., 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.

Huda, K., Banu, M., Tuteja, R., Tuteja, N., 2013. Global calcium transducer P-type Ca²⁺-ATPases open new avenues for agriculture by regulating stress signalling. J. Exp. Bot. 64(11), 3099–3109.

Inoue, S., Takemiya, A., Shimazaki, K., 2010. Phototropin signaling and stomatal opening as a model case. Curr. Opin. Plant Biol. 13, 587–593.

Iwano, M., Entani, T., Shiba, H., Kakita, M., Nagai, T., Mizuno, H., Miyawaki, A., Shoji, T., Kubo, K., Isogai, A., Takayama, S., 2009. Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol. 150, 1322–1334.

Iwano, M., Shiba, H., Miwa, T., Che, F., Takayama, S., Nagai, T., Miyawaki, A., Isogai, A., 2004. Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol. 136, 3562–3571.

Jammes, F., Hu, H.-C., Villiers, F., Bouten, R., Kwak, M., 2011. Calcium-permeable channels in plant cell. FEBS J. 27, 4262–4276.

Jeandroz, S., Lamotte, O., Astier, J., Rasul, S., Trapet, P., Besson-Bard, A., Bourque, S., Nicolas-Francès, V., Ma, W., Berkowitz, G.A., Wendehenne, D., 2013. There's more to the picture than meets the eye: Nitric oxide cross talk with Ca2+ signaling. Plant Physiol. 163, 459–470.

Kang, J., Turano, F., 2003. The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100, 6872–6877.

Kang, J., Mehta, S., Turano, F., 2004. The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signaling to control development and water loss. Plant Cell Physiol. 45, 1380–1389.

Knight, M., Campbell, A., Smith, S., Trewavas, A., 1991. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352, 524–526.

Konrad, K., Wudick, M., Feijу, J., 2011. Calcium regulation of tip growth: New genes for old mechanisms. Curr. Opin. Plant Biol. 14, 721–730.

Krebs, M., Beyhl, D., Gorlich, E., Al-Resheid, K., Marten, I., Stiernof, Y.-D., Hedrich, R., Schumacher, K., 2010. Arabidipsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Plant Physiol. 107(7), 3251–3256.

Kurusu, T., Hamada, J., Hamada, H., Hanamata, S., Kuchitsu, K., 2010. Roles of calcineurin B-like protein-interacting protein kinases in innate immunity in rice. Plant Signal Behav. 8(5), 1045–1047.

Li, J., Zhu, S., Song, X., Shen, Y., Chen, H., Yu, J., Yi, K., Liu, Y., Karplus, V.J., Wu, P., Deng, X.W., 2006. A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18, 340–349.

Ma, W., Zhi, Q., Smigel, A., Walker, R., Verma, R., Berkiwitz, G., 2009. Ca2+, cAMP, and transduction of non-self-perception during plant immune responses. Proc. Natl. Acad. Sci. USA 106, 20995–21000.

Magnan, F., Ranty, B., Charpenteau, M., Sotta, B., Galaud, J., Aldon, D., 2008. Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J. 56(4), 575–589.

Manzoor, H., Chiltz, A., Madani, S., Vatsa, P., Schoefs, B., Pugin, A., Garcia-Brugger, A., 2012. Calcium signatures and signaling in cytosol and organelles of tobacco cells induced by plant defense elicitors. Cell Calcium 51(6), 434–444.

Medvedev, C.C., 2005. Calcium signal system [Kalcievaya sygnalnaya systema]. Fisiologia Rasteniy 52(2), 282–305 (in Russian).

Miwa, H., Sun, J., Oldroyd, G.E., Downie, J.A., 2006. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J. 48, 883–894.

Miwa, H., Sun, J., Oldroyd, G., Downie, J., 2006. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol. Plant Microbe Interact. 19, 914–923.

Munemasa, S., Hossain, M., Nakamura, Y., Mori, I., Murata, Y., 2011. The Arabidopsis calcium-dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiol. 155, 553–561.

Nakagawa, Y., Katagiri, T., Shinozaki, K., Qi, Z., Tatsumi, H., Furuichi, T., Kishigami, A., Sokabe, M., Kojima, I., Sato, S., Kato, T., Tabata, S., Iida, K., Terashima, A., Nakano, M., Ikeda, M., Yamanaka, T., Iida, H., 2007. Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc. Nat. Acad. Sci. USA 104, 3639–3644.

Nalefski, A., Falke, J., 1996. The C2 domain calcium-binding motif: Structural and functional diversity. Protein Sci. 5, 2375–2390.

Ordenesa, V., Morenoc, I., Maturanac, D., Norambuenad, L., Trewavase, A., Orellana, A., 2012. In vivo analysis of the calcium signature in the plant Golgi apparatus reveals unique dynamics. Cell Calcium 52, 397–404.

Pei, Z., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., Schroeder, J.I., 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.

Peiter, E., 2011. The plant vacuole: Emitter and receiver of calcium signals. Cell Calcium 50, 120–128.

Peiter, E., Maathuis, F., Mills, L., Knight, H., Pelloux, J., Hetherington, A.M., Sanders, D., 2005. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434, 404–408.

Piao, H., Xuan, Y., Park, S.H., Je, B.I., Park, S.J., Park, S.H., Kim, C.M., Huang, J., Wang, G.K., Kim, M.J., Kang, S.M., Lee, I.J., Kwon, T.R., Kim, Y.H., Yeo, U.S., Yi, G., Son, D., Han, C.D., 2010. OsCIPK31, a CBL-interacting protein kinase is involved in germination and seedling growth under abiotic stress conditions in rice plants. Mol. Cells 30(1), 19–27.

Pittman, J., 2011. Vacuolar Ca2+ uptake. Cell Calcium 50, 139–146.

Pittman, J., Shigaki, T., Marshall, J., Morris, J., Cheng, N., Hirschi, K., 2004. Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol. Biol. 56, 959–971.

Potocký, M., Pejchar, P., Gutkowska, M., Jiménez-Quesada, M., Potocká, A., Alché Jde, D., Kost, B., Žárský, V., 2012. NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. J. Plant Physiol. 169(16), 1654–1663.

Roberts, N., Morieri, G., Kalsi, G., Rose, A., Stiller, J., Edwards, A., Xie, F., Gresshoff, P.M., Oldroyd, G.E., Downie, J.A., Etzler, M.E., 2013. Rhizobial and mycorrhizal symbioses in Lotus japonicus require lectin nucleotide phosphohydrolase, which acts upstream of calcium signaling. Plant Physiol. 161, 556–567.

Sanchez-Barrena, M., Martinez-Ripoll, M., Albert, A., 2013. Structural biology of a major signaling network that regulates plant abiotic stress: The CBL-CIPK mediated pathway. Int. J. Mol. Sci. 14, 5734–5749.

Schwessinger, B., Zipfel, C., 2008. News from the frontline: Recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11(4), 389–395.

Segonzac, C., Feike, D., Gimenez-Ibanez, S., Hann, D., Zipfel, C., Rathjen, J., 2011. Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol. 156(2), 687–699.

Shigaki, T., Pittman, J., Hirschi, K., 2003. Manganese specificity determinants in the Arabidopsis metal/H+ antiporter CAX2. J. Biol. Chem. 278, 6610–6617.

Sieberer, B., Chabaud, M., Fournier, J., Timmers, A., Barker, D., 2011. A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J. 69, 822–830.

Simontacchi, M., García-Mata, C., Bartoli, C., Santa-María, G., Lamattina, L., 2013. Nitric oxide as a key component in hormone-regulated processes. Plant Cell Rep. 32(6), 853–866.

Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K., Dolan, L., 2008. Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241–1244.

Tikhonova, L., Pottosin, I., Dietz, K., Schwnknecht, G., 1997. Fast-activating cation channel in barley mesophyll vacuoles. Inhibition by calcium. Plant J. 11, 1059–1070.

Vadassery, J., Ranf, S., Drzewiecki, C., Mithöfer, A., Mazars, C., Scheel, D., Lee, J., Oelmüller, R., 2009. A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J. 59(2), 193–206.

Vadassery, J., Reichelt, M., Hause, B., Gershenzon, J., Boland, W., Mithufe, A., 2012. CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiol. 159, 1159–1175.

Venkateshwaran, M., Cosme, A., Han, L., Banba, M., Satyshur, K.A., Schleiff, E., Parniske, M., Imaizumi-Anraku, H., Ané, J.M., 2012. The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24, 2528–2545.

Verhage, A., Vlaardingerbroek, I., Raaymakers, C., Van Dam, N., Dicke, M., Van Wees, S.C., Pieterse, C.M., 2011. Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front Plant Sci. 26(2), 47.

Waadt, R., Schmidt, L., Lohse, M., Hashimoto, K., Bock, R., Kudla, J., 2008. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505–516.

Wang, R., Li, L.L., Cao, Z.H., Zhao, Q., Li, M., Zhang, L.Y., Hao, Y.J., 2012. Molecular cloning and functional characterization of a novel apple MdCIPK6L gene reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Plant Mol. Biol. 79(1–2), 123–135.

Ward, J., Schroeder, J., 1994. Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6, 669–683.

White, P., 2000. Calcium channels in higher plants. Biochim. Biophys. Acta 1465, 171–189.

White, P., Bowen, H., Demidchik, V., Nichols, C., Davies, J., 2002. Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim. Biophys. Acta. 1564, 299–309.

Wu, J., Qu, H., Jin, C., Shang, Z., Wu, J., Xu, G., Gao, Y., Zhang, S., 2011. cAMP activates hyperpolarization-activated Ca2+ channels in the pollen of Pyrus pyrifolia. Plant Cell Rep. 30, 1193–1200.

Xu, J., Li, H.D., Chen, L.Q., Wang, Y., Liu, L.L., He, L., Wu, W.H., 2006. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125(7), 1347–1360.

Yang, W., Kong, Z., Omo-Ikerodah, E., Xu, W., Li, Q., 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(9), 531–543.

Yu, M., Yun, B., Spoel, S., Loake, G., 2012. A sleigh ride through the SNO: Regulation of plant immune function by protein S-nitrosylation. Curr. Opin. Plant Biol. 15, 424–430.

Zhang, H., Lv, F., Han, X., 2013. The calcium sensor PeCBL1, interacting with PeCIPK24/25 and PeCIPK26, regulates Na+/K+ homeostasis in Populus euphratica. Plant Cell Rep. 32(5), 611–621.

Zhao, J., Connorton, J., Guo, Y., Li, X., Shigaki, T., Hirschi, K.D., Pittman, J.K., 2009a. Functional studies of split Arabidopsis Ca2+/H+ exchangers. J. Biol. Chem. 284(49), 34075–34083.

Zhao, J., Shigaki, T., Mei, H., Gu, Y., Cheng, N., Hirschi, K., 2009b. Interaction between Arabidopsis Ca2+/H+ exchangers CAX1 and CAX3. J. Biol. Chem. 284(7), 4605–4615.

Zhao, L.-N., Shen, L.-K., Zhang, W.-Z., Zhang, W., Wang, Y., Wu, W.-H., 2013. Ca2+-dependent protein kinase11 and 24 modulate the activity of the inward rectifying K+ channels in Arabidopsis pollen tubes. Plant Cell 25(2), 649–661.

Zhao, X., Wang, Y.-L., Qiao, X.-R., Wang, J., Wang, L.-D., Xu, C.-S., Zhang, X., 2013. Phototropins function in high-intensity blue light-induced hypocotyl phototropism in Arabidopsis by altering cytosolic calcium. Plant Physiol. 162(3), 1539-1551.