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Calcium signaling system in plants

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Abstract

Calcium ions have unique properties and universal ability to transmit diverse signals that exert primary action on cells, such as hormones, pathogens, light, gravity, and stress factors. The principal elements in the system of calcium signaling of plant cells are different Ca2+ channels, Ca2+-ATPases, Ca2+/H+ antiporters, Ca2+-binding and Ca2+-dependent proteins. The system of calcium signaling also includes receptors, the cascades of amplifying Ca2+ signals, and transcription factors. The process of transmitting the calcium signal within the cell consists of at least two stages. At the first stage, the cytosolic calcium concentration undergoes temporal and usually local increase due to its entry through the Ca2+ channels. The second stage is related to the signal “decay” and represents the active removal of calcium excess from the cytosol to the extracellular medium or organelles (vacuoles, endoplasmic reticulum, mitochondria) by means of Ca2+-ATPases and/or Ca2+/H+ antiporters. The primary intracellular targets of calcium are various calcium-binding proteins. Some of these proteins ensure Ca2+ transport, others serve as a calcium buffer, and the others (e.g., calmodulin or Ca2+-dependent protein kinases) translate the calcium signal to intracellular operational mechanisms and initiate Ca2+-dependent physiological processes. An important feature of the calcium signal transduction is that this signal originates and propagates in the pulse mode. Such way of information transmission is not only faster than the diffusion but it also ensures the spatiotemporal regulation of cell functions, because the signal encoding can be realized via amplitude- and frequency-modulated oscillations in cytosolic calcium concentration.

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Abbreviations

CaM:

calmodulin

CDPK:

calcium-dependent protein kinase

IP3 :

inositol-1,4,5-trisphosphate

PIP2 :

phosphatidylinositol-4,5-diphosphate

cADPR:

cyclic ADP-ribose

CICR:

calcium-induced calcium release

Ca 2+cyt :

concentration of ionized calcium in the cytoplasm

MP:

membrane potential

Nod-factors:

symbiotic signals

REFERENCES

  1. Ringer, S., A Further Contribution Regarding the Influence of the Different Constituents of the Blood on the Contraction of the Heart, J. Physiol., 1883, vol. 4, pp. 29–42.

    Google Scholar 

  2. Rasmussen, H., Calcium and cAMP as a Synarchic Messengers, New York: Wiley, 1981.

    Google Scholar 

  3. Rasmussen, H., Barrett, P., and Smallwood, J., Calcium Ion as Intracellular Messenger and Cellular Messenger and Cellular Toxin, Environ. Helth. Perspect., 1990, vol. 84, pp. 17–25.

    Google Scholar 

  4. Avdonin, P.V. and Tkachuk, V.A., Retseptory i vnutrikletochnyi kal’tsii (Receptors and Intracellular Calcium). Moscow: Nauka, 1994.

    Google Scholar 

  5. Berridge, M.J., The AM and FM of Calcium Signalling, Nature, 1997, vol. 386, pp. 759–760.

    Google Scholar 

  6. Berridge, M.J., Bootman, M.D., and Lipp, P., Calcium — a Life and Death Signal, Nature, 1998, vol. 395, pp. 645–648.

    Google Scholar 

  7. Bootman, M.D., Berridge, M.J., and Roderick, H.L., Calcium Signalling: More Messengers, More Channels, More Complexity, Curr. Biol., 2002, vol. 12, pp. R563–R565.

    Google Scholar 

  8. Krutetskaya, Z.I., Lebedev, O.E., and Kurilova, L.S., Mekhanizmy vnutrikletochnoi signalizatsii (Mechanisms of Intracellular Signaling), St. Petersburg: St. Petersburg Gos. Univ., 2003.

    Google Scholar 

  9. Bush, D.S., Calcium Regulation in Plant Cells and Its Role in Signalling, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1995, vol. 46, pp. 95–122.

    Google Scholar 

  10. Trewavas, A.J. and Malho, R., Ca2+ Signalling in Plant Cells: The Big Network! Curr. Opin. Plant Biol., 1998, vol. 1, pp. 428–433.

    Google Scholar 

  11. Sanders, D., Brownlee, C., and Harper, J.F., Communication with Calcium, Plant Cell, 1999, vol. 11, pp. 691–706.

    Google Scholar 

  12. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J.F., Calcium at the Crossroads of Signalling, Plant Cell, 2002, vol. 14, pp. 401–417.

    Google Scholar 

  13. Roos, W., Ion Mapping in Plant Cells — Methods and Applications in Signal Transduction Research, Planta, 2000, vol. 210, pp. 347–370.

    Google Scholar 

  14. Rudd, J.J. and Franklin-Tong, V.E., Unravelling Response-Specificity in Ca2+ Signalling Pathways in Plant Cells, New Phytol., 2001, vol. 151, pp. 7–33.

    Google Scholar 

  15. Reddy, A.S.N., Calcium: Silver Bullet in Signalling, Plant Sci., 2001, vol. 160, pp. 381–404.

    Google Scholar 

  16. Trewavas, A.J., Signal Perception and Transduction, Biochemistry and Molecular Biology of Plants, Buchanan, B., Gruissem, W., and Jones, R., Ed., Rockville: Am. Soc. Plant Physiol., 2000, pp. 930–987.

    Google Scholar 

  17. Tarchevsky, I.A., Signal’nye sistemy kletok rastenii (Signal Transduction Pathways of Plant Cells), Moscow: Nauka, 2002.

    Google Scholar 

  18. Hepler, P.K. and Wayne, R.O., Calcium and Plant Development, Annu. Rev. Plant Physiol., 1985, vol. 36, pp. 397–439.

    Google Scholar 

  19. Medvedev, S.S., Fiziologicheskie osnovy polyarnosti rastenii (Physiological Basics of Plant Polarity), St. Petersburg: Kol’na, 1996.

    Google Scholar 

  20. Shacklock, P.S., Read, N.D., and Trewavas, A.J., Cytosolic Free Calcium Mediates Red Light Induced Photomorphogenesis, Nature, 1992, vol. 358, pp. 153–155.

    Google Scholar 

  21. Volotovski, I.D., Sokolovski, S.G., Nikiforov, E.L., and Zinchenko, V.P., Calcium Oscillations in Plant-Cell Cytoplasm Induced by Red and Far-Red Light Irradiation, J. Photochem. Photobiol., 1993, vol. 20, pp. 95–100.

    Google Scholar 

  22. Bowler, C., Neuhaus, G., Yamagata, H., and Chua, N.-H., Cyclic GMP and Calcium Mediate Phytochrome Phototransduction, Cell, 1994, vol. 77, pp. 73–81.

    Google Scholar 

  23. Medvedev, S.S., Polarity and Embryogeny in Plants, Embriologiya tsvetkovykh rastenii, (Embryology of Flowering Plants), vol. 2, Batygina, T.B., Ed., St. Petersburg: Mir i sem’ya, 1997, pp. 594–601.

    Google Scholar 

  24. Franklin-Tong, V.E., Hackett, G., and Hepler, P.K., Ratio-Imaging of Ca2+ in the Self-Incompatibility Response in Pollen Tubes of Papaver rhoeas, Plant J., 1997, vol. 12, pp. 1375–1386.

    Google Scholar 

  25. Franklin-Tong, V.E., Signaling and the Modulation of Pollen Tube Growth, Plant Cell, 1999, vol. 11, pp. 727–738.

    Google Scholar 

  26. Ehrhard, D.W., Wais, R., and Long, S.R., Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals, Cell, 1996, vol. 85, pp. 673–681.

    Google Scholar 

  27. Lhuissier, F.G.P., de Ruijter, N.C.A., Sieberer, B.J., Esseling, J.J., and Emons, A.M.C., The Course of Cell Biological Events Evoked in Legume Root Hairs by Rhizobium Nod Factors: State of the Art, Ann. Bot. (London), 2001, vol. 87, pp. 289–302.

    Google Scholar 

  28. Knigth, M.R., Campbell, A.K., Smith, S.M., and Trewavas, A.J., Transgenic Plant Aequorin Reports the Effects of Touch, Cold Shock, and Elicitors on Cytoplasmic Calcium, Nature, 1991, vol. 352, pp. 524–526.

    Google Scholar 

  29. Bach, M., Schnitzler, J.-P., and Seitz, H.U., Elicitor-Induced Changes in Ca2+ Influx, K+ Efflux, and 4-Hydroxybenzoic Acid Synthesis in Protoplasts of Daucus carota L., Plant Physiol., 1993, vol. 103, pp. 407–412.

    Google Scholar 

  30. Mithöfer, A., Ebel, J., Bhagwat, A.A., Boller, T., and Neuhaus, G., Transgenic Aequorin Monitors Cytosolic Calcium Transients in Soybean Cells Challenged with β-Glucan or Chitin Elicitors, Planta, 1999, vol. 207, pp. 566–574.

    Google Scholar 

  31. Blume, B., Nürnberger, T., Nass, N., and Scheel, D., Receptor-Mediated Increase in Cytoplasmic Free Calcium Required for Activation of Pathogen Defense in Parsley, Plant Cell, 2000, vol. 12, pp. 1425–1440.

    Google Scholar 

  32. Grant, M., Brown, I., Adams, S., Knight, M., Ainslie, A., and Mansfield, J., 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., 2000, vol. 23, pp. 1–11.

    Google Scholar 

  33. Poovaiah, B.W., McFadden, J.J., and Reddy, A.S.N., The Role of Calcium Ions in Gravity Signal Perception and Transduction, Physiol. Plant., 1987, vol. 71, pp. 401–407.

    Google Scholar 

  34. Medvedev, S.S. and Shtonda, I.A., The Role of Calcium Ions in Gravitropism, Biol. Nauki, 1989, no. 6, pp. 94–97.

  35. Medvedev, S.S., Maksimov, G.B., and Markova, I.V., The Role of Calcium Ions in the Regulation of Gravitropism, Exp. Biol. (Vilnius), 1991, no. 4, pp. 71–92.

  36. Sinclair, W. and Trewavas, A.J., Calcium in Gravitropism: Re-Examination, Planta, 1997, vol. 203, pp. 585–590.

    Google Scholar 

  37. Plieth, C. and Trewavas, A.J., Reorientation of Seedlings in the Earth’s Gravitational Field Induces Cytosolic Calcium Transients, Plant Physiol., 2002, vol. 129, pp. 786–796.

    Google Scholar 

  38. Gehring, C.A., Williams, D.A., Cody, S.H., and Parish, R.W., Phototropism and Geotropism in Maize Coleoptiles Are Spatially Correlated with Increases in Cytosolic Free Calcium, Nature, 1990, vol. 345, pp. 528–530.

    Google Scholar 

  39. Medvedev, S.S. and Markova, I.V., The Cytoskeleton and Plant Polarity, Fiziol. Rast. (Moscow), 1998, vol. 45, pp. 185–197 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  40. Neuhaus, G., Bowler, C., Hiratsuka, K., Yamagata, H., and Chua, N.-H., Phytochrome-Regulated Repression of Gene Expression Requires Calcium and cGMP, EMBO J., 1997, vol. 16, pp. 2554–2564.

    Google Scholar 

  41. Baum, G., Long, J.C., Jenkins, G.I., and Trewavas, A.J., Stimulation of the Blue Light Receptor NPH1 Causes a Transient Increase in Cytosolic Ca2+, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 13 554–13 559.

    Google Scholar 

  42. Gilroy, S., Read, N., and Trewavas, A., Elevation of Cytoplasmic Ca2+ by Caged Calcium or Caged Inositol Triphosphate Initiates Stomatal Closure, Nature, 1990, vol. 346, pp. 769–771.

    Google Scholar 

  43. Irving, H.R., Gehring, C.A., and Parish, R.W., Changes in Cytosolic pH and Calcium of Guard Cells Precede Stomatal Movement, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 1790–1794.

    Google Scholar 

  44. McAinsh, M.R., Browlee, C., and Hetherington, A.M., Calcium Ions as Second Messengers in Guard Cell Signalling, Physiol. Plant., 1997, vol. 100, pp. 16–29.

    Google Scholar 

  45. Ng, C.K.-Y., McAinsh, M.R., Gray, J.E., Hunt, L., Leckie, C.P., Mills, L., and Hetherington, A.M., Calcium-Based Signalling Systems in Guard Cells, New Phytol., 2001, vol. 151, pp. 109–120.

    Google Scholar 

  46. Pierson, E.S., Miller, D.D., Callaham, D.A., Shipley, A.M., and Rivers, B.A., Pollen Tube Growth Is Coupled to the Extracellular Calcium Ion Flux and the Intracellular Gradient: Effect of BAPTA-Type Buffers and Hypertonic Media, Plant Cell, 1994, vol. 6, pp. 1815–1828.

    Google Scholar 

  47. Pierson, E.S., Miller, D.D., Callaham, D.A., van Aken, J., Hackett, G., and Hepler, P.K., Tip-Localized Calcium Entry Fluctuates during Pollen Tube Growth, Dev. Biol., 1996, vol. 174, pp. 160–173.

    Google Scholar 

  48. Felle, H.H. and Hepler, P.K., The Cytosolic Ca2+ Concentration Gradient of Sinapsis alba Root Hairs as Revealed by Ca-Selective Microelectrodes Tests and Fura-Dextran Ratio Imaging, Plant Physiol., 1997, vol. 114, pp. 39–45.

    Google Scholar 

  49. Wymer, C.L., Bibikova, T.N., and Gilroy, S., Cytoplasmic Free Calcium Distribution during the Development of Root Hairs of Arabidopsis thaliana, Plant J., 1997, vol. 12, pp. 427–439.

    Google Scholar 

  50. Bibikova, T.N., Zhigilei, A., and Gilroy, S., Root Hair Growth in Arabidopsis thaliana Is Directed by Calcium and an Endogenous Polarity, Planta, 1997, vol. 203, pp. 495–505.

    Google Scholar 

  51. Brownlee, C. and Wood, J.W., A Gradient of Cytoplasmic Free Calcium in Growing Rhizoid Cells of Fucus serratus, Nature, 1986, vol. 320, pp. 624–626.

    Google Scholar 

  52. Taylor, A.R., Manison, N.F.H., Fernandez, C., Wood, J.W., and Brownlee, C., Spatial Organization of Calcium Signalling Involved in Cell Volume Control in the Fucus Rhizoid, Plant Cell, 1996, vol. 8, pp. 2015–2031.

    Google Scholar 

  53. Kropf, D.L., Induction of Polarity in Fucoid Zygotes, Plant Cell, 1997, vol. 9, pp. 1011–1020.

    Google Scholar 

  54. Knight, H., Calcium Signalling during Abiotic Stress in Plants, Int. Rev. Cytol., 2000, vol. 195, pp. 1011–1020.

    Google Scholar 

  55. Knight, H., Trewavas, A.J., and Knight, M.R., Cold Calcium Signalling in Arabidopsis Involves Two Cellular Pools and Change in Calcium Signature after Acclimation, Plant Cell, 1996, vol. 8, pp. 489–503.

    Google Scholar 

  56. Kiegle, E., Moore, K., Haseloff, J., Tester, M.A., and Knight, M.R., Cell-Type-Specific Calcium Responses to Drought, Salt, and Cold in the Arabidopsis Root, Plant J., 2000, vol. 23, pp. 267–278.

    Google Scholar 

  57. Zhu, J.-K., Cell Signalling under Salt, Water, and Cold Stresses, Curr. Opin. Plant Biol., 2001, vol. 4, pp. 401–406.

    Google Scholar 

  58. Gong, M., van de Luit, A.H., Knigth, M.R., and Trewavas, A.J., Heat-Shock-Induced Changes in Intracellular Ca2+ Level in Tobacco Seedlings in Relations to Thermotolerance, Plant Physiol., 1998, vol. 116, pp. 429–437.

    Google Scholar 

  59. Knight, H., Trewavas, A.J., and Knight, M.R., Calcium Signalling in Arabidopsis thaliana Responding to Drought and Salinity, Plant J., 1997, vol. 12, pp. 1067–1078.

    Google Scholar 

  60. Subbaiah, C.C., Bush, D.S., and Sachs, M.M., Elevation of Cytosolic Calcium Precedes Anoxic Gene Expression in Maize Suspension-Cultured Cells, Plant Cell, 1994, vol. 6, pp. 1747–1762.

    Google Scholar 

  61. Subbaiah, C.C., Bush, D.S., and Sachs, M.M., Mitochondrial Contribution to the Anoxic Ca2+ Signal in Maize Suspension-Cultured Cells, Plant Physiol., 1998, vol. 118, pp. 759–771.

    Google Scholar 

  62. Sedbrook, J.C., Kronebusch, P.J., Borisy, G.G., Trewavas, A.J., and Masson, P.H., Transgenic Aequorin Reveals Organ-Specific Cytosolic Ca2+ Responses to Anoxia in Arabidopsis thaliana Seedlings, Plant Physiol., 1996, vol. 111, pp. 243–257.

    Google Scholar 

  63. Fellbrich, G., Blume, B., Brunner, F., Hirt, H., Kroj, T., Ligterink, W., Romanski, A., and Nurnberger, T., Phytophthora parasitica Elicitor-Induced Reactions in Cells of Petroselinum crispum, Plant Cell Physiol., 2000, vol. 41, pp. 692–701.

    Google Scholar 

  64. Takahashi, K., Isobe, M., Knight, M.R., Trewavas, A.J., and Muto, S., Hypo-Osmotic Shock Induces Increases in Cytosolic Ca2+ in Tobacco Suspension Culture Cells, Plant Physiol., 1997, vol. 113, pp. 587–594.

    Google Scholar 

  65. Cessna, S.G., Chandra, S., and Low, P.S., Hypo-Osmotic Shock of Tobacco Cells Stimulates Ca2+ Fluxes Deriving First from External and Then Internal Ca2+ Stores, J. Biol. Chem., 1998, vol. 273, pp. 27286–27291.

    Google Scholar 

  66. Goddard, H., Manison, N.F.H., Tomos, D., and Brownlee, C., Elemental Propagation of Calcium Signals in Response-Specific Patterns Determined by Environmental Stimulus Strength, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 1932–1937.

    Google Scholar 

  67. Haley, A., Russell, A.J., Wood, N., Allan, A.C., Knigth, M., Campbell, A.K., and Trewavas, A.J., Effects of Mechanical Signalling on Plant Cell Cytosolic Calcium, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 4124–4128.

    Google Scholar 

  68. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., and Trewavas, A.J., Oxidative Signals in Tobacco Increase Cytosolic Calcium, Plant Cell, 1994, vol. 6, pp. 1301–1310.

    Google Scholar 

  69. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., and Schroeder, J.I., Calcium Channels Activated by Hydrogen Peroxide Mediate Abscisic Acid Signalling in Guard Cells, Nature, 2000, vol. 406, pp. 731–734.

    Google Scholar 

  70. Gilroy, S.G. and Jones, R.L., Gibberellic Acid and Abscisic Acid Coordinately Regulate Cytoplasmic Calcium and Secretory Activity in Barley Aleurone Protoplasts, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 3591–3595.

    Google Scholar 

  71. Gilroy, S., Signal Transduction in Barley Aleurone Protoplasts Is Calcium Dependent and Independent, Plant Cell, 1996, vol. 8, pp. 2193–2209.

    Google Scholar 

  72. Bethke, P.C., Schuurink, R.C., and Jones, R.L., Hormonal Signalling in Cereal Aleurone, J. Exp. Bot., 1997, vol. 48, pp. 1337–1356.

    Google Scholar 

  73. McAinsh, M.R., Brownlee, C., and Hetherington, A.M., Visualizing Changes in Cytosolic-Free Ca2+ during the Response of Stomatal Guard Cells to Abscisic Acid, Plant Cell, 1992, vol. 4, pp. 1113–1122.

    Google Scholar 

  74. Staxen, I., Pical, C., Montgomery, L.T., Gray, J.E., Hetherington, A.M., and McAinsh, M.R., Abscisic Acid Induces Oscillation in Guard-Cell Cytosolic Free Calcium That Involve Phosphoinositide-Specific Phospholipase C, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 1779–1784.

    Google Scholar 

  75. Schroeder, J.I., Allen, G.J., Hugovieux, V., Kwak, J.M., and Warner, D., Guard Cell Signal Transduction, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, vol. 52, pp. 627–658.

    Google Scholar 

  76. Polevoi, V.V., Rol’ auksina v sistemakh regulyatsii u rastenii. 44-e Timiryazevskoe chtenie (Role of Auxin in the Systems of Plant Regulation, the 44th Timiryazev Lecture), Leningrad: Nauka, 1986.

    Google Scholar 

  77. Felle, H., Auxin Causes Oscillation of Cytosolic Free Calcium and pH in Zea mays Coleoptiles, Planta, 1988, vol. 174, pp. 495–499.

    Google Scholar 

  78. Medvedev, S.S., Markova, I.V., Batov, A.Y., and Moshkov, A.V., Membrane Mechanism of IAA Action, Biologia, (Vilnius), 1998, no. 3, pp. 31–34.

  79. Medvedev, S.S., Batov, A.Yu., Moshkov, A.V., and Markova, I.V., The Role of Ion Channels in Transduction of the Auxin Signal, Fiziol. Rast. (Moscow), 1999, vol. 46, pp. 620–625 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  80. Medvedev, S.S and Markova, I.V., Role of Calcium Ions in Plant Growth and Mechanism of IAA Action, Phytohormones in Plant Biotechnology and Agriculture, Macháčková, I. and Romanov, G.A., Eds., Dordrecht: Kluwer, 2003, pp. 157–169.

    Google Scholar 

  81. Romanov, G.A., Kieber, J.J., and Schmülling, T., A Rapid Cytokinin Response Assay in Rapid Amaranthus Seedlings Test, Plant Growth Regul., 2000, vol. 32, pp. 337–344.

    Google Scholar 

  82. Romanov, G.A., Getman, I.A., and Schmülling, T., Investigation of Early Cytokinin Effects in a Rapid Arabidopsis Test Indicates a Role for Phospholipase D in Cytokinin Signalling, FEBS Lett., 2002, vol. 515, pp. 39–43.

    Google Scholar 

  83. Markova, I.V., Rumyantseva, E.A., Getman, I.A., Romanov, G.A., and Medvedev, S.S., Investigation of the Signal Role of Calcium Ions in Cytokinin-Dependent Responses in Amaranthus caudatus L., Vestn. St. Petersburg. Gos.Univ., Ser. 3, 2004, no. 19, pp. 47–55.

  84. Ng, C.K.-Y. and McAinsh, M.R., Encoding Specificity in Plant Calcium Signalling: Hot-Spotting the Ups and Downs and Waves, Ann. Bot. (London), 2003, vol. 92, pp. 477–485.

    Google Scholar 

  85. Levitskii, D.O., Kal’tsii i biologicheskie membrany (Calcium and Biological Membranes), Moscow: Vysshaya Shkola, 1990.

    Google Scholar 

  86. Miedema, H., Bothwell, J.H.F., Brownlee, C., and Davies, J., Calcium Uptake by Plant Cells — Channels and Pumps Acting in Concert, Trends Plant Sci., 2001, vol. 6, pp. 514–519.

    Google Scholar 

  87. Tsien, R.Y., A Non-Disruptive Technique for Loading Calcium Buffers and Indicators into Cells, Nature, 1981, vol. 290, pp. 527–528.

    Google Scholar 

  88. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J.M., Adams, J.A., Ikura, M., and Tsien, R.Y., Fluorescent Indicators for Ca2+ Based on Green Fluorescent Proteins and Calmodulin, Nature, 1997, vol. 388, pp. 882–887.

    Google Scholar 

  89. Brownlee, C., Cellular Calcium Imaging: So, What’s New? Trends Cell Biol., 2000, vol. 10, pp. 451–457.

    Google Scholar 

  90. Calcium Signalling: Practical Approach, Tepikin, A.V., Ed., Oxford: Oxford Univ. Press, 2001.

    Google Scholar 

  91. Takahashi, A., Camacho, P., Lechleitern, J., and Herman, B., Measurement of Intracellular Calcium, Physiol. Rev., 1999, vol. 79, pp. 1089–1125.

    Google Scholar 

  92. Antoine, A.F., Faure, J.-E., Cordeiro, S., Dumas, C., Rougier, M., and Feijo, J.A., A Calcium Influx Is Triggered and Propagates in the Zygote as Wavefront during In Vitro Fertilization of Flowering Plants, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 10 643–10 648.

    Google Scholar 

  93. Neher, E. and Sakmann, B., Single-Channel Currents Recorded from Membranes of Denervated Frog Muscle Fibres, Nature, 1976, vol. 260, pp. 779–802.

    Google Scholar 

  94. Pauly, N., Knight, M.R., Thuleau, P., van der Luit, A.H., Moreau, M., Trewavas, A.J., Ranjeva, R., and Mazars, C., Cell Signalling: Control of Free Calcium in Plant Cell Nuclei, Nature, 2000, vol. 405, pp. 754–755.

    Google Scholar 

  95. Geisler, M., Axelsen, K.B., Harper, J.F., and Palmdren, M.G., Molecular Aspects of Higher Plant P-Type Ca2+-ATPases, Biochim. Biophys. Acta, 2000, vol. 1465, pp. 52–78.

    Google Scholar 

  96. Sze, H., Liang, F., Hwang, I., Curran, A.C., and Harper, J.F., Diversity and Regulation of Plant Ca2+ Pumps: Insights from Expression in Yeast, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2000, vol. 51, pp. 433–462.

    Google Scholar 

  97. Hirschi, K., Vacuolar H+/Ca2+ Transport: Who Is Directing the Traffic? Trends Plant Sci., 2001, vol. 6, pp. 100–104.

    Google Scholar 

  98. White, P.J., Calcium Channels in Higher Plants, Biochim. Biophys. Acta, 2000, vol. 1465, pp. 171–189.

    Google Scholar 

  99. White, P.J., Bowen, H.C., Demidchik, V., Nichols, C., and Davies, J.M., Genes for Calcium-Permeable Channels in the Plasma Membrane of Plant Root Cells, Biochim. Biophys. Acta, 2002, vol. 1564, pp. 299–309.

    Google Scholar 

  100. Demidchik, V., Davenport, R.J., and Tester, M., Nonselective Cation Channels in Plants, Annu. Rev. Plant Phys. Plant Mol. Biol., 2002, vol. 53, pp. 67–107.

    Google Scholar 

  101. Véry, A.-A. and Sentenac, H., Cation Channels in the Arabidopsis Plasma Membrane, Trends Plant Sci., 2002, vol. 7, pp. 168–175.

    Google Scholar 

  102. White, P.J., Characterization of High-Conductance Voltage-Dependent Cation Channels from the Plasma Membrane of Rye Roots in Planar Lipid Bilayers, Planta, 1993, vol. 191, pp. 541–551.

    Google Scholar 

  103. Sokolik, A.I., Non-Selective Ion Conductance across the Plasmalemma — Important Component of Membrane Ion Transport in Plants, Dokl. Belor. AN, 1999, vol. 43, pp. 77–80.

    Google Scholar 

  104. White, P.J. and Ridout, M.S., An Energy-Barrier Model Describing the Permeation of Monovalent and Divalent Cations through the Maxi Cation-Channel in the Plasma Membrane of Rye Roots, J. Membr. Biol., 1999, vol. 168, pp. 63–75.

    Google Scholar 

  105. Krol, E. and Trebacz, K., Ways of Ion Channel Gating in Plant Cells, Ann. Bot. (London), 2000, vol. 86, pp. 449–469.

    Google Scholar 

  106. Markova, I.V., Batov, A.Yu., Moshkov, A.V., Maksimov, G.B., and Medvedev, S.S., Calcium-Transporting Systems in the Plasmalemma of Maize Coleoptiles, Fiziol. Rast. (Moscow), 1995, vol. 42, pp. 262–267 (Russ. J. Plant Physiol., Engl. Trasl.).

    Google Scholar 

  107. Thuleau, P., Ward, J.M., Ranjeva, R., and Shroeder, J.I., Voltage-Dependent Calcium Permeable Channels in the Plasma Membrane of Higher Plant Cell, EMBO J., 1994, vol. 13, pp. 2970–2975.

    Google Scholar 

  108. Thion, L., Mazars, C., Thuleau, P., Graziana, A., Rossignol, M., Moreau, M., and Ranjeva, R., Activation of Plasma Membrane Voltage-Dependent Calcium-Permeable Channels by Disruption of Microtubules in Carrot Cells, FEBS Lett., 1996, vol. 340, pp. 45–50.

    Google Scholar 

  109. Thion, L., Mazars, C., Nacry, P., Bouchez, D., Moreau, M., Ranjeva, R., and Thuleau, P., Plasma Membrane Depolarization-Activated Calcium Channels, Stimulated by Microtubule-Depolymerizing Drugs in Wild-Type Arabidopsis thaliana Protoplasts, Display Constitutively Large Activities and a Longer Half-Life in ton2 Mutant Cells Affected in the Organization of Cortical Microtubules, Plant J., 1998, vol. 13, pp. 603–610.

    Google Scholar 

  110. Piňeros, M. and Tester, M., Characterization of a Voltage-Dependent Ca2+-Selective Channel from Wheat Roots, Planta, 1995, vol. 195, pp. 478–488.

    Google Scholar 

  111. Piňeros, M. and Tester, M., Calcium Channels in Higher Plant Cells: Selectivity, Regulation and Pharmacology, J. Exp. Bot., 1997, vol. 48, pp. 551–557.

    Google Scholar 

  112. White, P.J., Piňeros, M., Tester, M., and Ridout, M.S., Cation Permeability and Selectivity of a Root Plasma Membrane Calcium Channel, J. Membr. Biol., 2000, vol. 174, pp. 71–83.

    Google Scholar 

  113. White, P.J., Specificity of Ion Channel Inhibitors for the Maxi Cation Channel in Rye Root Plasma Membranes, J. Exp. Bot., 1996, vol. 47, pp. 713–716.

    Google Scholar 

  114. White, P.J., Calcium Channels in the Plasma Membrane of Root Cells, Ann. Bot. (London), 1998, vol. 81, pp. 173–183.

    Google Scholar 

  115. Kiegle, E., Gilliham, M., Haseloff, J., and Tester, M.A., Hyperpolarization-Activated Calcium Currents Found Only in Cells from the Elongation Zone of Arabidopsis thaliana Roots, Plant J., 2000, vol. 21, pp. 225–229.

    Google Scholar 

  116. Véry, A.-A. and Davies, J.M., Hyperpolarization-Activated Calcium Channels at the Tip of Arabidopsis Root Hairs, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 9801–9806.

    Google Scholar 

  117. Schroeder, J.I. and Hagiwara, S., Repetitive Increases in Cytosolic Ca2+ of Guard Cells by Abscisic Acid Activation of Nonselective Ca2+ Permeable Channels, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, pp. 9305–9309.

    Google Scholar 

  118. Hamilton, D.W.A., Hills, A., Kohler, B., and Blatt, M.R., Ca2+ Channels at the Plasma Membrane of Stomatal Guard Cells Are Activated by Hyperpolarization and Abscisic Acid, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 4967–4972.

    Google Scholar 

  119. Hutcheson, S.W., Current Concepts of Active Defense in Plants, Annu. Rev. Phytopathol., 1998, vol. 36, pp. 59–90.

    Google Scholar 

  120. Gelli, A. and Blumwald, E., Hyperpolarization-Activated Ca2+-Permeable Channels in the Plasma Membrane of Tomato Cells, J. Membr. Biol., 1997, vol. 155, pp. 35–45.

    Google Scholar 

  121. Gelli, A., Higgins, V.J., and Blumwald, E., Activation of Plant Plasma Membrane Ca2+-Permeable Channels by Race-Specific Fungal Elicitors, Plant Physiol., 1997, vol. 113, pp. 269–279.

    Google Scholar 

  122. McAinsh, M.R., Brownlee, C., and Hetherington, A.M., Abscisic Acid-Induced Elevation of Guard Cell Cytosolic Ca2+ Precedes Stomatal Closure, Nature, 1990, vol. 343, pp. 186–188.

    Google Scholar 

  123. Ward, J.M., Pei, Z.-M., and Schroeder, J.I., Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants, Plant Cell, 1995, vol. 7, pp. 833–844.

    Google Scholar 

  124. Shishova, M.F., Lindberg, S., and Polevoi, V.V., Auxin Activation of Ca2+ Transport across the Plasmalemma of Plant Cells, Fiziol. Rast. (Moscow), 1999, vol. 46, pp. 1–9 (Russ. J. Plant Physiol., Engl. Transl.).

    Google Scholar 

  125. Zimmermann, S., Thomine, S., Guern, J., and Barbier-Brygoo, H., An Anion Current at the Plasma Membrane of Tobacco Protoplasts Shows ATP-Dependent Voltage Regulation and Is Modulated by Auxin, Plant J., 1994, vol. 6, pp. 707–716.

    Google Scholar 

  126. Marten, I., Lohse, G., and Hedrich, R., Plant Growth Hormones Control Voltage-Dependent Activity of Anion Channels in Plasma Membrane of Guard Cells, Nature, 1991, vol. 353, pp. 758–762.

    Google Scholar 

  127. Zimmermann, S., Nurnberger, T., Frachisse, J.M., Wirtz, W., Guern, J., Hedrich, R., and Scheel, D., Receptor-Mediated Activation of a Plant Ca2+-Permeable Ion Channel Involved in Pathogen Defense, Plant Biol., 1997, vol. 94, pp. 2751–2755.

    Google Scholar 

  128. Pickard, B.G. and Ding, J.P., The Mechanosensory Calcium-Selective Ion Channel: Key Component of a Plasmalemma Control Center? Aust. J. Plant Physiol., 1993, vol. 20, pp. 555–570.

    Google Scholar 

  129. Marshall, J., Corzo, A., Leigh, R.A., and Sanders, D., Membrane Potential-Dependent Calcium Transport in Right-Side-Out Plasma Membrane Vesicles from Zea mays L. Roots, Plant J., 1994, vol. 5, pp. 683–694.

    Google Scholar 

  130. Klüsener, B., Boheim, G., Lib, H., Engelberth, J., and Weiler, E.W., Gadolinium-Sensitive, Voltage-Dependent Calcium Release Channels in the Endoplasmic Reticulum of a Higher Plant Mechanoreceptor Organ, EMBO J., 1995, vol. 14, pp. 2708–2714.

    Google Scholar 

  131. Ding, J.P. and Pickard, B.G., Mechanosensory Calcium-Selective Cation Channels in Epidermal Cells, Plant J., 1993, vol. 3, pp. 83–110.

    Google Scholar 

  132. Furuichi, T., Cunningham, K.W., and Muto, S., A Putative Two-Pore Channel AtTPC1 Mediates Ca2+ Flux in Arabidopsis Leaf Cells, Plant Cell Physiol., 2001, vol. 42, pp. 900–905.

    Google Scholar 

  133. Schachtman, D.P., Kumar, R., Schroeder, J.I., and Marsh, E.L., Molecular and Functional Characterization of a Novel Low-Affinity Cation Transporter (LCT1) in Higher Plants, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 11 079–11 084.

    Google Scholar 

  134. Clemens, S., Antosiewicz, D.M., Ward, J.M., Schachtman, D.P., and Schroeder, J.I., The Plant cDNA LCT1 Mediates the Uptake of Calcium and Cadmium in Yeast, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 12 043–12 048.

    Google Scholar 

  135. Mäser, P., Thomine, S., Schroeder, J.I., Ward, J.M., Hirschi, K., Sze, H., Talke, I.N., Amtmann, A., Maathuis, F.J.M., Sanders, D., Harper, J.F., Tchieu, J., Gribskov, M., Persans, M.W., Salt, D.E., Kim, S.A., and Guerinot, M.L., Phylogenetic Relationships within Cation Transporter Families of Arabidopsis, Plant Physiol., 2001, vol. 126, pp. 1646–1667.

    Google Scholar 

  136. Lacombe, B., Becker, D., Hedrich, R., Desalle, R., Hollman, M., Kwak, J.M., Schroeder, J.I., le Novère, N., Nam, H.G., Spalding, E.P., Tester, M., Turano, E.J., Chiu, J., and Coruzzi, G., On the Identity of Plant Glutamate Receptors, Science, 2001, vol. 292, pp. 1486–1487.

    Google Scholar 

  137. Hille, B., Ionic Channels of Excitable Membranes, Massachusetts: Sinauer Associates, 2001.

    Google Scholar 

  138. Kohler, C., Merkle, T., and Neuhaus, G., Characterization of a Novel Gene Family of Putative Cyclic Nucleotide-and Calmodulin-Regulated Ion Channels in Arabidopsis thaliana, Plant J., 1999, vol. 18, pp. 97–104.

    Google Scholar 

  139. Schuurink, R.C., Shatzer, S.F., Fath, A., and Jones, R.L., Characterization of a Calmodulin-Binding Transporter from the Plasma Membrane of Barley Aleurone, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 1944–1949.

    Google Scholar 

  140. Arazi, T., Sunkar, R., Kaplan, B., and Fromm, H., A Tobacco Plasma Membrane Calmodulin-Binding Transporter Confers Ni2+Tolerance and Pb2+ Hypersensitivity in Transgenic Plants, Plant J., 1999, vol. 20, pp. 171–182.

    Google Scholar 

  141. Zagotta, W.N., Molecular Mechanism of Cyclic Nucleotide-Gate Channels, J. Bioenerg. Biomembr., 1996

  142. Arazi, T., Kaplan, B., and Fromm, H., A High-Affinity Calmodulin-Binding Site in a Tobacco Plasma-Membrane Channel Protein Coincides with Characteristic Element of Cyclic Nucleotide-Binding Domains, Plant. Mol. Biol., 2000, vol. 42, pp. 591–601.

    Google Scholar 

  143. Kohler, C. and Neuhaus, G., Characterization of Calmodulin Binding to Cyclic Nucleotide-Gated Ion Channels from Arabidopsis thaliana, FEBS Lett., 2000, vol. 471, pp. 133–136.

    Google Scholar 

  144. Kohler, C., Merkle, T., Roby, D., and Neuhaus, G., Developmentally Regulated Expression of a Cyclic Nucleotide-Gated Ion Channel from Arabidopsis Indicates Its Involvement in Programmed Cell Death, Planta, 2001, vol. 213, pp. 327–332.

    Google Scholar 

  145. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S.F., The Glutamate Receptor Ion Channels, Pharm. Rev., 1999, vol. 51, pp. 7–61.

    Google Scholar 

  146. Dennison, K.L. and Spalding, E.P., Glutamate-Gated Calcium Fluxes in Arabidopsis, Plant Physiol., 2000, vol. 124, pp. 1511–1514.

    Google Scholar 

  147. Lam, H.-M., Chiu, J., Hsieh, M.-H., Meisel, L., and Oliviera, I.C., Glutamate Receptor Genes in Plants, Nature, 1998, vol. 396, pp. 125–126.

    Google Scholar 

  148. Chiu, J., Desalle, R., Lam, H.-M., Maisel, L., and Coruzzi, G., Molecular Evolution of Glutamate Receptor: A Primitive Signalling Mechanism That Existed before Plants and Animals Diverged, Mol. Biol. Evol., 1999, vol. 16, pp. 826–838.

    Google Scholar 

  149. Allen, G.J. and Sanders, D., Vacuolar Ion Channels of Higher Plants, Adv. Bot. Res., 1997, vol. 25, pp. 218–252.

    Google Scholar 

  150. Johannes, E., Brosnan, J.M., and Sanders, D., Calcium Channels in the Vacuolar Membrane of Plants: Multiple Pathways for Intracellular Calcium Mobilization, Phil. Trans. R. Soc., London, Ser. B, 1992, vol. 338, pp. 105–112.

    Google Scholar 

  151. Gelli, A. and Blumwald, E., Calcium Retrieval from Vacuolar Pools, Plant Physiol., 1993, vol. 102, pp. 1139–1146.

    Google Scholar 

  152. Allen, G.J. and Sanders, D., Two Voltage-Gate Calcium Channels Coreside in the Vacuolar Membrane of Guard Cells, Plant Cell, 1994, vol. 6, pp. 685–694.

    Google Scholar 

  153. Ward, J.M. and Schroeder, J.I., 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, 1994, vol. 6, pp. 669–683.

    Google Scholar 

  154. Schultz-Lessdorf, B. and Hedrich, R., Protons and Calcium Modulate SV-Type Channels in the Vacuolar-Lysosomal Compartment-Channel Interaction with Calmodulin Inhibitors, Planta, 1995, vol. 197, pp. 655–671.

    Google Scholar 

  155. Allen, G.J. and Sanders, D., Control of Ionic Currents in Guard Cell Vacuoles by Cytosolic and Lumenal Calcium, Plant J., 1996, vol. 10, pp. 1055–1067.

    Google Scholar 

  156. Hedrich, R. and Neher, E., Cytoplasmic Calcium Regulates Voltage Dependent Ion Channels in Plant Vacuoles, Nature, 1987, vol. 329, pp. 833–836.

    Google Scholar 

  157. Ward, J.M., Pei, Z.M., and Schroeder, J.I., Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants, Plant Cell, 1995, vol. 7, pp. 833–844.

    Google Scholar 

  158. Bewell, M.A., Maathuis, F.J.M., Allen, G.J., and Sanders, D., Calcium-Induced Calcium Release Mediated by a Voltage-Activated Cation Channel in Vacuolar Vesicles from Red Beet, FEBS Lett., 1999, vol. 458, pp. 41–44.

    Google Scholar 

  159. Pottosin, I.I., Tikhonova, L.I., Hedrich, R., and Schonknecht, G., Slowly Activating Vacuolar Channels Cannot Mediate Ca2+-Induced Ca2+ Release, Plant J., 1997, vol. 12, pp. 1387–1398.

    Google Scholar 

  160. Gambale, F., Bergante, M., Stragepede, F., and Cantu, A.M., Ionic Channels of the Sugar Beet Tonoplast Are Regulated by Multi-Ion Single-File Permeation, J. Membr. Biol., 1996, vol. 154, pp. 69–79.

    Google Scholar 

  161. Johannes, E. and Sanders, D., Luminal Calcium Modulates Unitary Conductance and Gating of an Endomembrane Calcium Release Channel, J. Membr. Biol., 1995, vol. 146, pp. 211–224.

    Google Scholar 

  162. Schumaker, K.S. and Sze, H., Inositol 1,4,5-Trisphosphate Releases Ca2+ from Vacuolar Membrane Vesicles of Oat Roots, J. Biol. Chem., 1987, vol. 262, pp. 3944–3946.

    Google Scholar 

  163. Alexandre, J., Lassalles, J.P., and Kado, R.T., Opening of Ca2+ Channels in Isolated Red Beet Root Vacuole Membrane by Inositol 1,4,5-Trisphosphate, Nature, 1990, vol. 343, pp. 567–570.

    Google Scholar 

  164. Allen, G.J., Muir, S.R., and Sanders, D., Release of Ca2+ from Individual Plant Vacuoles by Both InsP3 and Cyclic ADP-Ribose, Science, 1995, vol. 268, pp. 735–737.

    Google Scholar 

  165. Muir, S.R., Bewell, M.A., Sanders, D., and Allen, G.J., Ligand-Gated Ca2+ Channels and Signalling in Higher Plants, J. Exp. Bot., 1997, vol. 48, pp. 589–597.

    Google Scholar 

  166. Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., and Hetherington, A.M., Abscisic Acid-Induced Stomatal Closure Mediated by Cyclic ADP-Ribose, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 15 837–15 842.

    Google Scholar 

  167. Allen, G.J. and Sanders, D., Osmotic Stress Enhances the Competence of Beta vulgaris Vacuoles to Respond to Inositol 1,4,5-Trisphosphate, Plant J., 1994, vol. 6, pp. 687–695.

    Google Scholar 

  168. Bezprozvanny, I., Watras, J., and Ehrlich, B.E., Bell-Shaped Calcium Response Curves of Ins(1,4,5)P3-and Calcium-Gated Channels from Endoplasmic Reticulum of Cerebellum, Nature, 1991, vol. 351, pp. 751–754.

    Google Scholar 

  169. Taylor, C.W. and Traynor, D., Calcium and Inositol Trisphosphate Receptors, J. Membr. Biol., 1995, vol. 145, pp. 109–118.

    Google Scholar 

  170. Klüsener, B., Boheim, G., and Weiler, E.W., Modulation of the ER Ca2+-Channel BCC1 from Tendrils of Bryonia dioica by Divalent Cations, Protons and H2O2, FEBS Lett., 1997, vol. 407, pp. 230–234.

    Google Scholar 

  171. Klüsener, B. and Weiler, E.W., A Calcium-Selective Channels from Root Tip Endomembranes of Cress, Plant Physiol., 1999, vol. 119, pp. 1399–1405.

    Google Scholar 

  172. Muir, S.R. and Sanders, D., Inositol 1,4,5-Trisphosphate-Sensitive Ca2+ Release across Non-Vacuolar Membranes in Cauliflower, Plant Physiol., 1997, vol. 114, pp. 1511–1521.

    Google Scholar 

  173. Navazio, L., Mariani, P., and Sanders, D., Mobilization of Ca2+ by Cyclic ADP-Ribose from the Endoplasmic Reticulum of Cauliflower Florets, Plant Physiol., 2001, vol. 125, pp. 2129–2138.

    Google Scholar 

  174. Navazio, L., Bewell, M.A., Siddiqua, A., Dickinson, G.D., Galione, A., and Sanders, D., Calcium Release from the Endoplasmic Reticulum of Higher Plants Elicited by the NADP Metabolite Nicotinic Acid Adenine Dinucleotide Phosphate, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 8693–8698.

    Google Scholar 

  175. Martineč, J., Feltl, T., Scanlon, C.H., Lumsden, P.J., and Macháčková, I., Subcellular Localization of a High Affinity Binding Site for D-Myo-Inositol 1,4,5-Trisphosphate from Chenopodium rubrum, Plant Physiol., 2000, vol. 124, pp. 475–483.

    Google Scholar 

  176. Pottosin, I.I. and Schönknecht, G., Ion Channel Permeable for Divalent and Monovalent Cations in Native Spinach Thylakoid Membranes, J. Membr. Biol., 1996, vol. 152, pp. 223–233.

    Google Scholar 

  177. Grygorczyk, C. and Grygorczyk, R.A., Ca2+ and Voltage-Dependent Cation Channel in the Nuclear Envelope of Red Beet, Biochim. Biophys. Acta, 1998, vol. 1375, pp. 117–130.

    Google Scholar 

  178. Pittman, J.K. and Hirshi, K.D., Don’t Shoot the (Second) Messenger: Endomembrane Transporters and Binding Proteins Modulate Cytosolic Ca2+ Levels, Curr. Opin. Plant Biol., 2003, vol. 6, pp. 257–262.

    Google Scholar 

  179. Axelsen, K.V. and Palmgren, M.G., Evolution of Substrate Specificities in the P-Type ATPase Superfamily, J. Mol. Evol., 1998, vol. 46, pp. 84–101.

    Google Scholar 

  180. Evans, D.E. and Williams, L.E., P-Type Calcium ATPases in Higher Plants — Biochemical, Molecular and Functional Properties, Biochim. Biophys. Acta, 1998, vol. 1376, pp. 1–25.

    Google Scholar 

  181. Malmstrom, S., Askerlund, P., and Palmgren, M.G., A Calmodulin-Stimulated Ca2+-ATPase from Plant Vacuolar Membranes with Putative Regulatory Domain at Its N-Terminus, FEBS Lett., 1997, vol. 400, pp. 324–328.

    Google Scholar 

  182. Hwang, I., Sze, H., and Harper, J.F., A Calcium-Dependent Protein Kinase Can Inhibit a Calmodulin-Stimulated Ca2+ Pump (ACA2) Located in the Endoplasmic Reticulum of Arabidopsis, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 6224–6229.

    Google Scholar 

  183. Huang, L., Berkelman, T., Franklin, A.E., and Hoffman, N.E., Characterization of a Gene Encoding a Ca2+-ATPase-Like Protein in Plastid Envelope, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 10066–10070.

    Google Scholar 

  184. Harper, J.F., Hong, B., Hwang, I., Guo, H.Q., Stoddard, R., Huang, L., Palmgren, M.G., and Sze, H., A Novel Calmodulin-Regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-Terminal Autoinhibitory Domain, J. Biol. Chem., 1998, vol. 273, pp. 1099–1106.

    Google Scholar 

  185. Wimmers, L.E., Ewing, N.N., and Bennett, A.B., Higher Plant Ca2+-ATPase: Primary Structure and Regulation of mRNA Abundance by Salt, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 9205–9209.

    Google Scholar 

  186. Chen, X., Chang, M., Wang, B., and Wu, B., Cloning of a Ca2+-ATPase Gene and the Role of Cytosolic Ca2+ in the Gibberellin-Dependent Signaling Pathway in Aleurone Cells, Plant J., 1997, vol. 11, pp. 363–371.

    Google Scholar 

  187. Liang, F., Cunningham, K.W., Harper, J.F., and Sze, H., ECA1 Complements Yeast Mutant Defective in Ca2+ Pumps and Encodes an Endoplasmic Reticulum-Type Ca2+-ATPase in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 8579–8584.

    Google Scholar 

  188. Blackford, S., Rea, P.A., and Sanders, D., Voltage Sensitivity of H+/Ca2+ Antiport in Higher Plant Tonoplast Suggests a Role in Vacuolar Calcium Accumulation, J. Biol. Chem., 1990, vol. 265, pp. 9617–9620.

    Google Scholar 

  189. Hirschi, K., Zhen, R.G., Cunningham, K.W., Rea, P.A., and Fink, G.R., CAX1: An H+/Ca2+ Antiporter from Arabidopsis, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 8782–8786.

    Google Scholar 

  190. Schumaker, K.S. and Sze, H., Calcium Transport into the Vacuole of Oat Root: Characterization of H+/Ca2+ Exchange Activity, J. Biol. Chem., 1986, vol. 261, pp. 12172–12178.

    Google Scholar 

  191. Kasai, N. and Muto, S., Ca2+ Pump and Ca2+/H+ Antiporter in Plasma Membrane Vesicles Isolated by Aqueous Two-Phase Partitioning from Maize Leaves, J. Membr. Biol., 1990, vol. 114, pp. 133–142.

    Google Scholar 

  192. Ueoka-Nakanishi, H., Nakanishi, Y., Tanaka, Y., and Maeshima, M., Properties and Molecular Cloning of a Ca2+/H+ Antiporter in the Vacuolar Membrane of Mung Bean, Eur. J. Biochem., 1999, vol. 262, pp. 417–425.

    Google Scholar 

  193. Dawson, A.P., Calcium Signalling: How Do IP3 Receptor Work? Curr. Biol., 1997, vol. 7, pp. R544–R547.

    Google Scholar 

  194. Malho, R., Moutinho, A., van der Luit, A., and Trewavas, A.J., Spatial Characteristics of Calcium Signalling: The Calcium Wave as a Basic Unit in Plant Cell Calcium Signalling, Phil. Trans. R. Soc., London, Ser. B, 1998, vol. 353, pp. 1463–1473.

    Google Scholar 

  195. Coelho, S.M., Taylor, A.R., Ryan, K.R., Sousa-Pinto, I., Brown, M.T., and Brownlee, C., Spatiotemporal Pattering of Reactive Oxygen Production and Ca2+ Wave Propagation in Fucus Rhizoid Cells, Plant Cell, 2002, vol. 14, pp. 2369–2381.

    Google Scholar 

  196. Wood, N.T., Allan, A.C., and Haley, A., Viry-Moussaïd, M., and Trewavas, A., The Characterization of Differential Calcium Signalling in Tobacco Guard Cells, Plant J., 2000, vol. 24, pp. 335–344.

    Google Scholar 

  197. Evans, N.H., McAinsh, M.R., and Hetherington, A.M., Calcium Oscillations in Higher Plants, Curr. Opin. Plant Biol., 2001, vol. 4, pp. 415–420.

    Google Scholar 

  198. Logan, D.C. and Knigth, M.R., Mitochondrial and Cytosolic Calcium Dynamics Are Differentially Regulated in Plants, Plant Physiol., 2003, vol. 133, pp. 21–24.

    Google Scholar 

  199. Knigth, M.R., Smith, S.M., and Trewavas, A.J., Wind-Induced Plant Motion Immediately Increases Cytosolic Calcium, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 4967–4971.

    Google Scholar 

  200. Scrase-Field, S. and Knight, M.R., Calcium: Just a Chemical Switch? Curr. Opin. Plant Biol., 2003, vol. 6, pp. 500–506.

    Google Scholar 

  201. Frohnmeyer, H., Loyall, L., Blatt, M.R., and Grabov, A., A Millisecond UV-B Irradiation Evokes Prolonged Elevation of Cytosolic Free Ca2+ and Stimulates Gene Expression in Transgenic Parsley Cell Culture, Plant J., 1999, vol. 20, pp. 109–117.

    Google Scholar 

  202. Harper, J.F., Dissecting Calcium Oscillators in Plant Cells, Trends Plant Sci., 2001, vol. 6, pp. 395–397.

    Google Scholar 

  203. Messerli, M. and Robinson, K.R., Tip Localized Ca2+ Pulses Coincident with Peak Pulsate Growth Rates in Pollen Tubes of Lilium longiflorum, J. Cell Sci., 1997, vol. 110, pp. 1269–1278.

    Google Scholar 

  204. Holdaway-Clarke, T.L., Feijo, J.A., Hackett, G.R., Kunkel, J.G., and Hepler, P.K., Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase While Extracellular Calcium Influx Is Delayed, Plant Cell, 1997, vol. 9, pp. 1999–2010.

    Google Scholar 

  205. Walker, S.A., Viprey, V., and Downie, J.A., Dissection of Nodulation Signalling Using Pea Mutants Defective for Calcium Spiking Induced Nod Factors and Chitin Oligomers, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 13413–13418.

    Google Scholar 

  206. Wais, R.J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R.V., Cook, D., Gough, C., Denarie, J., and Long, S.R., Genetic Analysis of Calcium Spiking Response in Nodulation Mutants of Medicago truncatula, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 13407–13412.

    Google Scholar 

  207. McAinsh, M.R., Webb, A.A.R., Taylor, J.E., and Hetherington, A.M., Stimulus-Induced Oscillations in Guard Cell Cytosolic Free Calcium, Plant Cell, 1995, vol. 7, pp. 1207–1219.

    Google Scholar 

  208. Hetherington, A.M., Gray, J.E., Leckie, C.P., McAinsh, M.R., Ng, C., Pical, C., Priestley, A.J., Staxen, I., and Webb, A.A.R., The Control of Specificity in Guard Cell Signal Transduction, Phil. Trans. R. Soc., London, Ser. B, 1998, vol. 353, pp. 1489–1494.

    Google Scholar 

  209. Allen, G.J., Chu, S.P., Harrington, C.L., Schumacher, K., Hoffmann, T., Tang, Y.Y., Grill, E., and Schroeder, J.I., A Defined Range of Guard Cell Calcium Oscillation Parameters Encodes Stomatal Movements, Nature, 2001, vol. 411, pp. 1053–1057.

    Google Scholar 

  210. Trewavas, A.J. and Malho, R., Signal Perception and Transduction: The Origin of the Phenotype, Plant Cell, 1997, vol. 7, pp. 1181–1195.

    Google Scholar 

  211. Tuckner, E.B. and Boss, W.F., Mastoparan-Induced Intracellular Ca2+ Fluxes May Regulate Cell-to-Cell Communications in Plants, Plant Physiol., 1996, vol. 111, pp. 459–467.

    Google Scholar 

  212. Messerli, M.A., Creton, R.C., Jaffe, L.F., and Robinson, K.R., Periodic Increases in Elongation Rate Precede Increases in Cytosolic Ca2+ during Pollen Tube Growth, Dev. Biol., 2000, vol. 222, pp. 84–98.

    Google Scholar 

  213. Digonnet, C., Aldon, D., Leduc, N., Dumas, C., and Rougier, M., First Evidence of Calcium Transient in Flowering Plants at Fertilization, Development, 1997, vol. 124, pp. 2867–2874.

    Google Scholar 

  214. Falke, J.J., Drake, S.K., Hazard, A.L., and Peersen, O.B., Molecular Tuning of Ion Binding to Calcium Signalling Proteins, Q. Rev. Biophys., 1994, vol. 27, pp. 219–290.

    Google Scholar 

  215. Kretsinger, R.H., Rudnick, S.E., and Weisman, L.J., Crystal Stucture of Calmodulin, J. Inorg. Biochem., 1986, vol. 28, pp. 289–302.

    Google Scholar 

  216. Concha, N.O., Head, J.F., Kaetzel, M.A., Dedman, J.R., and Seaton, B.A., Rat Annexin V Crystal Structure: Ca2+ Induced Conformational Changes, Science, 1993, vol. 261, pp. 1321–1324.

    Google Scholar 

  217. Kourie, J.I. and Wood, H.B., Biophysical and Molecular Properties of Annexin-Formed Channels, Prog. Biophys. Mol. Biol., 2000, vol. 73, pp. 91–134.

    Google Scholar 

  218. Gerke, V. and Moss, S.E., Annexins: From Structure to Function, Physiol. Rev., 2002, vol. 82, pp. 331–371.

    Google Scholar 

  219. Essen, L.O., Perisic, O., Cheung, R., Katan, M., and Williams, R.L., Crystal Structure of Mammalian Phosphoinositide-Specific Phospholipase Cδ, Nature, 1996, vol. 380, pp. 595–602.

    Google Scholar 

  220. Kopka, J., Pical, C., Hetherington, A.M., and Müller-Röber, B., Ca2+/Phospholipid-Binding (C2)Domain in Multiple Plant Proteins: Novel Components of the Calcium-Sensing Apparatus, Plant. Mol. Biol., 1998, vol. 36, pp. 627–637.

    Google Scholar 

  221. Roberts, D.M. and Harmon, A.C., Calcium-Modulated Proteins: Targets of Intracellular Calcium Signals in Higher Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1992, vol. 43, pp. 375–414.

    Google Scholar 

  222. Zielinski, R.E., Calmodulin and Calmodulin-Binding Protein in Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1998, vol. 49, pp. 697–725.

    Google Scholar 

  223. Snedden, W.A. and Fromm, H., Calmodulin, Calmodulin-Related Proteins and Responses to the Environment, Trends Plant Sci., 1998, vol. 3, pp. 299–304.

    Google Scholar 

  224. Snedden, W.A. and Fromm, H., Calmodulin as a Versatile Calcium Signal Transducer in Plants, New Phytol., 2001, vol. 151, pp. 35–66.

    Google Scholar 

  225. Chin, D. and Means, A.R., Calmodulin: A Prototypical Calcium Sensor, Trends Cell Biol., 2000, vol. 10, pp. 322–327.

    Google Scholar 

  226. Rhoads, A.R. and Friedberg, F., Sequence Motifs for Calmodulin Recognition, FASEB J., 1997, vol. 11, pp. 331–340.

    Google Scholar 

  227. Takezawa, D., Liu, Z.H., An, G., and Poovaiah, B.W., Calmodulin Gene Family in Potato: Developmental and Touch-Induced Expression of the mRNA Encoding a Novel Isoform, Plant. Mol. Biol., 1995, vol. 27, pp. 693–703.

    Google Scholar 

  228. Heo, W.D., Lee, S.H., Kim, M.C., Kim, J.C., Chung, W.C., Chun, H.J., Lee, K.J., Park, C.Y., Park, H.C., Choi, J.Y., and Cho, M.J., Involvement of Specific Calmodulin Isoforms in Salicylic Acid-Independent Activation of Plant Disease Resistance Responses, Proc. Natl. Acad. Sci. USA, 1999, vol. 19, pp. 766–771.

    Google Scholar 

  229. Liu, J. and Zhu, J.K., A Calcium Sensor Homolog Required for Plant Salt Tolerance, Science, 1998, vol. 280, pp. 1943–1945.

    Google Scholar 

  230. Kudla, J., Xu, Q., Harter, K., Gruissem, W., and Luan, S., Genes for Calcineurin B-Like Proteins in Arabidopsis Are Differentially Regulated by Stress Signals, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 4718–4723.

    Google Scholar 

  231. Shi, J., Kim, K.N., Ritz, O., Albrecht, V., Gupta, R., Harter, K., Luan, S., and Kudla, J., Novel Protein Kinases Associated with Calcineurin B-Like Calcium Sensors in Arabidopsis, Plant Cell, 1999, vol. 11, pp. 2393–2406.

    Google Scholar 

  232. Ward, J.M., Hirschi, K.D., and Sze, H., Plants Pass the Salt, Trends Plant Sci., 2003, vol. 8, pp. 200–201.

    Google Scholar 

  233. Braam, J., Sistrunk, M.L., Polisensky, D.H., Xu, W., Purugganan, M.M., Antosiewicz, D.M., Campbell, P., and Johnson, K.A., Plant Responses to Environmental Stress: Regulation and Function of the Arabidopsis TCH Genes, Planta, 1997, vol. 203, pp. 35–41.

    Google Scholar 

  234. Sistrunk, M.L., Antosiewicz, D.M., Purugganan, M.M., and Braam, J., Arabidopsis TCH3 Encodes a Novel Calcium-Binding Protein and Shows Environmentally Induced and Tissue Specific Regulation, Plant Cell, 1994, vol. 6, pp. 1553–1565.

    Google Scholar 

  235. Frandsen, G., Müller-Uri, F., Nielsen, M., Mundy, J., and Skriver, K., Novel Plant Ca2+-Binding Protein Expressed in Response to Abscisic Acid and Osmotic Stress, J. Biol. Chem., 1996, vol. 271, pp. 343–348.

    Google Scholar 

  236. Jang, H.J., Pih, K.T., Kang, S.G., Lim, J.H., Jin, J.B., Piao, H.L., and Hwang, I., Molecular Cloning of a Novel Ca2+-Binding Protein That Is Induced by NaCl Stress, Plant. Mol. Biol., 1998, vol. 37, pp. 839–847.

    Google Scholar 

  237. Cordeiro, M.C., Piqueras, R., de Oliveira, D.E., and Castresana, C., Characterization of Early Induced Genes in Arabidopsis thaliana Responding to Bacterial Inoculation: Identification of Centrin and of a Novel Protein with Two Regions Related to Kinase Domains, FEBS Lett., 1998, vol. 434, pp. 387–393.

    Google Scholar 

  238. Jakobek, J.L., Smith-Becker, J.A., and Lindgren, P.B., A Bean cDNA Expressed during a Hypersensitive Reaction Encodes a Putative Calcium-Binding Protein, Mol. Plant—Microbe Interact., 1999, vol. 12, pp. 712–719.

    Google Scholar 

  239. Harmon, A.C., Gribskov, M., and Harper, J.F., CDPKs — a Kinase for Every Ca2+ Signal? Trends Plant Sci., 2000, vol. 5, pp. 154–159.

    Google Scholar 

  240. Cheng, S.-H., Willmann, M.R., Chen, H.C., and Sheen, J., Calcium Signalling through Protein Kinases: The Arabidopsis Calcium-Dependent Protein Kinase Gene Family, Plant Physiol., 2002, vol. 129, pp. 469–485.

    Google Scholar 

  241. Zhang, L. and Lu, Y.-T., Calmodulin-Binding Protein Kinases in Plants, Trends Plant Sci., 2003, vol. 8, pp. 123–127.

    Google Scholar 

  242. Harmon, A.C., Gribskov, M., Gubrium, E., and Harper, J.F., The CDPK Superfamily of Protein Kinase, New Phytol., 2001, vol. 151, pp. 175–183.

    Google Scholar 

  243. Sheen, J., Ca2+-Dependent Protein Kinases and Stress Signal Transduction in Plants, Science, 1996, vol. 274, pp. 1900–1902.

    Google Scholar 

  244. Lee, J. and Rudd, J.J., Calcium-Dependent Protein Kinases: Versatile Plant Signalling Components Necessary for Pathogen Defense, Trends Plant Sci., 2002, vol. 7, pp. 97–98.

    Google Scholar 

  245. Clark, G.B. and Roux, S.J., Annexins of Plant Cells, Plant Physiol., 1995, vol. 109, pp. 1133–1139.

    Google Scholar 

  246. Crofts, A.J. and Denecke, J., Calreticulin and Calnexin in Plants, Trends Plant Sci., 1998, vol. 3, pp. 396–399.

    Google Scholar 

  247. Clark, G.B., Sessions, A., Eastburn, D.J., and Roux, S.J., Differential Expression of Members of the Annexin Multigene Family in Arabidopsis, Plant Physiol., 2001, vol. 126, pp. 1072–1084.

    Google Scholar 

  248. Pollard, H.B., Burns, A.L., and Rojas, E., Synexin (Annexin YII), a Cytosolic Calcium-Binding Protein, Which Promotes Membrane Fusion and Forms Calcium Channels in Artificial Bilayer and Natural Membranes, J. Membr. Biol., 1990, vol. 117, pp. 101–112.

    Google Scholar 

  249. Shi, J., Gonzales, R.A., and Bhattacharyya, M.K., Characterization of a Plasma Membrane-Associated Phosphoinositide-Specific Phospholipase C from Soybean, Plant J., 1995, vol. 8, pp. 381–390.

    Google Scholar 

  250. Pappan, K., Zheng, L., and Wang, X., Identification and Characterization of a Novel Plant Phospholipase D That Requires Polyphosphoinositides and Submicromolar Calcium for Activity in Arabidopsis, J. Biol. Chem., 1997, vol. 272, pp. 7048–7054.

    Google Scholar 

  251. Pappan, K., Qin, W., Dyer, J.H., Zheng, L., and Wang, X., Molecular Cloning and Functional Analysis of Polyphosphoinositide-Dependent Phospholipase D, PLDβ, from Arabidopsis, J. Biol. Chem., 1997, vol. 272, pp. 7055–7061.

    Google Scholar 

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  1. Department of Plant Physiology and Biochemistry, St. Petersburg State University, Universitetskaya nab. 7/9, 199034, St. Petersburg, Russia

    S. S. Medvedev

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Translated from Fiziologiya Rastenii, Vol. 52, No. 2, 2005, pp. 282–305.

Original Russian Text Copyright © 2005 by Medvedev.

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Medvedev, S.S. Calcium signaling system in plants. Russ J Plant Physiol 52, 249–270 (2005). https://doi.org/10.1007/s11183-005-0038-1

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