Advertisement

Calcium: Not Just Another Ion

  • Oliver Batistič
  • Jörg KudlaEmail author
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 17)

Abstract

Calcium (Ca2+) represents very likely the most versatile ion in living organisms. It is involved in nearly all aspects of plant development and participates in a plethora of regulatory processes. Calcium is an important signaling compound, regulates cellular metabolism and is important for endocytosis and exocytosis. Calcium can easily form complexes with proteins, membranes and other organic acids rendering this ion a versatile signaling constituent and simultaneously a toxic cellular compound. Consequently, the required tight spatial and temporal control of intracellular Ca2+ levels provided the basis for the emergence of calcium signaling. It is this apparent antagonism between the obvious cellular abundance of Ca2+ as a structural important ion in the plant and its required rareness in the cytoplasm as well as the evident question how this simple ion can specifically function in such a myriad of distinct process that has sparked considerable interest and research. Here we will discuss new insights into the signaling function of Ca2+ in the context of its diverse cell biological roles.

Keywords

Endoplasmic Reticulum Stomatal Closure Pollen Tube Growth Permeable Channel Voltage Dependent Channel 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063PubMedCrossRefGoogle Scholar
  2. Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470PubMedCrossRefGoogle Scholar
  3. Alexandre J (1990) Opening of Ca2+ channels in isolated red beet root vacuole membrane by inositol 1, 4, 5-trisphosphate. Nature 343:567–570CrossRefGoogle Scholar
  4. Ali R, Zielinski RE, Berkowitz GA (2006) Expression of plant cyclic nucleotide-gated cation channels in yeast. J Exp Bot 57:125–138PubMedCrossRefGoogle Scholar
  5. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA (2007) Death don’t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19:1081–1095PubMedCrossRefGoogle Scholar
  6. Allen GJ, Sanders D (1994) Two Voltage-Gated, Calcium Release Channels Coreside in the Vacuolar Membrane of Broad Bean Guard Cells. Plant Cell 6:685–694PubMedCrossRefGoogle Scholar
  7. Allen GJ, Muir SR, Sanders D (1995) Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268:735–737PubMedCrossRefGoogle Scholar
  8. Allen GJ, Kwak JM, Chu SP, Llopis J, Tsien RY, Harper JF, Schroeder JI (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19:735–747PubMedCrossRefGoogle Scholar
  9. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342PubMedCrossRefGoogle Scholar
  10. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057PubMedCrossRefGoogle Scholar
  11. Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182PubMedCrossRefGoogle Scholar
  12. Atkinson MM, Keppler LD, Orlandi EW, Baker CJ, Mischke CF (1990) Involvement of Plasma Membrane Calcium Influx in Bacterial Induction of the K/H and Hypersensitive Responses in Tobacco. Plant Physiol 92:215–221PubMedCrossRefGoogle Scholar
  13. Balague C, Lin B, Alcon C, Flottes G, Malmstrom S, Kohler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379PubMedCrossRefGoogle Scholar
  14. Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924PubMedCrossRefGoogle Scholar
  15. Batistic O, Kudla J (2009) Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophys Acta 1793:985–992PubMedCrossRefGoogle Scholar
  16. Batistic O, Sorek N, Schultke S, Yalovsky S, Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20:1346–1362PubMedCrossRefGoogle Scholar
  17. Batistic O, Waadt R, Steinhorst L, Held K, Kudla J (2009) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J, doi: 10.1111/j.1365-1313X.2009.04045.xPubMedGoogle Scholar
  18. Baum G, Long JC, Jenkins GI, Trewavas AJ (1999) Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+. Proc Natl Acad Sci USA 96:13554–13559PubMedCrossRefGoogle Scholar
  19. Belan P, Gardner J, Gerasimenko O, Gerasimenko J, Mills CL, Petersen OH, Tepikin AV (1998) Isoproterenol evokes extracellular Ca2+ spikes due to secretory events in salivary gland cells. J Biol Chem 273:4106–4111CrossRefGoogle Scholar
  20. Berridge MJ (2006) Calcium microdomains: organization and function. Cell Calcium 40:405–412PubMedCrossRefGoogle Scholar
  21. Bhalla A, Chicka MC, Tucker WC, Chapman ER (2006) Ca2+-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat Struct Mol Biol 13:323–330PubMedCrossRefGoogle Scholar
  22. Blume B, Nurnberger T, Nass N, Scheel D (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425–1440PubMedCrossRefGoogle Scholar
  23. Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI (2000) At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol 123:1495–1506PubMedCrossRefGoogle Scholar
  24. Braam J, Sistrunk ML, Polisensky DH, Xu W, Purugganan MM, Antosiewicz DM, Campbell P, Johnson KA (1997) Plant responses to environmental stress: regulation and functions of the Arabidopsis TCH genes. Planta 203:S35–S41CrossRefGoogle Scholar
  25. Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM (2000) Arabidopsis mutants resistant to S(+)-beta-methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol 124:1615–1624PubMedCrossRefGoogle Scholar
  26. Brett C, Waldron K (1996) Physiology and biochemistry of plant cell walls, second editionth edn. Chapman & Hall, LondonGoogle Scholar
  27. Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2003) Variation in the shoot calcium content of angiosperms. J Exp Bot 54:1431–1446PubMedCrossRefGoogle Scholar
  28. Bunney TD, Shaw PJ, Watkins PA, Taylor JP, Beven AF, Wells B, Calder GM, Drobak BK (2000) ATP-dependent regulation of nuclear Ca2+ levels in plant cells. FEBS Lett 476:145–149PubMedCrossRefGoogle Scholar
  29. Bush DS (1993) Regulation of cytosolic calcium in plants. Plant Physiol 103:7–13PubMedGoogle Scholar
  30. Bush DS (1996) Effects of gibberellic acid and environmental factors on cytosloic calcium in wheat aleurone cells. Planta 199:89–99CrossRefGoogle Scholar
  31. Bush DS, Biswas AK, Jones RL (1989a) Gibberellic-acid-stimulated Ca2+ accumulation in endoplasmic reticulum of barley aleurone: Ca2+ transport and steady-state levels. Planta 178:411–420CrossRefGoogle Scholar
  32. Bush DS, Sticher L, van Huystee R, Wagner D, Jones RL (1989b) The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone alpha-amylase. J Biol Chem 264:19392–19398PubMedGoogle Scholar
  33. Bush DS, Biswas AK, Jones RL (1993) Hormonal regulation of Ca2+ transport in the endomembrane system of the barley aleurone. Planta 189:507–515CrossRefGoogle Scholar
  34. Bussler W (1962) Die Entwicklung von Calcium-Mangelsymptomen. Z Pflanzenernahr Dung Bodenkde 100:53–58CrossRefGoogle Scholar
  35. Bygrave FL (1978) Mitochondria and the control of intracellular calcium. Biol Rev Camb Philos Soc 53:43–79PubMedCrossRefGoogle Scholar
  36. Carena M, Bonza MC, Harris R, Sanders D, De Michelis MI (2006) Abscisic acid stimulates the expression of two isoforms of plasma membrane Ca2+-ATPase in Arabidopsis thaliana seedlings. Plant Biol 8:572–578CrossRefGoogle Scholar
  37. Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951PubMedCrossRefGoogle Scholar
  38. Cessna SG, Chandra S, Low PS (1998) Hypo-osmotic shock of tobacco cells stimulates Ca2+ fluxes deriving first from external and then internal Ca2+ stores. J Biol Chem 273:27286–27291PubMedCrossRefGoogle Scholar
  39. Chan CW, Schorrak LM, Smith RK, Bent AF, Sussman MR (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol 132:728–731PubMedCrossRefGoogle Scholar
  40. 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 20:3467–3479PubMedCrossRefGoogle Scholar
  41. Chen X, Chang M, Wang B, Wu B (1997) Cloning of a Ca2+-ATPase gene and the role of cytosolic Ca2+ in the gibberellin-dependent signaling pathway in aleurone cells. Plant J 11:363–371PubMedCrossRefGoogle Scholar
  42. Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1. J Biol Chem 278:6503–6509PubMedCrossRefGoogle Scholar
  43. Cheng NH, Pittman JK, Shigaki T, Hirschi KD (2002a) Characterization of CAX4, an Arabidopsis H+/cation antiporter. Plant Physiol 128:1245–1254PubMedCrossRefGoogle Scholar
  44. Cheng SH, Willmann MR, Chen HC, Sheen J (2002b) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485PubMedCrossRefGoogle Scholar
  45. Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364PubMedCrossRefGoogle Scholar
  46. Cheng NH, Liu JZ, Nelson RS, Hirschi KD (2004a) Characterization of CXIP4, a novel Arabidopsis protein that activates the H+/Ca2+ antiporter, CAX1. FEBS Lett 559:99–106PubMedCrossRefGoogle Scholar
  47. Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004b) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926PubMedCrossRefGoogle Scholar
  48. Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060PubMedCrossRefGoogle Scholar
  49. Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845PubMedCrossRefGoogle Scholar
  50. Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223–239PubMedCrossRefGoogle Scholar
  51. Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322–328PubMedCrossRefGoogle Scholar
  52. Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761PubMedCrossRefGoogle Scholar
  53. Chung WS, Lee SH, Kim JC, Heo WD, Kim MC, Park CY, Park HC, Lim CO, Kim WB, Harper JF, Cho MJ (2000) Identification of a calmodulin-regulated soybean Ca2+-ATPase (SCA1) that is located in the plasma membrane. Plant Cell 12:1393–1407PubMedCrossRefGoogle Scholar
  54. Clapham DE (1995) Calcium signaling. Cell 80:259–268PubMedCrossRefGoogle Scholar
  55. Clayton H, Knight MR, Knight H, McAinsh MR, Hetherington AM (1999) Dissection of the ozone-induced calcium signature. Plant J 17:575–579PubMedCrossRefGoogle Scholar
  56. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328PubMedCrossRefGoogle Scholar
  57. Cosgrove DJ, Hedrich R (1991) Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta 186:143–153PubMedCrossRefGoogle Scholar
  58. D’Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872PubMedCrossRefGoogle Scholar
  59. Dammann C, Ichida A, Hong B, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol 132:1840–1848PubMedCrossRefGoogle Scholar
  60. De Silva DLR, Hetherington AM, Mansfield TA (1996) Where does all the calcium go? Evidence of an important regulatory role for trichomes in two calcicoles. Plant Cell Environ 19:880–886CrossRefGoogle Scholar
  61. Deisseroth K, Heist EK, Tsien RW (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198–202PubMedCrossRefGoogle Scholar
  62. Demarty M, Morvan C, Thellier M (1984) Calcium and the cell wall. Plant Cell Environ 7:441–448CrossRefGoogle Scholar
  63. Demidchik V, Maathuis FJ (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404PubMedCrossRefGoogle Scholar
  64. Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387PubMedCrossRefGoogle Scholar
  65. Demidchik V, Bowen HC, Maathuis FJ, Shabala SN, Tester MA, White PJ, Davies JM (2002) Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799–808PubMedCrossRefGoogle Scholar
  66. Demidchik V, Nichols C, Oliynyk M, Dark A, Glover BJ, Davies JM (2003) Is ATP a signaling agent in plants? Plant Physiol 133:456–461PubMedCrossRefGoogle Scholar
  67. Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J 49:377–386PubMedCrossRefGoogle Scholar
  68. Demidchik V, Shang Z, Shin R, Thompson E, Rubio L, Laohavisit A, Mortimer JC, Chivasa S, Slabas AR, Glover BJ, Schachtman DP, Shabala SN, Davies JM (2009) Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. Plant J 58:903–913PubMedCrossRefGoogle Scholar
  69. Demuro A, Parker I (2006) Imaging single-channel calcium microdomains. Cell Calcium 40:413–422PubMedCrossRefGoogle Scholar
  70. Dennison KL, Spalding EP (2000) Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol 124:1511–1514PubMedCrossRefGoogle Scholar
  71. Dieter P, Marme D (1980) Ca2+ transport in mitochondiral and microsomal fraction from higher plants. Planta 150:1–8CrossRefGoogle Scholar
  72. Dieter P, Marmé D (1983) The effect of calmodulin and far-red light on the kinetic properties of the mitochondrial and microsomal calcium-ion transport system from corn. Planta 159:277–281CrossRefGoogle Scholar
  73. Digonnet C, Aldon D, Leduc N, Dumas C, Rougier M (1997) First evidence of a calcium transient in flowering plants at fertilization. Development 124:2867–2874PubMedGoogle Scholar
  74. Dodd AN, Love J, Webb AA (2005) The plant clock shows its metal: circadian regulation of cytosolic free Ca2+. Trends Plant Sci 10:15–21PubMedCrossRefGoogle Scholar
  75. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM, Robertson FC, Jakobsen MK, Goncalves J, Sanders D, Webb AA (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789–1792PubMedCrossRefGoogle Scholar
  76. Du L, Poovaiah BW (2005) Ca2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741–745PubMedCrossRefGoogle Scholar
  77. Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy AS, Poovaiah BW (2009) Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158PubMedCrossRefGoogle Scholar
  78. Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406PubMedCrossRefGoogle Scholar
  79. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681PubMedCrossRefGoogle Scholar
  80. Epstein E (1961) The essential role of calcium in selective cation transport by plant cells. Plant Physiol 36:437–444PubMedCrossRefGoogle Scholar
  81. Epstein E (1998) How calcium enhances plant salt tolerance. Science 280:1906–1907PubMedCrossRefGoogle Scholar
  82. Estruch JJ, Kadwell S, Merlin E, Crossland L (1994) Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci USA 91:8837–8841PubMedCrossRefGoogle Scholar
  83. Etter EF, Minta A, Poenie M, Fay FS (1996) Near-membrane Ca2+ transients resolved using the Ca2+ indicator FFP18. Proc Natl Acad Sci USA 93:5368–5373PubMedCrossRefGoogle Scholar
  84. Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1386PubMedCrossRefGoogle Scholar
  85. Fairley-Grenot KA, Assmann SM (1992) Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells. J Membr Biol 128:103–113PubMedGoogle Scholar
  86. Farmer PK, Choi JH (1999) Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.). Biochim Biophys Acta 1434:6–17PubMedCrossRefGoogle Scholar
  87. Fasano JM, Massa GD, Gilroy S (2002) Ionic signaling in plant responses to gravity and touch. J Plant Growth Regul 21:71–88PubMedCrossRefGoogle Scholar
  88. Faure JE, Digonnet C, Dumas C (1994) An in Vitro System for Adhesion and Fusion of Maize Gametes. Science 263:1598–1600PubMedCrossRefGoogle Scholar
  89. Felle H (1988) Auxin causes oscillation of cytosolic free calcium and pH in Zea mays coleoptiles. Planta 174:495–499CrossRefGoogle Scholar
  90. Felle HH, Kondorosi E, Kondorosi A, Schultze M (1999) Elevation of the cytosolic free Ca2+ is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol 121:273–280PubMedCrossRefGoogle Scholar
  91. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  92. Franklin-Tong VE, Ride JP, Read ND, Trewavas A, Franklin FCH (1993) The self-incompatibiity response in Papaver rhoeas is mediated by cytosolic free calcium. Plant J 4:163–177CrossRefGoogle Scholar
  93. Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531–14536PubMedCrossRefGoogle Scholar
  94. Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634PubMedCrossRefGoogle Scholar
  95. Fujii H, Zhu JK (2009) An autophosphorylation site of the protein kinase SOS2 is important for salt tolerance in Arabidopsis. Mol Plant 2:183–190PubMedCrossRefGoogle Scholar
  96. Gao D, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Self-reporting Arabidopsis expressing pH and Ca2+ indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134:898–908PubMedCrossRefGoogle Scholar
  97. Gehring CA, Williams DA, Cody SH, Parish RW (1990) Phototropism and geotropism in maize coleoptiles are spatially correlated with increases in cytosolic free calcium. Nature 345:528–530PubMedCrossRefGoogle Scholar
  98. Geisler M, Frangne N, Gomes E, Martinoia E, Palmgren MG (2000) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124:1814–1827PubMedCrossRefGoogle Scholar
  99. George L, Romanowsky SM, Harper JF, Sharrock RA (2008) The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146:716–728PubMedCrossRefGoogle Scholar
  100. Gilroy S, Jones RL (1992) Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci USA 89:3591–3595PubMedCrossRefGoogle Scholar
  101. Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771PubMedCrossRefGoogle Scholar
  102. Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116:429–437CrossRefGoogle Scholar
  103. 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 23:441–450PubMedCrossRefGoogle Scholar
  104. Guo H, Mockler T, Duong H, Lin C (2001a) SUB1, an Arabidopsis Ca2+-binding protein involved in cryptochrome and phytochrome coaction. Science 291:487–490PubMedCrossRefGoogle Scholar
  105. Guo Y, Halfter U, Ishitani M, Zhu JK (2001b) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383–1400PubMedCrossRefGoogle Scholar
  106. Hahm SH, Saunders MJ (1991) Cytokinin increases intracellular Ca2+ in Funaria: detection with Indo-1. Cell Calcium 12:675–681PubMedCrossRefGoogle Scholar
  107. Haley A, Russell AJ, Wood N, Allan AC, Knight M, Campbell AK, Trewavas AJ (1995) Effects of mechanical signaling on plant cell cytosolic calcium. Proc Natl Acad Sci USA 92:4124–4128PubMedCrossRefGoogle Scholar
  108. Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740PubMedCrossRefGoogle Scholar
  109. Hamilton DW, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972PubMedCrossRefGoogle Scholar
  110. Han S, Tang R, Anderson LK, Woerner TE, Pei ZM (2003) A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425:196–200PubMedCrossRefGoogle Scholar
  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 100:8583–8588PubMedCrossRefGoogle Scholar
  112. Harper JF, Hong B, Hwang I, Guo HQ, Stoddard R, Huang JF, Palmgren MG, Sze H (1998) A novel calmodulin-regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-terminal autoinhibitory domain. J Biol Chem 273:1099–1106PubMedCrossRefGoogle Scholar
  113. Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288PubMedCrossRefGoogle Scholar
  114. Hauser H, Levine BA, Williams RJP (1976) Interaction of ions with membranes. Trends Biochem Sci 1:278–281Google Scholar
  115. Hedrich R, Neher E (1987) Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329:833–836CrossRefGoogle Scholar
  116. Helms K (1971) Calcium Deficiency of Dark-grown Seedlings of Phaseolus vulgaris L. Plant Physiol 47:799–804PubMedCrossRefGoogle Scholar
  117. Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155PubMedCrossRefGoogle Scholar
  118. Hepler PK, Wayne RO (1985) Calcium and plant development. Ann Rev Plant Physiol 36:397–439Google Scholar
  119. Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427PubMedCrossRefGoogle Scholar
  120. Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122PubMedCrossRefGoogle Scholar
  121. Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442PubMedCrossRefGoogle Scholar
  122. Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133PubMedCrossRefGoogle Scholar
  123. Ho LC, White PJ (2005) A cellular hypothesis for the induction of blossom-end rot in tomato fruit. Ann Bot (Lond) 95:571–581CrossRefGoogle Scholar
  124. Homann U, Tester M (1997) Ca2+-independent and Ca2+/GTP-binding protein-controlled exocytosis in a plant cell. Proc Natl Acad Sci USA 94:6565–6570PubMedCrossRefGoogle Scholar
  125. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680PubMedCrossRefGoogle Scholar
  126. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278PubMedCrossRefGoogle Scholar
  127. Hua BG, Mercier RW, Leng Q, Berkowitz GA (2003a) Plants do it differently. A new basis for potassium/sodium selectivity in the pore of an ion channel. Plant Physiol 132:1353–1361PubMedCrossRefGoogle Scholar
  128. Hua BG, Mercier RW, Zielinski RE, Berkowitz GA (2003b) Functional interaction of calmodulin with a plant cyclic nucleotide gated cation channel. Plant Physiol Biochem 41:945–954CrossRefGoogle Scholar
  129. Huang L, Berkelman T, Franklin AE, Hoffman NE (1993) Characterization of a gene encoding a Ca2+-ATPase-like protein in the plastid envelope. Proc Natl Acad Sci USA 90:10066–10070PubMedCrossRefGoogle Scholar
  130. Hwang I, Sze H, Harper JF (2000) 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 97:6224–6229PubMedCrossRefGoogle Scholar
  131. Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89:1790–1794PubMedCrossRefGoogle Scholar
  132. Ishida S, Yuasa T, Nakata M, Takahashi Y (2008) A tobacco Calcium-dependent protein kinase, CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTH in response to gibberellins. Plant Cell 20:3273–3288PubMedCrossRefGoogle Scholar
  133. Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678PubMedCrossRefGoogle Scholar
  134. Ivashuta S, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911–2921PubMedCrossRefGoogle Scholar
  135. Jaiswal JK (2001) Calcium - how and why? J Biosci 26:357–363PubMedCrossRefGoogle Scholar
  136. Jeter CR, Tang W, Henaff E, Butterfield T, Roux SJ (2004) Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. Plant Cell 16:2652–2664PubMedCrossRefGoogle Scholar
  137. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269:1863–1865PubMedCrossRefGoogle Scholar
  138. Jun T, Wu S, Bai J, Sun D (1996) Extracellular calmodulin-binding proteins in plants: purification of a 21-kDa calmodulin-binding protein. Planta 198:510–516CrossRefGoogle Scholar
  139. Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide-gated channels in plants. FEBS Lett 581:2237–2246PubMedCrossRefGoogle Scholar
  140. Kasai M, Muto S (1990) Ca2+ pump and Ca2+/H+ antiporter in plasma membrane vesicles isolated by aqueous two-phase partitioning from corn leaves. J Membr Biol 114:133–142PubMedCrossRefGoogle Scholar
  141. Kauss H (1987) Some aspects of Calcium-dependent regulation in plant metabolism. Ann Rev Plant Physiol 38:47–72CrossRefGoogle Scholar
  142. Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S (1998) Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transduction. Plant Cell Physiol 39:721–730Google Scholar
  143. Kesavan J, Borisovska M, Bruns D (2007) v-SNARE actions during Ca2+-triggered exocytosis. Cell 131:351–363PubMedCrossRefGoogle Scholar
  144. Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267–278PubMedCrossRefGoogle Scholar
  145. Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423PubMedCrossRefGoogle Scholar
  146. Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schultke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484PubMedCrossRefGoogle Scholar
  147. Kirkby EA, Pilbeam DJ (1984) Calcium as a plant nutrient. Plant Cell Environ 7:397–405CrossRefGoogle Scholar
  148. Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152–2163PubMedCrossRefGoogle Scholar
  149. Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526PubMedCrossRefGoogle Scholar
  150. Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12:1067–1078PubMedCrossRefGoogle Scholar
  151. Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687PubMedCrossRefGoogle Scholar
  152. Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134:43–58PubMedCrossRefGoogle Scholar
  153. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105:9823–9828PubMedCrossRefGoogle Scholar
  154. Kreimer G, Melkonian M, Holtum JA, Latzko E (1988) Stromal Free Calcium Concentration and Light-Mediated Activation of Chloroplast Fructose-1, 6-Bisphosphatase. Plant Physiol 86:423–428PubMedCrossRefGoogle Scholar
  155. Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723PubMedCrossRefGoogle Scholar
  156. Kushwaha R, Singh A, Chattopadhyay S (2008) Calmodulin7 plays an important role as transcriptional regulator in Arabidopsis seedling development. Plant Cell 20:1747–1759PubMedCrossRefGoogle Scholar
  157. Lam HM, Chiu J, Hsieh MH, Meisel L, Oliveira IC, Shin M, Coruzzi G (1998) Glutamate-receptor genes in plants. Nature 396:125–126PubMedCrossRefGoogle Scholar
  158. Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529PubMedCrossRefGoogle Scholar
  159. Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, Brownlee C, Hofmann A, Webb AA, Miedema H, Battey NH, Davies JM (2009) Zea mays Annexins Modulate Cytosolic Free Ca2+ and Generate a Ca2+-Permeable Conductance. Plant Cell 21:479–493PubMedCrossRefGoogle Scholar
  160. Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695PubMedCrossRefGoogle Scholar
  161. Leckie CP, McAinsh MR, Allen GJ, Sanders D, Hetherington AM (1998) Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc Natl Acad Sci USA 95:15837–15842PubMedCrossRefGoogle Scholar
  162. Leclerc E, Corti C, Schmid H, Vetter S, James P, Carafoli E (1999) Serine/threonine phosphorylation of calmodulin modulates its interaction with the binding domains of target enzymes. Biochem J 344(Pt 2):403–411PubMedCrossRefGoogle Scholar
  163. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14:2627–2641PubMedCrossRefGoogle Scholar
  164. Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38:527–538PubMedCrossRefGoogle Scholar
  165. Lee JS, Mulkey TJ, Evans ML (1983) Reversible Loss of Gravitropic Sensitivity in Maize Roots After Tip Application of Calcium Chelators. Science 220:1375–1376PubMedCrossRefGoogle Scholar
  166. Lee SH, Seo HY, Kim JC, Heo WD, Chung WS, Lee KJ, Kim MC, Cheong YH, Choi JY, Lim CO, Cho MJ (1997) Differential activation of NAD kinase by plant calmodulin isoforms. The critical role of domain I. J Biol Chem 272:9252–9259PubMedCrossRefGoogle Scholar
  167. Lee JY, Yoo BC, Harmon AC (1998) Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. Biochemistry 37:6801–6809PubMedCrossRefGoogle Scholar
  168. Lee SH, Johnson JD, Walsh MP, Van Lierop JE, Sutherland C, Xu A, Snedden WA, Kosk-Kosicka D, Fromm H, Narayanan N, Cho MJ (2000) Differential regulation of Ca2+/calmodulin-dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem J 350(Pt 1):299–306PubMedCrossRefGoogle Scholar
  169. Lee SM, Kim HS, Han HJ, Moon BC, Kim CY, Harper JF, Chung WS (2007) Identification of a calmodulin-regulated autoinhibited Ca2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett 581:3943–3949PubMedCrossRefGoogle Scholar
  170. Legue V, Blancaflor E, Wymer C, Perbal G, Fantin D, Gilroy S (1997) Cytoplasmic free Ca2+ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiol 114:789–800PubMedCrossRefGoogle Scholar
  171. Lemtiri-Chlieh F, MacRobbie EA, Webb AA, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA 100:10091–10095PubMedCrossRefGoogle Scholar
  172. Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6:427–437PubMedCrossRefGoogle Scholar
  173. Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630PubMedCrossRefGoogle Scholar
  174. Li X, Chanroj S, Wu Z, Romanowsky SM, Harper JF, Sze H (2008) A distinct endosomal Ca2+/Mn2+ pump affects root growth through the secretory process. Plant Physiol 147:1675–1689PubMedCrossRefGoogle Scholar
  175. Liang F, Cunningham KW, Harper JF, Sze H (1997) ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an endoplasmic reticulum-type Ca2+-ATPase in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:8579–8584PubMedCrossRefGoogle Scholar
  176. Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24PubMedCrossRefGoogle Scholar
  177. Long JC, Jenkins GI (1998) Involvement of plasma membrane redox activity and calcium homeostasis in the UV-B and UV-A/blue light induction of gene expression in Arabidopsis. Plant Cell 10:2077–2086PubMedCrossRefGoogle Scholar
  178. Love J, Dodd AN, Webb AA (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16:956–966PubMedCrossRefGoogle Scholar
  179. Lu SX, Hrabak EM (2002) An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol 128:1008–1021PubMedCrossRefGoogle Scholar
  180. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736–10741PubMedCrossRefGoogle Scholar
  181. Luo GZ, Wang HW, Huang J, Tian AG, Wang YJ, Zhang JS, Chen SY (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820PubMedCrossRefGoogle Scholar
  182. Lynch J, Polito VS, Lauchli A (1989) Salinity Stress Increases Cytoplasmic Ca Activity in Maize Root Protoplasts. Plant Physiol 90:1271–1274PubMedCrossRefGoogle Scholar
  183. Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65:511–518PubMedCrossRefGoogle Scholar
  184. Ma L, Xu X, Cui S, Sun D (1999) The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 11:1351–1364PubMedCrossRefGoogle Scholar
  185. Ma W, Smigel A, Tsai YC, Braam J, Berkowitz GA (2008) Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 148:818–828PubMedCrossRefGoogle Scholar
  186. MacRobbie EA (1989) Calcium influx at the plasmalemma of isolated guard cells of Commelina communis. Planta 178:231–241CrossRefGoogle Scholar
  187. Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D (2008) Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J 56:575–589PubMedCrossRefGoogle Scholar
  188. Martens S, Kozlov MM, McMahon HT (2007) How synaptotagmin promotes membrane fusion. Science 316:1205–1208PubMedCrossRefGoogle Scholar
  189. Martin ML, Busconi L (2000) Membrane localization of a rice calcium-dependent protein kinase (CDPK) is mediated by myristoylation and palmitoylation. Plant J 24:429–435PubMedCrossRefGoogle Scholar
  190. Martinec J, Feltl T, Scanlon CH, Lumsden PJ, Machackova I (2000) Subcellular localization of a high affinity binding site for D-myo-inositol 1, 4, 5-trisphosphate from Chenopodium rubrum. Plant Physiol 124:475–483PubMedCrossRefGoogle Scholar
  191. Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667PubMedCrossRefGoogle Scholar
  192. Mazars C, Bourque S, Mithofer A, Pugin A, Ranjeva R (2009) Calcium homeostasis in plant cell nuclei. New Phytol 181:261–274PubMedCrossRefGoogle Scholar
  193. McAinsh MR, Brownlee C, Hetherington AM (1990) Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. Nature 343:186–188CrossRefGoogle Scholar
  194. McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phyt 159:585–598CrossRefGoogle Scholar
  195. McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389PubMedCrossRefGoogle Scholar
  196. McCubbin AG, Ritchie SM, Swanson SJ, Gilroy S (2004) The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function. Plant J 39:206–218PubMedCrossRefGoogle Scholar
  197. McNamara VP, Gounaris K (1995) Granal photosystem II complexes contain only the high redox potential form of cytochrome b-559 which is stabilized by the ligation of calcium. Biochim Biophys Acta 1231:289–296CrossRefGoogle Scholar
  198. Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427PubMedCrossRefGoogle Scholar
  199. Menteyne A, Burdakov A, Charpentier G, Petersen OH, Cancela JM (2006) Generation of specific Ca2+ signals from Ca2+ stores and endocytosis by differential coupling to messengers. Curr Biol 16:1931–1937PubMedCrossRefGoogle Scholar
  200. Miedema H, Bothwell JH, Brownlee C, Davies JM (2001) Calcium uptake by plant cells–channels and pumps acting in concert. Trends Plant Sci 6:514–519PubMedCrossRefGoogle Scholar
  201. Miedema H, Demidchik V, Very AA, Bothwell JH, Brownlee C, Davies JM (2008) Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol 179:378–385PubMedCrossRefGoogle Scholar
  202. Miller AJ, Sanders D (1987) Depletion of cytosolic free calcium induced by photosynthesis. Nature 326:397–400CrossRefGoogle Scholar
  203. Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101:7–12Google Scholar
  204. Mills RF, Doherty ML, Lopez-Marques RL, Weimar T, Dupree P, Palmgren MG, Pittman JK, Williams LE (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol 146:116–128PubMedCrossRefGoogle Scholar
  205. Moore AL, Åkerman KEO (1984) Calcium and plant organelles. Plant Cell Environ 7:423–429CrossRefGoogle Scholar
  206. Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, Orellana A, Zurita-Silva A, Ordenes VR (2008) AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J Biol Chem 283:9633–9641PubMedCrossRefGoogle Scholar
  207. Mori IC, Murata Y, Yang Y, Munemasa S, Wang Y-F, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLOS Biology 4:1749–1762CrossRefGoogle Scholar
  208. Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM (2008) Annexins: multifunctional components of growth and adaptation. J Exp Bot 59:533–544PubMedCrossRefGoogle Scholar
  209. Muir SR, Sanders D (1997) Inositol 1, 4, 5-trisphosphate-sensitive Ca2+ release across nonvacuolar membranes in cauliflower. Plant Physiol 114:1511–1521PubMedCrossRefGoogle Scholar
  210. Mulder EG (1950) Mineral nutrition of plants. Annu Rev Plant Physiol 1:1–24CrossRefGoogle Scholar
  211. Nagae M, Nozawa A, Koizumi N, Sano H, Hashimoto H, Sato M, Shimizu T (2003) The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana. J Biol Chem 278:42240–42246PubMedCrossRefGoogle Scholar
  212. 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 Natl Acad Sci USA 104:3639–3644PubMedCrossRefGoogle Scholar
  213. Navazio L, Bewell MA, Siddiqua A, Dickinson GD, Galione A, Sanders D (2000) Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc Natl Acad Sci USA 97:8693–8698PubMedCrossRefGoogle Scholar
  214. Navazio L, Mariani P, Sanders D (2001) Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 125:2129–2138PubMedCrossRefGoogle Scholar
  215. Nemchinov LG, Shabala L, Shabala S (2008) Calcium efflux as a component of the hypersensitive response of Nicotiana benthamiana to Pseudomonas syringae. Plant Cell Physiol 49:40–46PubMedCrossRefGoogle Scholar
  216. Neuhaus G, Bowler C, Kern R, Chua NH (1993) Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73:937–952PubMedCrossRefGoogle Scholar
  217. Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:596–599PubMedCrossRefGoogle Scholar
  218. Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53:988–998PubMedCrossRefGoogle Scholar
  219. Ochiai E-I (1991) Why Calcium? J Chem Educ 68:10–12CrossRefGoogle Scholar
  220. Oh SH, Roberts DM (1990) Analysis of the State of Posttranslational Calmodulin Methylation in Developing Pea Plants. Plant Physiol 93:880–887PubMedCrossRefGoogle Scholar
  221. Ohta M, Guo Y, Halfter U, Zhu JK (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100:11771–11776PubMedCrossRefGoogle Scholar
  222. Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924PubMedCrossRefGoogle Scholar
  223. Pauly N, Knight MR, Thuleau P, Graziana A, Muto S, Ranjeva R, Mazars C (2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30:413–421PubMedCrossRefGoogle Scholar
  224. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  225. Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408PubMedCrossRefGoogle Scholar
  226. Perez V, Wherrett T, Shabala S, Muniz J, Dobrovinskaya O, Pottosin I (2008) Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ. J Exp Bot 59:3845–3855PubMedCrossRefGoogle Scholar
  227. Persson S, Wyatt SE, Love J, Thompson WF, Robertson D, Boss WF (2001) The Ca2+ status of the endoplasmic reticulum is altered by induction of calreticulin expression in transgenic plants. Plant Physiol 126:1092–1104PubMedCrossRefGoogle Scholar
  228. Pittman JK, Shigaki T, Cheng NH, Hirschi KD (2002a) Mechanism of N-terminal autoinhibition in the Arabidopsis Ca2+/H+ antiporter CAX1. J Biol Chem 277:26452–26459PubMedCrossRefGoogle Scholar
  229. Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002b) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062PubMedCrossRefGoogle Scholar
  230. Plieth C (2005) Calcium: just another regulator in the machinery of life? Ann Bot (Lond) 96:1–8CrossRefGoogle Scholar
  231. Plieth C, Hansen UP, Knight H, Knight MR (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J 18:491–497PubMedCrossRefGoogle Scholar
  232. Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci USA 104:4730–4735PubMedCrossRefGoogle Scholar
  233. Portis AR Jr, Heldt HW (1976) Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of CO2 fixation in intact chloroplasts. Biochim Biophys Acta 449:434–436PubMedCrossRefGoogle Scholar
  234. Pottosin II, Schonknecht G (2007) Vacuolar calcium channels. J Exp Bot 58:1559–1569PubMedCrossRefGoogle Scholar
  235. Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310PubMedCrossRefGoogle Scholar
  236. Putnam-Evans C, Harmon A, Palevitz BA, Fechheimer M, Cormier MJ (1989) Calcium-dependent protein kinase is localized with F-actin in plant cells. Cell Motil Cytoskel 12:12–22CrossRefGoogle Scholar
  237. Qi Z, Stephens NR, Spalding EP (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol 142:963–971PubMedCrossRefGoogle Scholar
  238. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441PubMedCrossRefGoogle Scholar
  239. Qudeimat E, Faltusz AM, Wheeler G, Lang D, Brownlee C, Reski R, Frank W (2008) A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105:19555–19560PubMedCrossRefGoogle Scholar
  240. Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99:9061–9066PubMedCrossRefGoogle Scholar
  241. Ranf S, Wunnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P (2008) Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J 53:287–299PubMedCrossRefGoogle Scholar
  242. Rathore KS, Cork RJ, Robinson KR (1991) A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Dev Biol 148:612–619PubMedCrossRefGoogle Scholar
  243. Raz V, Fluhr R (1992) Calcium Requirement for Ethylene-Dependent Responses. Plant Cell 4:1123–1130PubMedCrossRefGoogle Scholar
  244. Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852PubMedCrossRefGoogle Scholar
  245. Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479PubMedCrossRefGoogle Scholar
  246. Romeis T, Piedras P, Jones JD (2000) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12:803–816PubMedCrossRefGoogle Scholar
  247. Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. Embo J 20:5556–5567PubMedCrossRefGoogle Scholar
  248. Rudd JJ, Franklin-Tong VE (1999) Calcium signaling in plants. Cell Mol Life Sci 55:214–232CrossRefGoogle Scholar
  249. Sai J, Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14:1279–1291PubMedCrossRefGoogle Scholar
  250. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327PubMedCrossRefGoogle Scholar
  251. Sakai-Wada A, Yagi S (1993) Ultrastructural studies on the Ca2+ localization in the dividing cells of the maize root tip. Cell Struct Funct 18:389–397PubMedCrossRefGoogle Scholar
  252. Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345:1253–1264PubMedCrossRefGoogle Scholar
  253. Sanchez-Barrena MJ, Fujii H, Angulo I, Martinez-Ripoll M, Zhu JK, Albert A (2007) The structure of the C-terminal domain of the protein kinase AtSOS2 bound to the calcium sensor AtSOS3. Mol Cell 26:427–435PubMedCrossRefGoogle Scholar
  254. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417Google Scholar
  255. Satterlee JS, Sussman MR (1998) Unusual membrane-associated protein kinases in higher plants. J Membr Biol 164:205–213PubMedCrossRefGoogle Scholar
  256. Schaller GE, Harmon AC, Sussman MR (1992) Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat. Biochemistry 31:1721–1727PubMedCrossRefGoogle Scholar
  257. Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374–3388PubMedCrossRefGoogle Scholar
  258. Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507PubMedCrossRefGoogle Scholar
  259. Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427–430CrossRefGoogle Scholar
  260. Schumaker KS, Sze H (1987) Inositol 1, 4, 5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. J Biol Chem 262:3944–3946PubMedGoogle Scholar
  261. Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892PubMedCrossRefGoogle Scholar
  262. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ -permeable channels. Plant Physiol 141:1653–1665PubMedCrossRefGoogle Scholar
  263. Shacklock PS, Read ND, Trewavas A (1992) Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature 358:753–755CrossRefGoogle Scholar
  264. Shang ZL, Ma LG, Zhang HL, He RR, Wang XC, Cui SJ, Sun DY (2005) Ca2+ influx into lily pollen grains through a hyperpolarization-activated Ca2+-permeable channel which can be regulated by extracellular CaM. Plant Cell Physiol 46:598–608PubMedCrossRefGoogle Scholar
  265. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405PubMedCrossRefGoogle Scholar
  266. Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825PubMedCrossRefGoogle Scholar
  267. Shimada T, Watanabe E, Tamura K, Hayashi Y, Nishimura M, Hara-Nishimura I (2002) A vacuolar sorting receptor PV72 on the membrane of vesicles that accumulate precursors of seed storage proteins (PAC vesicles). Plant Cell Physiol 43:1086–1095PubMedCrossRefGoogle Scholar
  268. Simon EW (1978) The symptoms of calcium deficiency in plants. New Phytol 80:1–15CrossRefGoogle Scholar
  269. Staxen II, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR (1999) Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci USA 96:1779–1784PubMedCrossRefGoogle Scholar
  270. Stoelzle S, Kagawa T, Wada M, Hedrich R, Dietrich P (2003) Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway. Proc Natl Acad Sci USA 100:1456–1461PubMedCrossRefGoogle Scholar
  271. Strynadka NC, James MN (1989) Crystal structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem 58:951–998PubMedCrossRefGoogle Scholar
  272. Subbaiah CC, Bush DS, Sachs MM (1994) Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell 6:1747–1762PubMedCrossRefGoogle Scholar
  273. Subbaiah CC, Bush DS, Sachs MM (1998) Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol 118:759–771PubMedCrossRefGoogle Scholar
  274. Sun DY, Bian YQ, Zhao BH, Zhao LY (1995) The effects of CaM on cell wall regeneration and cell division of protoplasts. Plant Cell Physiol 36:133–138Google Scholar
  275. Sun QP, Guo Y, Sun Y, Sun DY, Wang XJ (2006) Influx of extracellular Ca2+ involved in jasmonic-acid-induced elevation of [Ca2+]cyt and JR1 expression in Arabidopsis thaliana. J Plant Res 119:343–350PubMedCrossRefGoogle Scholar
  276. Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJ, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–542PubMedCrossRefGoogle Scholar
  277. Szczegielniak J, Liwosz A, Jurkowski I, Loog M, Dobrowolska G, Ek P, Harmon AC, Muszynska G (2000) Calcium-dependent protein kinase from maize seedlings activated by phospholipids. Eur J Biochem 267:3818–3827PubMedCrossRefGoogle Scholar
  278. Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, Harmon AC, Muszynska G (2005) A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol 139:1970–1983PubMedCrossRefGoogle Scholar
  279. Sze H, Liang F, Hwang I, Curran AC, Harper JF (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462PubMedCrossRefGoogle Scholar
  280. Takahashi K, Isobe M, Knight MR, Trewavas AJ, Muto S (1997) Hypoosmotic Shock Induces Increases in Cytosolic Ca2+ in Tobacco Suspension-Culture Cells. Plant Physiol 113:587–594PubMedGoogle Scholar
  281. Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P (1998) 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 ton 2 mutant cells affected in the organization of cortical microtubules. Plant J 13:603–610PubMedCrossRefGoogle Scholar
  282. Trewavas A (1999) Le calcium, C’est la vie: calcium makes waves. Plant Physiol 120:1–6PubMedCrossRefGoogle Scholar
  283. Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plant. Plant J 58:778–790PubMedCrossRefGoogle Scholar
  284. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637PubMedCrossRefGoogle Scholar
  285. Urquhart W, Gunawardena AH, Moeder W, Ali R, Berkowitz GA, Yoshioka K (2007) The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. Plant Mol Biol 65:747–761PubMedCrossRefGoogle Scholar
  286. Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Aro E, Suorsa M, Scheller HV, Vener AV, Aro EM (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. Febs J 275:1767–1777PubMedCrossRefGoogle Scholar
  287. van Der Luit AH, Olivari C, Haley A, Knight MR, Trewavas AJ (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol 121:705–714CrossRefGoogle Scholar
  288. van Goor BJ, Wiersma D (1974) Redistribution of potassium, calcium, magnesium, and manganese in the plant. Physiol Plant 31:163–168CrossRefGoogle Scholar
  289. Volotovski ID, Sokolovsky SG, Molchan OV, Knight MR (1998) Second messengers mediate increases in cytosolic calcium in tobacco protoplasts. Plant Physiol 117:1023–1030PubMedCrossRefGoogle Scholar
  290. Wagner G, Rossbacher R (1980) X-ray microanalysis and chlorotetracycline staining of calcium vesicles in the green alg Mougeotia. Planta 149:298–305CrossRefGoogle Scholar
  291. Walter A, Mazars C, Maitrejean M, Hopke J, Ranjeva R, Boland W, Mithofer A (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed Engl 46:4783–4785PubMedCrossRefGoogle Scholar
  292. Watanabe E, Shimada T, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2002) Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S albumin. J Biol Chem 277:8708–8715PubMedCrossRefGoogle Scholar
  293. Webb AAR, McAinsh MR, Mansfield TA, Hetherington AM (1996) Carbon dioxide induces increases in guard cell cytosolic free calcium. Plant J 9:297–304CrossRefGoogle Scholar
  294. Wegner LH, De Boer AH (1997) Properties of Two Outward-Rectifying Channels in Root Xylem Parenchyma Cells Suggest a Role in K+ Homeostasis and Long-Distance Signaling. Plant Physiol 115:1707–1719PubMedGoogle Scholar
  295. Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686PubMedCrossRefGoogle Scholar
  296. Wheeler GL, Brownlee C (2008) Ca2+ signalling in plants and green algae–changing channels. Trends Plant Sci 13:506–514PubMedCrossRefGoogle Scholar
  297. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (Lond) 92:487–511CrossRefGoogle Scholar
  298. White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM (2002) Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim Biophys Acta 1564:299–309PubMedCrossRefGoogle Scholar
  299. Wick SM, Hepler PK (1980) Localization of Ca2+-containing antimonate precipitates during mitosis. J Cell Biol 86:500–513PubMedCrossRefGoogle Scholar
  300. Williams RJP (1970) The biochemistry of sodium, potassium, magnesium, and calcium. Quart Rev Chem Soc 24:331–365CrossRefGoogle Scholar
  301. Williams RJ (2004) Signalling: basics and evolution. Acta Biochim Pol 51:281–298PubMedGoogle Scholar
  302. Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, Foster R, Chua NH (1997) Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278:2126–2130PubMedCrossRefGoogle Scholar
  303. Wu Z, Liang F, Hong B, Young JC, Sussman MR, Harper JF, Sze H (2002) An endoplasmic reticulum-bound Ca2+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+ stress. Plant Physiol 130:128–137PubMedCrossRefGoogle Scholar
  304. Xiong TC, Jauneau A, Ranjeva R, Mazars C (2004) Isolated plant nuclei as mechanical and thermal sensors involved in calcium signalling. Plant J 40:12–21PubMedCrossRefGoogle Scholar
  305. Xu H, Heath MC (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10:585–598PubMedCrossRefGoogle Scholar
  306. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360PubMedCrossRefGoogle Scholar
  307. Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proc Natl Acad Sci USA 102:16107–16112PubMedCrossRefGoogle Scholar
  308. Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1. Plant Cell 20:3389–3404PubMedCrossRefGoogle Scholar
  309. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512PubMedCrossRefGoogle Scholar
  310. Yoon GM, Dowd PE, Gilroy S, McCubbin AG (2006) Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18:867–878PubMedCrossRefGoogle Scholar
  311. Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, Berkowitz G, Klessig DF (2006) The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18:747–763PubMedCrossRefGoogle Scholar
  312. Yu IC, Parker J, Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 95:7819–7824PubMedCrossRefGoogle Scholar
  313. Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669PubMedCrossRefGoogle Scholar
  314. Zhao J, Shigaki T, Mei H, Guo YQ, Cheng NH, Hirschi KD (2009) Interaction between Arabidopsis Ca2+/H+ Exchangers CAX1 and CAX3. J Biol Chem 284:4605–4615PubMedCrossRefGoogle Scholar
  315. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Institut für Botanik und Botanischer GartenUniversität MünsterMünsterGermany

Personalised recommendations