Crosstalk in Ca2+ Signaling Pathways

Signal Crosstalk in Plant Stress Responses

Volumn , Issue , 2009, Pages 59-95

  Mcainsh, Martin R ^a   Schroeder, Julian I ^b  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ca2+ role in gene transcription regulation; Ca2+ efflux pathways; Ca2+ sensitivity priming hypothesis and Ca2+ signaling specificity in eukaryotes; Ca2+ signals in abiotic and biotic stress responses; Ca2+ ATPases and H+ Ca2+ exchangers; Ca2+ independent pathway for stomatal closing; Crosstalk in Ca2+ signaling pathways; Plant defense responses; Pollen tube growth; Whole plant abiotic stress responses

Indexed keywords

EID: 84885208750     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780813805931.ch4     Document Type: Chapter

References (272)

1. Allan, A.C., Fricker, M.D., Ward, J.L., Beale, M.H., and Trewavas, A.J. 1994. 2 transduction pathways mediate rapid effects of abscisic acid in Commelia guard cell. Plant Cell 6:1319-1328.
2. Allen, G.J., Chu, S.P., Schumacher, K., Shimazaki, C.T., Vafeados, D., Kemper, A., Hawke, S.D., Tallman, G., Tsien, R.Y., Harper, J.F., Chory, J., and Schroeder, J.I. 2000. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutants. Science 289:2338-2342.
3. Allen, G.J., Chu, S.P., Harrington, C.L., Schumacher, K., Hoffmann, T., Tang, Y.Y., Grill, E., and Schroeder, J.I. 2001. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053-1057.
4. Allen, G.J., Kwak, J.M., Chu, S.P., Llopis, J., Tsien, R.Y., Harper, J.Y., and Schroeder, J.I. 1999. Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19:735-747.
5. Allen, G.J., Muir, S.R., and Sanders, D. 1995. Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268:735-737.
6. Allen, G.J., Murata, Y., Chu, S.P., Nafisi, M., and Schroeder, J.I. 2002. Hypersensitivity of abscisic acid-induced cytosolic calcium increases in Arabidopsis farnesyltransferase mutant era1-2. Plant Cell 14:1649-1662.
7. Allen, G.J., and Sanders, D. 1995. Calcineurin, A type 2B protein phosphatase, modulates the Ca2+-permeable slow vacuolar ion-channel of stomatal guard-cells. Plant Cell 7:1473-1483.
8. Axelsen, K.B., and Palmgren, M.G. 2001. Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126: 696-706.
9. Bachmann, M., McMicheal, R.W.J., Huber, J.L., Kaiser, W.M., and Huber, S.C. 1995. Partial purification and characterization of a calcium-dependent protein kinase and an inhibitor protein required for inactivation of spinach leaf nitrate reductase. Plant Physiol 108:1083-1091.
10. Balague, C., Lin, B., Alcon, C., Flottes, G., Malstrom, S., Kohler, C., Neuhaus, G., Pelletier, G., Gaymard, F., and 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 15:365-379.
11. Batistic, O., and Kudla, J. 2004. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 210:916-924.
12. Beauvois, M.C., Merezak, C., Jonas, J.C., Ravier, M.A., Henquin, J.C., and Gilon, P. 2006. Glucose-induced mixed [Ca2+]c oscillations in mouse beta-cells are controlled by the membrane potential and the SERCA3 Ca2+-ATPase of the endoplasmic reticulum. Am J Physiol Cell Physiol 290:C1503-C1511.
13. Benedict, C., Geisler, M., Trygg, J., Huner, N., and Hurry, V. 2006. Consensus by democracy. Using metaanalyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiol 141:1219-1232.
14. Berridge, M.J. 2007. Cell Signalling Biology. Colchester, UK: Portland Press.
15. Berridge, M.J. Bootman, M.D., and Roderick, H.L. 2003. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517-529.
16. Berridge, M.J., Lipp, P., and Bootman, M.D. 2000. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21.
17. Bethke, P.C., and Jones, R.L. 1994. Ca2+-calmodulin modulates ion-channel activity in storage protein vacuoles of barley aleurone cells. Plant Cell 6:277-285.
18. Bethke, P.C., and Jones, R.L. 1997. Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel. Plant J 11:1227-1235.
19. Bewell, M.A., Maathuis, F.J.M., Allen, G.J., Sanders, D. 1999. Calcium induced calcium release mediated by a voltage-activated cation channel in vacuolar vesicles from red beet. FEBS Lett 458:41-44.
20. Blatt, M.R., Thiel, G., Trentham, D.R. 1990. Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature 346:766-769.
21. 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 12:1425-1440.
22. Bonza, M.C., Morandini, P., Luoni, L., Geisler, M., Palmgren, M.G., and De Michelis, M.I. 2000. At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol 123:1495-1505.
23. Bothwell, J.H.F., and Ng, C.K.Y. 2005. The evolution of Ca2+ signalling in photosynthetic eukaryotes. New Phytol 166:21-38.
24. Bouche, N., Scharlat, A., Snedden, W., Bouchez, D., and Fromm, H. 2002. A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851-21861.
25. Bouche, N., Yellin, A., Snedden, W.A., and Fromm H. 2005. Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435-466.
26. Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., and Neill, S.J. 2006. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113-122.
27. Burgoyne, R.D., and Weiss, J.L. 2001. The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J 353:1-12.
28. Camello-Almaraz, C., Pariente, J.A., Salido, G., Camello, P.J. 2000. Differential involvement of vacuolar H+-ATPase in the refilling of thapsigargin-and agonist-mobilized Ca2+ stores. Biochem Biophys Res Comm 271:311-317.
29. Cardenas, L., Vidali, L., Dominguez, J., Perez, H., Sanchez, F., Hepler, P.K., and Quinto, C. 1998. Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 116:871-877.
30. Carrion, A.M., Link, W.A., Ledo, F., Mellstrom, B., and Naranjo, J.R. 1999. DREAM is a Ca2+-regulated transcriptional repressor. Nature 398:80-84.
31. Carpaneto, A., Cantu, A.M., and Gambale, F. 2001. Effects of cytoplasmic Mg2+ on slowly activating channels in isolated vacuoles of Beta vulgaris. Planta 213:457-468.
32. Catala, R., Santos, E., Alonso, J.M., Ecker, J.R., Martinez-Zapater, J.M., and Salinas, J. 2003. Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940-2951.
33. Catoira, R., Galera, C., de Billy, F., Penmetsa, R.V., Journet, E.P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., and Denarie J. 2000. Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647-1665.
34. Cheng, N.H., Pittman, J.K., Shigaki, T., Lachmansingh, J., LeClere, S., Lahner, B., Salt, D.E., and Hirschi, K.D. 2005. Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048-2060.
35. Cheng, N.H., Pittman, J.K., Zhu, J.K., and Hirschi, K.D. 2004. The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922-2926.
36. Cheng, S-H., Willmann, M.R., Chen H-C., and Sheen, J. 2002. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469-485.
37. Cheong, Y.H., Kim, K.N., Pandey, G.K., Gupta, R., Grant, J.J., and Luan, S. 2003. CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833-1845.
38. Clayton, H., Knight, M.R., Knight, H., McAinsh, M.R., and Hetherington, A.M. 1999. Dissection of the ozoneinduced calcium signature. Plant J 17:575-579.
39. Clough, S.J., Fengler, K.A., Yu, I.C., Lippok, B., Smith, R.K., and Bent, A.F. 2000. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323-9328.
40. Coelho, S.M., Taylor, A.R., Ryan, K.P., Sousa-Pinto, I., Brown, M.T., and Brownlee, C. 2002. Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cells. Plant Cell 14:2369-2381.
41. Cosgrove, D.J., and Hedrich, R. 1991. Stretch-activated chloride, potassium, and calcium channels coexisting in plasma-membranes of guard cells of Vicia faba L. Planta 186:143-153.
42. Corneliussen, B., Holm, M., Waltersson, Y., Onions, J., Hallberg, B., Thornell, A., and Grundstrom, T. 1994. Calcium/calmodulin inhibition of basic-helix-loop-helix transcription factor domains. Nature 368:760-764.
43. D'Angelo, C., Weinl, S., Batistic, O., Pandey, G.K., Cheong, Y.H., Schultke, S., Albrecht, V., Ehlert, B., Schulz, B., Harter, K., Luan, S., Bock, R., and 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 48:857-872.
44. De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J.M., Thomine, S., Gambale, F., and Barbier-Brygoo, H. 2006. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939-942.
45. Demidchik, V., Bowen, H.C., Maathuis, F.J.M., Shabala, S.N., Tester, M.A., White, P.J., and Davies, J.M. 2002. Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799-808.
46. Demidchik, V., Davenport, R.J., and Tester, M. 2002. Nonselective cation channels in plants. Annu Rev Plant Biol 53:67-107.
47. Dennison, K.L., and Spalding E.P. 2000. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol 124:1511-1514.
48. Denis, V., and Cyert, M.S. 2002. Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Biol Chem 156:29-34.
49. DeWald, D.B., Torabinejad, J., Jones, C.A., Shope, J.C., Cangelosi, A.R., Thompson, J.E., Prestwich, G.D., and Hama, H. 2001. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 126:759-769.
50. Dodd, A.N., Gardner, M.J., Hotta, C.T., Hubbard, K.E., Dalchau, N., Love, J., Assie, J.M., Robertson, F.C., Jakobsen, M.K., Goncalves, J., Sanders, D., and Webb, A.A.R. 2007. The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789-1792.
51. Dodd, A.N., Jakobsen, M.K., Baker, A.J., Telzerow, A., Hou, S.W., Laplaze, L., Barrot, L., Poethig, R.S., Haseloff, J., and Webb, A.A.R. 2006. Time of day modulates low-temperature Ca2+ signals in Arabidopsis. Plant J 48:962-973.
52. Dolmetsch, R.E., Xu, K., and Lewis, R.S. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933-936.
53. Drobak, B.K., and Watkins, P.A.C. 2000. Inositol(1,4,5. trisphosphate production in plant cells: an early response to salinity and hyperosmotic stress. FEBS Lett 481:240-244.
54. Dumas, C., and Gaude, T. 2006. Fertilization in plants: Is calcium a key player? Semin Cell Dev Biol 17:244-253.
55. Durr, G., Strayle, J., Plemper, R., Elbs, S., Klee, S.K., Catty, P., Wolf, D.H., and Rudolph, H.K. 1998. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum associated protein degradation. Mol Biol Cell 9:1149-1162.
56. Dutta, R., and Robinson K.R. 2004. Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135: 1398-1406.
57. Ehrhardt, D.W., Wais, R., and Long, S.R. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673-681.
58. Evans, N.H., McAinsh, M.R., and Hetherington, A.M. 2001. Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415-420.
59. Evans, N.H., McAinsh, M.R., Hetherington, A.M., and Knight, M.R. 2005. ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41:615-626.
60. Fan L-.M., Zhao, Z., and Assmann, S.M. 2004. Guard cells: a dynamic signalling model. Curr Opin Plant Biol 7:537-546.
61. Fellbrich, G., Blume, B., Brunner, F., Hirt, H., Kroj, T., Ligterink, W., Romanski, A., and Nurnberger, T. 2000. Phytopthora parasitica elicitor induced reactions in cells of Petroselinum crispum. Plant Cell Physiol 41:692-701.
62. Felle, H.H., Kondorosi, E., Kondorosi, A., and Schultze, M. 1998. The role of ion fluxes in Nod factor signalling in Medicago sativa. Plant J 13:455-463.
63. Finkler, A., Ashery-Padan, R., and Fromm, H. 2007. CAMTAs: Calmodulin-binding transcription activators from plants to human. FEBS Lett 581:3893-3898.
64. Foreman, J., Demidchik, V., Bothwell, J.H.F., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D.G., Davies, J.M., Dolan L. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-446.
65. Franklin-Tong, V.E., Hackett, G., Hepler, P.K. 1997. Ratio-imaging of Ca2+ in the self-incompatibility response in pollen tubes of Papaver rhoeas. Plant J 12:1375-1386.
66. Franklin-Tong, V.E., Holdaway-Clarke, T.L., Straatman, K.R., Kunke, J.G., Hepler, P.K. 2002. Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas. Plant J 29:333-345.
67. Franklin-Tong, V.E., Ride, J.P., Franklin, F.C.H. 1995. Recombinant stigmatic self-incompatibility. S-protein elicits a Ca2+ transient in pollen of Papaver rhoeas. Plant J 8:299-307.
68. Franklin-Tong, V.E., Ride, J.P., Read, N.D., Trewavas, A.J., and Franklin, F.C.H. 1993. The self-incompatibility reaction in Papaver rhoeas is mediated by cytosolic free calcium. Plant J 4:163-177.
69. Frietsch, S., Wang, Sladek, C., Poulsen, L.R., Romanowsky, S.M., Schroeder, J.I., and Harper, J.F. 2007. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531-14536.
70. Furuichi, T., Cunningham, K.W., and Muto, S. 2001. A putative two pore channel AtTPC1 mediates Ca2+ flux in Arabidopsis leaf cells. Plant Cell Physiol 42:900-905.
71. Fuglsang, A.T., Guo, Y., Cuin, T.A., Qiu, Q.S., Song, C.P., Kristiansen, K.A., Bych, K., Schulz, A., Shabala, S., Schumaker, K.S., Palmgren, M.G., and Zhu, J.K. 2007. Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617-1634.
72. Gaedeke, N., Klein, M., Kolukisaoglu, U., Forestier, C., Muller, A., Ansorge, M., Becker, D., Mamnun, Y., Kuchler, K., Schulz, B., Mueller-Roeber, B., and Martinoia, E. 2001. The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20:1875-1887.
73. Geisler, M., Frangne, N., Gomes, E., Martinoia, E., and Palmgren, M.G. 2000. The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124:1814-1827.
74. Gelli, A., and Blumwald, E. 1997. Hyperpolarization-activated Ca2+-permeable channels in the plasma membrane of tomato cells. J Membr Biol 155:35-45.
75. Gilroy, S., Fricker, M.D., Read, N.D., and Trewavas, A.J. 1991. Role of calcium in signal transduction in Commelina guard cells. Plant Cell 3:333-343.
76. Gilroy, S., Read, N.D., and Trewavas, A.J. 1990. Elevation in cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346:769-771.
77. Gehring, C.A., Irving, H.R., Kabbara, A.A., Parish, R.W., Boukli, N.M., and Broughton, W.J. 1997. Rapid, plateaulike increases in intracellular free calcium are associated with Nod-factor-induced root hair deformation. Mol Plant-Microbe Interact 10:791-802.
78. Geurts, R., and Bisseling, T. 2002. Rhizobium nod factor perception and signaling. Plant Cell 14:S239-S249.
79. Gleason, C., Chaudhuri, S., Yang, T.B., Munoz, A., Poovaiah, B.W., and Oldroyd, G.E.D. 2006. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149-1152.
80. Goddard, H., Manison, N.F.H., Tomos, D., and Brownlee, C. 2000. Elemental propagation of calcium signals in response-specific patterns determined by environmental stimulus strength. Proc Natl Acad Sci USA 97:1932-1937.
81. Grabov, A., and Blatt, M.R. 1998. Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc Natl Acad Sci USA 95:4778-4783.
82. Grabov, A., and Blatt, M.R. 1999. A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarisation in guard cells. Plant Physiol 119:277-287.
83. Grant, M., Brown, I., Adams, S., Knight, M., Ainslie, A., and 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 23:1-11.
84. Grygorczyk, C., and Grygorczyk, R. 1998. A Ca2+-and voltage-dependent cation channel in the nuclear envelope of red beet. Biochim Biophys Acta Biomembr 1375:117-130.
85. Haley, A., Russell, A.J., Wood, N., Allan, A.C., Knight, M., Campbell, A.K., and Trewavas, A.J. 1995. Effects of mechanical signaling on plant cell cytosolic calcium. Proc Natl Acad Sci USA 92:4124-4128.
86. Hamilton, D.W.A., Hills, A., Kohler, B., and Blatt, M.R. 2000. Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967-4972.
87. Han, S.C., Tang, R.H., Anderson, L.K., Woerner, T.E., and Pei, Z.M. 2003. A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425:196-200.
88. Hardingham, G.E., Chawla, S., Johnson, C.M., Bading, H. 1997. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385:260-265.
89. Harmon, A.C., Gribskov, M., and Harper, J.F. 2000. CDPKs-a kinase for every Ca2+ signal? Trends Plant Sci 5:154-159.
90. Harper, J.F. 2001. Dissecting calcium oscillators in plants. Trends Plant Sci 6:395-397.
91. Harper J.F., Breton, G., and Harmon A. 2004. Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263-288.
92. Harper, J.F., and Harmon A. 2005. Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6:555-566.
93. Harper, J.F., Hong, B.M., Hwang, I.D., Guo, H.Q., Stoddard, R., Huang, J.F., Palmgren, M.G., and Sze, H. 1998. A novel calmodulin-regulated Ca2+-ATPase ACA2 from Arabidopsis with an N-terminal autoinhibitory domain. J Biol Chem 273:1099-1106.
94. Harper, J.F., Hung, J.F., and Lloyd, S.J. 1994. Genetic identification of an autoinhibitor in CDPK, a protein-kinase with a calmodulin-like domain. Biochemistry 33:7267-7277.
95. Harper, J.F., Sussman, M.R., Schaller, G.E., Putnam-Evans, C., Charbonneau, H., and Harmon, A.C. 1991. A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252:951-954.
96. Harris, J.M., Wais, R., and Long, S.R. 2003. Rhizobium-induced calcium spiking in Lotus japonicus. Mol Plant Micr Interact 16:335-341.
97. Hedrich, R., Barbierbrygoo, H., Felle, H., Flugge, U.I., Luttge, U., Maathuis, F.J.M., Marx, S., Prins, H.B.A., Raschke, K., Schnabl, H., Chroeder, J.I., Struve, I., Taiz, L., and Zeiger P. 1988. General mechanisms for solute transport across the tonoplast of plant vacuoles-a patch-clamp survey of ion channels and proton pumps. Botan Acta 101:7-13.
98. Hedrich, R., and Neher E. 1987. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329:833-836.
99. Hetherington, A.M., and Brownlee C. 2004. The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401-427.
100. 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. 1998. The control of specificity in guard cell signal transduction. Phil Trans Royal Soc London B 353:1489-1494.
101. Hetherington, A.M., and Woodward, F.I. 2003. The role of stomata in sensing and driving environmental change. Nature 424:901-908.
102. Hirschi, K.D. 1999. Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113-2122.
103. Holdaway-Clarke, T.L., Feijo, J.A., Hackett, G.R., Kunkel, J.G., and Hepler, P.K. 1997. Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9:1999-2010.
104. Holdaway-Clarke, T.L., and Hepler, P.K. 2003. Control of pollen tube growth: the role of ion gradients and fluxes. New Phytol 159:539-563.
105. Hrabak, E.M., Chan, C.W.M., Gribskov, M., Harper, J.F., Choi, J.H., Halford, N., Kudla, J., Luan, S., Nimmo, H.G., Sussman, M.R., Thomas, M., Walker-Simmons, K., Zhu, J.K., and Harmon, A.C. 2003. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666-680.
106. Hu, X.Y., Neill, S.J., Cai, W.M., and Tang, Z.C. 2004. Induction of defence gene expression by oligogalacturonic acid requires increases in both cytosolic calcium and hydrogen peroxide in Arabidopsis thaliana. Cell Res 14:234-240.
107. Huang, J.W., Grunes, D.L., and Kochian, L.V. 1993. Calcium-transport in right-side-out plasma membrane vesicles of wheat roots-characterization of vacuole-gated calcium channels. Plant Physiol S102:22-22.
108. Huang, J.W.W., Grunes, D.L., and Kochian, L.V. 1994. Voltage-dependent Ca2+ influx into right-side-out plasmamembrane vesicles isolated from wheat roots-characterization of a putative Ca2+ channel. Proc Natl Acad Sci USA 91:3473-3477.
109. Hudmon, A., and Schulman, H. 2002. NeuronalCa2+/calmodulin-dependent protein kinase II: The role of structure and autoregulation in cellular function. Annu Rev Biochem 71:473-510.
110. Hwang, I., Harper, J.F., Liang, F., and Sze, H. 2000a. Calmodulin activation of an endoplasmic reticulumlocated calcium pump involves an interaction with the N-terminal autoinhibitory domain. Plant Physiol 122:157-167.
111. Hwang, I., Sze, H., and Harper J.F. 2000b. A calcium-dependent protein kinase can inhibit a calmodulinstimulated Ca2+ pump ACA2 located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97:6224-6229.
112. Ikura, M., Osawa, M., and Ames, J.B. 2002. The role of calcium-binding proteins in the control of transcription: structure to function. Bioessays 24:625-636.
113. Irving, H.R., Gehring, C.A., and Parish, R.W. 1992. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89:1790-1794.
114. Ishibashi, K., Suzuki, M., and Imai, M. 2000. Molecular cloning of a novel form. two-repeat. protein related to voltage-gated sodium and calcium channels. Biochem Biophys Res Comm 270: 370-376.
115. Israelsson, M., Siegel, R.S., Young, J., Hashimoto, M., Iba, K., and Schroeder, J.I. 2006. Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis. Curr Opin Plant Biol 9:654-663.
116. Ito, K., Miyashita, Y., and Kasai, H. 1997. Micromolar and submicromolar Ca2+ spikes regulating distinct cellular functions in pancreatic acinar cells. EMBO J 16:242-251.
117. Ivashuta, S., Liu, J., Liu, J., Lohar, D.P., Haridas, S., Bucciarelli, B., VandenBosch, K.A., Vance, C.P., Harrison, M.J., and Gantt, J.S. 2005. RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911-2921.
118. Johannes, E., Brosnan, J.M., and Sanders, D. 1992. Parallel pathways for intracellular Ca2+ release from the vacuole of higher-plants. Plant J 2:97-102.
119. Kaplan, B., Davydov, O., Knight, H., Galon, Y., Knight, M.R., Fluhr, R., and Fromm, H. 2006. Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive ciselements in Arabidopsis. Plant Cell 18:2733-2748.
120. Kiegle, E., Moore, C., Haseloff, J., Tester, M.A., and Knight, M.R. 2000. Cell-type specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267-278.
121. Kim, B.G., Waadt, R., Cheong, Y.H., Pandey, G.K., Dominguez-Solis, J.R., Schultke, S., Lee, S.C., Kudla, J., and Luan, S. 2007. The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473-484.
122. Kim, K.N., Cheong, Y.H., Grant, J.J., Pandey, G.K., and Luan, S. 2003. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411-423.
123. Kim, K.N., Cheong, Y.H., Gupta, R., and Luan, S. 2000. Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol 124:1844-1853.
124. Klusener, B., Young, J.J., Murata, Y., Allen, G.J., Mori IC, Hugouvieux, V., and Schroeder, J.I. 2002. Convergence of calcium signalling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152-2163.
125. Knight, H., Brandt, S., and Knight, M.R. 1998. A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681-687.
126. Knight, H., Trewavas, A.J., and Knight, M.R. 1996. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 3:489-503.
127. Knight, H., Trewavas, A.J., and Knight, M.R. 1997. Calcium signalling in Arabidopsis thaliana in response to drought and salinity. Plant J 12:1067-1078.
128. Knight, M.R., Campbell, A.K., Smith, S.M., and Trewavas, A.J. 1991. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524-526.
129. Knight, M.R., Smith, S.M., and Trewavas, A.J. 1992. Wind-induced plant motion immediately increases cytosolic calcium. Proc Natl Acad Sci USA 89:4967-4971.
130. Kohler, B., and Blatt, M.R. 2002. Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid. Plant J 32:185-194.
131. Kolukisaoglu, U., Weinl, S., Blazevic, D., Batistic, O., and Kudla, J. 2004. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. J Plant Physiol 134:43-58.
132. Kudla, J., Xu, Q, Harter, K., Gruissem, W., and Luan, S. 1999. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by salt stress. Proc Natl Acad Sci USA 96:4718-4723.
133. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D.G., and Schroeder, J.I. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis. EMBO J 22:2623-2633.
134. Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., and Hetherington, A.M. 1998. Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc Natl Acad Sci USA 95:15837-15842.
135. Lecourieux, D., Lamotte, O., Bourque, S., Wendehenne, D., Mazars, C., Ranjeva, R., and Pugin A. 2005. Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38:527-538.
136. Lecourieux, D., Mazars, C., Pauly, N., Ranjeva, R., and Pugin A. 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14:2627-2641.
137. Lecourieux, D., Raneva, R., and Pugin A. 2006. Calcium in plant defence-signalling pathways. New Phytol 171:249-269.
138. Lee, Y.S, Choi, Y.B., Suh, S., Lee, J., Assmann, S.M., Joe, C.O., Kelleher, J.F., and Crain, R.C. 1996. Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. Plant Physiol 110:987-996.
139. Leonhardt, N., Kwak, J.M., Robert, N., Waner, D., Leonhardt, G., and Schroeder, J.I. 2004. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596-615.
140. Lemtiri-Chlieh, F., and Berkowitz, G.A. 2004. Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J Biol Chem 279:35306-35312.
141. Lemtiri-Chlieh, F., MacRobbie, E.A.C., Webb, A.A.R., Manison, N.F., Brownlee, C., Skepper, J.N., Chen, J., Prestwich, G.D., and Brearley, C.A. 2003. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA 100:10091-10095.
142. Levchenko, V., Konrad, K.R., Dietrich, P., Roelfsema, M.R.G., and Hedrich, R. 2005. Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals. Proc Natl Acad Sci USA 102:4203-4208.
143. Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.P., Ane, J.M., Lauber, E., Bisseling, T., Denarie, J., Rosenberg, C., and Debelle, F. 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361-1364.
144. Li, J., Lee, Y.R., and Assmann, S.M. 1998. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol 116:785-795.
145. Li, S., Assmann, S.M., and Albert, R. 2006. Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol 4:e312.
146. Li, Y., Wang, G.X., Xin, M., Yang, H.M., Wu, X.J., and Li, T. 2004. The parameters of guard cell calcium oscillation encodes stomatal oscillation and closure in Vicia faba. Plant Sci 166:415-421.
147. Li, Y.Q., Zhang, H.Q., Pierson, E.S., Huang, F.Y., Linskens, H.F., Hepler, P.K., and Cresti, M. 1996. Enforced growth-rate fluctuation causes pectin ring formation in the cell wall of Lilium longiflorum pollen tubes. Planta 200:41-49.
148. Liang, F., Cunningham, K.W., Harper, J.F., and Sze, H. 1997. ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an ER-type Ca2+-ATPase in Arabidopsis thaliana. Plant Physiol s114:54-54.
149. Liu, J., and Zhu, J-.K. 1998. A calcium sensor homolog required for plant salt tolerance. Science 280:1943-1945.
150. Logan, D.C., and Knight, M.R. 2003. Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21-24.
151. Lommel, C, and Felle, H. 1997. Transport of Ca2+ across the tonoplast of intact vacuoles from Chenopodium album L suspension cells: ATP-dependent import and inositol-1,4,5-trisphosphate-induced release. Planta 201:477-486.
152. Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S., and Gruissem, W. 2002. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389-S400.
153. Maathius, F. 2004. Ligand-gated ion channels. In: Blatt, M.R. (ed.), Membrane Transport in Plants, Vol. 15. Oxford: Blackwell, pp. 193-220.
154. MacRobbie, E.A.C. 2000. ABA activates multiple Ca2+ fluxes in stomatal guard cells, triggering vacuolar K+(Rb+) release. Proc Natl Acad Sci USA 97:12361-12368.
155. Malho, R., Read, N.D., Pais, M., and Trewavas, A.J. 1994. Role of cytosolic calcium in the reorientation of pollen tube growth. Plant J 5:331-341.
156. Malho, R., Read, N.D., Trewavas, A.J., and Pais, M. 1995. Calcium channel activity during pollen tube growth and re-orientation. Plant Cell 7:1173-1184.
157. Malho, R., and Trewavas, A.J. 1996. Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8:1935-1949.
158. Marshall, J., Corzo, A., Leigh, R.A., and Sanders, D. 1994. Membrane potential-dependent calcium-transport in right-side-out plasma-membrane vesicles from zea-mays l roots. Plant J 5:683-694.
159. Martinec, J., Feltl, T., Scanlon, C.H., Lumsden, P.J., and Machackova I. 2000. Subcellular localization of a high affinity binding site for D-myo-inositol 1,4,5-trisphosphate from Chenopodium rubrum. Plant Physiol 124:475-483.
160. McAinsh, M.R. 2007. Calcium oscillations in guard cell adaptive responses to the environment. In: Mancuso, S., and Shabala, S. (eds.), Rhythms in Plants: Phenomenology, Mechanisms, and Adaptive Significance. Berlin/Heidelberg: Springer-Verlag, 135-155.
161. McAinsh, M.R., Brownlee, C., and Hetherington, A.M. 1990. Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. Nature 343:186-188.
162. McAinsh, M.R., Brownlee, C., and Hetherington, A.M. 1992. Visualising changes in cytosolic-free Ca2+ during the response of stomatal guard cells to abscisic acid. Plant Cell 4:1113-1122.
163. McAinsh, M.R., Clayton, H., Mansfield, T.A., and Hetherington, A.M. 1996. Changes in stomatal behaviour and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031-1042.
164. McAinsh, M.R., Evans, N.H., Montgomery, L.T., and North, K.A. 2002. Calcium signalling in stomatal responses to pollutants. New Phytol 153:441-447.
165. McAinsh, M.R., and Hetherington, A.M. 1998. Encoding specificity in Ca2+ signalling systems. Trends Plant Sci 3:32-36.
166. McAinsh, M.R., Webb, A.A.R., Taylor, J.E., and Hetherington, A.M. 1995. Stimulus-induced oscillations in guard cell cytosolic-free calcium. Plant Cell 7:1207-1219.
167. McCormack, E., Tsai, Y.C., and Braam, J. 2005. Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383-389.
168. Mei, H., Zhao, J., Pittman, J.K., Lachmansingh, J., Park, S., and Hirschi, K.D. 2007. In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Biol 58:3419-3427.
169. Meinrenken, C.J., Borst, J.G.G., and Sakmann, B. 2003. Local routes revisited: the space and time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol London 547:665-689.
170. Messerli, M., and Robinson, K.R. 1997. Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J Cell Sci 110:1269-1278.
171. Messerli, M.A., Creton, R., Jaffe, L.F., and Robinson, K.R. 2000. Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev Biol 222:84-98.
172. Messerli, M.A., and Robinson, K.R. 2003. Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models. Planta 217:147-157.
173. Miller, D.D., Callaham, D.A., Gross, D.J., and Hepler, P.K. 1992. Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101:7-12.
174. Mithofer, A., Ebel, J., Bhagwat, A.A., Boller, T., and Neuhaus-Url, G. 1999. Transgenic aequorin monitors cytosolic calcium transients in soybean cells challenged with β-glucan or chitin elicitors. Planta 207:566-574.
175. Mitra, R.M., Shaw, S.L., and Long, S.R. 2004. Six nonnodulating plant mutants defective for Nod factorinduced transcriptional changes associated with the legume-rhizobia symbiosis. Proc Natl Acad Sci USA 101:10217-10222.
176. Miwa, H., Sun, J., Oldroyd, G.E.D., and Downie, J.A. 2006. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883-894.
177. Monshausen, G.B., Bibikova, T.N., Messerli, M.A., Shi, C., and Gilroy, S. 2007. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996-21001.
178. Mori, I.C., Murata, Y., Yang YZ, Munemasa, S., Wang, Y.F., Andreoli, S., Tiriac, H., Alonso, J.M., Harper, J.F., Ecker, J.R., Kwak, J.M., and Schroeder, J.I. 2006. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion-and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:1749-1762.
179. Mori, I.C., Uozumi, N., and Muto, S. 2000. Phosphorylation of the inward-rectifying potassium channel KAT1 by ABR kinase in Vicia guard cells. Plant Cell Physiol 41:850-856.
180. Muir, S.R., and Sanders, D. 1997. Inositol 1,4,5-trisphosphate-sensitive Ca2+ release across non-vacuolar membranes in cauliflower. Plant Physiol 114:1511-1521.
181. Murata, Y., Pei, Z.M., Mori, I.C., and Schroeder, J. 2001. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NADPH and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513-2523.
182. Mustilli, A.C., Merlot, S., Vavasseur, A., Fenzi, F., and Giraudat, J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089-3099.
183. Nagata, T., Iizumi, S., Satoh, K., Ooka, H., Kawai, J., Carninci, P., Hayashizaki, Y., Otomo, Y., Murakami, K., Matsubara, K., and Kikuchi, S. 2004. Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol Biol Evol 10:1855-1870.
184. Navazio, L., Bewell, M.A., Siddiqua, A., Dickinson, G.D., Galione, A., and 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 97:8693-8698.
185. Navazio, L., Mariani, P., and Sanders, D. 2001. Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 125:2129-2138.
186. Navazio, L., Moscatiello, R., Genre A, Novero, M., Baldan, B., Bonfante, P., and Mariani P. 2007. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673-681.
187. Negi, J., Matsuda, O., Nagasawa, T., Oba, Y., Takahashi, H., Kawai-Yamada, M., Uchimiya, H., Hashimoto, M., and Iba K. 2008. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483-486.
188. Ng, C.K.Y., Carr, K., McAinsh, M.R., Powell, B., and Hetherington, A.M. 2001. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:596-599.
189. Ng, C.K.Y., and McAinsh, M.R. 2003. Encoding specificity in plant calcium signalling: hot-spotting the ups and downs and waves. Ann Botany 92:477-485.
190. Nurnberger, T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K., and Scheel, D. 1994. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449-460.
191. Nurnberger, T., and Scheel, D. 2001. Signal transmission in the plant immune response. Trends Plant Sci 6:372-379.
192. Obermeyer, G., and Weisenseel, M.H. 1991. Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56:319-327.
193. Okada, M., Takezawa, D., Tachibanaki, S., Kawamura, S., Tokumitsu, H., and Kobayashi, R. 2003. Neuronal calcium sensor proteins are direct targets of the insulinotropic agent repaglinide. Biochem J 375:87-97.
194. Oldroyd, G.E.D., and Downie, J.A. 2004. Calcium, kinases and nodulation signalling in legumes. NatureNatl Rev Mol Cell Biol 5:566-576.
195. Oldroyd, G.E.D., and Downie, J.A. 2006. Nuclear calcium changes at the core of symbiosis signaling. Curr Opin Plant Sci 9:351-357.
196. Patil, S., Takezawa, D., and Poovaiah, B.W. 1995. Chimeric plant calcium/calmodulin-dependent protein-kinase gene with a neural visinin-like calcium-binding domain. Proc Natl Acad Sci USA 92:4897-4901.
197. Pauly, N., Knight, M.R., Thuleau, P., Van Der Luit, A.H., Moreau, M., Trewavas, A.J., Ranjeva, R., and Mazars, C. 2000. Cell signalling-control of free calcium in plant cell nuclei. Nature 405:754-755.
198. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., and Schroeder, J.I. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731-734.
199. Pei, Z.M., Ward, J.M., Harper, J.F., and Schroeder, J.I. 1996. A novel chloride channel in Vicia faba guard cell vacuoles activated by the serine/threonine kinase, CDPK. EMBO J 15:6564-6574.
200. Pei, Z.M., Ward, J.M., and Schroeder, J.I. 1999. Magnesium sensitizes slow vacuolar channels to physiological cytosolic calcium and inhibits fast vacuolar channels in fava bean guard cell vacuoles. Plant Physiol 121:977-986.
201. Peiter, E., Maathuis, F.J.M., Mills, L.N., Knight, H., Pelloux, M., Hetherington, A.M., and Sanders, D. 2005. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404-408.
202. Peiter, E., Sun, J., Heckmann, A.B., Venkateshwaran, M., Riely, B.K., Otegui, M.S., Edwards, A., Freshour, G., Hahn, M.G., Cook, D.R., Sanders, D., Oldroyd, G.E.D., Downie, J.A., and Ane, J.M. 2007. The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145:192-203.
203. Perera, I.Y., Heilmann, I., and Boss, W.F. 1999. Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. Proc Natl Acad Sci USA 96:5838-5843.
204. Pierson, E.S., Miller, D.D., Callaham, D.A., Shipley, A.M., Rivers, B.A., Cresti, M., and Hepler, P.K. 1994. Pollen tube growth is coupled to the extracellular calcium ion-flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6:1815-1828.
205. Pierson, E.S., Miller, D.D., Callaham, D.A., van Aken, J., Hackett, G., and Hepler, P.K. 1996. Tip-localized entry fluctuates during pollen tube growth. Dev Biol 174:160-173.
206. Pittman, J.K., and Hirschi, K.D. 2001. Regulation of CAX1, an Arabidopsis Ca2+/H+ antiporter. Identification of an N-terminal autoinhibitory domain. Plant Physiol 127:1020-1029.
207. Pittman, J.K., and Hirschi, K.D. 2003. Don't shoot the second messenger: endomembrane transporters and binding proteins modulate cytosolic Ca2+ levels. Curr Opin Plant Sci 6:257-262.
208. Pittman, J.K., Mills, R.F., O'Connor, C.D., and Williams, L.E. 1999. Two additional type IIA Ca2+-ATPases are expressed in Arabidopsis thaliana: evidence that type IIA sub-groups exist. Gene 236:137-147.
209. Pittman, J.K., Shigaki, T., Marshall, J.L., Morris, J.L., Cheng, N.H., and Hirschi, K.D. 2004. Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol Biol 56:959-971.
210. Poinssot, B., Vandelle, E., Bentejac, M., Adrian, M., Levis, C., Brygoo, Y., Garin, J., Sicilia, F., Coutos-Thevenot, P., and Pugin A. 2003. The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant-Micr Interact 16:553-564.
211. Poovaiah, B.W., Xia, M., Liu, Z.H., Wang, W.Y., Yang, T.B., Sathyanarayanan, P.V., and Franceschi, V.R. 1999. Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers. Planta 209:161-171.
212. Pottosin, I.I., and Schonknecht, G. 2007. Vacuolar calcium channels. J Exp Botany 58:1559-1569.
213. Pottosin, I.I., Tikhonova, L.I., Hedrich, R., and Schonknecht, G. 1997. Slowly activating vacuolar channels can not mediate Ca2+-induced Ca2+ release. Plant J 12:1387-1398.
214. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J., and Knight, M.R. 1994. Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301-1310.
215. Qi, Z., Stephens, N.R., and Spalding, E.P. 2006. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol 142:963-971.
216. Ranf, S., Wunnenberg, P., Lee, J., Becker, D., Dunkel, M., Hedrich, R., Scheel, D., and Dietrich P. 2008. Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J 53:287-299.
217. Rathore, K.S., Cork, R.J., and Robinson, K.R. 1991. A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Dev Biol 148:612-619.
218. Romano, L.A., Jacob, T., Gilroy, S., and Assmann, S.M. 2000. Increases in cytosolic Ca2+ are not required for abscisic acid-inhibition of inward K+ currents in guard cells of Vicia faba L. Planta 211:209-217.
219. Romeis, T., Ludwig, A.A., Martin, R., and Jones, J.D. 2001. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556-5567.
220. Romeis, T., Piedras, P., and Jones, J.D.G. 2000. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12:803-815.
221. Rooney, E.K., Gross, J.D., and Satre, M. 1994. Characterization of an intracellular Ca2+ pump in Dictyostelium. Cell Calcium 16:509-522.
222. Rudd, J.J., and Franklin-Tong V. 2001. Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol 151:7-33.
223. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J.F. 2002. Calcium at the crossroads of signalling. Plant Cell 14:S401-S417.
224. Sathyanarayanan, P.V., Cremo, C.R., and Poovaiah, B.W. 2000. Plant chimericCa2+/calmodulin-dependent protein kinase-role of the neural visinin-like domain in regulating autophosphorylation and calmodulin affinity. J Biol Chem 275:30417-30422.
225. Sathyanarayanan, P.V., Siems, W.F., Jones, J.P., and Poovaiah, B.W. 2001. Calcium-stimulated autophosphorylation site of plant chimeric calcium/calmodulin-dependent protein kinase. J Biol Chem 276:32940-32947.
226. Schroeder, J.I. 2006. Physiology-nitrate at the ion exchange. Nature 442:877-878.
227. Schroeder, J.I., Allen, G.J., Hugouvieux, V., Kwak, J.M., and Waner, D. 2001. Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627-658.
228. Schroeder, J.I., and Hagiwara, S. 1990. Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci USA 87:9305-9309.
229. Schneggenburger, R., and Neher, E. 2005. Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15:266-274.
230. Schulz-Lessdorf, B., and Hedrich, R. 1995. Proton and calcium modulate SV-channels in the vacuolar lysosomal compartment-channel interaction with calmodulin inhibitors. Planta 197:655-671.
231. Schumacher, K., Vafeados, D., McCarthy, M., Sze, H., Wilkins, T., and Chory, J. 1999. The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development. Genes Dev 13:3259-3270.
232. Schumaker, K.S., and Sze, H. 1986. Calcium-transport into the vacuole of oat roots-characterization of H+/Ca2+ exchange activity. J Biol Chem 26:2172-2178.
233. Shacklock, P.S., Read, N.D., and Trewavas, A.J. 1992. Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature 358:753-755.
234. Shaw, S.L., and Long, S.R. 2003. Nod factor elicits two separable calcium responses in Medicago truncatula root hairs. Plant Physiol 131:976-984.
235. Sheen, J. 1996. Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274: 1900-1902.
236. Shi, J., Kim K-.N., Ritz, O., Albrecht, V., Gupta, R., Harter, K., Luan, S., and Kudla, J. 1999. Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393-2405.
237. Shigaki, T., Rees, I., Nakhleh, L., and Hirschi, K.D. 2006. Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815-825.
238. Staxen, I., Pical, C., Montgomery, L.T., Gray, J.E., and Hetherington, A.M. 1999. Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci USA 96:1779-1784.
239. Suh, S.J., Wang, Y.F., Frelet, A., Leonhardt, N., Klein, M., Forestier, C., Mueller-Roeber, B., Cho, M.H., Martinoia, E., and Schroeder, J.I. 2007. The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. J Biol Chem 282:1916-1924.
240. Sze, H., Li, X., and Palmgren, M.G. 1999. Energization of plant cell membranes by H+-pumping ATPases. Regulation and biosynthesis. Plant Cell 11:677-690.
241. Sze, H., Liang, F., Hwang, I., Curran, A.C., and Harper, J.F. 2000. Diversity and regulation of plant Ca2+ pumps: Insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433-462.
242. Tang, R.H., Han, S.C., Zheng, H.L., Cook, C.W., Choi, C.S., Woerner, T.E., Jackson, R.B., and Pei, Z.M. 2007. Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315:1423-1426.
243. Thion, L., Mazars, C., Nacry, P., Bouchez, D., Moreau, M., Ranjeva, R., and 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 13:603-610.
244. Thuleau, P., Ward, J.M., Ranjeva, R., and Schroeder, J.I. 1994a. Voltage-dependent calcium-permeable channels in the plasma-membrane of a higher-plant cell. EMBO J 13:2970-2975.
245. Thuleau, P., Moreau, M., Schroeder, J.I., and Ranjeva, R. 1994b. Recruitment of plasma-membrane voltagedependent calcium-permeable channels in carrot cells. EMBO J 13:5843-5847.
246. Tirichine, L., Imaizumi-Anraku, H., Yoshida, S., Murakami, Y., Madsen, L.H., Miwa, H., Nakagawa, T., Sandal, N., Albrektsen, A.S., Kawaguchi, M., Downie, A., Sato, S., Tabata, S., Kouchi, H., Parniske, M., Kawasaki, S., and Stougaard, J. 2006. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153-1156.
247. Tsien, R.W., and Tsien, R.Y. 1990. Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6:715-760.
248. Vahisalu, T., Kollist, H., Wang, Y.F., Nishimura, N., Chan, W.Y., Valerio, G., Lamminmaki, A., Brosche, M., Moldau, H., Desikan, R., Schroeder, J.I., and Kangasjarvi, J. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487-491.
249. Vandelle, E., Poinssot, B., Wendehenne, D., Bentejac, M., and Pugin A. 2006. Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kin in BcPG1-elicited grapevine defenses. Mol Plant Micr Interact 19:429-440.
250. van den Wijngaard, P.W.J., Bunney, T.D., Roobeek, I., Schonknecht, G., and de Boer, A.H. 2001. Slow vacuolar channels from barley mesophyll cells are regulated by 14-3-3 proteins. FEBS Lett 488:100-104.
251. Very, A.A, and Davies, J.M. 2000. Hyperpolarization-activated calcium influx channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97:9801-9806.
252. Wais, R.J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R.V., Cook, D., Gough, C., Denarie, J., and Long, S.R. 2000. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci USA 97:13407-13412.
253. Walker, S.A., Viprey, V., and Downie, J.A. 2000. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proc Natl Acad Sci USA 97:13413-13418.
254. Ward, J.M., Pei, Z.M., and Schroeder, J.I. 1995. Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7:833-844.
255. Ward, J.M., and Schroeder, J.I. 1994. Calcium-activated K+ channels and calcium-induced calcium-release by slow vacuolar ion channels in guard-cell vacuoles implicated in the control of stomatal closure. Plant Cell 6:669-683.
256. Webb, A.A.R., McAinsh, M.R., Mansfield, T.A., and Hetherington, A.M. 1996. Carbon dioxide induces increases in guard cell cytosolic free calcium. Plant J 9:297-304.
257. Wu, Y., Kuzma, J., Marechal, E., Graeff, R., Lee, H.C., Foster, R., and Chua N-H. 1997. Abscisic acid signalling through cyclic ADP-ribose in plants. Science 278:2126-2130.
258. Wu, Z.Y., Liang, F., Hong, B.M., Young, J.C., Sussman, M.R., Harper, J.F., and Sze, H. 2002. An endoplasmic reticulum-bound Ca2+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+ stress. Plant Physiol 130:128-137.
259. Xie, Y., Coukell, M.B., and Gombos, Z. 1996. Antisense RNA inhibition of the putative vacuolar H+-ATPase proteolipid of Dictyostelium reduces intracellular Ca2+ transport and cell viability. J Cell Sci 109:489-497.
260. Xu, H., Heath, M.C. 1998. Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea frust fungus. Plant Cell 10:585-598.
261. Xu, J., Li, H.D., Chen, L.Q., Wang, Y., Liu, L.L., He, L., and Wu, W.H. 2006. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 7:1347-1360.
262. Yang, T.B., Du, L.Q., and Poovaiah, B.W. 2007. Concept of redesigning proteins by manipulating calcium/calmodulin-binding domains to engineer plants with altered traits. Funct Plant Biol 34:343-352.
263. Yang, Y., Costa, A., Leonhardt, N., Siegel, R.S., and Schroeder, J.I. 2008. Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Meth 4:6.
264. Yang, T., and Poovaiah, B.W. 2002. A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signalling pathways in plants. J Biol Chem 277:45049-45058.
265. Yoo, B.C., and Harmon, A.C. 1996. Intramolecular binding contributes to the activation of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 35:12029-12037.
266. Yoon, G.M., Dowd, P.E., Gilroy, S., and McCubbin, A.G. 2006. Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18:867-878.
267. Yoshioka, K., Moeder, W., Kang, H.G., Kachroo, P., Masmoudi, K., Berkowitz, G., and Klessig DF. 2006. The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18:747-763.
268. Young, J.J., Mehta, S., Israelsson, M., Godoski, J., Grill, E., and Schroeder, J.I. 2006. CO2 signaling in guard cells: calcium sensitivity response modulation, a Ca2+-independent phase, and CO2 insensitivity of the gca2 mutant. Proc Natl Acad Sci USA 103:7506-7511.
269. Zhang, X., Zhang, L., Dong, F.C., Gao, J.F., Galbraith, D.W., and Song, C.P. 2001. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438-1448.
270. Zhu, J.K. 2003. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441-445.
271. Zhu, S.Y., Yu, X.C., Wang, X.J., Zhao, R., Li, Y., Fan, R.C., Shang, Y., Du, S.Y., Wang, X.F., Wu, F.Q., Xu, Y.H., Zhang, X.Y., and Zhang, D.P. 2007. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019-3036.
272. Zimmermann, S., Nurnberger, T., Frachisse, J.M., Wirtz, W., Guern, J., Hedrich, R., and Scheel, D. 1997. Receptormediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94:2751-2755.