The plant vacuole: Emitter and receiver of calcium signals

Cell Calcium

Volumn 50, Issue 2, 2011, Pages 120-128

  Peiter, Edgar ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Calcium channel; Ligand gated channels; Phosphorylation; Plant; Tonoplast; TPC1; Vacuole

Indexed keywords

CALCIUM ION; CARRIER PROTEIN; LIGAND GATED ION CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL TRANSPORT; CELL TYPE; CELL VACUOLE; CYTOSOL; ELECTROPHYSIOLOGY; ENVIRONMENT; FEEDBACK SYSTEM; GENETIC CODE; MOLECULAR CLONING; NONHUMAN; PLANT; PLANT GENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SPECIES DIFFERENCE; TONOPLAST; TPC1 GENE;

EID: 79958826531     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.02.002     Document Type: Review

References (148)

1. Webb A.A.R., Larman M.G., Montgomery L.T., Taylor J.E., Hetherington A.M. The role of calcium in ABA-induced gene expression and stomatal movements. Plant J. 2001, 26:351-362.
2. + channels in Arabidopsis guard cells. Plant J. 2009, 59:207-220.
3. Knight H., Trewavas A.J., Knight M.R. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 1997, 12:1067-1078.
4. Oldroyd G.E.D., Downie J.A. Nuclear calcium changes at the core of symbiosis signalling. Curr. Opin. Plant Biol. 2006, 9:351-357.
5. 2+ signaling. Annu. Rev. Plant Biol. 2010, 61:561-591.
6. 2+ signals: their role in regulating stomatal movements. Plant Cell Environ. 2010, 33:305-321.
7. Kudla J., Batistic O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563.
8. Dodd A.N., Kudla J., Sanders D. The language of calcium signaling. Annu. Rev. Plant Biol. 2010, 61:593-620.
9. McAinsh M.R., Pittman J.K. Shaping the calcium signature. New Phytol. 2009, 181:275-294.
10. 2+ signals in plants. Annu. Rev. Plant Biol. 2004, 55:401-427.
11. Ng C.K.Y., McAinsh M.R. Encoding specificity in plant calcium signalling: hot-spotting the ups and downs and waves. Ann. Bot. 2003, 92:477-485.
12. 2+ signal in maize suspension-cultured cells. Plant Physiol. 1998, 118:759-771.
13. Isayenkov S., Isner J.C., Maathuis F.J.M. Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Lett. 2010, 584:1982-1988.
14. Martinoia E., Maeshima M., Neuhaus H.E. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 2007, 58:83-102.
15. Karley A.J., Leigh R.A., Sanders D. Differential ion accumulation and ion fluxes in the mesophyll and epidermis of barley. Plant Physiol. 2000, 122:835-844.
16. Storey R., Leigh R.A. Processes modulating calcium distribution in citrus leaves. An investigation using x-ray microanalysis with strontium as a tracer. Plant Physiol. 2004, 136:3838-3848.
17. 2+ and pH?. Planta 1988, 176:248-255.
18. 2+ fluxes in situ. J. Exp. Bot. 2008, 59:3845-3855.
19. 2+-selective electrodes. J. Exp. Bot. 1997, 48:337-344.
20. Schroeder J.I., Allen G.J., Hugouvieux V., Kwak J.M., Waner D. Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52:627-658.
21. MacRobbie E.A.C., Kurup S. Signalling mechanisms in the regulation of vacuolar ion release in guard cells. New Phytol. 2007, 175:630-640.
22. 2+-binding protein in radish vacuoles. Plant Physiol. 2000, 124:1069-1078.
23. Ishijima J., Nagasaki N., Maeshima M., Miyano M. RVCaB, a calcium-binding protein in radish vacuoles, is predominantly an unstructured protein with a polyproline type II helix. J. Biochem. 2007, 142:201-211.
24. 2+-deficient conditions. Plant Mol. Biol. 2001, 47:633-640.
25. Heyen B.J., Alsheikh M.K., Smith E.A., Torvik C.F., Seals D.F., Randall S.K. The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiol. 2002, 130:675-687.
26. 2+- and pH-dependent manner. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:16107-16112.
27. Lecourieux D., Ranjeva R., Pugin A. Calcium in plant defence-signalling pathways. New Phytol. 2006, 171:249-269.
28. White P.J., Broadley M.R. Calcium in plants. Ann. Bot. 2003, 92:487-511.
29. 2+ stores. J. Biol. Chem. 1998, 273:27286-27291.
30. Price A.H., Taylor A., Ripley S.J., Griffiths A., Trewavas A.J., Knight M.R. Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 1994, 6:1301-1310.
31. 2+ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiol. 1997, 114:789-800.
32. Knight M.R., Smith S.M., Trewavas A.J. Wind-induced plant motion immediately increases cytosolic calcium. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:4967-4971.
33. Gilroy S., Fricker M.D., Read N.D., Trewayas A.J. Role of calcium in signal transduction of Commelina guard cells. Plant Cell 1991, 3:333-344.
34. McAinsh M.R., Webb A.A.R., Taylor J.E., Hetherington A.M. Stimulus-induced oscillations in guard cell cytoplasmic free calcium. Plant Cell 1995, 7:1207-1219.
35. 2+ during the response of stomatal guard cells to abscisic acid. Plant Cell 1992, 4:1113-1122.
36. 2+ increases with abscisic acid in stomatal guard cells. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:4778-4783.
37. Knight H., Trewavas A.J., Knight M.R. Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 1996, 8:489-503.
38. Allen G.J., Chu S.P., Schumacher K., et al. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 2000, 289:2338-2342.
39. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 2005, 434:404-408.
40. Islam M.M., Munemasa S., Hossain M.A., Nakamura Y., Mori I.C., Murata Y. Roles of AtTPC1, vacuolar two pore channel 1, in Arabidopsis stomatal closure. Plant Cell Physiol. 2010, 51:302-311.
41. Allen G.J., Sanders D. Vacuolar ion channels of higher plants. Adv. Bot. Res. 1997, 25:217-252.
42. Pottosin I.I., Schönknecht G. Vacuolar calcium channels. J. Exp. Bot. 2007, 58:1559-1569.
43. 2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 1995, 268:735-737.
44. Leckie C.P., McAinsh M.R., Allen G.J., Sanders D., Hetherington A.M. Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15837-15842.
45. 2+ release from red beet microsomes suggests the presence of ryanodine receptor homologs in higher plants. FEBS Lett. 1996, 395:39-42.
46. 2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol. 2001, 125:2129-2138.
47. Klüsener B., Young J.J., Murata Y., et al. Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol. 2002, 130:2152-2163.
48. Garcia-Mata C., Gay R., Sokolovski S., Hills A., Lamattina L., Blatt M.R. Nitric oxide regulates K+ and Cl- channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11116-11121.
49. Wu Y., Kuzma J., Maréchal E., et al. Abscisic acid signaling through cyclic ADP-ribose in plants. Science 1997, 278:2126-2130.
50. Sánchez J.-P., Duque P., Chua N.-H. ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. Plant J. 2004, 38:381-395.
51. Dodd A.N., Gardner M.J., Hotta C.T., et al. The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 2007, 318:1789-1792.
52. Xu X., Graeff R., Xie Q., Gamble K.L., Mori T., Johnson C.H. Comment on "The Arabidopsis circadian clock incorporates a cADPR-based feedback loop" Science 2009, 326:230-b.
53. Dodd A.N., Gardner M.J., Hotta C.T., et al. Response to comment on "The Arabidopsis circadian clock incorporates a cADPR-based feedback loop" Science 2009, 326:230-c.
54. 3 pathway in Arabidopsis. Science 2007, 315:1423-1426.
55. Calcraft P.J., Ruas M., Pan Z., et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 2009, 459:596-600.
56. Brailoiu E., Churamani D., Cai X., et al. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 2009, 186:201-209.
57. Navazio L., Bewell M.A., Siddiqua A., Dickinson G.D., Galione A., Sanders D. Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8693-8698.
58. Krinke O., Novotna Z., Valentova O., Martinec J. Inositol trisphosphate receptor in higher plants: is it real?. J. Exp. Bot. 2007, 58:361-376.
59. 2+ from vacuolar membrane vesicles of oat roots. J. Biol. Chem. 1987, 262:3944-3946.
60. Ranjeva R., Carrasco A., Boudet A.M. Inositol trisphosphate stimulates the release of calcium from intact vacuoles isolated from Acer cells. FEBS Lett. 1988, 230:137-141.
61. 2+ across the tonoplast of intact vacuoles from Chenopodium album L. suspension cells: ATP-dependent import and inositol-1 4,5-trisphosphate-induced release. Planta 1997, 201:477-486.
62. 2+ channels in isolated red beet root vacuole membrane by inositol 1 4,5-trisphosphate. Nature 1990, 343:567-570.
63. Allen G.J., Sanders D. Osmotic stress enhances the competence of Beta vulgaris vacuoles to respond to inositol 1 4,5-trisphosphate. Plant J. 1994, 6:687-695.
64. 2+ release across nonvacuolar membranes in cauliflower. Plant Physiol. 1997, 114:1511-1521.
65. 2+ release in beet microsomes is inhibited by heparin. FEBS Lett. 1990, 260:70-72.
66. Brosnan J.M., Sanders D. Identification and characterization of high-affinity binding sites for inositol trisphosphate in red beet. Plant Cell 1993, 5:931-940.
67. 2+-dependent high-affinity binding site for inositol-1 4,5-trisphosphate from Chenopodium rubrum. Plant Physiol. 1996, 110:867-874.
68. Martinec J., Feltl T., Scanlon C.H., Lumsden P.J., Machackova I. Subcellular localization of a high affinity binding site for d-myo-inositol 1 4,5-trisphosphate from Chenopodium rubrum. Plant Physiol. 2000, 124:475-483.
69. Gilroy S., Read N.D., Trewavas A.J. Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 1990, 346:769-771.
70. Blatt M.R., Thiel G., Trentham D.R. Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1 4,5-trisphosphate. Nature 1990, 346:766-769.
71. Staxén I., Pical C., Montgomery L.T., Gray J.E., Hetherington A.M., McAinsh M.R. Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1779-1784.
72. DeWald D.B., Torabinejad J., Jones C.A., et al. Rapid accumulation of phosphatidylinositol 4 5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol. 2001, 126:759-769.
73. Parre E., Ghars M.A., Leprince A.-S., et al. Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiol. 2007, 144:503-512.
74. 2+-regulated stomatal responses. New Phytol. 2008, 179:675-686.
75. Munnik T., Testerink C. Plant phospholipid signaling: "in a nutshell" J. Lipid Res. 2009, 50:S260-S265.
76. Lemtiri-Chlieh F., MacRobbie E.A.C., Webb A.A.R., et al. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10091-10095.
77. +-inward rectifying conductance in guard cells. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8687-8692.
78. Johannes E., Sanders D. Lumenal calcium modulates unitary conductance and gating of a plant vacuolar calcium release channel. J. Membr. Biol. 1995, 146:211-224.
79. 2+ release from the vacuole of higher plants. Plant J. 1992, 2:97-102.
80. Allen G.J., Sanders D. Two voltage-gated, calcium release channels coreside in the vacuolar membrane of broad bean guard cells. Plant Cell 1994, 6:685-694.
81. Hedrich R., Flügge U.I., Fernandez J.M. Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Lett. 1986, 204:228-232.
82. Hedrich R., Barbier-Brygoo H., Felle H., et al. General mechanisms for solute transport across the tonoplast of plant vacuoles: a patch-clamp survey of ion channels and proton pumps. Bot. Acta 1988, 101:7-13.
83. Schulz-Lessdorf B., Hedrich R. Protons and calcium modulate SV-type channels in the vacuolar-lysosomal compartment-channel Interaction with calmodulin inhibitors. Planta 1995, 197:655-671.
84. Allen G.J., Sanders D. Control of ionic currents in guard cell vacuoles by cytosolic and luminal calcium. Plant J. 1996, 10:1055-1069.
85. Gambale F., Bregante M., Stragapede F., Cantu A.M. Ionic channels of the sugar beet tonoplast are regulated by a multi-ion single-file permeation mechanism. J. Membr. Biol. 1996, 154:69-79.
86. + channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 1994, 6:669-683.
87. 2+-permeable slow vacuolar ion channel of stomatal guard cells. Plant Cell 1995, 7:1473-1483.
88. Pottosin I.I, Dobrovinskaya O.R., Muniz J. Conduction of monovalent and divalent cations in the slow vacuolar channel. J. Membr. Biol. 2001, 181:55-65.
89. Gradogna A., Scholz-Starke J., Gutla P.V.K., Carpaneto A. Fluorescence combined with excised patch: measuring calcium currents in plant cation channels. Plant J. 2009, 58:175-182.
90. Hedrich R., Neher E. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 1987, 329:833-836.
91. Rienmüller F., Beyhl D., Lautner S., et al. Guard cell-specific calcium sensitivity of high density and activity SV/TPC1 channels. Plant Cell Physiol. 2010, 51:1548-1554.
92. Bewell M.A., Maathuis F.J.M., Allen G.J., Sanders D. Calcium-induced calcium release mediated by a voltage-activated cation channel in vacuolar vesicles from red beet. FEBS Lett. 1999, 458:41-44.
93. 2+ release. Plant J. 1997, 12:1387-1398.
94. 2+ action on the vacuolar slowly activating channels. Planta 2004, 219:1057-1070.
95. + currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. Plant J. 2005, 41:606-614.
96. 2+ release during intracellular signaling. FEBS Lett. 2009, 583:921-926.
97. Pei Z.-M., Ward J.M., Schroeder J.I. Magnesium sensitizes slow vacuolar channels to physiological cytosolic calcium and inhibits fast vacuolar channels in fava bean guard cell vacuoles. Plant Physiol. 1999, 121:977-986.
98. 2+ on slowly activating channels in isolated vacuoles of Beta vulgaris. Planta 2001, 213:457-468.
99. Miedema H., Pantoja O. Anion modulation of the slowly activating vacuolar channel. J. Membr. Biol. 2001, 183:137-145.
100. Carpaneto A., Cantu A.M., Gambale F. Redox agents regulate ion channel activity in vacuoles from higher plant cells. FEBS Lett. 1999, 442:129-132.
101. Scholz-Starke J., De Angeli A., Ferraretto C., Paluzzi S., Gambale F., Carpaneto A. Redox-dependent modulation of the carrot SV channel by cytosolic pH. FEBS Lett. 2004, 576:449-454.
102. Dobrovinskaya O.R., Muniz J., Pottosin I.I. Inhibition of vacuolar ion channels by polyamines. J. Membr. Biol. 1999, 167:127-140.
103. Van den Wijngaard P.W.J., Bunney T.D., Roobeek I., Schönknecht G., de Boer A.H. Slow vacuolar channels from barley mesophyll cells are regulated by 14-3-3 proteins. FEBS Lett. 2001, 488:100-104.
104. + channel is activated by 14-3-3 proteins. Plant J. 2007, 52:449-459.
105. Bethke P.C, Jones R.L. Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel. Plant J. 1997, 11:1227-1235.
106. Ishibashi K., Suzuki M., Imai M. Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem. Biophys. Res. Commun. 2000, 270:370-376.
107. 2+ flux in Arabidopsis leaf cells. Plant Cell Physiol. 2001, 42:900-905.
108. 2+ channels. Biochem. Biophys. Res. Commun. 2004, 324:40-45.
109. 2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J. 2005, 42:798-809.
110. 2+ channel, OsTPC1, in rice. Plant Biotechnol. 2005, 22:235-239.
111. Szponarski W., Sommerer N., Boyer J.-C., Rossignol M., Gibrat R. Large-scale characterization of integral proteins from Arabidopsis vacuolar membrane by two-dimensional liquid chromatography. Proteomics 2004, 4:397-406.
112. Carter C., Pan S., Zouhar J., Avila E.L., Girke T., Raikhel N.V. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 2004, 16:3285-3303.
113. Endler A., Meyer S., Schelbert S., et al. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 2006, 141:196-207.
114. 2+ signals induced by abiotic and biotic stresses. Plant J. 2008, 53:287-299.
115. Marmagne A., Ferro M., Meinnel T., et al. A high content in lipid-modified peripheral proteins and integral receptor kinases features in the Arabidopsis plasma membrane proteome. Mol. Cell. Proteomics 2007, 6:1980-1996.
116. 2+ channel, OsTPC1, expressed in yeast cells lacking its homologous gene CCH1. Plant Cell Physiol. 2004, 45:496-500.
117. 2+ transients and defense responses in tobacco BY-2 cells. Biochem. Biophys. Res. Commun. 2004, 317:823-830.
118. 2+ channel gene TaTPC1 from wheat. J. Exp. Bot. 2005, 56:3051-3060.
119. Beyhl D., Hörtensteiner S., Martinoia E., et al. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J. 2009, 58:715-723.
120. Bonaventure G., Gfeller A., Proebsting W.M., et al. A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J. 2007, 49:889-898.
121. 2+ permeable channels NtTPC1A/B in tobacco BY-2 cells. Biochem. Biophys. Res. Commun. 2005, 336:1259-1267.
122. 2+ influx and regulation of growth and development in rice. Plant Cell Physiol. 2004, 45:693-702.
123. Bonaventure G., Gfeller A., Rodríguez V.M., Armand F., Farmer E.E. The fou2 gain-of-function allele and the wild-type allele of Two Pore Channel 1 contribute to different extents or by different mechanisms to defense gene expression in Arabidopsis. Plant Cell Physiol. 2007, 48:1775-1789.
124. Amtmann A., Blatt M.R. Regulation of macronutrient transport. New Phytol. 2009, 181:35-52.
125. Gilroy S., Jones R.L. Gibberelic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:3591-3595.
126. +) release. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:12361-12368.
127. Tikhonova L.I., Pottosin I.I., Dietz K.J., Schönknecht G. Fast-activating cation channel in barley mesophyll vacuoles. Inhibition by calcium. Plant J. 1997, 11:1059-1070.
128. + homeostasis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10726-10731.
129. + channel using yeast tonoplasts. J. Biol. Chem. 2008, 283:1911-1920.
130. 2+ dependency. EMBO J. 1997, 16:2565-2575.
131. 2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:19555-19560.
132. 2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett. 2007, 581:3943-3949.
133. Geisler M., Frangne N., Gomès E., Martinoia E., Palmgren M.G. The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol. 2000, 124:1814-1827.
134. Boursiac Y., Lee S.M., Romanowsky S., et al. Disruption of the vacuolar calcium-ATPases in Arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway. Plant Physiol. 2010, 154:1158-1171.
135. Pei Z.-M., Ward J.M., Harper J.F., Schroeder J.I. A novel chloride channel in Vicia faba guard cell vacuoles activated by the serine/threonine kinase, CDPK. EMBO J. 1996, 15:6564-6574.
136. Batistic O., Waadt R., Steinhorst L., Held K., Kudla J. CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J. 2010, 61:211-222.
137. 2+ signaling complexes in Arabidopsis. Plant Cell 2008, 20:1346-1362.
138. Kim B.-G., Waadt R., Cheong Y.H., et al. The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 2007, 52:473-484.
139. Quan R.D., Lin H.X., Mendoza I., et al. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 2007, 19:1415-1431.
140. Liu J., Zhu J.-K. A calcium sensor homolog required for plant salt tolerance. Science 1998, 280:1943-1945.
141. + exchange in Arabidopsis thaliana by the Salt-Overly-Sensitive (SOS) pathway. J. Biol. Chem. 2004, 279:207-215.
142. 2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J. Biol. Chem. 2004, 279:2922-2926.
143. +-ATPase and upregulating its transport activity. Mol. Cell. Biol. 2007, 27:7781-7790.
144. Hwang Y.-S., Bethke P.C., Cheong Y.H., Chang H.-S., Zhu T., Jones R.L. A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function. Plant Physiol. 2005, 138:1347-1358.
145. Haiech J., Klee C.B., Demaille J.G. Effects of cations on affinity of calmodulin for calcium: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes. Biochemistry 1981, 20:3890-3894.
146. Schwacke R., Schneider A., van der Graaff E., et al. ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 2003, 131:16-26.
147. Marchler-Bauer A., Anderson J.B., Chitsaz F., et al. CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res. 2009, 37:D205-D210.
148. Blom N., Gammeltoft S., Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 1999, 294:1351-1362.