The language of calcium signaling

Annual Review of Plant Biology

Volumn 61, Issue , 2010, Pages 593-620

  Dodd, Antony N ^a   Kudla, Jörg ^b   Sanders, Dale ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Calcium; Membrane transport; Signal transduction; Systems biology

Indexed keywords

CALCIUM; VEGETABLE PROTEIN;

CALCIUM SIGNALING; METABOLISM; PHOTOTRANSDUCTION; PLANT; REVIEW;

CALCIUM; CALCIUM SIGNALING; LIGHT SIGNAL TRANSDUCTION; PLANT PROTEINS; PLANTS;

EID: 77952530584     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-070109-104628     Document Type: Article

References (172)

1. 2+-regulated kinases. EMBO J. 20:1051-1063
2. AlbrechtV, WeinlS, BlazevicD, D'AngeloC, Batistic O, et al. 2003. The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J. 36:457-470
3. AliR, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, et al. 2007. Death Don't Have NoMercy and Neither Does Calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and Innate Immunity. Plant Cell 19:1081-1095
4. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, et al. 2001. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053-1057
5. 2+ from individual plant vacuoles by both InsP(3) and cyclic ADP-ribose. Science 268:735-737
6. 2+-permeable slow vacuolar ion-channel of stomatal guard-cells. Plant Cell 7:1473-1483
7. Arazi T, Kaplan B, Fromm H. 2000. A high-affinity calmodulin-binding site in a tobacco plasma-membrane channel protein coincides with a characteristic element of cyclic nucleotide-binding domains. Plant Mol. Biol. 42:591-601
8. 2+-ATPases by terminal domains. J. Bioenerg. Biomembr. 37:369-374
9. Balague C, Lin BQ, Alcon C, Flottes G, Malmstrom S, et al. 2003. HLM1, an essential signaling component in the hypersensitive response, is a member ofthe cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365-379
10. Batistic O, Kudla J. 2004. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219: 915-924
11. Batistic O, Kudla J. 2009. Plant calcineurin B-like proteins and their interacting protein kinases. Biochim. Biophys. Acta 1793:985-992
12. 2+ signaling complexes in Arabidopsis. Plant Cell 20:1346-1362
13. 2+. Proc. Natl. Acad. Sci. USA 96:13554-13559
14. Bonaventure G, Gfeller A, Proebsting WM, Hortensteiner S, Chetelat A, et al. 2007. A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J. 49:889-898
15. 2+-ATPase activity by acidic phospholipids. Physiol. Plantarum 112:315-320
16. Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI. 2000. AtACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol. 123:1495-1505
17. 2+ pumps in plants. J. Bioenerg. Biomembr. 39:409-414
18. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, et al. 2005. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013-1016
19. Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV. 2004. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16:3285-3303
20. + transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940-2951
21. 2+-ATPase in Arabidopsis thaliana seedlings. Plant Biol. 8:572-578
22. 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 20:3467-3479
23. 2+ antiporter, CAX 1. FEBS Lett. 559:99-106
24. 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 15:347-364
25. Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, et al. 2005. Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol. 138:2048-2060
26. 2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J. Biol. Chem. 279:2922-2926
27. 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 15:1833-1845
28. Cheong YH, Pandey GK, Grant JJ, Batistic? O, Li L, et al. 2007. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 52:223-239
29. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK, Bent AF. 2000. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl. Acad. Sci. USA97:9323-9328
30. Csete M, Doyle J. 2004. Bow ties, metabolism and disease. Trends Biotechnol. 22:446-450
31. 2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J. 48:857-872
32. Davenport R. 2002. Glutamate receptors in plants. Ann. Bot. 90:549-557
33. de Graaf BHJ, Rudd JJ, Wheeler MJ, Perry RM, Bell EM, et al. 2006. Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen. Nature 444:490-493
34. DeBlasio SL, Luesse DL, Hangarter RP. 2005. A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol. 139:101-114
35. Demidchik V, Maathuis FJM. 2007. Physiological roles of nonselective cation channels in plants: from salt stress to signaling and development. New Phytol. 175:387-404
36. 2+ channels. Plant J. 58:903-913
37. Dennison KL, Spalding EP. 2000. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol. 124:1511-1514
38. Ding YL, Kalo P, Yendrek C, Sun JH, Liang Y, et al. 2008. Abscisic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20:2681-2695
39. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, et al. 2007. The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789-1792
40. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF. 2009. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972-984
41. 2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154-1158
42. 2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741-745
43. Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM. 2003. A role for glycine in the gating of plant NMDA-like receptors. Plant J. 35:800-810
44. Finkler A, Ashery-Padan R, Fromm H. 2007. CAMTAs: Calmodulin-binding transcription activators from plants to human. FEBS Lett. 581:3893-3898
45. 2+-responsiveciselements inplants. Plant Signal. Behav. 2:17-19
46. Folta KM, Lieg EJ, Durham T, Spalding EP. 2003. Primary inhibition of hypocotyl growth and pho-totropism depend differently on phototropin-mediated increases in cytoplasmic calcium induced by blue light. Plant Physiol. 133:1464-1470
47. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-446
48. 2+ in the self-incompatibility response in pollen tubes of Papaver rhoeas. Plant J. 12:1375-1386
49. Franklin-Tong VE, Ride JP, Read ND, Trewavas AJ, Franklin FCH. 1993. The self incompatibility response of Papaver rhoeas is mediated by cytosolic free calcium. Plant J. 4:163-177
50. Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, et al. 2007. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc. Natl. Acad. Sci. USA 104:14531-14536
51. Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H. 2008. Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett. 582:943-948
52. Geisler M, Frangne N, Gomes E, Martinoia E, Palmgren MG. 2000. The ACA4 gene of Arabidopsis encodesavacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol. 124:1814-1827
53. 2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol. 146:716-728
54. Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJM. 2006. Arabidopsis thaliana Cyclic Nucleotide Gated Channel 3 forms a nonselective ion transporter involved in germination and cation transport. J. Exp. Bot. 57:791-800
55. 2+-binding protein involved in cryptochrome and phytochrome coaction. Science 291:487-490
56. Guo Y, Halfter U, Ishitani M, Zhu JK. 2001. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383-1399
57. Halfter U, Ishitani M, Zhu JK. 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS 3. Proc. Natl. Acad. Sci. USA 97:3735-3740
58. 2+ differently in Arabidopsis leaves. Proc. Natl. Acad. Sci. USA 100:8583-8588
59. 2+ in Arabidopsis guard cells and mesophyll cells in response to blue light. Plant Cell Physiol. 50:360-373
60. 2+ signals through plant protein kinases. Annu. Rev. Plant Biol. 55:263-288
61. Harper JF, Harmon A. 2005. Plants, symbiosis and parasites: A calcium signaling connection. Nat. Rev. Mol. Cell Biol. 6:555-566
62. Hedrich R, Barbierbrygoo H, Felle H, Flugge UI, Luttge U, et al. 1988. General mechanisms for solute transport across the tonoplast of plant vacuoles\a patch-clamp survey of ion channels and proton pumps. Botanica Acta 101:7-13
63. Hepler PK, Vidali L, Cheung AY. 2001. Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17:159-187
64. Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change. Nature 424:901-908
65. Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd GED. 2009. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545-557
66. Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, et al. 2003. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132:666-680
67. Huang Z, Hahn J. 2009. Fuzzy modeling of signal transduction networks. Chem. Eng. Sci. 64:2044-2056
68. 2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc. Natl. Acad. Sci. USA 97:6224-6229
69. Ikura M, Osawa M, Ames JB. 2002. The role of calcium-binding proteins in the control of transcription: structure to function. BioEssays 24:625-636
70. 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 20:3273-3288
71. 2+ sensor priming hypothesis. Curr. Opin. Plant Biol. 9:654-663
72. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, et al. 1995. Circadian oscillations ofcytosolic and chloroplastic free calcium in plants. Science 269:1863-1865
73. Jones MA, Raymond MJ, Yang ZB, Smirnoff N. 2007. NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J. Exp. Bot. 58:1261-1270
74. Kang JM, Turano FJ. 2003. The putative glutamate receptor 1. 1 (AtGLR 1. 1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100:6872-6877
75. 2+-responsive cis elements in Arabidopsis. Plant Cell 18:2733-2748
76. 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. 23:267-278
77. Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, et al. 2007. The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 52:473-484
78. 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 15:411-423
79. Knight H, Trewavas AJ, Knight MR. 1996. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489-503
80. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, et al. 2007. Calcium-dependent protein kinases regulate the productionofreactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065-80
81. 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. 134:43-58
82. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, et al. 2008. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc. Natl. Acad. Sci. USA 105:9823-9828
83. 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 96:4718-4723
84. Kushwaha R, Singh A, Chattopadhyay S. 2008. Calmodulin7 plays an important role as transcriptional regulator in Arabidopsis seedling development. Plant Cell 20:1747-1759
85. 2+-permeable conductance. Plant Cell 21:479-493
86. Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, et al. 2005. Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38:527-538
87. Lee SC, Lan WZ, Kim BG, Li LG, Cheong YH, et al. 2007. A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc. Natl. Acad. Sci. USA 104:15959-15964
88. 2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett. 581:3943-3949
89. Leng Q, Mercier RW, Hua BG, Fromm H, Berkowitz GA. 2002. Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol. 128:400-410
90. Leng Q, Mercier RW, Yao WZ, Berkowitz GA. 1999. Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol. 121:753-761
91. 2+ signals. Proc. Natl. Acad. Sci. USA 102:4203-4208
92. Li S, Assmann SM, Albert R. 2006. Predicting essential components of signal transduction networks: A dynamic model of guard cell abscisic acid signaling. PLoS Biol. 4:1732-1748
93. 2+ pump affects root growth through the secretory process. Plant Physiol. 147:1675-1689
94. Liu JP, Ishitani M, Halfter U, Kim CS, Zhu JK. 2000. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. USA 97:3730-3734 (Pubitemid 30183371)
95. Liu JP, Zhu JK. 1997. An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc. Natl. Acad. Sci. USA 94:14960-14964
96. Love J, Dodd AN, Webb AAR. 2004. Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16:956-966
97. Luan S. 2009. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci. 14:37-42
98. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. 2002. Calmodulins and calcineurin B-like proteins: Calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389-400
99. Luan S, Lan W, Chul Lee S. 2009. Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network. Curr. Opin. Plant Biol. 12:339-346
100. Ludwig AA, Romeis T, Jones JDG. 2004. CDPK-mediated signaling pathways: specificity and cross-talk. J. Exp. Bot. 55:181-188
101. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, et al. 2005. Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc. Natl. Acad. Sci. USA 102:10736-10741
102. Ma S, Gong Q, Bohnert HJ. 2007. An Arabidopsis gene network based on the graphical Gaussian model. Genome Res. 17:1614-1625
103. Ma W, Berkowitz GA. 2007. The grateful dead: calcium and cell death in plant innate immunity. Cell. Microbiol. 9:2571-2585
104. +) release. Proc. Natl. Acad. Sci. USA 97:12361-12368
105. Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, et al. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126:1646-1667
106. Masuda W, Takenaka S, Inageda K, Nishina H, Takahashi K, et al. 1997. Oscillation of ADP-ribosyl cyclase activity during the cell cycle and function of cyclic ADP-ribose in a unicellular organism, Euglena gracilis. FEBS Lett. 405:104-106
107. Mazel T, Raymond R, Raymond-Stintz M, Jett S, Wilson BS. 2009. Stochastic modeling of calcium in 3D geometry. Biophys. J. 96:1691-1706
108. McAinsh MR, Pittman JK. 2009. Shaping the calcium signature. New Phytol. 181:275-294
109. McCormack E, Tsai YC, Braam J. 2005. Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci. 10:383-389
110. + antiporter CAX 1. J. Exp. Bot. 58:3419-3427
111. Mills RF, Doherty ML, Lopez-Marques RL, Weimar T, Dupree P, et al. 2008. ECA3, a Golgi-localized P-2 A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 146:116-128
112. 2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 147:1690-1698
113. 2+-permeable channels and stomatal closure. PLoS Biol. 4:1749-1762
114. Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, et al. 2008. Annexins: multifunctional components of growth and adaptation. Presented at Annu. Meet. Soc. Exper. Biol., Glasgow, UK
115. MoscatielloR, MarianiP, SandersD, Maathuis FJM. 2006. Transcriptional analysisofcalcium-dependent and calcium-independent signaling pathways induced by oligogalacturonides. J. Exp. Bot. 57:2847-2865
116. 2+ release across nonvacuolar membranes in cauliflower. Plant Physiol. 114:1511-1521
117. 2+ channels in guard cells requires cytosolic NAD(P)H 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
118. 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 97:8693-8698
119. 2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol. 125:2129-2138
120. Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, et al. 2007. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol. 144:673-681
121. Ng CKY, McAinsh MR, Gray JE, Hunt L, Leckie CP, et al. 2001. Calcium-based signaling systems in guard cells. New Phytol. 151:109-120.
122. OhtaM, GuoY, HalfterU, Zhu JK. 2003. Anovel domaininthe protein kinase SOS2 mediates interaction with the protein phosphatase 2C AB 12. Proc. Natl. Acad. Sci. USA 100:11771-11776
123. Oldroyd GED, Downie JA. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59:519-546
124. Oldroyd GED, Harrison MJ, Paszkowski U. 2009. Reprogramming plant cells for endosymbiosis. Science 324:753-754
125. Pandey GK, Cheong YH, Kim KN, Grant JJ, Li LG, et al. 2004. The calcium sensor calcineurin B-like CBL9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912-1924
126. Pandey GK, Grant JJ, Cheong YH, Kim BG, Li LG, Luan S. 2008. Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol. Plant 1:238-248
127. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, et al. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731-734
128. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404-408
129. Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK, et al. 2007. The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol. 145:192-203
130. Polouliakh N, Nock R, Nielsen F, Kitano H. 2009. G-protein coupled receptor signaling architecture of mammalian immune cells. PLoS One 4:e4189
131. 2+ release during intra-cellular signaling. FEBS Lett. 583:921-926
132. Qi Z, Stephens NR, Spalding EP. 2006. Calcium entry mediated by GLR 3. 3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol. 142:963-971
133. Quan RD, Lin HX, Mendoza I, Zhang YG, Cao WH, et al. 2007. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415-1431
134. 2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc. Natl. Acad. Sci. USA 105:19555-19560
135. 2+ signals induced by abiotic and biotic stresses. Plant J. 53:287-299
136. Reddy VS, Reddy ASN. 2004. Proteomics of calcium-signaling components in plants. Phytochemistry 65:1745-1776
137. Romeis T, Ludwig AA, Martin R, Jones JDG. 2001. Calcium-dependent protein kinases play an essential role in a plant defense response. EMBO J. 20:5556-5567
138. Sánchez JP, Duque P, Chua NH. 2004. ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. Plant J. 38:381-395
139. Sanders D, Brownlee C, Harper JF. 1999. Communicating with calcium. Plant Cell 11:691-706
140. Sanders D, Johannes E, Hedrich R. 1990. Opening plant calcium channels. Nature 344:593-594
141. Sanders D, Pelloux J, Brownlee C, Harper JF. 2002. Calcium at the crossroads of signaling. Plant Cell 14:S401-17
142. 2+ pumps expressed in stomatal guard cells show opposite expression patterns during cold stress. Physiol. Plantarum 124:278-283
143. 2+ pump is required for normal pollen tube growth and fertilization. Proc. Natl. Acad. Sci. USA 101:9502-9507
144. Schuurink RC, Shartzer SF, Fath A, Jones RL. 1998. Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc. Natl. Acad. Sci. USA 95:1944-1949
145. Shi JR, Kim KN, Ritz O, Albrecht V, Gupta R, et al. 1999. Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393-2405
146. + exchangers in plants. Plant Biol. 8:419-429
147. Shimazaki KI, Doi M, Assmann SM, Kinoshita T. 2007. Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58:219-247
148. + channels in Arabidopsis guard cells. Plant J. 59:207-220
149. Spalding EP. 2000. Ion channels and the transduction of light signals. Plant Cell Environ. 23:665-674
150. Stephens NR, Qi Z, Spalding EP. 2008. Glutamate receptor subtypes evidenced by differences in de-sensitization and dependence on the GLR 3. 3 and GLR 3. 4 genes. Plant Physiol. 146:529-538.
151. Sun J, Miwa H, Downie JA, Oldroyd GED. 2007. Mastoparan activates calcium spiking analogous to nod factor-induced responses in Medicago truncatula root hair cells. Plant Physiol. 144:695-702
152. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. 2008. Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241-1244
153. Thomas SG, Franklin-Tong VE. 2004. Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305-309
154. Thul R, Bellamy TC, Roderick HL, Bootman MD, Coombes S. 2008. Calcium oscillations. In Advances in Experimental Medicine and Biology: Cellular Oscillatory Mechanisms, ed. M Maroto, NAM Monk, pp. 1-22. New York: Springer
155. 2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ. 31:1063-1073
156. Tucker EB, Lee M, Alli S, Sookhdeo V, Wada M, et al. 2005. UV-A induces two calcium waves in Physcomitrella patens. Plant Cell Physiol. 46:1226-1236
157. 2+ dependent manner. Plant Mol. Biol. 65:747-761
158. Vadassery J, Ranf S, Drewiecki C, Mithöfer A, Mazars C, et al. 2009. A cell wall extract from the endophytic fungusPiriformospora indicapromotes growth ofArabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J. 59:193-206
159. Veresov VG, Kabak AG, Volotovsky ID. 2003. Modeling the calcium signaling in stomatal guard cells under the action of abscisic acid. Russian J. Plant Physiol. 50:573-579
160. Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, Kudla J. 2008. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56:505-516
161. Ward JM, Maser P, Schroeder JI. 2009. Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71:59-82
162. + 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
163. 2+-decoding network: function and perspectives. New Phy-tologist. 184:517-528
164. Wheeler MJ, de Graaf BHJ, Hadjiosif N, Perry RM, Poulter NS, et al. 2009. Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459:992-995
165. Whiteman SA, Nuhse TS, Ashford DA, Sanders D, Maathuis FJM. 2008. A proteomic and phospho-proteomic analysis of Oryza sativa plasma membrane and vacuolar membrane. Plant J. 56:146-156
166. 2+ stress. Plant Physiol. 130:128-137
167. + transporter AKT1 in Arabidopsis. Cell 125:1347-1360
168. 2+ oscillations and rhythmic CHLOROPHYLL A/B BINDING PROTEIN2 promoter activity in Arabidopsis. Plant Cell 19:3474-3490
169. Yang T, Poovaiah BW. 2002. A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J. Biol. Chem. 277:45049-45058
170. Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, et al. 2006. The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18:747-763
171. +-ATPase activity. Planta 227:659-669
172. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, et al. 2007. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019-3036