Calcium channels in photosynthetic eukaryotes: Implications for evolution of calcium-based signalling

New Phytologist

Volumn 187, Issue 1, 2010, Pages 23-43

  Verret, Frédéric ^a   Wheeler, Glen ^c   Taylor, Alison R ^b   Farnham, Garry ^c   Brownlee, Colin ^a  

^a THE LABORATORY   (United Kingdom)

^b UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^c PLYMOUTH MARINE LABORATORY   (United Kingdom)

Author keywords

Algae; Ca2+ signalling; Channels; Embryophytes; Evolution; Photosynthetic eukaryotes; Plants

Indexed keywords

CALCIUM CHANNEL;

ALGA; BIOCHEMISTRY; CALCIUM; EUKARYOTE; EVOLUTIONARY BIOLOGY; GENE TRANSFER; GENOMICS; LIFE HISTORY; PHOTOSYNTHESIS; PHYSIOLOGY; SIGNALING;

CALCIUM SIGNALING; EUKARYOTE; HORIZONTAL GENE TRANSFER; METABOLISM; MOLECULAR EVOLUTION; PHOTOSYNTHESIS; REVIEW;

CALCIUM CHANNELS; CALCIUM SIGNALING; EUKARYOTA; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; PHOTOSYNTHESIS;

ALGAE; ANIMALIA; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; EUKARYOTA; VIRIDIPLANTAE;

EID: 77954606430     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03271.x     Document Type: Review

References (203)

1. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA. Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 2007, 19:1081-1095.
2. Allaway WG, Ashford AE, Heath IB, Hardham AR. Vacuolar reticulum in oomycete hyphal tips: an additional component of the Ca2+ regulatory system? Fungal Genetics and Biology 1997, 22:209-220.
3. Anderson PAV, Greenberg RM. Phylogeny of ion channels: clues to structure and function. Comparative Biochemistry and Physiology B: Biochemistry & Molecular Biology 2001, 129:17-28.
4. Anderson PAV, Roberts-Misterly J, Greenberg RM. The evolution of voltage-gated sodium channels: were algal toxins involved? Harmful Algae 2005, 4:95-107.
5. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 2004, 306:79-86.
6. Baldauf SL. An overview of the phylogeny and diversity of eukaryotes. Journal of Systematics and Evolution 2008, 46:263-273.
7. Becker B, Hoef-Emden K, Melkonian M. Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evolutionary Biology 2008, 8:203.
8. Beilby MJ. Electrophysiology of giant algal cells. Methods in Enzymology 1989, 174:403-443.
9. Beilby MJ. Action potential in charophytes. International Review of Cytology -A Survey of Cell Biology 2007, 257:43-82.
10. Berestovsky GN, Kataev AA. Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara. European Biophysics Journal with Biophysics Letters 2005, 34:973-986.
11. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nature Reviews Molecular Cell Biology 2003, 4:517-529.
12. Berthold P, Tsunoda SP, Ernst OP, Mages W, Gradmann D, Hegemann P. Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell 2008, 20:1665-1677.
13. Beyhl D, Hörtensteiner S, Martinoia E, Farmer EE, Fromm J, Marten I, Hedrich R. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant Journal 2009, 58:715-723.
14. Bhattacharya D, Yoon HS, Hackett JD. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 2004, 26:50-60.
15. Biskup B, Gradmann D, Thiel G. Calcium release from InsP3-sensitive internal stores initiates action potential in Chara. FEBS Letters 1999, 453:72-76.
16. Bocquet N, de Carvalho LP, Cartaud J, Neyton J, Le Poupon C, Taly A, Grutter T, Changeux JP, Corringer PJ. A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature 2007, 445:116-119.
17. Bothwell JHF, Brownlee C, Hetherington AM, Ng CKY, Wheeler GL, McAinsh MR. Biolistic delivery of Ca2+ dyes into plant and algal cells. Plant Journal 2006, 46:327-335.
18. Bothwell JHF, Kisielewska J, Genner MJ, McAinsh MR, Brownlee C. Ca2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 2008, 135:2173-2181.
19. Bothwell JHF, Ng CKY. The evolution of Ca2+ signalling in photosynthetic eukaryotes. New Phytologist 2005, 166:21-38.
20. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456:239-244.
21. Brailoiu E, Churamani D, Cai X, Schrlau MG, Brailoui GC, Gao X, Hooper R, Boulware MJ, Dun NJ, Marchant JS. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signalling. Journal of Cell Biology 2009, 182:201-209.
22. Brehm P, Eckert R, Tillotson D. Calcium-mediated inactivation of calcium current in Paramecium. Journal of Physiology 1980, 306:193-203.
23. Brownlee C. Diatom signalling: deadly messages. Current Biology 2008, 18:R518-R519.
24. Brownlee C, Taylor AR. Calcification in coccolithophores: a cellular perspective. Coccolithophores: from molecular processes to global impact 2004, 31-49. Thierstein HR, Young JR. eds, Berlin, Germany, Springer
25. Brownlee C, Wood JW. A gradient of cytoplasmic free calcium in growing rhizoid cells of Fucus serratus. Nature 1986, 320:624-626.
26. Cai XJ. Unicellular Ca2+ signaling 'toolkit' at the origin of metazoa. Molecular Biology and Evolution 2008, 25:1357-1361.
27. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang K-T. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 2009, 459:596-600.
28. Case RM, Eisner D, Gurney A, Jones O, Muallem S, Verkhratsky A. Evolution of calcium homeostasis: from birth of the first cell to an omnipresent signalling system. Cell Calcium 2007, 42:345-350.
29. Catterall WA. Structure and regulation of voltage-gated Ca2+ channels. Annual Review of Cell and Developmental Biology 2000, 16:521-555.
30. Cavalier-Smith T. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 2003, 358:109-133.
31. Chen AK, Latz MI, Sobolewski P, Frangos JA. Evidence for the role of G-proteins in flow stimulation of dinoflagellate bioluminescence. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 2007, 292:R2020-R2027.
32. Chen GQ, Cui CH, Mayer ML, Gouaux E. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 1999, 402:817-821.
33. Chin WC, Orellana MV, Quesada I, Verdugo P. Secretion in unicellular marine phytoplankton: demonstration of regulated exocytosis in Phaeocystis globosa. Plant and Cell Physiology 2004, 45:535-542.
34. Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
35. Clemens S, Antosiewicz DM, Ward JM, Schachtman DP, Schroeder JI. The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proceedings of the National Academy of Sciences, USA 1998, 95:12043-12048.
36. Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury JM, Badger JH. The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. Nature 2010
37. Coelho SM, Taylor AR, Ryan KP, Sousa-Pinto I, Brown MT, Brownlee C. Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cells. Plant Cell 2002, 14:2369-2381.
38. von Dassow P, Latz MI. The role of Ca2+ in stimulated bioluminescence of the dinoflagellate Lingulodinium polyedrum. Journal of Experimental Biology 2002, 205:2971-2986.
39. Demidchik V, Maathuis FJ. Physiological roles of non-selective cation channels in plants: from salt stress to signalling and development. New Phytologist 2007, 175:387-404.
40. Demidchik V, Shang ZL, Shin R, Thompson E, Rubio L, Laohavisit A, Mortimer JC, Chivasa S, Slabas AR, Glover BJ. Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. Plant Journal 2009, 58:903-913.
41. Dennison KL, Spalding EP. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiology 2000, 124:1511-1514.
42. Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynié S, Cooke R. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proceedings of the National Academy of Sciences, USA 2006, 103(31):11647-11652.
43. DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiology 2001, 126:759-769.
44. Dolphin AC. Calcium channel diversity: multiple roles of calcium channel subunits. Current Opinion in Neurobiology 2009, 19:237-244.
45. Dubos C, Willment J, Huggins D, Grant GH, Campbell MM. Kanamycin reveals the role played by glutamate receptors in shaping plant resource allocation. Plant Journal 2005, 43:348-355.
46. Durell SR, Guy HR. A putative prokaryote voltage-gated Ca2+ channel with only one 6TM motif per subunit. Biochemical and Biophysical Research Communications 2001, 281:741-746.
47. Eckert R, Brehm P. Ionic mechanisms of excitation in Paramecium. Annual Review of Biophysics and Bioengineering 1979, 8:353-383.
48. Eckert R, Sibaoka T. The flash-triggering action potential of the luminescent dinoflagellate Noctiluca. Journal of General Physiology 1968, 52:258-282.
49. Egan TM, Khakh BS. Contribution of calcium ions to P2X channel responses. Journal of Neuroscience 2004, 24:3413-3420.
50. Ermilova E, Zalutskaya Z, Munnik T, van den Ende H, Gromov B. Calcium in the control of chemotaxis in Chlamydomonas. Biologia 1998, 53:577-581.
51. Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, Perez-Reyes E, Schwartz A, Snutch TP, Tanabe T, Birnbaumer L. Nomenclature of voltage-gated calcium channels. Neuron 2000, 25:533-535.
52. Falciatore A, d'Alcala MR, Croot P, Bowler C. Perception of environmental signal by a marine diatom. Science 2000, 288:2363-2366.
53. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJ. The evolution of modern eukaryotic phytoplankton. Science 2004, 305:354-360.
54. Fountain SJ, Cao LS, Young MT, North RA. Permeation properties of a P2X receptor in the green algae Ostreococcus tauri. Journal of Biological Chemistry 2008, 283:15122-15126.
55. Fountain SJ, Parkinson K, Young MT, Cao LS, Thompson CRL, North RA. An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 2007, 448:200-203.
56. Franklin DJ, Brussaard CPD, Berges JA. What is the role and nature of programmed cell death in phytoplankton ecology? European Journal of Phycology 2006, 41:1-14.
57. FranklinTong VE, Drobak BK, Allan AC, Watkins PAC, Trewavas AJ. Growth of pollen tubes of Papaver rhoeas is regulated by a slow-moving calcium wave propagated by inositol 1,4,5-trisphosphate. Plant Cell 1996, 8:1305-1321.
58. Fujiu K, Nakayama Y, Yanagisawa A, Sokabe M, Yoshimura K. Chlamydomonas CAV2 encodes a voltage-dependent calcium channel required for the flagellar waveform conversion. Current Biology 2009, 19:133-139.
59. Garrill A, Jackson SL, Lew RR, Heath IB. Ion channel activity and tip growth. Tip-localized stretch-activated channels generate an essential Ca2+ gradient in the oomycete Saprolegnia ferax. European Journal of Cell Biology 1993, 60:358-365.
60. Garrill A, Lew RR, Heath IB. Stretch activated Ca2+ and Ca2+-activated K+ channels in the hyphal tip plasma-membrane of the oomycete Saprolegnia ferax. Journal of Cell Science 1992, 101:721-730.
61. Geffeney SL, Fujimoto E, Brodie ED, Ruben PC. Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature 2005, 434:759-763.
62. Gerke V, Moss SE. Annexins: from structure to function. Physiological Reviews 2002, 82:337-371.
63. Gilroy S, Read ND, Trewavas AJ. Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 1990, 346:769-771.
64. Goddard H, Manison NFH, Tomos D, Brownlee C. Elemental propagation of calcium signals in response-specific patterns determined by environmental stimulus strength. Proceedings of the National Academy of Sciences, USA 2000, 97:1932-1937.
65. Goldin AL. Diversity of mammalian voltage-gated sodium channels. Molecular and Functional Diversity of Ion Channels and Receptors 1999, 868:38-50.
66. Goodenough UW, Shames B, Small L, Saito T, Crain RC, Sanders MA, Salisbury JL. The role of calcium in the Chlamydomonas reinhardtii mating reaction. Journal of Cell Biology 1993, 121:365-374.
67. Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rummele SE, Bhattacharya D. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of Rhizaria with Chromalveolates. Molecular Biology and Evolution 2007, 24:1702-1713.
68. Hader DP, Richter PR, Schuster M, Daiker V, Lebert M. Molecular analysis of the graviperception signal transduction in the flagellate Euglena gracilis: involvement of a transient receptor potential-like channel and a calmodulin. Advances in Space Research 2009, 43:1179-1184.
69. Hall, TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclear Acids Symposium Series 1999, 41:95-98.
70. Harada H, Nakajima K, Sakaue K, Matsuda Y. CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiology 2006, 142:1318-1328.
71. Harz H, Hegemann P. Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 1991, 351:489-491.
72. Harz H, Nonnengasser C, Hegemann P. The photoreceptor current of the green-alga Chlamydomonas. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 1992, 338:39-52.
73. Haswell ES, Meyerowitz EM. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Current Biology 2006, 16:1-11.
74. Haswell ES, Peyronnet R, Barbier-Brygoo H, Meyerowitz EM, Frachisse JM. Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Current Biology 2008, 18:730-734.
75. Hauser DCR, Levandowsky M, Glassgold JM. Ultrasensitive chemosensory responses by a protozoan to epinephrine and other neurochemicals. Science 1975, 190:285-286.
76. Hegemann P. Algal sensory photoreceptors. Annual Review of Plant Biology 2008, 59:167-189.
77. Hellunglarsen P, Leick V, Tommerup N. Chemoattraction in Tetrahymena- on the role of chemokinesis. Biological Bulletin 1986, 170:357-367.
78. Hetherington AM, Brownlee C. The generation of Ca2+ signals in plants. Annual Review of Plant Biology 2004, 55:401-427.
79. Hille B. Ion channels of excitable membranes 2001, 3rdedn, Sunderland, MA, USA, Sinauer Associates, Inc
80. Holland EM, Braun FJ, Nonnengasser C, Harz H, Hegemann P. Nature of rhodopsin-triggered photocurrents in Chlamydomonas. I. Kinetics and influence of divalent ions. Biophysical Journal 1996, 70:924-931.
81. Huang K, Diener DR, Mitchell A, Pazour GJ, Witman GB, Rosenbaum JL. Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. Journal of Cell Biology 2007, 179:501-514.
82. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology 1952, 117:500-544.
83. Hyde GJ, Heath IB. Ca2+-dependent polarization axis establishment in the tip-growing organism Saprolegnia ferax, by gradients of the ionophore A23187. European Journal of Cell Biology 1995, 67:356-362.
84. Iida K, Teng J, Tada T, Saka A, Tamai M, Izumi-Nakaseko H, Adachi-Akahane S, Iida H. Essential, completely conserved glycine residue in the domain III s2-s3 linker of voltage-gated calcium channel alpha(1) subunits in yeast and mammals. Journal of Biological Chemistry 2007, 282:25659-25667.
85. Ishibashi K, Suzuki M, Imai M. Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochemical and Biophysical Research Communications 2000, 270:370-376.
86. Ito M, Xu HX, Guffanti AA, Wei Y, Zvi L, Clapham DE, Krulwich TA. The voltage-gated Na+ channel NavBP has a role in motility, chemotaxis, and pH homeostasis of an alkaliphilic Bacillus. Proceedings of the National Academy of Sciences, USA 2004, 101:10566-10571.
87. Jackson SL, Heath IB. Effects of exogenous calcium ions on tip growth, intracellular Ca2+ concentration and actin arrays in hyphae of the fungus Saprolegnia ferax. Experimental Mycology 1989, 13:1-12.
88. Jeter CR, Tang WQ, Henaff E, Butterfield T, Roux SJ. Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. Plant Cell 2004, 16:2652-2664.
89. Jeziorski MC, Greenberg RM, Anderson PAV. The molecular biology of invertebrate voltage-gated Ca2+ channels. Journal of Experimental Biology 2000, 203:841-856.
90. Kamiya R, Witman GB. Submicromolar levels of calcium control the balance of beating between the 2 flagella in demembranated models of Chlamydomonas. Journal of Cell Biology 1984, 98:97-107.
91. Keeling P. A brief history of plastids and their hosts. Protist 2004, 155:3-7.
92. Keeling P. Chromalveolates and the evolution of plastids by secondary endosymbiosis. Journal of Eukaryote Microbiology 2009, 56:1-8.
93. Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006, 442:527-532.
94. Kianianmomeni A, Stehfest K, Nematollahi G, Hegemann P, Hallmann A. Channelrhodopsins of Volvox carteri are photochromic proteins that are specifically expressed in somatic cells under control of light, temperature, and the sex inducer. Plant Physiology 2009, 151:347-366.
95. Koishi R, Xu HX, Ren DJ, Navarro B, Spiller BW, Shi Q, Clapham DE. A superfamily of voltage-gated sodium channels in bacteria. Journal of Biological Chemistry 2004, 279:9532-9538.
96. Kuriu T, Saitow F, Nakaoka Y, Oosawa Y. Calcium current activated by cooling in Paramecium. Journal of Comparative Physiology A - Sensory Neural and Behavioral Physiology 1998, 183:135-141.
97. Kurusu T, Yagala T, Miyao A, Hirochika H, Kuchitsu K. Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant Journal 2005, 42:798-809.
98. Ladenburger EM, Korn I, Kasielke N, Wassmer T, Plattner H. An Ins(1,4,5)P-3 receptor in Paramecium is associated with the osmoregulatory system. Journal of Cell Science 2006, 119:3705-3717.
99. Lam CMC, New DC, Wong JTY. cAMP in the cell cycle of the dinoflagellate Crypthecodinium cohnii (Dinophyta). Journal of Phycology 2001, 37:79-85.
100. Lam CMC, Yeung PKK, Wong JTY. Monitoring cytosolic calcium in the dinoflagellate Crypthecodinium cohnii with calcium orange-AM. Plant and Cell Physiology 2005, 46:1021-1027.
101. Lam HM, Chiu J, Hsieh MH, Meisel L, Oliveira IC, Shin M, Coruzzi G. Glutamate-receptor genes in plants. Nature 1998, 396:125-126.
102. Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, MacPherson M, Brownlee C, Hofmann A, Webb AAR, Miedima H. Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+-permeable conductance. Plant Cell 2009, 21:471-493.
103. Latz MI, Bovard M, VanDelinder V, Segre E, Rohr J, Grossman A. Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device. Journal of Experimental Biology 2008, 211:2865-2875.
104. Lee WY, Free CR, Sine SM. Binding to gating transduction in nicotinic receptors: cys-loop energetically couples to pre-M1 and M2-M3 regions. Journal of Neuroscience 2009, 29:3189-3199.
105. Leick V, Hellunglarsen P. Chemosensory responses in Tetrahymena- the involvement of peptides and other signal substances. Journal of Protozoology 1985, 32:550-553.
106. Levandowsky M, Hauser DC. Chemosensory responses of swimming algae and protozoa. International Review of Cytology 1978, 53:145-210.
107. Levandowsky M, Klafter J, White BS. Feeding and swimming behavior in grazing microzooplankton. Journal of Protozoology 1988, 35:243-246.
108. Levina NN, Lew RR, Heath IB. Cytoskeletal regulation of ion channel distribution in the tip-growing organism Saprolegnia ferax. Journal of Cell Science 1994, 107:127-134.
109. Li J, Zhu SH, Song XW, Shen Y, Chen HM, Yu J, Yi KK, Liu YF, Karplus VJ, Wu P. A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 2006, 18:340-349.
110. Lin SY, Corey DP. TRP channels in mechanosensation. Current Opinion in Neurobiology 2005, 15:350-357.
111. Littleton JT, Ganetzky B. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 2000, 26:35-43.
112. Locke EG, Bonilla M, Liang L, Takita Y, Cunningham KW. A homolog of voltage-gated Ca2+ channels stimulated by depletion of secretory Ca2+ in yeast. Molecular and Cellular Biology 2000, 20:6686-6694.
113. Lucas J, Riddle M, Bartholomew J, Thomas B, Forni J, Nickerson LE, Van Heukelum B, Paulick J, Kuruvilla H. PACAP-38 signaling in Tetrahymena thermophila involves NO and cGMP. Acta Protozoologica 2004, 43:15-20.
114. Martinac B. Mechanosensitive ion channels: molecules of mechanotransduction. Journal of Cell Science 2004, 117:2449-2460.
115. Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 2004, 428:653-657.
116. McAinsh MR, Gray JE, Hetherington AM, Leckie CP, Ng C. Ca2+ signalling in stomatal guard cells. Biochemical Society Transactions 2000, 28:476-481.
117. McAinsh MR, Pittman JK. Shaping the calcium signature. New Phytologist 2009, 181:275-294.
118. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318:245-250.
119. Meyerhoff O, Muller K, Roelfsema MR, Latz A, Lacombe B, Hedrich R, Dietrich P, Becker D. AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta 2005, 222:418-427.
120. Miedema H, Demidchik V, Very AA, Bothwell JHF, Brownlee C, Davies JM. Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytologist 2008, 179:378-385.
121. Minke B. TRP channels and Ca2+ signaling. Cell Calcium 2006, 40:261-275.
122. Montsant A, Allen AE, Coesel S, De Martino A, Falciatore A, Mangogna M, Siaut M, Heijde M, Jabbari K, Maheswari U. Identification and comparative genomic analysis of signaling and regulatory components in the diatom Thalassiosira pseudonana. Journal of Phycology 2007, 43:585-604.
123. Moore RB, Obornik M, Janouskovec J, Chrudimsky T, Vancova M, Green DH, Wright SW, Davies NW, Bolch CJS, Heimann K. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 2008, 451:959-963.
124. Moss SE, Morgan RO. The annexins. Genome Biology 2004, 5:219.
125. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 2009, 324:1724-1726.
126. Nagata T, Iizumi S, Satoh K, Ooka H, Kawai J, Carninci P, Hayashizaki Y, Otomo Y, Murakami K, Matsubara K. Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Molecular Biology and Evolution 2004, 21:1855-1870.
127. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Mustl AM, Bamberg E, Hegemann P. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 2002, 296:2395-2398.
128. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proceedings of the National Academy of Sciences, USA 2003, 100:13940-13945.
129. Naitoh Y, Sugino K. Ciliary movement and its control in Paramecium. Journal of Protozoology 1984, 31:31-40.
130. Nakayama Y, Fujiu K, Sokabe M, Yoshimura K. Molecular and electrophysiological characterization of a mechanosensitive channel expressed in the chloroplasts of Chlamydomonas. Proceedings of the National Academy of Sciences, USA 2007, 104:5883-5888.
131. Nawata T, Sibaoka T. Local ion currents controlling the localised cytoplasmic movement associated with feeding initiation Noctiluca. Protoplasma 1987, 137:125-133.
132. Nurani G, Radford M, Charalambous K, O'Reilly AO, Cronin NB, Haque S, Wallace BA. Tetrameric bacterial sodium channels: characterization of structure, stability, and drug binding. Biochemistry 2008, 47:8114-8121.
133. Oami K. Correlation between membrane potential responses and tentacle movement in the dinoflagellate Noctiluca miliaris. Zoological Science 2004, 21:131-138.
134. Oami K, Naitoh Y. Bioelectrical control of effector responses in the marine dinoflagellate, Noctiluca miliaris. Zoological Science 1989, 6:833-850.
135. Oami K, Naitoh Y, Sibaoka T. Modification of voltage-sensitive inactivation of Na+ current by external Ca2+ in the marine dinoflagellate Noctiluca miliaris. Journal of Comparative Physiology A - Sensory Neural and Behavioral Physiology 1995, 176:635-640.
136. Ohta M, Suzuki T. Participation of the inositol phospholipid signaling pathway in the increase in cytosolic calcium induced by tributyltin chloride intoxication of chlorophyllous protozoa Euglena gracilis Z and its achlorophyllous mutant SM-ZK. Comparative Biochemistry and Physiology. C. Toxicology and Pharmacology 2007, 146:523-530.
137. Oldroyd GED, Downie JA. Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 2006, 9:351-357.
138. Padan E, Bibi E, Ito M, Krulwich TA. Alkaline pH homeostasis in bacteria: new insights. Biochimica et Biophysica Acta-Biomembranes 2005, 1717:67-88.
139. Paidhungat M, Garrett S. Homolog of mammalian, voltage-gated calcium channels mediates yeast pheromone-stimulated Ca2+ uptake and exacerbates the cdc1(Ts) growth defect. Molecular and Cellular Biology 1997, 17:6339-6347.
140. Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proceedings of the National Academy of Sciences, USA 2007, 104:7705-7710.
141. Patron NJ, Inagaki Y, Keeling PJ. Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Current Biology 2007, 17:887-891.
142. Pazour GJ, Agrin N, Leszyk J, Witman GB. Proteomic analysis of a eukaryotic cilium. Journal of Cell Biology 2005, 170:103-113.
143. Peiter E, Fischer M, Sidaway K, Roberts SK, Sanders D. The Saccharomyces cerevisiae Ca2+ channel Cch1pMid1p is essential for tolerance to cold stress and iron toxicity. FEBS Letters 2005a, 579:5697-5703.
144. Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 2005b, 434:404-408.
145. Pivetti CD, Yen MR, Miller S, Busch W, Tseng YH, Booth IR, Saier MH. Two families of mechanosensitive channel proteins. Microbiology and Molecular Biology Reviews 2003, 67:66-85.
146. Plattner H, Diehl S, Husser MR, Hentschel J. Sub-second calcium coupling between outside medium and subplasmalemmal stores during overstimulation/depolarisation-induced ciliary beat reversal in Paramecium cells. Cell Calcium 2006, 39:509-516.
147. Plattner H, Flotenmeyer M, Kissmehl R, Pavlovic N, Hauser K, Momayezi M, Braun N, Tack J, Bachmann L. Microdomain arrangement of the SERCA-type Ca2+ pump (Ca2+-ATPase) in subplasmalemmal calcium stores of Paramecium cells. Journal of Histochemistry & Cytochemistry 1999, 47:841-853.
148. Plattner H, Klauke N. Calcium in ciliated protozoa: sources, regulation, and calcium-regulated cell functions. International Review of Cytology - A Survey of Cell Biology 2001, 201:115-208.
149. Pottosin II, Tikhonova LI, Hedrich R, Schoenknecht G. Slowly activating vacuolar channels cannot mediate Ca2+-induced Ca2+ release. Plant Journal 1997, 12:1387-1398.
150. Qi Z, Stephens NR, Spalding EP. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiology 2006, 142:963-971.
151. Quarmby LM. Signal-transduction in the sexual life of Chlamydomonas. Plant Molecular Biology 1994, 26:1271-1287.
152. Quarmby LM, Yueh YG, Cheshire JL, Keller LR, Snell WJ, Crain RC. Inositol phospholipid-metabolism may trigger flagellar excision in Chlamydomonas reinhardtii. Journal of Cell Biology 1992, 116:737-744.
153. Quesada I, Chin WC, Verdugo P. Mechanisms of signal transduction in photo-stimulated secretion in Phaeocystis globosa. FEBS Letters 2006, 580:2201-2206.
154. Ramoino P, Scaglione S, Diaspro A, Beltrame F, Fato M, Usai C. GABA(A) receptor subunits identified in Paramecium by immunofluorescence confocal microscopy. FEMS Microbiology Letters 2004, 238:449-453.
155. Ramoino P, Usai C, Beltrame F, Fato M, Gallus L, Tagliafierro G, Magrassi R, Diaspro A. GABA(B) receptor intracellular trafficking after internalization in Paramecium. Microscopy Research and Technique 2005, 68:290-295.
156. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annual Review of Physiology 2006, 68:619-647.
157. Ranf S, Wunnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P. Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant Journal 2008, 53:287-299.
158. Ren DJ, Navarro B, Xu HX, Yue LX, Shi Q, Clapham DE. A prokaryotic voltage-gated sodium channel. Science 2001, 294:2372-2375.
159. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 2008, 319:64-69.
160. Roberts S, Brownlee C. Calcium influx, fertilization potential and egg activation in Fucus erratus. Zygote 1995, 3:191-197.
161. Roberts SK, Gillot I, Brownlee C. Cytoplasmic calcium and Fucus egg activation. Development 1994, 120:155-163.
162. Robinson KR, Jaffe LF. Ion movements in a developing Fucoid egg. Developmental Biology 1973, 35:349-361.
163. Rogers MB, Watkins RF, Harper JT, Durnford DG, Gray MW, Keeling PJ. A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evolutionary Biology 2007, 7:89.
164. Rosner BN, Bartholomew JN, Gaines CD, Riddle ML, Everett HA, Rulapaugh KG, Nickerson LE, Marshall MR, Kuruvilla HG. Biochemical evidence for a P2Y-like receptor in Tetrahymena thermophila. Journal of Comparative Physiology A - Neuroethology, Sensory, Neural and Behavioral Physiology 2003, 189:781-789.
165. Roux SJ, Steinebrunner I. Extracellular ATP: an unexpected role as a signaler in plants. Trends in Plant Science 2007, 12:522-527.
166. Roy SJ, Gilliham M, Berger B, Essah PA, Cheffings C, Miller AJ, Davenport RJ, Liu LH, Skynner MJ, Davies JM. Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant, Cell & Environment 2008, 31:861-871.
167. Ruelland E, Cantrel C, Gawer M, Kader JC, Zachowski A. Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiology 2002, 130:999-1007.
168. Sanders D, Pelloux J, Brownlee C, Harper JF. Calcium at the crossroads of signaling. Plant Cell 2002, 14:S401-S417.
169. Schmidt M, Gessner G, Matthias L, Heiland I, Wagner V, Kaminski M, Geimer S, Eitzinger N, Reissenweber T, Voytsekh O. Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements. Plant Cell 2006, 18:1908-1930.
170. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D. Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 2001, 52:627-658.
171. Steinbacher S, Bass R, Strop P, Rees DC. Structures of the prokaryotic mechanosensitive channels MscL and MscS. Mechanosensitive Ion Channels, Part A 2007, 58:1-24.
172. Strong M, Chandy KG, Gutman GA. Molecular evolution of voltage-sensitive ion channel genes - on the origins of electrical excitability. Molecular Biology and Evolution 1993, 10:221-242.
173. Suzuki T, Yamasaki K, Fujita S, Oda K, Iseki M, Yoshida K, Watanabe M, Daiyasu H, Toh H, Asamizu E. Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochemical and Biophysical Research Communications 2003, 301:711-717.
174. Takahashi F, Yamagata D, Ishikawa M, Fukamatsu Y, Ogura Y, Kasahara M, Kiyosue T, Kikuyama M, Wada M, Kataoka H. AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proceedings of the National Academy of Sciences, USA 2007, 104:19625-19630.
175. Talke IN, Blaudez D, Maathuis FJM, Sanders D. CNGCs: prime targets of plant cyclic nucleotide signalling? Trends in Plant Science 2003, 8:286-293.
176. Tang RH, Han SC, Zheng HL, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei ZM. Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 2007, 315:1423-1426.
177. Tapken D, Hollmann M. Arabidopsis thaliana glutamate receptor ion channel function demonstrated by ion pore transplantation. Journal of Molecular Biology 2008, 383:36-48.
178. Tasneem A, Iyer LM, Jakobsson E, Aravind L. Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biology 2005, 6:R4.
179. Taylor AR. A fast Na+/Ca2+ based action potential in a marine diatom. PLoS ONE 2009, 4:e4966.
180. Taylor A, Brownlee C. Calcium and potassium currents in the Fucus egg. Planta 1993, 189:109-119.
181. Taylor AR, Brownlee C. A novel Cl- inward-rectifying current in the plasma membrane of the calcifying marine phytoplankton Coccolithus pelagicus. Plant Physiology 2003, 131:1391-1400.
182. Taylor AR, Manison NFH, Fernandez C, Wood J, Brownlee C. Spatial organization of calcium signaling involved in cell volume control in the Fucus rhizoid. Plant Cell 1996, 8:2015-2031.
183. Taylor AR, Russell MA, Harper GM, Collins TFT, Brownlee C. Dynamics of the formation and secretion of hetercoccoliths by Coccolithus pelagicus ssp. (Braarudii). European Journal of Phycology 2007, 42:125-1336.
184. Tazawa M, Kikuyama M. Is Ca2+ release from internal stores involved in membrane excitation in characean cells? Plant and Cell Physiology 2003, 44:518-526.
185. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
186. Thompson SEM, Taylor AR, Brownlee C, Callow ME, Callow JA. The role of nitric oxide in diatom adhesion in relation to substratum properties. Journal of Phycology 2008, 44:967-976.
187. Tuxhorn J, Daise T, Dentler WL. Regulation of flagellar length in Chlamydomonas. Cell Motility and the Cytoskeleton 1998, 40:133-146.
188. Tyler BM, Tripathy S, Zhang XM, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006, 313:1261-1266.
189. Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A, Levine A. Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Current Biology 1999, 9:1061-1064.
190. Vardi A, Bidie KD, Kwityn C, Hirsh DJ, Thompson SM, Callow JA, Falkowski P, Bowler C. A diatom gene regulating nitric-oxide signaling and susceptibility to diatom-derived aldehydes. Current Biology 2008, 18:895-899.
191. Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F, Miralto A, Bowler C. A stress surveillance system based on calcium and nitric oxide in marine diatoms. Plos Biology 2006, 4:411-419.
192. Wacke M, Thiel G. Electrically triggered all-or-none Ca2+-liberation during action potential in the giant alga Chara. Journal of General Physiology 2001, 118:11-21.
193. Wacke M, Thiel G, Hutt MT. Ca2+ dynamics during membrane excitation of green alga Chara: model simulations and experimental data. Journal of Membrane Biology 2003, 191:179-192.
194. Wang YJ, Yu JN, Chen T, Zhang ZG, Hao YJ, Zhang JS, Chen SY. Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat. Journal of Experimental Botany 2005, 56:3051-3060.
195. Ward JM, Maser P, Schroeder JI. Plant ion channels: gene families, physiology, and functional genomics analyses. Annual Review of Physiology 2009, 71:59-82.
196. Wheeler GL, Brownlee C. Ca2+ signalling in plants and green algae - changing channels. Trends in Plant Science 2008, 13:506-514.
197. Wheeler GL, Joint I, Brownlee C. Rapid spatiotemporal patterning of cytosolic Ca2+ underlies flagellar excision in Chlamydomonas reinhardtii. Plant Journal 2008, 53:401-413.
198. White P, Broadley MR. Calcium in plants. Annals of Botany 2003, 92:487-511.
199. Worden AZ, Lee JH, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 2009, 324:268-272.
200. Yang WQ, Braun C, Plattner H, Purvee J, Van Houten JL. Cyclic nucleotides in glutamate chemosensory signal transduction of Paramecium. Journal of Cell Science 1997, 110:2567-2572.
201. Yeung PKK, Lam CMC, Ma ZY, Wong YH, Wong JTY. Involvement of calcium mobilization from caffeine-sensitive stores in mechanically induced cell cycle arrest in the dinoflagellate Crypthecodinium cohnii. Cell Calcium 2006, 39:259-274.
202. Yoon HS, Muller KM, Sheath RG, Ott FD, Bhattacharya D. Defining the major lineages of red algae (Rhodophyta). Journal of Phycology 2006, 42:482-492.
203. Yue LX, Navarro B, Ren DJ, Ramos A, Clapham DE. The cation selectivity filter of the bacterial sodium channel, NaChBac. Journal of General Physiology 2002, 120:845-853.