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Calcium-Dependent Signalling Processes in Chlamydomonas

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Chlamydomonas: Molecular Genetics and Physiology

Part of the book series: Microbiology Monographs ((MICROMONO,volume 30))

Abstract

Like all organisms, the motile green alga Chlamydomonas has evolved an array of sensory mechanisms to enable it to detect and respond to an array of abiotic and biotic stimuli. It is clear that Ca2+-dependent signalling mechanisms are central to many responses in Chlamydomonas, from flagella function through to stress signalling and photosynthesis. Chlamydomonas has long been used as a model organism for flagella function and this aspect of signalling has received much attention, with well-characterised roles for Ca2+ in flagella beat, phototaxis, mating and deflagellation. Recent progress has identified a series of ion channels and Ca2+-sensor kinases that underpin these responses and direct imaging of flagella Ca2+ in Chlamydomonas cells has demonstrated the highly dynamic nature of Ca2+ signalling in these organelles. The role of Ca2+ in other signalling processes in Chlamydomonas has been less well explored, although exciting recent developments have demonstrated novel Ca2+-dependent signalling processes associated with the regulation of photosynthesis. These developments highlight the diverse roles of Ca2+ in Chlamydomonas physiology and the potential for the discovery of novel Ca2+ signalling mechanisms within this organism.

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References

  • Aksoy M, Pootakham W, Grossman AR (2014) Critical function of a Chlamydomonas reinhardtii putative polyphosphate polymerase subunit during nutrient deprivation. Plant Cell 26:4214–4229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arias-Darraz L, Cabezas D, Colenso CK, Alegria-Arcos M, Bravo-Moraga F, Varas-Concha I, Almonacid DE, Madrid R, Brauchi S (2015) A transient receptor potential ion channel in Chlamydomonas shares key features with sensory transduction-associated TRP channels in mammals. Plant Cell 27:177–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauer CS, Plieth C, Hansen UP, Sattelmacher B, Simonis W, Schonknecht G (1997) Repetitive Ca2+ spikes in a unicellular green alga. FEBS Lett 405:390–393

    Article  CAS  PubMed  Google Scholar 

  • Berthold P, Tsunoda SP, Ernst OP, Mages W, Gradmann D, Hegemann P (2008) Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell 20:1665–1677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besschetnova TY, Kolpakova-Hart E, Guan Y, Zhou J, Olsen BR, Shah JV (2010) Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 20:182–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bessen M, Fay RB, Witman GB (1980) Calcium control of waveform in isolated flagellar axonemes of Chlamydomonas. J Cell Biol 86:446–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bickerton P, Sello S, Brownlee C, Pittman JK, Wheeler GL (2016) Spatial and temporal specificity of Ca2+ signalling in Chlamydomonas reinhardtii in response to osmotic stress. New Phytol 212(4):920–933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloodgood RA (1981) Flagella-dependent gliding motility in Chlamydomonas. Protoplasma 106:183–192

    Article  Google Scholar 

  • Bloodgood RA (1995) Flagellar surface motility: gliding and microsphere movements. Methods Cell Biol 47:273–279

    Article  CAS  PubMed  Google Scholar 

  • Bloodgood RA (2009) The Chlamydomonas flagellar membrane and its dynamic properties. In: Witman GB (ed) The Chlamydomonas sourcebook. Academic, Oxford, pp 309–368

    Chapter  Google Scholar 

  • Bloodgood RA, Salomonsky NL (1990) Calcium influx regulates antibody-induced glycoprotein movements within the Chlamydomonas flagellar membrane. J Cell Sci 96(Pt 1):27–33

    CAS  PubMed  Google Scholar 

  • Bloodgood RA, Workman LJ (1984) A flagellar surface glycoprotein mediating cell-substrate interaction in Chlamydomonas. Cell Motil 4:77–87

    Article  CAS  PubMed  Google Scholar 

  • Bothwell JHF, Brownlee C, Hetherington AM, Ng CKY, Wheeler GL, McAinsh MR (2006) Biolistic delivery of Ca2+ dyes into plant and algal cells. Plant J 46:327–335

    Article  CAS  PubMed  Google Scholar 

  • Braun FJ, Hegemann P (1999) Direct measurement of cytosolic calcium and pH in living Chlamydomonas reinhardtii cells. Eur J Cell Biol 78:199–208

    Article  CAS  PubMed  Google Scholar 

  • Brownlee C (1994) Tansley review No-70 – signal-transduction during fertilization in algae and vascular plants. New Phytol 127:399–423

    Article  Google Scholar 

  • Casey DM, Inaba K, Pazour GJ, Takada S, Wakabayashi K, Wilkerson CG, Kamiya R, Witman GB (2003a) DC3, the 21-kDa subunit of the outer dynein arm-docking complex (ODA-DC), is a novel EF-hand protein important for assembly of both the outer arm and the ODA-DC. Mol Biol Cell 14:3650–3663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casey DM, Yagi T, Kamiya R, Witman GB (2003b) DC3, the smallest subunit of the Chlamydomonas flagellar outer dynein arm-docking complex, is a redox-sensitive calcium-binding protein. J Biol Chem 278:42652–42659

    Article  CAS  PubMed  Google Scholar 

  • Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V et al (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheshire JL, Keller LR (1991) Uncoupling of Chlamydomonas flagellar gene expression and outgrowth from flagellar excision by manipulation of Ca2+. J Cell Biol 115:1651–1659

    Article  CAS  PubMed  Google Scholar 

  • Cheshire JL, Evans JH, Keller LR (1994) Ca2+ signaling in the Chlamydomonas flagellar regeneration system: cellular and molecular responses. J Cell Sci 107(Pt 9):2491–2498

    CAS  PubMed  Google Scholar 

  • Collingridge P, Brownlee C, Wheeler GL (2013) Compartmentalized calcium signaling in cilia regulates intraflagellar transport. Curr Biol 23:2311–2318

    Article  CAS  PubMed  Google Scholar 

  • DeCoursey TE (2013) Voltage-gated proton channels: molecular biology, physiology, and pathophysiology of the H(V) family. Physiol Rev 93:599–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DiPetrillo CG, Smith EF (2010) Pcdp1 is a central apparatus protein that binds Ca(2+)-calmodulin and regulates ciliary motility. J Cell Biol 189:601–612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DiPetrillo CG, Smith EF (2013) Methods for analysis of calcium/calmodulin signaling in cilia and flagella. Methods Enzymol 524:37–57

    Article  CAS  PubMed  Google Scholar 

  • Docampo R, Huang G (2016) Acidocalcisomes of eukaryotes. Curr Opin Cell Biol 41:66–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dymek EE, Smith EF (2007) A conserved CaM- and radial spoke associated complex mediates regulation of flagellar dynein activity. J Cell Biol 179:515–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edel KH, Kudla J (2015) Increasing complexity and versatility: how the calcium signaling toolkit was shaped during plant land colonization. Cell Calcium 57:231–246

    Article  CAS  PubMed  Google Scholar 

  • Ehlenbeck S, Gradmann D, Braun FJ, Hegemann P (2002) Evidence for a light-induced H(+) conductance in the eye of the green alga Chlamydomonas reinhardtii. Biophys J 82:740–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emery L, Whelan S, Hirschi KD, Pittman JK (2012) Protein phylogenetic analysis of Ca(2+)/cation antiporters and insights into their evolution in plants. Front Plant Sci 3:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ermilova E, Zalutskaya Z, Munnik T, van den Ende H, Gromov B (1998) Calcium in the control of chemotaxis in Chlamydomonas. Biologia 53:577–581

    CAS  Google Scholar 

  • Evans JH, Keller LR (1997) Calcium influx signals normal flagellar RNA induction following acid shock of Chlamydomonas reinhardtii. Plant Mol Biol 33:467–481

    Article  CAS  PubMed  Google Scholar 

  • Finst RJ, Kim PJ, Griffis ER, Quarmby LM (2000) Fa1p is a 171 kDa protein essential for axonemal microtubule severing in Chlamydomonas. J Cell Sci 113(Pt 11):1963–1971

    CAS  PubMed  Google Scholar 

  • Foster KW, Smyth RD (1980) Light antennas in phototactic algae. Microbiol Rev 44:572–630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiu K, Nakayama Y, Yanagisawa A, Sokabe M, Yoshimura K (2009) Chlamydomonas CAV2 encodes a voltage- dependent calcium channel required for the flagellar waveform conversion. Curr Biol 19:133–139

    Article  CAS  PubMed  Google Scholar 

  • Fujiu K, Nakayama Y, Iida H, Sokabe M, Yoshimura K (2011) Mechanoreception in motile flagella of Chlamydomonas. Nat Cell Biol 13:630–632

    Article  CAS  PubMed  Google Scholar 

  • Goodenough UW, Shames B, Small L, Saito T, Crain RC, Sanders MA, Salisbury JL (1993) The role of calcium in the Chlamydomonas reinhardtii mating reaction. J Cell Biol 121:365–374

    Article  CAS  PubMed  Google Scholar 

  • Govorunova EG, Sineshchekov OA (2003) Integration of photo- and chemosensory signaling pathways in Chlamydomonas. Planta 216:535–540

    CAS  PubMed  Google Scholar 

  • Govorunova EG, Sineshchekov OA (2005) Chemotaxis in the green flagellate alga Chlamydomonas. Biochemistry (Mosc) 70:717–725

    Article  CAS  Google Scholar 

  • Hamel LP, Sheen J, Seguin A (2014) Ancient signals: comparative genomics of green plant CDPKs. Trends Plant Sci 19:79–89

    Article  CAS  PubMed  Google Scholar 

  • Harz H, Hegemann P (1991) Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 351:489–491

    Article  CAS  Google Scholar 

  • Hegemann P, Berthold P (2009) Sensory photoreceptors and light control of flagellar activity. In: Witman GB (ed) The Chlamydomonas sourcebook. Academic, Oxford, pp 395–429

    Chapter  Google Scholar 

  • Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF (2008) Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J Neurosci 28:7399–7411

    Article  CAS  PubMed  Google Scholar 

  • Hill K, Hemmler R, Kovermann P, Calenberg M, Kreimer G, Wagner R (2000) A Ca(2+)- and voltage-modulated flagellar ion channel is a component of the mechanoshock response in the unicellular green alga Spermatozopsis similis. Biochim Biophys Acta 1466:187–204

    Article  CAS  PubMed  Google Scholar 

  • Hilton LK, Meili F, Buckoll PD, Rodriguez-Pike JC, Choutka CP, Kirschner JA, Warner F, Lethan M, Garces FA, Qi J, Quarmby LM (2016) A forward genetic screen and whole genome sequencing identify deflagellation defective mutants in Chlamydomonas, including assignment of ADF1 as a TRP channel. G3 6(10):3409–3418

    PubMed  PubMed Central  Google Scholar 

  • Hochmal AK, Zinzius K, Charoenwattanasatien R, Gabelein P, Mutoh R, Tanaka H, Schulze S, Liu G, Scholz M, Nordhues A et al (2016) Calredoxin represents a novel type of calcium-dependent sensor-responder connected to redox regulation in the chloroplast. Nat Commun 7:11847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holland EM, Braun FJ, Nonnengasser C, Harz H, Hegemann P (1996) Nature of rhodopsin-triggered photocurrents in Chlamydomonas.1. Kinetics and influence of divalent ions. Biophys J 70:924–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holland EM, Harz H, Uhl R, Hegemann P (1997) Control of phobic behavioral responses by rhodopsin-induced photocurrents in Chlamydomonas. Biophys J 73:1395–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong-Hermesdorf A, Miethke M, Gallaher SD, Kropat J, Dodani SC, Chan J, Barupala D, Domaille DW, Shirasaki DI, Loo JA et al (2014) Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas. Nat Chem Biol 10:1034–1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horst CJ, Witman GB (1993) ptx1, a nonphototactic mutant of Chlamydomonas, lacks control of flagellar dominance. J Cell Biol 120:733–741

    Article  CAS  PubMed  Google Scholar 

  • Huang K, Diener DR, Mitchell A, Pazour GJ, Witman GB, Rosenbaum JL (2007) Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J Cell Biol 179:501–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyams JS, Borisy GG (1978) Isolated flagellar apparatus of Chlamydomonas: characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro. J Cell Sci 33:235–253

    CAS  PubMed  Google Scholar 

  • Im CS, Matters GL, Beale SI (1996) Calcium and calmodulin are involved in blue light induction of the gsa gene for an early chlorophyll biosynthetic step in Chlamydomonas. Plant Cell 8:2245–2253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kam V, Moseyko N, Nemson J, Feldman LJ (1999) Gravitaxis in Chlamydomonas reinhardtii: characterization using video microscopy and computer analysis. Int J Plant Sci 160:1093–1098

    Article  CAS  PubMed  Google Scholar 

  • Kamiya R, Okamoto M (1985) A mutant of Chlamydomonas reinhardtii that lacks the flagellar outer dynein arm but can swim. J Cell Sci 74:181–191

    CAS  PubMed  Google Scholar 

  • Kamiya R, Witman GB (1984) Submicromolar levels of calcium control the balance of beating between the 2 flagella in demembranated models of Chlamydomonas. J Cell Biol 98:97–107

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12:1067–1078

    Article  CAS  PubMed  Google Scholar 

  • Kreimer G, Witman GB (1994) Novel touch-induced, Ca(2+)-dependent phobic response in a flagellate green alga. Cell Motil Cytoskeleton 29:97–109

    Article  CAS  PubMed  Google Scholar 

  • Lefebvre PA, Nordstrom SA, Moulder JE, Rosenbaum JL (1978) Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis. J Cell Biol 78:8–27

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Pan J (2013) Regulation of flagellar biogenesis by a calcium dependent protein kinase in Chlamydomonas reinhardtii. PLoS One 8:e69902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang Y, Pang Y, Wu Q, Hu Z, Han X, Xu Y, Deng H, Pan J (2014) FLA8/KIF3B phosphorylation regulates kinesin-II interaction with IFT-B to control IFT entry and turnaround. Dev Cell 30:585–597

    Article  CAS  PubMed  Google Scholar 

  • Lohret TA, McNally FJ, Quarmby LM (1998) A role for katanin-mediated axonemal severing during Chlamydomonas deflagellation. Mol Biol Cell 9:1195–1207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruyama S, Tokutsu R, Minagawa J (2014) Transcriptional regulation of the stress-responsive light harvesting complex genes in Chlamydomonas reinhardtii. Plant Cell Physiol 55:1304–1310

    Article  CAS  PubMed  Google Scholar 

  • Matsuda A, Yoshimura K, Sineshchekov OA, Hirono M, Kamiya R (1998) Isolation and characterization of novel Chlamydomonas mutants that display phototaxis but not photophobic response. Cell Motil Cytoskeleton 41:353–362

    Article  CAS  PubMed  Google Scholar 

  • McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294

    Article  CAS  PubMed  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagel G, Ollig D, Fuhrmann M, Kateriya S, Mustl AM, Bamberg E, Hegemann P (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398

    Article  CAS  PubMed  Google Scholar 

  • Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100:13940–13945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53:988–998

    Article  CAS  PubMed  Google Scholar 

  • Nonnengasser C, Holland EM, Harz H, Hegemann P (1996) The nature of rhodopsin-triggered photocurrents in Chlamydomonas. II. Influence of monovalent ions. Biophys J 70:932–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okita N, Isogai N, Hirono M, Kamiya R, Yoshimura K (2005) Phototactic activity in Chlamydomonas ‘non-phototactic’ mutants deficient in Ca2+-dependent control of flagellar dominance or in inner-arm dynein. J Cell Sci 118:529–537

    Article  CAS  PubMed  Google Scholar 

  • Pan J, Snell WJ (2000) Signal transduction during fertilization in the unicellular green alga, Chlamydomonas. Curr Opin Microbiol 3:596–602

    Article  CAS  PubMed  Google Scholar 

  • Pan J, Wang Q, Snell WJ (2004) An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev Cell 6:445–451

    Article  CAS  PubMed  Google Scholar 

  • Pasquale SM, Goodenough UW (1987) Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105:2279–2292

    Article  CAS  PubMed  Google Scholar 

  • Patel-King RS, Gorbatyuk O, Takebe S, King SM (2004) Flagellar radial spokes contain a Ca2+-stimulated nucleoside diphosphate kinase. Mol Biol Cell 15:3891–3902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pazour GJ, Agrin N, Leszyk J, Witman GB (2005) Proteomic analysis of a eukaryotic cilium. J Cell Biol 170:103–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petroutsos D, Busch A, Janssen I, Trompelt K, Bergner SV, Weinl S, Holtkamp M, Karst U, Kudla J, Hippler M (2011) The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell 23:2950–2963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pittman JK, Edmond C, Sunderland PA, Bray CM (2009) A cation-regulated and proton gradient-dependent cation transporter from Chlamydomonas reinhardtii has a role in calcium and sodium homeostasis. J Biol Chem 284:525–533

    Article  CAS  PubMed  Google Scholar 

  • Quarmby LM (1996) Ca2+ influx activated by low pH in Chlamydomonas. J Gen Physiol 108:351–361

    Article  CAS  PubMed  Google Scholar 

  • Quarmby LM (2004) Cellular deflagellation. Int Rev Cytol 233(233):47–91

    Article  CAS  PubMed  Google Scholar 

  • Quarmby LM, Hartzell HC (1994) Two distinct, calcium-mediated, signal transduction pathways can trigger deflagellation in Chlamydomonas reinhardtii. J Cell Biol 124:807–815

    Article  CAS  PubMed  Google Scholar 

  • Quarmby LM, Yueh YG, Cheshire JL, Keller LR, Snell WJ, Crain RC (1992) Inositol phospholipid-metabolism may trigger flagellar excision in Chlamydomonas reinhardtii. J Cell Biol 116:737–744

    Article  CAS  PubMed  Google Scholar 

  • Rasi MQ, Parker JD, Feldman JL, Marshall WF, Quarmby LM (2009) Katanin knockdown supports a role for microtubule severing in release of basal bodies before mitosis in Chlamydomonas. Mol Biol Cell 20:379–388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz FA, Marchesini N, Seufferheld M, Govindjee D, R. (2001) The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 276:46196–46203

    Article  CAS  PubMed  Google Scholar 

  • Sakato M, Sakakibara H, King SM (2007) Chlamydomonas outer arm dynein alters conformation in response to Ca2+. Mol Biol Cell 18:3620–3634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, Aspenstrom P, Rizzuto R, Hajnoczky G (2008) Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci U S A 105:20728–20733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider F, Gradmann D, Hegemann P (2013) Ion selectivity and competition in channelrhodopsins. Biophys J 105:91–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shih SM, Engel BD, Kocabas F, Bilyard T, Gennerich A, Marshall WF, Yildiz A (2013) Intraflagellar transport drives flagellar surface motility. elife 2:e00744

    Article  PubMed  PubMed Central  Google Scholar 

  • Sineshchekov OA, Jung KH, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 99:8689–8694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sjoblad RD, Frederikse PH (1981) Chemotactic responses of Chlamydomonas reinhardtii. Mol Cell Biol 1:1057–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith EF (2002) Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol Biol Cell 13:3303–3313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swarbreck SM, Colaco R, Davies JM (2013) Plant calcium-permeable channels. Plant Physiol 163:514–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi K, Isobe M, Knight MR, Trewavas AJ, Muto S (1997) Hypoosmotic shock induces increases in cytosolic Ca2+ in tobacco suspension-culture cells. Plant Physiol 113:587–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terashima M, Petroutsos D, Hudig M, Tolstygina I, Trompelt K, Gabelein P, Fufezan C, Kudla J, Weinl S, Finazzi G et al (2012) Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc Natl Acad Sci U S A 109:17717–17722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson SE, Callow JA, Callow ME, Wheeler GL, Taylor AR, Brownlee C (2007) Membrane recycling and calcium dynamics during settlement and adhesion of zoospores of the green alga Ulva linza. Plant Cell Environ 30:733–744

    Article  CAS  PubMed  Google Scholar 

  • Tuxhorn J, Daise T, Dentler WL (1998) Regulation of flagellar length in Chlamydomonas. Cell Motil Cytoskeleton 40:133–146

    Article  CAS  PubMed  Google Scholar 

  • Verret F, Wheeler G, Taylor AR, Farnham G, Brownlee C (2010) Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling. New Phytol 187:23–43

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi K, Ide T, Kamiya R (2009) Calcium-dependent flagellar motility activation in Chlamydomonas reinhardtii in response to mechanical agitation. Cell Motil Cytoskeleton 66:736–742

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Snell WJ (2003) Flagellar adhesion between mating type plus and mating type minus gametes activates a flagellar protein-tyrosine kinase during fertilization in Chlamydomonas. J Biol Chem 278:32936–32942

    Article  CAS  PubMed  Google Scholar 

  • Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686

    Article  CAS  PubMed  Google Scholar 

  • Wheeler GL, Brownlee C (2008) Ca2+ signalling in plants and green algae - changing channels. Trends Plant Sci 13:506–514

    Article  CAS  PubMed  Google Scholar 

  • Wheeler GL, Joint I, Brownlee C (2008) Rapid spatiotemporal patterning of cytosolic Ca2+ underlies flagellar excision in Chlamydomonas reinhardtii. Plant J 53:401–413

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura K (1996) A novel type of mechanoreception by the flagella of Chlamydomonas. J Exp Biol 199:295–302

    CAS  PubMed  Google Scholar 

  • Yoshimura K, Matsuo Y, Kamiya R (2003) Gravitaxis in Chlamydomonas reinhardtii studied with novel mutants. Plant Cell Physiol 44:1112–1118

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Dunand C, Snedden W, Galaud JP (2015) CaM and CML emergence in the green lineage. Trends Plant Sci 20:483–489

    Article  CAS  PubMed  Google Scholar 

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Wheeler, G.L. (2017). Calcium-Dependent Signalling Processes in Chlamydomonas. In: Hippler, M. (eds) Chlamydomonas: Molecular Genetics and Physiology. Microbiology Monographs, vol 30. Springer, Cham. https://doi.org/10.1007/978-3-319-66365-4_8

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