Clocks in algae

Biochemistry

Volumn 54, Issue 2, 2015, Pages 171-183

  Noordally, Zeenat B ^a   Millar, Andrew J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLOCKS; ECOLOGY; FATTY ACIDS; MOLECULAR BIOLOGY; PHYSIOLOGICAL MODELS;

BIOCHEMICAL LEVEL; CHLAMYDOMONAS REINHARDTII; EUGLENA GRACILIS; EVOLUTIONARY DIVERSITY; MATHEMATICAL METHOD; MOLECULAR APPROACH; OSTREOCOCCUS TAURI; QUANTITATIVE DATA;

ALGAE;

ACETABULARIA; ALGA; ARTICLE; CHLAMYDOMONAS REINHARDTII; CIRCADIAN RHYTHM; COMPUTATIONAL FLUID DYNAMICS; CORAL REEF; CYANIDIOSCHYZON MEROLAE; DINOFLAGELLATE; ECOPHYSIOLOGY; EUGLENA GRACILIS; EUKARYOTE EVOLUTION; GENOMICS; GREEN ALGA; LINGULODINIUM POLYEDRUM; MATHEMATICAL ANALYSIS; METABOLOMICS; MOLECULAR CLOCK; NONHUMAN; ORGANISMAL INTERACTION; OSTREOCOCCUS; OSTREOCOCCUS TAURI; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE STUDY; RED ALGA; SYMBIODINIUM; SYMBIONT; TRANSCRIPTOMICS; BIOLOGY; PHYSIOLOGY;

ACETABULARIA; ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; CYANIDIOSCHYZON MEROLAE; DINOPHYCEAE; EUGLENA GRACILIS; EUGLENOZOA; LINGULODINIUM POLYEDRUM; OSTREOCOCCUS TAURI; RHODOPHYTA; SYMBIODINIUM;

CHLOROPHYTA; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; COMPUTATIONAL BIOLOGY; DINOFLAGELLIDA; EUGLENA GRACILIS; RHODOPHYTA;

EID: 84922464567     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501089x     Document Type: Article

References (127)

1. Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F., and De Clerck, O. (2012) Phylogeny and Molecular Evolution of the Green Algae Crit. Rev. Plant Sci. 31, 1-46
2. Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G., and Bhattacharya, D. (2004) A molecular timeline for the origin of photosynthetic eukaryotes Mol. Biol. Evol. 21, 809-818
3. Keeling, P. J. (2010) The endosymbiotic origin, diversification and fate of plastids Philos. Trans. R. Soc., B 365, 729-748
4. Dodd, A. N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J. M., Millar, A. J., and Webb, A. A. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage Science 309, 630-633
5. Hastings, J. W. (2007) The Gonyaulax clock at 50: Translational control of circadian expression Cold Spring Harbor Symp. Quant. Biol. 72, 141-144
6. Mittag, M., Kiaulehn, S., and Johnson, C. H. (2005) The circadian clock in Chlamydomonas reinhardtii. What is it for? What is it similar to? Plant Physiol. 137, 399-409
7. McClung, C. R. (2006) Plant circadian rhythms Plant Cell 18, 792-803
8. Chow, B. Y. and Kay, S. A. (2013) Global approaches for telling time: Omics and the Arabidopsis circadian clock Semin. Cell Dev. Biol. 24, 383-392
9. McWatters, H. G. and Devlin, P. F. (2011) Timing in plants: A rhythmic arrangement FEBS Lett. 585, 1474-1484
10. Hsu, P. Y. and Harmer, S. L. (2014) Wheels within wheels: The plant circadian system Trends Plant Sci. 19, 240-249
11. Fogelmark, K. and Troein, C. (2014) Rethinking transcriptional activation in the Arabidopsis circadian clock PLoS Comput. Biol. 10, e1003705
12. Pokhilko, A., Fernandez, A. P., Edwards, K. D., Southern, M. M., Halliday, K. J., and Millar, A. J. (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops Mol. Syst. Biol. 8, 574
13. Nakajima, M., Imai, K., Ito, H., Nishiwaki, T., Murayama, Y., Iwasaki, H., Oyama, T., and Kondo, T. (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro Science 308, 414-415
14. Edgar, R. S., Green, E. W., Zhao, Y., van Ooijen, G., Olmedo, M., Qin, X., Xu, Y., Pan, M., Valekunja, U. K., Feeney, K. A., Maywood, E. S., Hastings, M. H., Baliga, N. S., Merrow, M., Millar, A. J., Johnson, C. H., Kyriacou, C. P., O'Neill, J. S., and Reddy, A. B. (2012) Peroxiredoxins are conserved markers of circadian rhythms Nature 485, 459-464
15. van Ooijen, G. and Millar, A. J. (2012) Non-transcriptional oscillators in circadian timekeeping Trends Biochem. Sci. 37, 484-492
16. Johnson, C. and Kondo, T. (2001) Circadian Rhythms in Unicellular Organisms. In Circadian Clocks (Takahashi, J., Turek, F., and Moore, R., Eds.) pp 61-77, Springer, Secaucus, NJ.
17. Hallick, R. B., Hong, L., Drager, R. G., Favreau, M. R., Monfort, A., Orsat, B., Spielmann, A., and Stutz, E. (1993) Complete sequence of Euglena gracilis chloroplast DNA Nucleic Acids Res. 21, 3537-3544
18. de Vries, J., Habicht, J., Woehle, C., Huang, C., Christa, G., Wagele, H., Nickelsen, J., Martin, W. F., and Gould, S. B. (2013) Is ftsH the key to plastid longevity in sacoglossan slugs? Genome Biol. Evol. 5, 2540-2548
19. Beauchemin, M., Roy, S., Daoust, P., Dagenais-Bellefeuille, S., Bertomeu, T., Letourneau, L., Lang, B. F., and Morse, D. (2012) Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic Proc. Natl. Acad. Sci. U.S.A. 109, 15793-15798
20. Hagiwara, S.-y., Bolige, A., Zhang, Y., Takahashi, M., Yamagishi, A., and Goto, K. (2002) Circadian Gating of Photoinduction of Commitment to Cell-cycle Transitions in Relation to Photoperiodic Control of Cell Reproduction in Euglena Photochem. Photobiol. 76, 105-115
21. Bolige, A., Hagiwara, S. Y., Zhang, Y., and Goto, K. (2005) Circadian G2 arrest as related to circadian gating of cell population growth in Euglena Plant Cell Physiol. 46, 931-936
22. Tong, J., Carre, I. A., and Edmunds, L. N. (1991) Circadian rhythmicity in the activities of adenylate cyclase and phosphodiesterase in synchronously dividing and stationary-phase cultures of the achlorophyllous ZC mutant of Euglena gracilis J. Cell Sci. 100, 365-369
23. Carre, I. A. and Edmunds, L. N. (1993) Oscillator control of cell division in Euglena: Cyclic AMP oscillations mediate the phasing of the cell division cycle by the circadian clock J. Cell Sci. 104, 1163-1173
24. Iseki, M., Matsunaga, S., Murakami, A., Ohno, K., Shiga, K., Yoshida, K., Sugai, M., Takahashi, T., Hori, T., and Watanabe, M. (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis Nature 415, 1047-1051
25. Schroder-Lang, S., Schwarzel, M., Seifert, R., Strunker, T., Kateriya, S., Looser, J., Watanabe, M., Kaupp, U. B., Hegemann, P., and Nagel, G. (2007) Fast manipulation of cellular cAMP level by light in vivo Nat. Methods 4, 39-42
26. Bolige, A. and Goto, K. (2007) High irradiance responses involving photoreversible multiple photoreceptors as related to photoperiodic induction of cell division in Euglena J. Photochem. Photobiol., B 86, 109-120
27. Sweeney, B. M. and Haxo, F. T. (1961) Persistence of a Photosynthetic Rhythm in Enucleated Acetabularia Science 134, 1361-1363
28. Mergenhagen, D. and Schweiger, H. G. (1975) The effect of different inhibitors of transcription and translation on the expression and control of circadian rhythm in individual cells of Acetabularia Exp. Cell Res. 94, 321-326
29. Kloppstech, K. and Schweiger, H. G. (1982) Stability of poly(A)(+)RNA in nucleate and anucleate cells of Acetabularia Plant Cell Rep. 1, 165-167
30. Mandoli, D. F. (1998) What ever happened to Acetabularia ? Bringing a once-classic model system into the age of molecular genetics Int. Rev. Cytol. 182, 1-67
31. Neuhaus, G., Neuhausurl, G., Degroot, E. J., and Schweiger, H. G. (1986) High-Yield and Stable Transformation of the Unicellular Green-Alga Acetabularia by Microinjection of Sv40 DNA and Psv2neo EMBO J. 5, 1437-1444
32. Driessche, T. V., Vries, G. M. P.-d., and Guisset, J.-L. (1997) Tansley Review No. 91 Differentiation, Growth and Morphogenesis: Acetabularia as a Model System New Phytol. 135, 1-20
33. Schweiger, E., Wallraff, H. G., and Schweiger, H. G. (1964) Endogenous Circadian Rhythm in Cytoplasm of Acetabularia: Influence of the Nucleus Science 146, 658-659
34. Koop, H. U., Schmid, R., Heunert, H. H., and Milthaler, B. (1978) Chloroplast Migration: New Circadian-Rhythm in Acetabularia Protoplasma 97, 301-310
35. Woolum, J. C. (1991) A re-examination of the role of the nucleus in generating the circadian rhythm in Acetabularia J. Biol. Rhythms 6, 129-136
36. Grote, M., Engelhard, M., and Hegemann, P. (2014) Of ion pumps, sensors and channels: Perspectives on microbial rhodopsins between science and history Biochim. Biophys. Acta 1837, 533-545
37. +-pumping rhodopsin from the marine alga Acetabularia Biophys. J. 91, 1471-1479
38. Wada, T., Shimono, K., Kikukawa, T., Hato, M., Shinya, N., Kim, S. Y., Kimura-Someya, T., Shirouzu, M., Tamogami, J., Miyauchi, S., Jung, K. H., Kamo, N., and Yokoyama, S. (2011) Crystal structure of the eukaryotic light-driven proton-pumping rhodopsin, Acetabularia rhodopsin II, from marine alga J. Mol. Biol. 411, 986-998
39. Njus, D., Mcmurry, L., and Hastings, J. W. (1977) Conditionality of Circadian Rhythmicity: Synergistic Action of Light and Temperature J. Comp. Physiol. 117, 335-344
40. Hastings, J. W. and Sweeney, B. M. (1957) On the Mechanism of Temperature Independence in a Biological Clock Proc. Natl. Acad. Sci. U.S.A. 43, 804-811
41. Roenneberg, T., Nakamura, H., Cranmer, L. D., Ryan, K., Kishi, Y., and Hastings, J. W. (1991) Gonyauline: A Novel Endogenous Substance Shortening the Period of the Circadian Clock of a Unicellular Alga Experientia 47, 103-106
42. Roenneberg, T., Nakamura, H., and Hastings, J. W. (1988) Creatine Accelerates the Circadian Clock in a Unicellular Alga Nature 334, 432-434
43. Nassoury, N., Morse, D., and Hastings, J. W. (2005) The mechanism of the Gonyaulax (Lingulodinium) circadian clock: Input and output, Landes Bioscience/Eurekah, Georgetown, TX.
44. Hardeland, R. and Poeggeler, B. (2003) Non-vertebrate melatonin J. Pineal Res. 34, 233-241
45. Roenneberg, T. and Morse, D. (1993) 2 Circadian Oscillators in One Cell Nature 362, 362-364
46. Morse, D., Hastings, J. W., and Roenneberg, T. (1994) Different Phase Responses of the 2 Circadian Oscillators in Gonyaulax J. Biol. Rhythms 9, 263-274
47. Roenneberg, T. and Hastings, J. W. (1988) 2 Photoreceptors Control the Circadian Clock of a Unicellular Alga Naturwissenschaften 75, 206-207
48. Bruce, V. G. (1970) Biological Clock in Chlamydomonas reinhardtii J. Protozool. 17, 328-334
49. Bruce, V. G. (1972) Mutants of the biological clock in Chlamydomonas reinhardtii Genetics 70, 537-548
50. Bruce, V. G. (1974) Recombinants between clock mutants of Chlamydomonas reinhardtii Genetics 77, 221-230
51. Mergenhagen, D. and Mergenhagen, E. (1987) The biological clock of Chlamydomonas reinhardtii in space Eur. J. Cell Biol. 43, 203-207
52. Byrne, T. E., Wells, M. R., and Johnson, C. H. (1992) Circadian rhythms of chemotaxis to ammonium and of methylammonium uptake in Chlamydomonas Plant Physiol. 98, 879-886
53. Goto, K. and Johnson, C. H. (1995) Is the cell division cycle gated by a circadian clock? The case of Chlamydomonas reinhardtii J. Cell Biol. 129, 1061-1069
54. Nikaido, S. S. and Johnson, C. H. (2000) Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii Photochem. Photobiol. 71, 758-765
55. Pittendrigh, C. S. (1993) Temporal organization: Reflections of a Darwinian clock-watcher Annu. Rev. Physiol. 55, 16-54
56. Hastings, J. W. (2001) Cellular and Molecular Mechanisms of Circadian Regulation in the Unicellular Dinoflagellate Gonyaulax polyedra. In Circadian Clocks (Takahashi, J., Turek, F., and Moore, R., Eds.) pp 321-334, Springer, Secaucus, NJ.
57. Morse, D., Milos, P. M., Roux, E., and Hastings, J. W. (1989) Circadian regulation of bioluminescence in Gonyaulax involves translational control Proc. Natl. Acad. Sci. U.S.A. 86, 172-176
58. Fagan, T., Morse, D., and Hastings, J. W. (1999) Circadian synthesis of a nuclear-encoded chloroplast glyceraldehyde-3-phosphate dehydrogenase in the dinoflagellate Gonyaulax polyedra is translationally controlled Biochemistry 38, 7689-7695
59. Milos, P., Morse, D., and Hastings, J. W. (1990) Circadian control over synthesis of many Gonyaulax proteins is at a translational level Naturwissenschaften 77, 87-89
60. Mittag, M., Lee, D. H., and Hastings, J. W. (1994) Circadian Expression of the Luciferin-Binding Protein Correlates with the Binding of a Protein to the 3′ Untranslated Region of Its Messenger RNA Proc. Natl. Acad. Sci. U.S.A. 91, 5257-5261
61. Liu, B., Lo, S. C., Matton, D. P., Lang, B. F., and Morse, D. (2012) Daily changes in the phosphoproteome of the dinoflagellate Lingulodinium Protist 163, 746-754
62. Mittag, M. (1996) Conserved circadian elements in phylogenetically diverse algae Proc. Natl. Acad. Sci. U.S.A. 93, 14401-14404
63. Iliev, D., Voytsekh, O., Schmidt, E. M., Fiedler, M., Nykytenko, A., and Mittag, M. (2006) A heteromeric RNA-binding protein is involved in maintaining acrophase and period of the circadian clock Plant Physiol. 142, 797-806
64. Voytsekh, O., Seitz, S. B., Iliev, D., and Mittag, M. (2008) Both Subunits of the circadian RNA-binding protein CHLAMY1 can integrate temperature information Plant Physiol. 147, 2179-2193
65. Seitz, S. B., Weisheit, W., and Mittag, M. (2010) Multiple Roles and Interaction Factors of an E-Box Element in Chlamydomonas reinhardtii Plant Physiol. 152, 2243-2257
66. Dathe, H., Prager, K., and Mittag, M. (2012) Novel interaction of two clock-relevant RNA-binding proteins C3 and XRN1 in Chlamydomonas reinhardtii FEBS Lett. 586, 3969-3973
67. Matsuo, T., Okamoto, K., Onai, K., Niwa, Y., Shimogawara, K., and Ishiura, M. (2008) A systematic forward genetic analysis identified components of the Chlamydomonas circadian system Genes Dev. 22, 918-930
68. Brunner, M. and Merrow, M. (2008) The green yeast uses its plant-like clock to regulate its animal-like tail Genes Dev. 22, 825-831
69. Corellou, F., Schwartz, C., Motta, J. P., Djouani-Tahri el, B., Sanchez, F., and Bouget, F. Y. (2009) Clocks in the green lineage: Comparative functional analysis of the circadian architecture of the picoeukaryote Ostreococcus Plant Cell 21, 3436-3449
70. Matsuo, T., Iida, T., and Ishiura, M. (2012) N-terminal acetyltransferase 3 gene is essential for robust circadian rhythm of bioluminescence reporter in Chlamydomonas reinhardtii Biochem. Biophys. Res. Commun. 418, 342-346
71. Cashmore, A. R., Jarillo, J. A., Wu, Y. J., and Liu, D. M. (1999) Cryptochromes: Blue light receptors for plants and animals Science 284, 760-765
72. Beel, B., Prager, K., Spexard, M., Sasso, S., Weiss, D., Muller, N., Heinnickel, M., Dewez, D., Ikoma, D., Grossman, A. R., Kottke, T., and Mittag, M. (2012) A Flavin Binding Cryptochrome Photoreceptor Responds to Both Blue and Red Light in Chlamydomonas reinhardtii Plant Cell 24, 2992-3008
73. Okajima, K., Aihara, Y., Takayama, Y., Nakajima, M., Kashojiya, S., Hikima, T., Oroguchi, T., Kobayashi, A., Sekiguchi, Y., Yamamoto, M., Suzuki, T., Nagatani, A., Nakasako, M., and Tokutomi, S. (2014) Light-induced Conformational Changes of LOV1 (Light Oxygen Voltage-sensing Domain 1) and LOV2 Relative to the Kinase Domain and Regulation of Kinase Activity in Chlamydomonas Phototropin J. Biol. Chem. 289, 413-422
74. Millar, A. J. (2003) Suite of photoreceptors entrains the plant circadian clock J. Biol. Rhythms 18, 217-226
75. Suetsugu, N. and Wada, M. (2013) Evolution of three LOV blue light receptor families in green plants and photosynthetic stramenopiles: Phototropin, ZTL/FKF1/LKP2 and aureochrome Plant Cell Physiol. 54, 8-23
76. Niwa, Y., Matsuo, T., Onai, K., Kato, D., Tachikawa, M., and Ishiura, M. (2013) Phase-resetting mechanism of the circadian clock in Chlamydomonas reinhardtii Proc. Natl. Acad. Sci. U.S.A. 110, 13666-13671
77. Reisdorph, N. A. and Small, G. D. (2004) The CPH1 gene of Chlamydomonas reinhardtii encodes two forms of cryptochrome whose levels are controlled by light-induced proteolysis Plant Physiol. 134, 1546-1554
78. Forbes-Stovall, J., Howton, J., Young, M., Davis, G., Chandler, T., Kessler, B., Rinehart, C. A., and Jacobshagen, S. (2014) Chlamydomonas reinhardtii strain CC-124 is highly sensitive to blue light in addition to green and red light in resetting its circadiari clock, with the blue-light photoreceptor plant cryptochrome likely acting as negative modulator Plant Physiol. Biochem. 75, 14-23
79. Schmidt, M., Gessner, G., Matthias, L., Heiland, I., Wagner, V., Kaminski, M., Geimer, S., Eitzinger, N., Reissenweber, T., Voytsekh, O., Fiedler, M., Mittag, M., and Kreimer, G. (2006) Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements Plant Cell 18, 1908-1930
80. Boesger, J., Wagner, V., Weisheit, W., and Mittag, M. (2012) Application of phosphoproteomics to find targets of casein kinase 1 in the flagellum of Chlamydomonas Int. J. Plant Genomics 2012, 581460
81. O'Neill, J. S., van Ooijen, G., Dixon, L. E., Troein, C., Corellou, F., Bouget, F. Y., Reddy, A. B., and Millar, A. J. (2011) Circadian rhythms persist without transcription in a eukaryote Nature 469, 554-558
82. Filonova, A., Haemsch, P., Gebauer, C., Weisheit, W., and Wagner, V. (2013) Protein Disulfide Isomerase 2 of Chlamydomonas reinhardtii Is Involved in Circadian Rhythm Regulation Mol. Plant 6, 1503-1517
83. Merchant, S. S., Prochnik, S. E., Vallon, O., Harris, E. H., Karpowicz, S. J., Witman, G. B., Terry, A., Salamov, A., Fritz-Laylin, L. K., Marechal-Drouard, L., Marshall, W. F., Qu, L. H., Nelson, D. R., Sanderfoot, A. A., Spalding, M. H., Kapitonov, V. V., Ren, Q., Ferris, P., Lindquist, E., Shapiro, H., Lucas, S. M., Grimwood, J., Schmutz, J., Cardol, P., Cerutti, H., Chanfreau, G., Chen, C. L., Cognat, V., Croft, M. T., Dent, R., Dutcher, S., Fernandez, E., Fukuzawa, H., Gonzalez-Ballester, D., Gonzalez-Halphen, D., Hallmann, A., Hanikenne, M., Hippler, M., Inwood, W., Jabbari, K., Kalanon, M., Kuras, R., Lefebvre, P. A., Lemaire, S. D., Lobanov, A. V., Lohr, M., Manuell, A., Meier, I., Mets, L., Mittag, M., Mittelmeier, T., Moroney, J. V., Moseley, J., Napoli, C., Nedelcu, A. M., Niyogi, K., Novoselov, S. V., Paulsen, I. T., Pazour, G., Purton, S., Ral, J. P., Riano-Pachon, D. M., Riekhof, W., Rymarquis, L., Schroda, M., Stern, D., Umen, J., Willows, R., Wilson, N., Zimmer, S. L., Allmer, J., Balk, J., Bisova, K., Chen, C. J., Elias, M., Gendler, K., Hauser, C., Lamb, M. R., Ledford, H., Long, J. C., Minagawa, J., Page, M. D., Pan, J., Pootakham, W., Roje, S., Rose, A., Stahlberg, E., Terauchi, A. M., Yang, P., Ball, S., Bowler, C., Dieckmann, C. L., Gladyshev, V. N., Green, P., Jorgensen, R., Mayfield, S., Mueller-Roeber, B., Rajamani, S., Sayre, R. T., Brokstein, P., Dubchak, I., Goodstein, D., Hornick, L., Huang, Y. W., Jhaveri, J., Luo, Y., Martinez, D., Ngau, W. C., Otillar, B., Poliakov, A., Porter, A., Szajkowski, L., Werner, G., Zhou, K., Grigoriev, I. V., Rokhsar, D. S., and Grossman, A. R. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions Science 318, 245-250
84. Van Damme, T., Blancquaert, D., Couturon, P., Van Der Straeten, D., Sandra, P., and Lynen, F. (2014) Wounding stress causes rapid increase in concentration of the naturally occurring 2′,3′-isomers of cyclic guanosine- and cyclic adenosine monophosphate (cGMP and cAMP) in plant tissues Phytochemistry 103, 59-66
85. O'Neill, J. S., Maywood, E. S., and Hastings, M. H. (2013) Cellular mechanisms of circadian pacemaking: Beyond transcriptional loops Handb. Exp. Pharmacol. 67-103
86. Schauble, S., Heiland, I., Voytsekh, O., Mittag, M., and Schuster, S. (2011) Predicting the physiological role of circadian metabolic regulation in the green alga Chlamydomonas reinhardtii PLoS One 6, e23026
87. Toepel, J., Albaum, S. P., Arvidsson, S., Goesmann, A., la Russa, M., Rogge, K., and Kruse, O. (2011) Construction and evaluation of a whole genome microarray of Chlamydomonas reinhardtii BMC Genomics 12, 579
88. Bolling, C. and Fiehn, O. (2005) Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation Plant Physiol. 139, 1995-2005
89. Courties, C., Vaquer, A., Troussellier, M., Lautier, J., Chretiennotdinet, M. J., Neveux, J., Machado, C., and Claustre, H. (1994) Smallest Eukaryotic Organism Nature 370, 255
90. Palenik, B., Grimwood, J., Aerts, A., Rouze, P., Salamov, A., Putnam, N., Dupont, C., Jorgensen, R., Derelle, E., Rombauts, S., Zhou, K. M., Otillar, R., Merchant, S. S., Podell, S., Gaasterland, T., Napoli, C., Gendler, K., Manuell, A., Tai, V., Vallon, O., Piganeau, G., Jancek, S., Heijde, M., Jabbari, K., Bowler, C., Lohr, M., Robbens, S., Werner, G., Dubchak, I., Pazour, G. J., Ren, Q. H., Paulsen, I., Delwiche, C., Schmutz, J., Rokhsar, D., Van de Peer, Y., Moreau, H., and Grigoriev, I. V. (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation Proc. Natl. Acad. Sci. U.S.A. 104, 7705-7710
91. Monnier, A., Liverani, S., Bouvet, R., Jesson, B., Smith, J. Q., Mosser, J., Corellou, F., and Bouget, F. Y. (2010) Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles BMC Genomics 11, 192
92. Moulager, M., Monnier, A., Jesson, B., Bouvet, R., Mosser, J., Schwartz, C., Garnier, L., Corellou, F., and Bouget, F. Y. (2007) Light-dependent regulation of cell division in Ostreococcus: Evidence for a major transcriptional input Plant Physiol. 144, 1360-1369
93. Farinas, B., Mary, C., de O Manes, C. L., Bhaud, Y., Peaucellier, G., and Moreau, H. (2006) Natural Synchronisation for the Study of Cell Division in the Green Unicellular Alga Ostreococcus tauri Plant Mol. Biol. 60, 277-292
94. van Ooijen, G., Knox, K., Kis, K., Bouget, F. Y., and Millar, A. J. (2012) Genomic transformation of the picoeukaryote Ostreococcus tauri J. Visualized Exp. e4074
95. Lozano, J. C., Schatt, P., Botebol, H., Verge, V., Lesuisse, E., Blain, S., Carre, I. A., and Bouget, F. Y. (2014) Efficient gene targeting and removal of foreign DNA by homologous recombination in the picoeukaryote Ostreococcus Plant J. 78, 1073-1083
96. Djouani-Tahri el, B., Sanchez, F., Lozano, J. C., and Bouget, F. Y. (2011) A phosphate-regulated promoter for fine-tuned and reversible overexpression in Ostreococcus: Application to circadian clock functional analysis PLoS One 6, e28471
97. Le Bihan, T., Martin, S. F., Chirnside, E. S., van Ooijen, G., Barrios-Llerena, M. E., O'Neill, J. S., Shliaha, P. V., Kerr, L. E., and Millar, A. J. (2011) Shotgun proteomic analysis of the unicellular alga Ostreococcus tauri J. Proteomics 74, 2060-2070
98. 15N metabolic labeling mass spectrometry J. Proteome Res. 11, 476-486
99. Djouani-Tahri el, B., Motta, J. P., Bouget, F. Y., and Corellou, F. (2010) Insights into the regulation of the core clock component TOC1 in the green picoeukaryote Ostreococcus Plant Signaling Behav. 5, 332-335
100. van Ooijen, G., Dixon, L. E., Troein, C., and Millar, A. J. (2011) Proteasome function is required for biological timing throughout the twenty-four hour cycle Curr. Biol. 21, 869-875
101. Djouani-Tahri el, B., Christie, J. M., Sanchez-Ferandin, S., Sanchez, F., Bouget, F. Y., and Corellou, F. (2011) A eukaryotic LOV-histidine kinase with circadian clock function in the picoalga Ostreococcus Plant J. 65, 578-588
102. Heijde, M., Zabulon, G., Corellou, F., Ishikawa, T., Brazard, J., Usman, A., Sanchez, F., Plaza, P., Martin, M., Falciatore, A., Todo, T., Bouget, F. Y., and Bowler, C. (2010) Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes Plant, Cell Environ. 33, 1614-1626
103. Bouget, F. Y., Lefranc, M., Thommen, Q., Pfeuty, B., Lozano, J. C., Schatt, P., Botebol, H., and Verge, V. (2014) Transcriptional versus non-transcriptional clocks: A case study in Ostreococcus Mar. Genomics 14C, 17-22
104. Hindle, M. M., Martin, S. F., Noordally, Z. B., van Ooijen, G., Barrios-Llerena, M. E., Simpson, T. I., Le Bihan, T., and Millar, A. J. (2014) The reduced kinome of Ostreococcus tauri: Core eukaryotic signalling components in a tractable model species BMC Genomics 15, 640
105. van Ooijen, G., Hindle, M., Martin, S. F., Barrios-Llerena, M., Sanchez, F., Bouget, F. Y., O'Neill, J. S., Le Bihan, T., and Millar, A. J. (2013) Functional Analysis of Casein Kinase 1 in a Minimal Circadian System PLoS One 8, e70021
106. van Ooijen, G., Martin, S. F., Barrios-Llerena, M. E., Hindle, M., Le Bihan, T., O'Neill, J. S., and Millar, A. J. (2013) Functional analysis of the rodent CK1(tau) mutation in the circadian clock of a marine unicellular alga BMC Cell Biol. 14, 46
107. Ocone, A., Millar, A. J., and Sanguinetti, G. (2013) Hybrid regulatory models: A statistically tractable approach to model regulatory network dynamics Bioinformatics 29, 910-916
108. Thommen, Q., Pfeuty, B., Corellou, F., Bouget, F. Y., and Lefranc, M. (2012) Robust and flexible response of the Ostreococcus tauri circadian clock to light/dark cycles of varying photoperiod FEBS J. 279, 3432-3448
109. Troein, C., Corellou, F., Dixon, L. E., van Ooijen, G., O'Neill, J. S., Bouget, F. Y., and Millar, A. J. (2011) Multiple light inputs to a simple clock circuit allow complex biological rhythms Plant J. 66, 375-385
110. Gendron, J. M., Pruneda-Paz, J. L., Doherty, C. J., Gross, A. M., Kang, S. E., and Kay, S. A. (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor Proc. Natl. Acad. Sci. U.S.A. 109, 3167-3172
111. Rand, D. A., Shulgin, B. V., Salazar, J. D., and Millar, A. J. (2006) Uncovering the design principles of circadian clocks: Mathematical analysis of flexibility and evolutionary goals J. Theor. Biol. 238, 616-635
112. Dixon, L. E., Hodge, S. K., van Ooijen, G., Troein, C., Akman, O. E., and Millar, A. J. (2014) Light and circadian regulation of clock components aids flexible responses to environmental signals New Phytol. 203, 568-577
113. Dodd, A. N., Dalchau, N., Gardner, M. J., Baek, S. J., and Webb, A. A. (2014) The circadian clock has transient plasticity of period and is required for timing of nocturnal processes in Arabidopsis New Phytol. 201, 168-179
114. Schaum, E., Rost, B., Millar, A. J., and Collins, S. (2013) Variation in plastic responses of a globally distributed picoplankton species to ocean acidification Nat. Clim. Change 3, 298-302
115. Imoto, Y., Yoshida, Y., Yagisawa, F., Kuroiwa, H., and Kuroiwa, T. (2011) The cell cycle, including the mitotic cycle and organelle division cycles, as revealed by cytological observations J. Electron Microsc. 60 (Suppl. 1) S117-S136
116. Miyagishima, S. Y., Fujiwara, T., Sumiya, N., Hirooka, S., Nakano, A., Kabeya, Y., and Nakamura, M. (2014) Translation-independent circadian control of the cell cycle in a unicellular photosynthetic eukaryote Nat. Commun. 5, 3807
117. Asimgil, H. and Kavakli, I. H. (2012) Purification and characterization of five members of photolyase/cryptochrome family from Cyanidioschyzon merolae Plant Sci. 185-186, 190-198
118. Kanesaki, Y., Imamura, S., Minoda, A., and Tanaka, K. (2012) External light conditions and internal cell cycle phases coordinate accumulation of chloroplast and mitochondrial transcripts in the red alga Cyanidioschyzon merolae DNA Res. 19, 289-303
119. Noordally, Z. B., Ishii, K., Atkins, K. A., Wetherill, S. J., Kusakina, J., Walton, E. J., Kato, M., Azuma, M., Tanaka, K., Hanaoka, M., and Dodd, A. N. (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal Science 339, 1316-1319
120. Sorek, M., Diaz-Almeyda, E. M., Medina, M., and Levy, O. (2014) Circadian clocks in symbiotic corals: The duet between Symbiodinium algae and their coral host Mar. Genomics 14, 47-57
121. Fitt, W. K. and Trench, R. K. (1983) The Relation of Diel Patterns of Cell-Division to Diel Patterns of Motility in the Symbiotic Dinoflagellate Symbiodinium microadriaticum Freudenthal in Culture New Phytol. 94, 421-432
122. Sorek, M., Yacobi, Y. Z., Roopin, M., Berman-Frank, I., and Levy, O. (2013) Photosynthetic circadian rhythmicity patterns of Symbiodinium, [corrected] the coral endosymbiotic algae Proc. R. Soc. B 280, 20122942
123. Sorek, M. and Levy, O. (2012) Influence of the quantity and quality of light on photosynthetic periodicity in coral endosymbiotic algae PLoS One 7, e43264
124. Levy, O., Kaniewska, P., Alon, S., Eisenberg, E., Karako-Lampert, S., Bay, L. K., Reef, R., Rodriguez-Lanetty, M., Miller, D. J., and Hoegh-Guldberg, O. (2011) Complex diel cycles of gene expression in coral-algal symbiosis Science 331, 175
125. Cardozo, K. H., Guaratini, T., Barros, M. P., Falcao, V. R., Tonon, A. P., Lopes, N. P., Campos, S., Torres, M. A., Souza, A. O., Colepicolo, P., and Pinto, E. (2007) Metabolites from algae with economical impact Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 146, 60-78
126. Okamoto, O. K. and Hastings, J. W. (2003) Genome-wide analysis of redox-regulated genes in a dinoflagellate Gene 321, 73-81
127. Van Dolah, F. M., Lidie, K. B., Morey, J. S., Brunelle, S. A., Ryan, J. C., Monroe, E. A., and Haynes, B. L. (2007) Microarray analysis of diurnal- and circadian-regulated genes in the Florida red-tide dinoflagellate Karenia brevis (Dinophyceae) J. Phycol. 43, 741-752