Circadian photosynthetic reductant flow in the dinoflagellate Lingulodinium is limited by carbon availability

Plant, Cell and Environment

Volumn 34, Issue 4, 2011, Pages 669-680

  Mackenzie, Tyler D B ^a   Morse, David ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Carbon limitation; Circadian rhythm; Dinoflagellate; Photosynthesis

Indexed keywords

CARBON DIOXIDE; NITRATE; OXYGEN; REDUCING AGENT;

ADAPTATION; BIOCHEMICAL COMPOSITION; CARBON; CIRCADIAN RHYTHM; DINOFLAGELLATE; ELECTRON; NUTRIENT AVAILABILITY; NUTRIENT LIMITATION; OXYGEN; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; SELECTION;

ARTICLE; BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; DINOFLAGELLATE; ELECTRON TRANSPORT; METABOLISM; PHOTOPERIODICITY; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY;

BIOLOGICAL CLOCKS; CARBON DIOXIDE; CIRCADIAN RHYTHM; DINOFLAGELLIDA; ELECTRON TRANSPORT; NITRATES; OXYGEN; PHOTOPERIOD; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; REDUCING AGENTS;

DINOPHYCEAE; LINGULODINIUM;

EID: 79952494522     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02271.x     Document Type: Article

References (47)

1. Akimoto H., Wu C., Kinumi T. & Ohmiya Y. (2004) Biological rhythmicity in expressed proteins of the marine dinoflagellate Lingulodinium polyedrum demonstrated by chronological proteomics. Biochemical and Biophysical Research Communications 315, 306-312.
2. Bush K.J. & Sweeney B.M. (1972) The activity of ribulose diphosphate carboxylase in extracts of Gonyaulax polyedra in the day and the night phases of the circadian rhythm of photosynthesis. Plant Physiology 50, 446-451.
3. Caldeira K. & Wickett M.E. (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365.
4. Dagenais-Bellefeuille S., Bertomeu T. & Morse D. (2008) S-phase and M-phase timing are under independent circadian control in the dinoflagellate Lingulodinium. Journal of Biological Rhythms 23, 400-408.
5. Eisensamer B. & Roenneberg T. (2004) Extracellular pH is under circadian control in Gonyaulax polyedra and forms a metabolic feedback loop. Chronobiology International 21, 27-41.
6. Field C.B., Behrenfeld M.J., Randerson J.T. & Falkowski P. (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240.
7. Fritz L., Morse D. & Hastings J.W. (1990) The circadian bioluminescence rhythm of Gonyaulax is related to daily variations in the number of light-emitting organelles. Journal of Cell Science 95, 321-328.
8. Fritz L., Stringher C.G. & Colepicolo P. (1996) Imaging oscillations in Gonyaulax: a chloroplast rhythm of nitrate reductase visualized by immunocytochemistry. Brazilian Journal of Medical and Biological Research 29, 111-117.
9. Genty B., Briantais J.M. & Baker N. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87-92.
10. Giordano M., Beardall J. & Raven J.A. (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56, 99-131.
11. Glibert P.M., Anderson D.M., Gentien P., Granéli E. & Sellner K. (2005) The global, complex phenomena of harmful algal blooms. Oceanography 18, 132-141.
12. Hackett J.D., Yoon H.S., Soares M.B., Bonaldo M.F., Casavant T.L., Scheetz T.E., Nosenko T. & Bhattacharya D. (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Current Biology 14, 213-218.
13. Hastings J.W. (2007) The Gonyaulax clock at 50: translational control of circadian expression. Cold Spring Harbor Symposia on Quantitative Biology 72, 141-144.
14. Hastings J.W., Astrachan L. & Sweeney B.M. (1961) A persistent daily rhythm in photosynthesis. The Journal of General Physiology 45, 69-76.
15. Herman E.M. & Sweeney B.M. (1975) Circadian rhythm of chloroplast ultrastructure in Gonyaulax polyedra, concentric organization around a central cluster of ribosomes. Journal of Ultrastructure Research 50, 347-354.
16. Hinga K.R. (1992) Co-occurrence of dinoflagellate blooms and high pH in marine enclosures. Marine Ecology Progress Series 86, 181-187.
17. Hoegh-Guldberg O., Mumby P.J., Hooten A.J., etal. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742.
18. Hofmann E., Wrench P.M., Sharples F.P., Hiller R.G., Welte W. & Diederichs K. (1996) Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 272, 1788-1791.
19. Hollnagel H.C., Pinto E., Morse D. & Colepicolo P. (2002) The oscillation of photosynthetic capacity in Gonyaulax polyedra is not related to differences in Rubisco, peridinin or chlorophyll a amounts. Biological Rhythms Research 33, 443-458.
20. Jeffrey S., Seilicki M. & Haxo F. (1975) Chloroplast pigment patterns in dinoflagellates. Journal of Phycology 11, 374-384.
21. Johnson C.H., Roeber J.F. & Hastings J.W. (1984) Circadian changes in enzyme concentration account for rhythm of enzyme activity in Gonyaulax. Science 223, 1428-1430.
22. Keeling P.J. (2010) The endosymbiotic origin, diversification and fate of plastids. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 729-748.
23. Koivuniemi A., Aro E.M. & Andersson B. (1995) Degradation of the D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34, 16022-16029.
24. Lapointe M., MacKenzie T. & Morse D. (2008) An external delta-carbonic anhydrase in a free living marine dinoflagellate may circumvent diffusion limited carbon acquisition. Plant Physiology 147, 1427-1436.
25. Le Q., Jovine R., Markovic P. & Morse D. (2001) PCP is not implicated in the photosynthesis rhythm of Gonyaulax despite circadian regulation of its translation. Biological Rhythms Research 32, 579-594.
26. Markovic P., Roenneberg T. & Morse D. (1996) Phased protein synthesis at several circadian times does not change protein levels in Gonyaulax. Journal of Biological Rhythms 11, 57-67.
27. Morgan D.O. (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annual Review of Cell and Developmental Biology 13, 261-291.
28. Morse D., Milos P.M., Roux E. & Hastings J.W. (1989) Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proceedings of the National Academy of Sciences of the United States of America 86, 172-176.
29. Morse D., Salois P., Markovic P. & Hastings J.W. (1995) A nuclear encoded form II rubisco in dinoflagellates. Science 268, 1622-1624.
30. Nassoury N., Fritz L. & Morse D. (2001) Circadian changes in ribulose-1, 5-bisphosphate carboxylase/oxygenase distribution inside individual chloroplasts can account for the rhythm in dinoflagellate carbon fixation. The Plant Cell 13, 923-934.
31. Nassoury N., Cappadocia M. & Morse D. (2003) Plastid ultrastructure defines the protein import pathway in dinoflagellates. Journal of Cell Science 116, 2867-2874.
32. Nassoury N., Wang Y. & Morse D. (2005) Brefeldin a inhibits circadian remodeling of chloroplast structure in the dinoflagellate gonyaulax. Traffic 6, 548-561.
33. Nimer N.A., Brownlee C. & Merrett M.J. (1999) Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiology 120, 105-112.
34. Prezelin B. (1987) Photosynthetic physiology of dinoflagellates. In The Biology of Dinoflagellates (ed. F.J.R. Taylor) pp. 174-223. Blackwell Scientific publication, Oxford, England.
35. Prezelin B. & Haxo F. (1976) Purification and characterization of peridinin-chlorophyll a-proteins from the marine dinoflagellates Glenodinium and Gonyaulax. Planta 130, 251-256.
36. Ramalho C.B., Hastings J.W. & Colepicolo P. (1995) Circadian oscillation of nitrate reductase activity in Gonyaulax polyedra is due to changes in cellular protein levels. Plant Physiology 107, 225-231.
37. Roenneberg T. & Morse D. (1993) Two circadian clocks in a single cell. Nature 362, 362-364.
38. Roenneberg T. & Merrow M. (1998) Molecular circadian oscillators: an alternative hypothesis. Journal of Biological Rhythms 13, 167-179.
39. Roenneberg T., Colfax G.N. & Hastings J.W. (1989) A circadian rhythm of population behavior in Gonyaulax polyedra. Journal of Biological Rhythms 4, 201-216.
40. Rowan R., Whitney S.M., Fowler A. & Yellowlees D. (1996) Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. The Plant Cell 8, 539-553.
41. Samuelsson G., Sweeney B.M., Matlick H.A. & Prezelin B.B. (1983) Changes in photosystem II account for the circadian rhythm in photosynthesis in Gonyaulax polyedra. Plant Physiology 73, 329-331.
42. Schmitter R. (1971) The fine structure of Gonyaulax polyedra, a bioluminescent marine dinoflagellate. Journal of Cell Science 9, 147-173.
43. Sukenik A., Bennett J. & Falkowski P.G. (1987) Light-saturated photosynthesis-limitation by electron transport or carbon fixation? Biochimica et Biophysica Acta 891, 205-215.
44. Sweeney B.M. (1960) The photosynthetic rhythm in single cells of Gonyaulax polyedra. Cold Spring Harbor Symposia on Quantitative Biology 25, 145-148.
45. Wang Y. & Morse D. (2006) Rampant polyuridylylation of plastid gene transcripts in the dinoflagellate Lingulodinium. Nucleic Acids Research 34, 613-619.
46. Wang Y., Jensen L., Hojrup P. & Morse D. (2005) Synthesis and degradation of dinoflagellate plastid-encoded psbA proteins are light-regulated, not circadian-regulated. Proceedings of the National Academy of Sciences of the United States of America 102, 2844-2849.
47. Zhang Z., Green B.R. & Cavalier-Smith T. (1999) Single gene circles in dinoflagellate chloroplast genomes. Nature 400, 155-159.