UVB effects on the photosystem II-D1 protein of phytoplankton and natural phytoplankton communities

Photochemistry and Photobiology

Volumn 82, Issue 4, 2006, Pages 936-951

  Bouchard, Josée Nina ^a   Roy, Suzanne ^a   Campbell, Douglas A ^b  

^a INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^b MOUNT ALLISON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPLAST; CYANOBACTERIUM; DOWN REGULATION; ECOSYSTEM; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYTOPLANKTON; PROTEIN BINDING; RADIATION EXPOSURE; REVIEW; ULTRAVIOLET RADIATION;

CHLOROPLASTS; CYANOBACTERIA; DOWN-REGULATION; ECOSYSTEM; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PHYTOPLANKTON; PROTEIN BINDING; ULTRAVIOLET RAYS;

CYANOBACTERIA;

EID: 33748999562     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1562/2005-08-31-IR-666     Document Type: Review

References (161)

1. Strid, Å., W. S. Chow and J. M. Anderson (1990) Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochim. Biophys. Acta 1020, 260-268.
2. Melis, A., J. A. Nemson and M. A. Harrison (1992) Damage to the functional components and partial degradation of photosystem II reaction center proteins upon chloroplast exposure to ultraviolet-B radiation. Biochim. Biophys. Acta 1100, 312-320.
3. Vu, C. V., L. H. Allen and L. A. Garrard (1984) Effects of UV-B radiation (280-320 nm) on ribulose-1,5-bisphosphate carboxylase in pea and soybean. Env. Exp. Bot. 24, 131-143.
4. Bischof, K., G. Kräbs, C. Wiencke and D. Hanelt (2002) Solar ultraviolet radiation affects the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta, 215, 502-509.
5. DeLucia, E. H., T. A. Day and T. C. Vogelmann (1992) Ultraviolet-B and visible light penetration into needles of two species of subalpine conifers during foliar development. Plant Cell Env. 15, 921-929.
6. Huang, L., M. P. McCluskey, H. Ni and R. A. LaRossa (2002) Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J. Bacteriol. 184, 6845-6858.
7. Jansen, M. A. K., V. Gaba and B. Greenberg (1998) Higher plants and UV-B radiation: Balancing damage, repair and acclimation. Trends Plant Sci. 3, 131-135.
8. Mohovic, B., S. M. F. Gianesella, I. Laurion, and S. Roy (2006) UVB-photoprotection efficiency of mesocosm-enclosed natural phytoplankton communities from different latitudes: Rimouski (Canada) and Ubatuba (Brazil). Photochem. Photobiol. 82, 952-961.
9. Villafañe, V. E., K. Sundbäck, F. L. Figueroa and E. W. Helbling (2003) Photosynthesis in the aquatic environment as affected by UVR. In UV Effects in Aquatic Organisms and Ecosystems (Edited by E. W. Helbling and H. Zagarese), pp. 357-397. The Royal Society of Chemistry, Cambridge.
10. Wilson, M. I., S. Ghosh, K. E. Gerhardt, N. Holland, T. Sudhakar Babu, M. Edelman, E. B. Dumbroff and B. M. Greenberg (1995) In vivo photomodification of ribulose-1,5-biphosphatase carboxylase/oxygenase holoenzyme by ultraviolet-B radiation. Plant Physiol. 109, 221-229.
11. Baker, N. R., S. Nogués and D. J. Allen (1997) Photosynthesis and photoinhibition. In Plants and UV-B. Responses to Environmental Change (Edited by P. Lumsden), pp. 95-111. Cambridge University Press, United Kingdom.
12. Raven, J. A. and J. Beardall (1981) Respiration and photorespiration. Can. Bull. Fish. Aquat. Sci. 210, 55-82.
13. Geider, R. J., H. L. MacIntyre and T. M Kana (1996) A dynamic model of photoadaptation in phytoplankton. Limnol. Oceanogr. 41, 1-15.
14. Raven, J. A., J. E. Külber and J. Beardall (2000) Put out the light, then put out the light. J. Mar. Biol. Assoc. U.K. 80, 1-27.
15. Nishiyama, Y., H. Yamamoto, S. Allakhverdiev, M. Inaba, A. Yokota and N. Murata (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 20, 5587-5594.
16. Allakhverdiev, S. I., Y. Nishiyama, S. Miyairi, N. Yamamoto, Y. Inagaki, N. Kanesaki and N. Murata (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol. 130, 1443-1453.
17. Allakhverdiev, S. I. and N. Murata (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta 1657, 23-32.
18. Barber, J. (1992) The Photosystems: Structure, Function and Molecular Biology. Elsevier Science Publishers, New York.
19. Mattoo, A. K., H. Hoffman-Falk, J. B. Marder and M. Edelman (1984) Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of chloroplast membranes. Proc. Natl. Acad. Sci. U S A 81, 1380-1384.
20. Aro, E.-M., I. Virgin and B. Andersson (1993) Photoinhibition of photosystem II: Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134.
21. Aro, E.-M., S. McCaffery and J. M. Anderson (1993) Photoinhibition and D1 Protein degradation in peas acclimated to different growth irradiances. Plant Physiol. 104, 1033-1041.
22. Long, S. P., S. Humphries and P. G. Falkowski (1994) Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 633-662.
23. Demmig-Adams, B. and W. W. Adams III (1992) Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 599-626.
24. Hanelt, D. (1996) Photoinhibition of photosynthesis in marine macroalgae. Sci. Mar. 60, 243-248.
25. Vassiliev, I. R., O. Prášil, K. D. Wyman, Z. Kolber, A. K. Hanson Jr., J. E. Prentice and P. G. Falkowski (1994) Inhibition of PII photochemistry by PAR and UV radiation in natural phytoplankton communities. Photosynth. Res. 42, 51-64.
26. Osmond, C. B. (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In Photoinhibition of Photosynthesis, from the Molecular Mechanisms to the Field (Edited by N. R. Baker and N. R. Bowyer), pp. 1-24. Oxford University Press, Oxford.
27. Cleland, R. E., R. T. Ramage and C. Critchley (1990) Photoinhibition causes loss of photochemical activity without degradation of D1 protein. Aust. J. Plant Physiol. 17, 641-651.
28. Ottander, C., T. Hundal, B. Andersson, N. P. A. Huner and G. Öquist (1993) Photosystem II reaction centres stay intact during low temperature photoinhibition. Photosynth. Res. 35, 191-200.
29. Franklin, L. A. (1994) The effects of temperature acclimation on the photoinhibitory responses of Ulva rotundata Blid. Planta 192, 324-331.
30. Herrmann, B., R. Kilian, S. Peter and C. Schafer (1997) Light-stress - related changes in the properties of photosystem I. Planta 201, 456-462.
31. Yamamoto, Y. and T. Akasaka (1995) Degradation of antenna chlorophyll-bonding protein CP43 during photoinhibition of photosystem II. Biochem. 34, 9038-9045.
32. Huner, N. P. A., G. Öquist and S. Sarhan (1998) Energy balance and acclimation to light and cold. Trends Plant Sci. 3, 224-230.
33. Öquist, G. and N. P. A. Huner (2003) Photosynthesis of overwintering evergreen plants. Annu. Rev. Plant Biol. 54, 329-355.
34. Adir, N., H. Zer, S. Schochat and I. Ohad (2003) Photoinhibition - A historical perspective. Photosynth. Res. 76, 343-370.
35. Prášil, O., N. Adir and I. Ohad (1992) Dynamics of photosystem II: Mechanism of photoinhibition and recovery processes. In The Photosystems: Structure, Function and Molecular Biology (Edited by J. Barber), pp. 295-348. Elsevier Science Publishers, New York.
36. Mulo, P., S. Laakso, P. Mäenpää and E.-M. Aro (1998) Stepwise photoinhibition of photosystem II. Plant Physiol. 117, 483-490.
37. A species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. U S A 89, 1408-1412.
38. Hideg, E., C. Spetea and I. Vass (1994) Singlet oxygen and free radical production during acceptor- and donor-side-induced photo-inhibition: studies with spin trapping EPR spectroscopy. Biochim. Biophys. Acta 1186, 143-152.
39. Hideg, E., I. Vass, T. Kálai and K. Hideg (2000) Singlet oxygen detection with sterically hindered amine derivatives in plants under light stress. Meth. Enzymol. 319, 77-85.
40. De Las Rivas, J., B. Andersson and J. Barber (1992) Two sites of primary degradation of the D1-protein induced by acceptor or donor side photo-inhibition in photosystem II core complexes. FEBS Lett. 301, 246-252.
41. Blaubaugh, D. J. and G. M. Cheniae (1990) Kinetics of photo-inhibition in hydroxylamide-extracted photosystem II membranes - Relevance to photoactivation and sites of electron donation. Biochem. 29, 5109-5118.
42. Eckert, H. J., B. Geiken, J. Bernarding, A. Napiwotzki, H. J. Eichler and G. Renger (1991) Two sites of photoinhibition of the electron-transfer in oxygen evolving and tris-treated PSII membrane-fragments from spinach. Photosynth. Res. 27, 97-108.
43. Tyystjärvi, E. and E.-M. Aro (1996) The rate constant of photo-inhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc. Natl. Acad. Sci. U S A 93, 2213-2218.
44. Park, Y. I., W. S. Chow and J. M. Anderson (1995) The quantum yield of photoinactivation of photosystem-II in pea leaves is greater at low than high photon exposure. Plant Cell Physiol. 36, 1163-1167.
45. Baroli, I. and A. Melis (1996) Photoinhibition and repair in Dunaliella salina acclimated to different growth irradiances. Planta 198, 640-646.
46. Anderson, J. M., Y.-I. Park and W. S. Chow (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiol. Plant. 100, 214-233.
47. Mizusawa, N., T. Tomo, K. Satoh and M. Miyao (2003) Degradation of the D1 protein of photosystem II under illumination in vivo: Two different pathways involving cleavage or intermolecular cross-linking. Biochem. 42, 10034-10044.
48. Babu, T. S., M. A. K. Jansen, B. M. Greenberg, V. Gaba, S. Malkin and M. Edelman (1999) Amplified degradation of the photosystem II D1 and D2 proteins under a mixture of photosynthetically active radiation and ultraviolet-B radiation: Dependence on redox-status of photosystem II. Photochem. Photobiol. 69, 553-559.
49. Greenberg, B. M., V. Gaba, O. Canaani, S. Malkin, A. K. Mattoo and M. Edelman (1989) Separate photosensitizers mediate degradation of the 32-kDa photosystem II reaction centre protein in the visible and UV spectral regions. Proc. Natl. Acad. Sci. U S A 86, 6617-6620.
50. Jansen, M. A. K., V. Gaba, B. Greenberg, K. A. Mattoo and M. Edelman (1994) UVB driven degradation of the D1-reaction-center protein of photosystem II proceeds via plastosemiquinone. In Photosynthetic Responses to the Environment (Edited by H. Y. Yamamoto and C. M. Smith), pp. 142-149. American Society of Plant Physiologists, Rockville, MD.
51. Renger, G., M. Völker, H. J. Eckert, R. Fromme, S. Hohm-Veit and P. Graäber (1989) On the mechanism of photosystem II deterioration by UVB irradiation. Photochem. Photobiol. 49, 97-105.
52. Vass, I., L. Sass, C. Spetea, A. Bakou, D. F. Ghanotakis and V. Petrouleas (1996) UV-B induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence: Impairment of donor and acceptor side components. Biochem. 35, 8964-8973.
53. Vass, I., D. Kirilovsky and A.-L. Etienne (1999) UVB radiation induced donor- and acceptor-side modifications of the photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochem. 38, 12786-12794.
54. Larkum, A. W. D., M. Karge, F. Reifarth, H.-J. Eckert, A. Post and G. Renger (2001) Effect of monochromatic UV-B radiation on electron transfer reactions of photosystem II. Photosynth. Res. 68, 49-60.
55. Ohnishi, N., S. I. Allakhverdiev, S. Takahashi, S. Higashi, M. Watanabe, Y. Nishiyama and N. Murata (2005) Two-step mechanism of photodamage to photosystem II: Step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochem. 44, 8494-8499.
56. Melis, A. (1999) Photosystem-II damage and repair cycle in chloroplasts: What modulates the rate of photodamage in vivo? Trends Plant Sci. 4, 130-135.
57. Allakhverdiev, S. I., Y. Nishiyama, S. Takahashi, S. Miyairi, I. Suzuki and N. Murata (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol. 137, 263-273.
58. Allakhverdiev, S. I., N. Tsvetkova, P. Mohanty, B. Szalontai, B. Y. Moon, M. Debreczeny and N. Murata (2005) Irreversible photo-inhibition of photosystem II is caused by exposure of Synechocystis cells to strong light for a prolonged period. Biochim. Biophys. Acta 1708, 342-351.
59. Hakala, M., I. Tuominen, M. Keränen, T. Tyystjärvi and E. Tyystjärvi (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim. Biophys. Acta 1706, 68-80.
60. Yamamoto, Y. (2001) Quality control of photosystem II. Plant Cell Physiol. 42, 121-128.
61. Adam, Z. and A. K. Clarke (2002) Cutting edge of chloroplast proteolysis. Trends Plant Sci. 7, 451-456.
62. Aro, E.-M., M. Suorsa, A. Rokka, Y. Allahverdiyeva, V. Paakkarinen, A. Saleem, N. Battchikova and E. Rintamäki (2005) Dynamics of photosystem II: A proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347-356.
63. Haußühl, K., B. Andersson and I. Adamska (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J. 20, 713-722.
64. Lindahl, M., C. Spetea, T. Hundal, A. B. Oppenheim, Z. Adam and B. Andersson (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12, 419-431.
65. Nixon, P. J., M. Baker, M. Boehm, R. de Vries and J. Komenda (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J. Exp. Bot. 56, 357-363.
66. Silva, P., E. Thompson, S. Bailey, O. Kruse, C. W. Mullineaux, C. Robinson, N. H. Mann and P. J. Nixon (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15, 2152-2164.
67. Lesser, M. P., J. J. Cullen and P. J. Neale (1994) Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: Relative importance of damage and repair. J. Phycol. 30, 183-192.
68. Böttger, E. C., B. Springer, T. Prammananan, Y. Kidan and P. Sander (2001) Structural basis for selectivity and toxicity of ribosomal antibiotics. EMBO Reports 41, 318-323.
69. Ekelund, N. G. A. (1996) Effects of protein synthesis inhibitors on photoinhibition by UVB (280-320 nm) radiation in the flagellate Euglena gracilis. Sci. Mar. 60, 95-100.
70. Rae, R., C. Howard-Williams, I. Hawes and W. Vincent (2000) Temperature dependence of photosynthetic recovery from solar damage in Antarctic phytoplankton. In Antarctic Ecosystems: Models for Wider Ecological Understanding (Edited by W. Davison, C. Howard-Williams and P. Broady), pp. 183-189. SCRA VII Proceedings, The Caxton Press, Christchurch, New Zealand.
71. Bouchard, J. N., D. A. Campbell and S. Roy (2005) Effects of UV-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, Argentina). J. Phycol. 41, 287-293.
72. B site and dependent on protein synthesis. Biochem. 34, 9625-9631.
73. Gong, H. S. (1994) Light-dependent degradation of the photosystem-II D1 protein is retarded by inhibitors of chloroplast transcription and translation - Possible involvement of a chloroplast-encoded proteinase. Biochim. Biophys. Acta 1188, 422-426.
74. Komenda, J., H. A. G. Hassan, B. A. Diner, R. J. Debus, J. Barber and P. J. Nixon (2000) Degradation of the photosystem II D1 and D2 proteins in different strains of the cyanobacterium Synechocystis PCC 6803 varying with respect to the type and level of psbA transcript. Plant Mol. Biol. 42, 635-645.
75. vanWijk, K. J., S. Bingsmark, E.-M. Aro and B. Andersson (1995) In vitro synthesis and assembly of photosystem II core proteins - The D1 protein can be incorporated into photosystem II in isolated chloroplasts and thylakoids. J. Biol. Chem. 270, 25 685-25 695.
76. vanWijk, K. J., B. Andersson and E.-M. Aro (1996) Kinetic resolution of the incorporation of the D1 protein into photosystem II and localization of assembly of intermediates in thylakoid membranes of spinach chloroplasts. J. Biol. Chem. 271, 9627-9636.
77. Rintamaki, E., R. Salo, E. Lehtonen and E.-M. Aro (1995) Regulation of D1 protein-degradation during photoinhibition of photosystem-II in vivo-phosphorylation of the D1 protein in various plant groups. Planta 195, 379-386.
78. Vasilikiotis, C. and A. Melis (1995) The role of chloroplast-encoded protein biosynthesis on the rate of D1 protein-degradation in Dunaliella salina. Photosynth. Res. 45, 147-155.
79. Franklin, L. A., C. B. Osmond and A. W. D. Larkum (2003). Photoinhibition, UV-B and algal photosynthesis. In Photosynthesis in Algae. (Edited by A. W. D. Larkum, S. E. Douglas and J. A. Raven), pp. 351-384. Kluwer Academic Publishers, Dordrecht.
80. Sicora, C., Z. Máté and I. Vass (2003) The interaction of visible and UVB light during photodamage and repair of PSII. Photosynth. Res. 75, 127-137.
81. Shelly, K., P. Heraud and J. Beardall (2003) Interactive effects of PAR and UVB radiation on the PSII electron transport in the marine alga Dunaliella tertiolecta (Chlorophyceae). J. Phycol. 39, 509-512.
82. Greer, D. H., J. A. Berry and O. Björkman (1986) Photoinhibition of photosynthesis in intact bean leaves: Role of light, temperature and requirement for chloroplast-protein synthesis during recovery. Planta 168, 253-260.
83. Kanervo, E., E.-M. Aro and N. Murata (1995) Low unsaturation level of thylakoid membrane lipids limits turnover of the D1 protein of photosystem II at high irradiance. FEBS Lett. 364, 239-242.
84. Kanervo, E., Y. Tasaka, N. Murata and E.-M. Aro (1997) Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperature. Plant Physiol. 114, 841-849.
85. Warner, M. E., W. K. Fitt and G. W. Schmidt (1999) Damage to the photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl. Acad. Sci. U S A 96, 8007-8012.
86. Lesser, M. P. (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16, 187-192.
87. Lesser, M. P. and J. H. Farrell (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23, 367-377.
88. Murata, N. and H. Wada (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatisation to cold of cyanobacteria. Biochem. J. 308, 1-8.
89. B. J. Biol Chem. 227, 32739-32745.
90. Sippola, K., E. Kanervo, N. Murata and E.-M. Aro (1998) A genetically engineered increase in fatty acid unsaturation in Synechococcus sp. PCC 7942 allows exchange of D1 protein forms and sustenance of photosystem II activity at low temperature. Eur. J. Biochem. 251, 641-648.
91. Berges, J. A., D. O. Charlebois, D. C. Mauzerall and P. G. Falkowski (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol. 110, 689-696.
92. Steglich, C., M. Behrenfeld, M. Koblizek, H. Claustre, S. Penno, O. Prášil, F. Partensky and W. R. Hess (2001) Nitrogen deprivation strongly affects photosystem II but not phycoerythrin level in divinyl-chlorophyll b-containing cyanobacteirum Prochlorococcus marinus. Biochim. Biophys. Acta 1503, 341-349.
93. Geider, R. J., J. La Roche, R. M. Greene and M. Olaizola (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate and iron starvation. J. Phycol. 29, 755-766.
94. Litchman, E., P. J. Neale and A. T. Banaszak (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: Photoprotection and repair. Limnol. Oceanogr. 47, 86-94.
95. Shelly, K., P. Heraud and J. Beardall (2002) Nitrogen limitation in Dunaliella tertiolecta (Chlorophyceae) leads to increased susceptibility to damage by ultraviolet-B radiation but also increased repair capacity. J. Phycol. 38, 713-720.
96. Longhi, M. L., S. Roy, G. Ferreyra and I. Schloss. (2006) Variable phytoplankton responses to enhanced UV-B and nitrate addition in mesocosms experiments at three latitudes (Canada, Brazil, Argentina). J. Mar. Ecol. Progr. Ser. 313, 57-72.
97. Bergmann, T., T. L. Richardson, H. W. Paerl, J. L. Pinckney and O. Schofield (2002) Synergy of light and nutrients on the photosynthetic efficiency of phytoplankton populations from the Neuse River Estuary, North Carolina. J. Plankton Res. 24, 923-933.
98. Finazzi, G., R. P. Barbagallo, E. Bergo, R. Barbato and G. Forti (2001) Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2. J. Biol. Chem. 276, 22251-22257.
99. MacKenzie, T. D. B., R. A. Burns and D. A. Campbell (2004) Carbon status constrains light acclimation in the cyanobacterium Synechococcus elongatus. Plant Physiol. 136, 3301-3312.
100. Sobrino, C., P. J. Neale and L. M. Lubián (2005) Interaction of UV radiation and inorganic carbon supply in the inhibition of photosynthesis: Spectral and temporal responses of two marine picoplankters. Photochem. Photobiol. 81, 384-393.
101. Falkowski, P. G. and J. A. Raven (1997) Aquatic Photosynthesis. Blackwell Publishers, Maiden, MA.
102. Larkum, A. W. D. and M. Vesk (2003) Algal plastids: Their fine structure and properties. In Photosynthesis in Algae (Edited by A. W. D. Larkum, S. E. Douglas and J. A. Raven.), pp. 11-28. Kluwer Academic Publishers, Dordrecht.
103. Zurawski, G., H. J. Bohnert, P. R. Whitefeld and W. Bottomley (1982) Nucleotide sequence of the gene for the Mr 32,000 thylakoid membrane protein from Spinacea oleracea and Nicotiana debneyi predicts a totally conserved primary translation product of Mr 38,950. Proc. Natl. Acad. Sci. U S A 79, 7699-7703.
104. Golden, S. S. (1995) Light-responsive gene expression in cyanobacteria. J. Bacteriol. 177, 1651-1654.
105. Sicora, C. I., S. E. Appleton, C. M. Brown, J. Chung, J. Chandler, A. M. Cockshutt, I. Vass and D. A. Campbell (2006) Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB induced D1 isoforms. Biochim. Biophys. Acta, 1757, 47-56.
106. Mohamed, A. and C. Jansson (1989) Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol. Biol. 13, 693-700.
107. Hihara, Y., A. Kamei, M. Kanehisa, A. Kaplan and M. Ikeuchi (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13, 793-806.
108. Mohamed, A. and C. Jansson (1989) Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechococcus 6803. Plant. Mol. Biol. 16, 891-897.
109. Kanervo, E., P. Mäenpää and A.-M. Aro (1993) D1 protein degradation and psbA transcript levels in Synechocystis PCC 6803 during photoinhibition in vivo. J. Plant Physiol. 142, 669-675.
110. Constant, S., I. Perewoska, M. Alfonso and D. Kirilovsky (1997) Expression of the psbA gene during photoinhibition and recovery in the Synechocystis PCC 6714: Inhibition and damage of transcriptional and translational machinery prevent the restoration of photosystem II activity. Plant Mol. Biol. 34, 1-13.
111. Máté, Z., L. Sass, M. Szekeres, I. Vass and F. Nagy (1998) UVB-induced differential transcription of psbA genes encoding the D1 protein of the photosystem II in the cyanobacterium Synechocystis 6803. J. Biol. Chem. 273, 17439-17444.
112. Vass, I., D. Kirilovsky, I. Perewoska, Z. Máté, F. Nagy and A.-L. Etienne (2000) UVB radiation induced exchange of the D1 reaction centre subunits produced from the psbA2 and the psbA3 genes in the cyanobacterium Synechocystis sp. PCC 6803. Eur. J. Biochem. 267, 2640-2648.
113. Campbell, D., G. Zhou, P. Gustafsson, G. Öquist and A. K. Clarke (1995) Electron transport regulates exchange of two forms of photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J. 14, 5457-5466.
114. Kulkarni, R. D. and S. S. Golden (1994) Adaptation to high light intensity in Synechococcus sp. Strain PCC 7942: Regulation of three psbA genes and forms of the D1 protein, J. Bacteriol. 176, 959-965.
115. Campbell, D., M.-J. Eriksson, G. Öquist, P. Gustafsson and A. Clarke (1998) The cyanobacterium Synechococcus resists UVB by exchanging photosystem II reaction-center D1 proteins. Proc. Natl. Acad. Sci. U S A 95, 364-369.
116. Clarke, A. K., D. Campbell, P. Gustafsson and G. Öquist (1995) Dynamic responses of photosystem II and phycobilisomes to changing light in the cyanobacterium Synechococcus sp. PCC 7942. Planta 197, 553-562.
117. Öquist, G., D. Campbell, A. K. Clarke and P. Gustafsson (1995) The cyanobacterium Synechococcus modulates photosystem II function in response to excitation stress through D1 exchange. Photosynth. Res. 45, 151-158.
118. 2 assimilation transcripts and proteins to moderate UVB: Light acclimation potentiates resistance to UVB. Photochem. Photobiol. 77, 405-412.
119. Komenda, J., M. Koblížek and J. Masojídek (1999) The regulatory role of photosystem II photoinactivation and de novo synthesis in the degradation and exchange of two forms of the D1 protein in the cyanobacterium Synechococcus PCC 7942. J. Photochem. Photobiol. B. 48, 114-119.
120. Ivanov, A. G., E. Miskiewicz, A. K. Clarke, B. M. Greenberg and N. P. A. Huner (2000) Protection of photosystem II against UV-A and UVB radiation in the cyanobaterium Plectonema boryanum: The role of growth temperature and growth irradiance. Photochem. Photobiol. 72, 772-779.
121. Soitamo, A. J., G. Zhou, A. K. Clarke, G. Öquist, P. Gustafsson and E.-M. Aro (1996) Over-production of the D1:2 protein makes Synechococcus cells more tolerant to photoinhibition of photosystem II. Plant Mol. Biol. 30, 467-478.
122. Tichy, M., L. Lupinkova, C. Sicora, I. Vass, S. Kuvikova, O. Prasil and J. Komenda (2003) Synechocystis 6803 mutants expressing distinct forms of the photosystem II D1 protein from Synechococcus 7942: Relationship between the psbA coding region and sensitivity to visible and UV-B radiation. Biochim. Biophys. Acta 1605, 55-66.
123. Sass, L., C. Spetea, Z. Máté, F. Nagy and I. Vass (1997) Repair of UVB induced damage of photosystem II via de novo synthesis of the D1 and D1 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynth. Res. 54, 55-62.
124. Jansen, M. A. K., A. K. Mattoo and M. Edelman (1999) D1-D2 protein degradation in the chloroplast. Complex light saturation kinetics. Eur. J. Biochem. 260, 527-532.
125. Jansen, M. A. K., V. Gaba, B. Greenberg, A. K. Mattoo and M. Edelman (1996) Low threshold levels of ultraviolet-B in a background of photosynthetically active radiation trigger rapid degradation of the D2 protein of photosystem-II. Plant J. 9, 693-699.
126. Booij-James, I. S., S. K. Dube, M. A. K. Jansen, M. Edelman and A. K. Mattoo (2000) Ultraviolet-B radiation impacts light-mediated turnover of the photosystem II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiol. 124, 1275-1283.
127. Shapira, M., A. Lers, P. B. Heifetz, V. Irihimovitz, C. B. Osmond, N. W. Gillham and J. E. Boynton (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: Light stress transiently suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PSII D1 protein. Plant Mol. Biol. 33, 1001-1011.
128. Chaturvedi, R. and R. Shyam (2000) Degradation and de novo synthesis of D1 protein and psbA transcript levels in Chlamydomonas reinhardtii during UVB inactivation of photosynthesis and its reactivation. J. Biosci. 25, 65-71.
129. Jordan, B. R., W. S. Chow, A. Strid and J. M. Anderson (1991) Reduction in cab and psbA RNA transcripts in response to supplementary ultraviolet-B radiation. FEBS Lett. 284, 5-8.
130. Heraud, P. and J. Beardall (2000) Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynth. Res. 63, 123-134.
131. Kim, J. H., J. A. Nemson and A. Melis (1993) Photosystem II reaction center damage and repair in Dunaliella salina (green alga). Plant Physiol. 103, 181-189.
132. Vasilikiotis, C. and A. Melis (1994) Photosystem II reaction center damage and repair cycle: Chloroplast acclimation strategy to irradiance stress. Proc. Natl. Acad. Sci. U S A 91, 7222-7226.
133. Baroli, I. and A. Melis (1998) Photoinhibitory damage is modulated by the rate of photosynthesis and by the photosystem II light-harvesting chlorophyll antenna size. Planta 205, 288-296.
134. Xiong, F. (2001) Evidence that UVB tolerance of the photosynthetic apparatus in microalgae is related to the D1-turnover mediated repair cycle in vivo. J. Plant Physiol. 158, 285-294.
135. Xiong, F., J. Komenda, J. Kopecký and L. Nedbal (1997) Strategies of ultraviolet-B protection in microscopic algae. Physiol. Plant. 100, 378-388.
136. Grzymski, J., C. Orrico and O. M. Schofield (2001) Monochromatic ultraviolet light induced damage to photosystem II efficiency and carbon fixation in the marine diatom Thalassisira pseudonana (3H). Photosynth. Res. 68, 181-192.
137. Hazzard, C., M. Lesser and R. A. Kinzie III (1997) Effects of ultraviolet radiation on photosynthesis in the subtropical marine diatom, Chaetoceros gracilis (Bacillariophyceae). J. Phycol. 33, 960-968.
138. Gerber, S. and D.-P. Häder (1995) Effects of artificial UVB and simulated solar radiation on the flagellate Euglena gracilis: Physiological, spectroscopical and biochemical investigations. Acta Protozool. 34, 13-20.
139. Warner, M. E., W. K. Fitt and G. W. Schmidt (1996) The effect of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species reef coral: A novel approach. Plant Cell Environ. 19, 291-299.
140. Hill, R., A. W. D. Larkum, C. Frankart, M. Kühl and P. J. Ralph (2004) Loss of functional photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: Using fluorescence rise kinetics. Photosynth. Res. 82, 59-72.
141. Lesser, M. P., W. R. Stochaj, D. W. Tapley and J. M Shick (1990) Bleaching of coral reef Anthozoans: Effects of irradiance ultraviolet radiation, and temperature, on the activities of protective enzymes against active oxygen. Coral Reefs 8, 225-232.
142. Gleason, D. F. and G. M. Wellington (1993) Ultraviolet radiation and coral bleaching. Nature 365, 836-838.
143. Dunne, R. P. and B. E. Brown (2001) The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993-1998. Coral Reefs 20, 201-210.
144. 2 fixation metabolism in zooxanthellae. Plant Cell Environ. 21, 1219-1230.
145. Lesser, M. P. and M. Y. Gorbunov (2001) Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Mar. Ecol. Progr. Ser. 212, 69-77.
146. Takahashi, S., T. Makamura, M. Sakamizu, R. van Woesik and H. Yamasaki (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol. 45, 251-255.
147. Calkins, J. and T. Thordardottir (1980) The ecological significance of solar UV radiation on aquatic organisms. Nature 283, 563-566.
148. Jokiel, P. L. and R. H. York (1984) Importance of ultraviolet radiation in photoinhibition of microalgal growth. Limnol. Oceanogr. 29, 192-199.
149. Lesser, M., P. J. Neale and J. J. Cullen (1996) Acclimation of Antarctic phytoplankton to ultraviolet radiation: Ultraviolet-absorbing compounds and carbon fixation. Mol. Mar. Biol. Biotechnol. 5, 314-325.
150. Bracher, A. U. and C. Wiencke (2000) Simulation of the effects of naturally enhanced UV radiation on photosynthesis on Antarctic phytoplankton. Mar. Ecol. Prog. Ser. 196, 127-141.
151. Marwood, C. A., R. E. H. Smith, J. A. Furgal, M. N. Charlton, K. R. Solomon and B. M. Greenberg (2000) Photoinhibition of natural phytoplankton assemblages in Lake Erie exposed to solar ultraviolet radiation. Can. J. Fish. Aquat. Sci. 57, 371-379.
152. Bouchard, J. N., S. Roy, G. Ferreyra, D. A. Campbell and A. Curtosi (2005) Ultraviolet-B effects on photosystem II efficiency of natural phytoplankton communities from Antarctica. Polar Biol. 28, 607-618.
153. Marshall, H. L., R. J. Geider and K. J. Flynn (2000) A mechanistic model of photoinhibition. New Phytol. 145, 347-359.
154. Han, B.-P., M. Virtanen, J. Koponen and M. Straškraba (2000) Effect of photoinhibition on algal photosynthesis: A dynamic model. J. Plankton Res. 22, 865-885.
155. Tyystjärvi, E., P. Mäenpää and E.-M. Aro (1994) Mathematical modeling of photoinhibition and photosystem II repair cycle. I. Photoinhibition and D1 protein degradation in vitro and in the absence of chloroplast protein synthesis in vivo. Photosynth. Res. 41, 439-449.
156. Han, B.-P. (2002) A mechanistic model of algal photoinhibition induced by photodamage to photosystem II. J. Theor. Biol. 214, 519-527.
157. Flynn, K. J. and K. Flynn (1998) Release of nitrite by marine dinoflagellates: Development of mathematical simulation. Mar. Biol. 13, 455-470.
158. Geider, R. J., H. L. MacIntyre and T.M. Kana (1998) A dynamic regulatory model of phytoplanktonic acclimation to light, nutrients and temperature. Limnol. Oceanogr. 43, 679-694.
159. Anning, T., S. M. Pratt, P. J. Sammes, H. L. MacIntyre, S. Gibb and R. J. Geider (2000) Photoacclimation in the marine diatom Skeletonema costatum. Limnol. Oceanogr. 45, 1807-1817.
160. Neale, P. J., E. W. Helbling and H. E. Zagarese (2003) Modulation of UVR exposure and effects by vertical mixing and advection. In UV effects in Aquatic Organisms and Ecosystems. Comprehensive Series in Photochemistry & Photobiology - Vol. 1 (Edited by E. W. Helbling and H. Zagarese), pp. 107-134. The Royal Society of Chemistry, Cambridge.
161. Buma, A. G. J., P. Boelen and W. H. Jeffrey (2003) UVR-induced DNA damage in aquatic organisms. In UV effects in Aquatic Organisms and Ecosystems. Comprehensive Series in Photochemistry & Photobiology - Vol. 1 (Edited by E. W. Helbling and H. Zagarese), pp. 291-327. The Royal Society of Chemistry, Cambridge.