Dynamic regulation of photoprotection determines thermal tolerance of two phylotypes of symbiodinium clade a at two photon fluence rates

Photochemistry and Photobiology

Volumn 88, Issue 2, 2012, Pages 398-413

  Krämer, Wiebke E ^a   Caamaño Ricken, Isabel ^a   Richter, Claudio ^b   Bischof, Kai ^a  

^a UNIVERSITY OF BREMEN   (Germany)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIATOXANTHINE; GLUTATHIONE; XANTHOPHYLL;

ADAPTATION; ANIMAL; ANTHOZOA; ARTICLE; DINOFLAGELLATE; HEAT; LIGHT; METABOLISM; PHOTON; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; RADIATION EXPOSURE; SPECIES DIFFERENCE; SYMBIOSIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTHOZOA; DINOFLAGELLIDA; GLUTATHIONE; HOT TEMPERATURE; LIGHT; PHOTONS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; SPECIES SPECIFICITY; SYMBIOSIS; XANTHOPHYLLS;

ANTHOZOA; DINOPHYCEAE; SCLERACTINIA; SYMBIODINIUM;

EID: 84857996302     PISSN: 00318655     EISSN: 17511097     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2011.01048.x     Document Type: Article

References (119)

1. Connell, J. H., (1978) Diversity in tropical rain forests and coral reefs. Science 199, 1302-1310.
2. Freudenthal, H. D., (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: Taxonomy, life cycle, and morphology. J. Eukaryot. Microbiol. 9, 45-52.
3. Muscatine, L., (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In Ecosystems of the World. Vol. 25: Coral Reefs (Edited by, Z. Dubinsky,), pp. 75-87. Elsevier, New York.
4. Muscatine, L., and, J. Porter, (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454-460.
5. Falkowski, P., Z. Dubinsky, L. Muscatine, and, L. McCloskey, (1993) Population control in symbiotic corals: Ammonium ions and organic molecules maintain the density of zooxanthellae. Bioscience 43, 606-611. (Pubitemid 2000421)
6. IPCC (2007) Climate change 2007: The physical science basis. In Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Edited by, S. Solomon, D. Qin, M. Mannin, Z. Chen, M. Marquis, K. Averty, M. Tignor, and, H. Miller,), pp. 747-845. Cambridge University Press, Cambridge, New York.
7. Coles, S., P. Jokiel, and, C. Lewis, (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac. Sci. 30, 159-166.
8. Glynn, P., (1993) Coral reef bleaching: Ecological perspectives. Coral Reefs 12, 1-17. (Pubitemid 24411337)
9. Hoegh-Guldberg, O., (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res. 50, 839-866. (Pubitemid 30018479)
10. Hoegh-Guldberg, O., (2011) Coral reef ecosystems and anthropogenic climate change. Reg. Environ. Change 11, 215-227.
11. McPhaden, M., (2004) Evolution of the 2002/03 El Ni o. B. Am. Meteorol. Soc. 85, 677-695.
12. Klein, S., B. Soden, and, N.-C. Lau, (1999) Remote sea surface temperature variations during ENSO: Evidence for a tropical atmospheric bridge. J. Clim. 12, 917-932. (Pubitemid 29346271)
13. Eakin, C., J. Lough, and, S. Heron, (2009) Climate variability and change: Monitoring data and evidence for increased coral bleaching stress. In Coral Bleaching: Patterns, Processes, Causes and Consequences (Edited by, M. van Oppen, and, J. Lough,), pp. 41-67. Springer, Berlin.
14. 2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21, 1219-1230. (Pubitemid 29051743)
15. Lesser, M. P., (2011) Coral bleaching: Causes and mechanisms. In Coral Reefs: An Ecosystem in Transition (Edited by, Z. Dubinsky, and, N. Stambler,), pp. 405-419. Springer, Dordrecht, The Netherlands.
16. Smith, D., D. Suggett, and, N. Baker, (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biol. 11, 1-11. (Pubitemid 40134041)
17. Niyogi, K., (1999) Photoprotection revisited: Genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359. (Pubitemid 129491966)
18. Hennige, S., D. Suggett, M. Warner, K. McDougall, and, D. Smith, (2009) Photobiology of Symbiodinium revisited: Bio-physical and bio-optical signatures. Coral Reefs 28, 179-195.
19. Falkowski, P., and, Z. Dubinsky, (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289, 172-174.
20. Falkowski, P., P. Jokiel, and, R. Kinzie III, (1990) Irradiance and corals. In Ecoystems of the World. Vol. 25: Coral Reefs (Edited by, Z. Dubinsky,), p. 550. Elsevier, New York.
21. Brown, B., R. Dunne, I. Ambarsari, M. Le Tissier, and, U. Satapoomin, (1999) Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar. Ecol. Prog. Ser. 191, 53-69. (Pubitemid 30061635)
22. Winters, G., S. Beer, B. Zvi, I. Brickner, and, Y. Loya, (2009) Spatial and temporal photoacclimation of Stylophora pistillata: Zooxanthella size, pigmentation, location and clade. Mar. Ecol. Prog. Ser. 384, 107-119.
23. Long, S., S. Humphries, and, P. Falkowski, (1994) Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 633-662.
24. Brown, B., I. Ambarsari, M. Warner, W. Fitt, R. Dunne, S. Gibb, and, D. Cummings, (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: Evidence for photoinhibition and photoprotection. Coral Reefs 18, 99-105. (Pubitemid 29365520)
25. Warner, M., and, S. Berry-Lowe, (2006) Differential xanthophyll cycling and photochemical activity in symbiotic dinoflagellates in multiple locations of three species of Caribbean coral. J. Exp. Mar. Biol. Ecol. 339, 86-95. (Pubitemid 44528526)
26. Demmig-Adams, B., (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1-24.
27. 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. (Pubitemid 36080303)
28. Osmond, C., (1994) What is photoinhibition? Insights from comparisons of shade and sun plants. In Photoinhibition of Photosynthesis From Molecular Mechanisms to the Field (Edited by, N. Baker, and, J. Bowyer,), pp. 1-24. BIOS Scientific Publishers, Oxford.
29. Warner, M., W. Fitt, and, G. Schmidt, (1999) Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl Acad. Sci. USA 96, 8007-8012. (Pubitemid 29328398)
30. Tchernov, D., M. Gorbunov, C. de Vargas, S. Narayan Yadav, A. Milligan, M. Haggblom, and, P. Falkowski, (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl Acad. Sci. USA 101, 13531-13535. (Pubitemid 39238437)
31. Wooldridge, S., (2009) A new conceptual model for the warm-water breakdown of the coral-algae endosymbiosis. Mar. Freshwater Res. 60, 483-496.
32. Nishiyama, Y., S. Allakhverdiev, and, N. Murata, (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 1757, 742-749. (Pubitemid 44160685)
33. Takahashi, S., T. Nakamura, M. Sakamizu, R. V. 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. (Pubitemid 38318832)
34. Takahashi, S., S. Whitney, and, M. Badger, (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc. Natl Acad. Sci. USA 106, 3237-3242.
35. Lesser, M., (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol. Oceanogr. 41, 271-283. (Pubitemid 26311204)
36. Leggat, W., S. Whitney, and, D. Yellowlees, (2004) Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37, 137-154.
37. Lilley, R., P. Ralph, and, A. Larkum, (2010) The determination of activity of the enzyme Rubisco in cell extracts of the dinoflagellate alga Symbiodinium sp. by manganese chemiluminescence and its response to short-term thermal stress of the alga. Plant Cell Environ. 33, 995-1004.
38. Asada, K., (1999) The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639. (Pubitemid 129491975)
39. Fotopoulos, V., V. Ziogas, G. Tanou, and, A. Molassiotis, (2010) Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In Ascorbate-Glutathione Pathway and Stress Tolerance in Plants (Edited by, N. A. Anjum, M.-T. Chan, and, S. Umar,), pp. 265-302. Springer, Dordrecht, The Netherlands.
40. Downs, C., E. Mueller, S. Phillips, J. Fauth, and, C. Woodley, (2000) A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar. Biotechnol. 2, 533-544. (Pubitemid 32140026)
41. Suggett, D., M. Warner, D. Smith, P. Davey, S. Hennige, and, N. Baker, (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrophyta) phylotypes with different thermal tolerances. J. Phycol. 44, 948-956.
42. Yakovleva, I., R. Bhagooli, A. Takemura, and, M. Hidaka, (2004) Differential susceptibility to oxidative stress of two scleractinian corals: Antioxidant functioning of mycosporine-glycine. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 139, 721-730. (Pubitemid 39586557)
43. Downs, C., J. Fauth, J. Halas, P. Dustan, J. Bemiss, and, C. Woodley, (2002) Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 33, 533-543. (Pubitemid 34874974)
44. Mitchelmore, C., E. Alan Verde, A. Ringwood, and, V. Weis, (2003) Differential accumulation of heavy metals in the sea anemone Anthopleura elegantissima as a function of symbiotic state. Aquat. Toxicol. 64, 317-329. (Pubitemid 36808795)
45. Sunagawa, S., J. Choi, H. Forman, and, M. Medina, (2008) Hyperthermic stress-induced increase in the expression of glutamate-cysteine ligase and glutathione levels in the symbiotic sea anemone Aiptasia pallida. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 151, 133-138.
46. Gates, R., G. Baghdasarian, and, L. Muscatine, (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: Implications for coral bleaching. Biol. Bull. 182, 324-332. (Pubitemid 23402250)
47. Lesser, M., and, J. Farrell, (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 24, 367-377. (Pubitemid 39320598)
48. Dunn, S., J. Thomason, M. Le Tissier, and, J. Bythell, (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ. 11, 1213-1222. (Pubitemid 39529964)
49. Rowan, R., and, D. Powers, (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar. Ecol. Prog. Ser. 71, 65-73.
50. Coffroth, M., and, S. Santos, (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156, 19-34. (Pubitemid 40728123)
51. Pochon, X., and, R. D. Gates, (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol. Phylogenet. Evol. 56, 492-497.
52. Toller, W. W., R. Rowan, and, N. Knowlton, (2001) Zooxanthellae of the Montastraea annularis species complex: Patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol. Bull. 201, 348-359. (Pubitemid 34057131)
53. Rowan, R., and, N. Knowlton, (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc. Natl Acad. Sci. USA 92, 2850-2853.
54. LaJeunesse, T., (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141, 387-400.
55. Karako-Lampert, S., D. Katcoff, Y. Achituv, Z. Dubinsky, and, N. Stambler, (2004) Do clades of symbiotic dinoflagellates in scleractinian corals of the Gulf of Eilat (Red Sea) differ from those of other coral reefs? J. Exp. Mar. Biol. Ecol. 311, 301-314. (Pubitemid 39290146)
56. Baker, A., (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Syst. 34, 661-689. (Pubitemid 38171434)
57. Rowan, R., N. Knowlton, A. Baker, and, J. Jara, (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265-269. (Pubitemid 27317968)
58. Iglesias-Prieto, R., and, R. Trench, (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar. Ecol. Prog. Ser. 113, 163-175.
59. Iglesias-Prieto, R., and, R. Trench, (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photonfux densities. Mar. Biol. 130, 23-33. (Pubitemid 28084499)
60. Robison, J., and, M. Warner, (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42, 568-579. (Pubitemid 43807266)
61. Fitt, W., B. Brown, M. Warner, and, R. Dunne, (2001) Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51-65. (Pubitemid 32770401)
62. Iglesias-Prieto, R., J. Matta, W. Robins, and, R. Trench, (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl Acad. Sci. USA 89, 10302-10305.
63. Bhagooli, R., and, M. Hidaka, (2003) Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. J. Exp. Mar. Biol. Ecol. 291, 181-197. (Pubitemid 36684746)
64. Bhagooli, R., and, M. Hidaka, (2004) Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 137, 547-555. (Pubitemid 38270408)
65. Reynolds, J., B. Bruns, W. Fitt, and, G. Schmidt, (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc. Natl Acad. Sci. USA 105, 13674-13678.
66. Tausz, M., (2001) The role of glutathione in plant response and adaptation to natural stress. In Significance of Glutathione to Plant Adaptation to the Environment, Vol. 2. (Edited by, D. Grill, M. Tausz, and, L. J. Kok,), pp. 101-122. Springer, Dordrecht, The Netherlands.
67. LaJeunesse, T., (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: In search of a "species" level marker. J. Phycol. 37, 866-880.
68. Guillard, R. R., and, J. H. Ryther, (1962) Studies of marine planktonic diatoms. 1. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229-239.
69. Perez, S., and, V. Weis, (2006) Nitric oxide and cnidarian bleaching: An eviction notice mediates breakdown of a symbiosis. J. Exp. Biol. 209, 2804-2810. (Pubitemid 44213126)
70. Bouchard, J. N., and, H. Yamasaki, (2008) Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: A possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol. 49, 641-652.
71. Middlebrook, R., O. Hoegh-Guldberg, and, W. Leggat, (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211, 1050-1056. (Pubitemid 351631903)
72. Cosgrove, J., and, M. Borowitzka, (2006) Applying pulse amplitude modulation (PAM) fluorometry to microalgae suspensions: Stirring potentially impacts fluorescence. Photosynthesis Res. 88, 343-350. (Pubitemid 44289256)
73. Schreiber, U., (2004) Pulse-amplitude (PAM) fluorometry and saturation pulse method. In Chlorophyll Fluorescence: A Signature of Photosynthesis (Edited by, G. Papageorgiou, and, Govindjee,), pp. 279-319. Kluwer Academic Publishers, Dordrecht, The Netherlands.
74. Davies-Colley, R. J., R. D. Pridmore, and, J. E. Hewitt, (1986) Optical properties of some freshwater phytoplanktonic algae. Hydrobiologia 133, 165-178.
75. Geider, R., and, B. Osborne, (1992) Algal Photosynthesis: The Measurement of Algal Gas Exchange. Chapman and Hall, New York.
76. Berberoglu, H., L. Pilon, and, A. Melis, (2008) Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX and tla1-CW+. Int. J. Hydrogen Energy 33, 6467-6483.
77. Morel, A., and, A. Bricaud, (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep-Sea Res. 28A, 1375-1393.
78. Tietze, F., (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Anal. Biochem. 27, 502-522.
79. Bradford, M., (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
80. Ljung, G., and, G. Box, (1978) On a measure of lack of fit in time series models. Biometrika 65, 297-303. (Pubitemid 8379490)
81. Westfall, P., and, S. Young, (1993) Resampling-Based Multiple Testing: Examples and Methods for p-Value Adjustment. Wiley, New York.
82. Kaniewska, P., S. H. Magnusson, K. R. N. Anthony, R. Reef, M. Kühl, and, O. Hoegh-Guldberg, (2011) Importance of macro- versus micro-structure in modulating light levels inside coral colonies. J. Phycol. 47, 846-860.
83. Kühl, M., Y. Cohen, T. Dalsgaard, B. B. Jørgensen, and, N. P. Revsbach, (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Prog. Ser. 117, 159-172.
84. Baker, N., (2008) Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89-113. (Pubitemid 351813025)
85. Warner, M., G. Chilcoat, F. McFarland, and, W. Fitt, (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar. Biol. 141, 31-38. (Pubitemid 36064877)
86. Gorbunov, M., Z. Kolber, M. Lesser, and, P. Falkowski, (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol. Oceanogr. 46, 75-85. (Pubitemid 32106538)
87. Hoegh-Guldberg, O., and, R. Jones, (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar. Ecol. Prog. Ser. 183, 73-86. (Pubitemid 29355165)
88. Coleman, J. R., and, B. Colman, (1980) Effect of oxygen and temperature on the efficiency of photosynthetic carbon assimilation in two microscopic algae. Plant Physiol. 65, 980-983.
89. Karako-Lampert, S., D. Katcoff, Y. Achituv, Z. Dubinsky, and, N. Stambler, (2005) Responses of Symbiodinium microadriaticum clade B to different environmental conditions. J. Exp. Mar. Biol. Ecol. 318, 11-20.
90. Rowan, R., S. M. Whitney, A. Fowler, and, D. Yellowlees, (1996) Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8, 539-553. (Pubitemid 126635926)
91. Bertucci, A., E. Tambutte, S. Tambutte, D. Allemand, and, D. Zoccola, (2010) Symbiosis-dependent gene expression in coral-dinoflagellate association: Cloning and characterization of a P-type H+-ATPase gene. Proc. R. Soc. Lond. B Biol. Sci. 277, 87-95.
92. Leggat, W., M. R. Badger, and, D. Yellowlees, (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol. 121, 1247-1255. (Pubitemid 30018510)
93. Warner, M. E., W. K. Fitt, and, G. W. Schmidt, (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: A novel approach. Plant Cell Environ. 19, 291-299.
94. Takahashi, S., and, M. Badger, (2011) Photoprotection in plants: A new light on photosystem II damage. Trends Plant Sci. 16, 53-60.
95. Takahashi, S., and, N. Murata, (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 13, 178-182.
96. Rogers, J., and, R. Davis, (2006) Application of a new micro-culturing technique to assess the effects of temperature and salinity on specific growth rates of six Symbiodinium isolates. Bull. Mar. Sci. 79, 113-126. (Pubitemid 44298554)
97. Helmuth, B. S. T., K. P. Sebens, and, T. L. Daniel, (1997) Morphological variation in coral aggregations: Branch spacing and mass flux to coral tissues. J. Exp. Mar. Biol. Ecol. 209, 233-259. (Pubitemid 27087734)
98. Dove, S., J. Ortiz, S. Enrríquez, M. Fine, P. Fisher, R. Iglesias-Prieto, D. Thornhill, and, O. Hoegh-Guldberg, (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol. Oceanogr. 51, 1149-1158.
99. Takahashi, S., S. Whitney, S. Itoh, T. Maruyama, and, M. Badger, (2008) Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium. Proc. Natl Acad. Sci. USA 105, 4203-4208. (Pubitemid 351754358)
100. Fujiki, T., and, S. Taguchi, (2002) Variability in chlorophyll a specific absorption coefficient in marine phytoplankton as a function of cell size and irradiance. J. Plankton Res. 24, 859-874.
101. Haardt, H., and, H. Maske, (1987) Specific in vivo absorption coefficient of chlorophyll a at 675 nm. Limnol. Oceanogr. 32, 608-619.
102. Levy, O., Y. Achituv, Y. Yacobi, N. Stambler, and, Z. Dubinsky, (2006) The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus. J. Exp. Mar. Biol. Ecol. 328, 35-46. (Pubitemid 41814920)
103. Havaux, M., F. Tardy, J. Ravenel, D. Chanu, and, P. Parot, (1996) Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: Influence of the xanthophyll content. Plant Cell Environ. 19, 1359-1368. (Pubitemid 27103083)
104. Havaux, M., and, K. Niyogi, (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl Acad. Sci. USA 96, 8762-8767. (Pubitemid 29354865)
105. Goericke, R., and, N. A. Welschmeyer, (1992) Pigment turnover in the marine diatom Thalassiosira weissflogii. II. The 14CO2-labeling kinetics of carotenoids. J. Phycol. 28, 507-517.
106. Lohr, M., and, C. Wilhelm, (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc. Natl Acad. Sci. USA 96, 8784-8789. (Pubitemid 29354869)
107. Noctor, G., and, C. Foyer, (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249-279.
108. Noctor, G., A.-C. M. Arisi, L. Jouanin, and, C. H. Foyer, (1999) Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. J. Exp. Bot. 50, 1157-1167.
109. Crawley, A., D. I. Kline, S. Dunn, K. E. N. Anthony, and, S. Dove, (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol. 16, 851-863.
110. Dalle-Donne, I., R. Rossi, G. Colombo, D. Giustarini, and, A. Milzani, (2009) Protein S-glutathionylation: A regulatory device from bacteria to humans. Trends Biochem. Sci. 34, 85-96.
111. Bouchard, J. N., and, H. Yamasaki, (2009) Implication of nitric oxide in the heat-stress-induced cell death of the symbiotic alga Symbiodinium microadriaticum. Mar. Biol. 156, 2209-2220.
112. Marrs, K. A., (1996) The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 127-158.
113. Brown, B., C. Downs, R. Dunne, and, S. Gibb, (2002) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 242, 119-129. (Pubitemid 35352840)
114. Foyer, C. H., and, S. Shigeoka, (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 155, 93-100.
115. Sampayo, E. M., L. Franceschinis, O. V. E. Hoegh-Guldberg, and, S. Dove, (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol. Ecol. 16, 3721-3733. (Pubitemid 47383098)
116. Glynn, P. W., J. L. Maté, A. C. Baker, and, M. Calderõn, (2001) Coral bleaching and mortality in Panama and Ecuador during the 19971998 El Nino Southern Oscillation Event: Spatial/temporal patterns and comparisons with the 19821983 event. Bull. Mar. Sci. 69, 79-109. (Pubitemid 33037252)
117. Magalon, H., J. F. Flot, and, E. Baudry, (2007) Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26, 551-558. (Pubitemid 350104747)
118. Santos, S., D. Taylor, and, M. Coffroth, (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. J. Phycol. 37, 900-912. (Pubitemid 33017016)
119. Salih, A., A. Larkum, G. Cox, M. Kühl, and, O. Hoegh-Guldberg, (2000) Fluorescent pigments in corals are photoprotective. Nature 408, 850-853. (Pubitemid 32016093)