Host coenzyme Q redox state is an early biomarker of thermal stress in the coral Acropora millepora

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Lutz, Adrian ^a,b,c   Raina, Jean Baptiste ^a,b,d   Motti, Cherie A ^b   Miller, David J ^a   Van Oppen, Madeleine J H ^a,b,c  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CHLOROPHYLL; PLASTOQUINONE; REACTIVE OXYGEN METABOLITE; UBIQUINONE;

ACROPORA MILLEPORA; ALGA; ARTICLE; BLEACHING; CELL COUNT; CELL DENSITY; CELL ORGANELLE; CELL WALL; CELLULAR PARAMETERS; CONTROLLED STUDY; HOST; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MORTALITY; NECROSIS; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE SHIFT; PHOTOCHEMICAL EFFICIENCY; PHOTOCHEMICAL QUENCHING; PHOTOSYSTEM II; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SYMBIODINIUM; SYMBIONT; SYMBIOSIS; TEMPERATURE STRESS; THYLAKOID MEMBRANE; ANIMAL; ANTHOZOA; DINOFLAGELLATE; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TEMPERATURE;

ANIMALS; ANTHOZOA; BIOMARKERS; DINOFLAGELLIDA; OXIDATION-REDUCTION; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TEMPERATURE; UBIQUINONE;

EID: 84947273343     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139290     Document Type: Article

References (101)

1. Hoegh-Guldberg O, Bruno JF. The impact of climate change on the world's marine ecosystems. Science. 2010; 328(5985):1523-8. doi: 10.1126/science.1189930 PMID: 20558709
2. Hoegh-Guldberg O, Smith GJ. The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol. 1989; 129(3):279-303. doi: 10.1016/0022-0981(89) 90109-3
3. Szmant AM, Gassman NJ. The effects of prolonged "bleaching" on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs. 1990; 8(4):217-24. doi: 10.1007/BF00265014
4. Eakin CM, Lough JM, Heron SF. Climate variability and change: monitoring data and evidence for increased coral bleaching stress. In: van Oppen MJH, Lough JM, editors. Coral Bleaching: Patterns, Processes, Causes and Consequences. Berlin Heidelberg: Springer; 2009. p. 41-67.
5. Gates RD, Baghdasarian G, Muscatine L. Temperature stress causes host cell detachment in symbiotic cnidarians: Implications for coral bleaching. Biol Bull. 1992; 182(3):324-32.
6. Dunn SR, Schnitzler CE, Weis VM. Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc B. 2007; 274 (1629):3079-85. doi: 10.1098/rspb.2007.0711 PMID: 17925275
7. Lesser MP. Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N, editors. Coral Reefs: An Ecosystem in Transition: Springer Netherlands; 2011. p. 405-20.
8. Weis VM. Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol. 2008; 211(19):3059-66. doi: 10.1242/jeb.009597
9. Venn AA, Loram JE, Douglas AE. Photosynthetic symbioses in animals. J Exp Bot. 2008; 59 (5):1069-80. doi: 10.1093/jxb/erm328 PMID: 18267943
10. Warner ME, Fitt WK, Schmidt GW. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl Acad Sci U S A. 1999; 96(14):8007-12. doi: 10.1073/pnas.96.14. 8007 PMID: 10393938
11. Takahashi S, Whitney SM, Badger MR. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci U S A. 2009; 106 (9):3237. doi: 10.1073/pnas.0808363106 PMID: 19202067
12. Hill R, Brown CM, DeZeeuw K, Campbell DA, Ralph PJ. Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation. Limnol Oceanogr. 2011; 56 (1):139-46. doi: 10.4319/lo.2011.56.1.0139
13. Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 2008; 13(4):178-82. doi: 10.1016/j.tplants.2008.01.005 PMID: 18328775
14. 2 fixation mechanism in zooxanthellae. Plant Cell Environ. 1998; 21:1219-30. doi: 10.1046/j.1365-3040.1998.00345.x
15. Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Haggblom M, et al. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. PNAS. 2004; 101(37):13531-5. doi: 10.1073/pnas.0402907101 PMID: 15340154
16. Buxton L, Takahashi S, Hill R, Ralph PJ. Variability in the primary site of photosynthetic damage in Symbiodinium sp. (dinophyceae) exposed to thermal stress. J Phycol. 2012; 48:117-26. doi: 10.1111/j.1529-8817.2011.01099.x
17. Paxton CW, Davy SK, Weis VM. Stress and death of cnidarian host cells play a role in cnidarian bleaching. The Journal of Experimental Biology. 2013; 216(15):2813-20. doi: 10.1242/jeb.087858
18. Ainsworth TD, Hoegh-Guldberg O, Heron SF, Skirving WJ, Leggat W. Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. J Exp Mar Biol Ecol. 2008; 364(2):63-71. doi: 10.1016/j.jembe.2008.06.032
19. Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG. Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: Are the batteries of the reef going to run out? PLoS ONE. 2012; 7(7):e39024. doi: 10.1371/journal.pone.0039024 PMID: 22815696
20. Hawkins TD, Krueger T, Becker S, Fisher PL, Davy SK. Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals. Coral Reefs. 2014; 33(1):141-53. doi: 10.1007/s00338-013-1103-4
21. Tolleter D, Seneca François O, DeNofrio Jan C, Krediet Cory J, Palumbi Stephen R, Pringle John R, et al. Coral bleaching independent of photosynthetic activity. Curr Biol. 2013; 23(18):1782-6. doi: 10.1016/j.cub.2013.07.041 PMID: 24012312
22. Lesser MP. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs. 1997; 16(3):187-92. doi: 10.1007/s003380050073
23. Lesser MP, Farrell JH. Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs. 2004; 23(3):367-77. doi: 10.1007/s00338-004-0392-z
24. Dykens JA, Shick JM, Benoit C, Buettner GR, Winston GW. Oxygen radical production in the sea anemone Anthopleura elegantissima and its endosymbiotic algae. J Exp Biol. 1992; 168(1):219-41.
25. Bellantuono AJ, Granados-Cifuentes C, Miller DJ, Hoegh-Guldberg O, Rodriguez-Lanetty M. Coral thermal tolerance: Tuning gene expression to resist thermal stress. PLoS ONE. 2012; 7(11):e50685. doi: 10.1371/journal.pone.0050685 PMID: 23226355
26. DeSalvo MK, Estrada A, Sunagawa S, Medina M. Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs. 2012; 31(1):215-28. doi: 10.1007/s00338-011-0833-4
27. Ernster L, Forsmark-Andrée P. Ubiquinol: An endogenous antioxidant in aerobic organisms. Clin Investig. 1993; 71(8):S60-S5. doi: 10.1007/bf00226842 PMID: 8241707
28. Bentinger M, Brismar K, Dallner G. The antioxidant role of coenzyme Q. Mitochondrion. 2007; 7(S): S41-50. doi: 10.1016/j.mito.2007.02.006 PMID: 17482888
29. Nowicka B, Kruk J. Plastoquinol is more active than α-tocopherol in singlet oxygen scavenging during high light stress of Chlamydomonas reinhardtii. BBA-Bioenergetics. 2012; 1817(3):389-94. doi: 10.1016/j.bbabio.2011.12.002 PMID: 22192719
30. Hundal T, Forsmark-Andree P, Ernster L, Andersson B. Antioxidant activity of reduced plastoquinone in chloroplast thylakoid membranes. Arch Biochem Biophys. 1995; 324(1):117-22. doi: 10.1006/abbi. 1995.9920 PMID: 7503545
31. Mukai K, Itoh S, Morimoto H. Stopped-flow kinetic study of vitamin E regeneration reaction with biological hydroquinones (reduced forms of ubiquinone, vitamin K, and tocopherolquinone) in solution. J Biol Chem. 1992; 267(31):22277-81. PMID: 1429580
32. Turunen M, Olsson J, Dallner G. Metabolism and function of coenzyme Q. BBA-Biomembranes. 2004; 1660(1-2):171-99. doi: 10.1016/j.bbamem.2003.11.012 PMID: 14757233
33. Kruk J, Trebst A. Plastoquinol as a singlet oxygen scavenger in photosystem II. BBA-Bioenergetics. 2008; 1777(2):154-62. doi: 10.1016/j.bbabio.2007.10.008 PMID: 18005659
34. Yadav DK, Kruk J, Sinha RK, Pospísil P. Singlet oxygen scavenging activity of plastoquinol in photosystem II of higher plants: Electron paramagnetic resonance spin-trapping study. BBA-Bioenergetics. 2010; 1797:1807-11. doi: 10.1016/j.bbabio.2010.07.003 PMID: 20637718
35. Yamamoto Y, Yamashita S. Plasma ratio of ubiquinol and ubiquinone as a marker of oxidative stress. Mol Aspects Med. 1997; 18:79-84. doi: 10.1016/S0098-2997(97)00007-1
36. Miles L, Miles MV, Tang PH, Horn PS, Quinlan JG, Wong B, et al. Ubiquinol: A potential biomarker for tissue energy requirements and oxidative stress. Clin Chim Acta. 2005; 360(1):87-96. doi: 10.1016/j. cccn.2005.04.009
37. Lutz A, Motti CA, Freckelton ML, van Oppen MJH, Miller DJ, Dunlap WC. Simultaneous determination of coenzyme Q and plastoquinone redox states in the coral-Symbiodinium symbiosis during thermally induced bleaching. J Exp Mar Biol Ecol. 2014; 455(0):1-6. doi: 10.1016/j.jembe.2014.02.006
38. Levy O, Achituv Y, Yacobi YZ, Dubinsky Z, Stambler N. Diel 'tuning' of coral metabolism: physiological responses to light cues. J Exp Biol. 2006; 209(2):273-83. doi: 10.1242/jeb.01983
39. Gleason DF, Wellington GM. Ultraviolet radiation and coral bleaching. Nature. 1993; 365:836-8. doi: 10.1038/365836a0
40. Berkelmans R. Bleaching and mortality thresholds: How much is too much? In: Oppen MJH, Lough JM, editors. Coral Bleaching: Patterns, Processes, Causes and Consequences. Ecological Studies. 205: Springer Berlin Heidelberg; 2009. p. 103-19.
41. Schreiber U. Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee, editors. Chlorophyll Fluorescence: A signature of photosynthesis. Advances in Photosynthesis and Respiration. 19: Springer Netherlands; 2004. p. 279-319.
42. Veal CJ, Carmi M, Fine M, Hoegh-Guldberg O. Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs. 2010; 29(4):893-7. doi: 10.1007/s00338-010-0647-9
43. Warren CR. Rapid measurement of chlorophylls with a microplate reader. Journal of Plant Nutrition. 2008; 31(7):1321-32. doi: 10.1080/01904160802135092
44. Ritchie RJ. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res. 2006; 89(1):27-41. doi: 10.1007/s11120-006-9065-9 PMID: 16763878
45. van Oppen MJH, Palstra FP, Piquet AM-T, Miller DJ. Patterns of coral-dinoflagellate associations in Acropora: Significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc B. 2001; 268(1478):1759-67. doi: 10.1098/rspb.2001.1733 PMID: 11522193
46. Wilson K, Li Y, Whan V, Lehnert S, Byrne K, Moore S, et al. Genetic mapping of the black tiger shrimp Penaeus monodon with amplified fragment length polymorphism. Aquaculture. 2002; 204(3):297-309. doi: 10.1016/S0044-8486(01)00842-0
47. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol. 2004; 13(8):2445-58. doi: 10.1111/j.1365-294X.2004.02230.x PMID: 15245416
48. 2-driven acidification during the initiation of calcification. Mol Ecol. 2012; 21(10):2440-54. doi: 10.1111/j.1365-294X.2012.05554.x PMID: 22490231
49. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, et al. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature. 2011; 476 (7360):320-3. doi: 10.1038/nature10249 PMID: 21785439
50. Dunlap WC, Starcevic A, Baranasic D, Diminic J, Zucko J, Gacesa R, et al. KEGG orthology-based annotation of the predicted proteome of Acropora digitifera: ZoophyteBase-an open access and searchable database of a coral genome. BMC Genomics. 2013; 14(1):1-59. doi: 10.1186/1471-2164-14-509
51. Pinheiro JC, Bates DM. Mixed-effects models in S and S-PLUS. Chambers J, Eddy W, Härdle W, Sheather S, Tierney L, editors. New York: Springer Verlag; 2000.
52. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. Gail M, Krickeberg K, Samet J, Tsiatis A, Wong W, editors. New York: Springer; 2009.
53. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990; 9(7):811-8. doi: 10.1002/sim.4780090710 PMID: 2218183
54. Lesser MP, Stochaj WR, Tapley DW, Shick JM. Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs. 1990; 8(4):225-32. doi: 10.1007/BF00265015
55. Dunne R, Brown B. The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993-1998. Coral Reefs. 2001; 20(3):201-10. doi: 10.1007/s003380100160
56. Uthicke S, Klumpp DW. Microphytobenthos community production at a near-shore coral reef: Seasonal variation and response to ammonium recycled by holothurians. Mar Ecol Prog Ser. 1998; 169:1-11. doi: 10.3354/meps169001
57. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR. Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol. 2008; 44(4):948-56. doi: 10.1111/j.1529-8817.2008.00537.x
58. McGinty ES, Pieczonka J, Mydlarz LD. Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol. 2012; 64(4):1000-7. doi: 10.1007/s00248-012-0085-z PMID: 22767124
59. Nii CM, Muscatine L. Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): Contribution of the animal to superoxide ion production at elevated temperature. Biol Bull. 1997; 192(3):444-56.
60. Ainsworth TD, Wasmund K, Ukani L, Seneca F, Yellowlees D, Miller D, et al. Defining the tipping point. A complex cellular life/death balance in corals in response to stress. Scientific Reports. 2011; 1: 160. doi: 10.1038/srep00160 PMID: 22355675
61. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, et al. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol. 2008; 17(17):3952-71. doi: 10.1111/j.1365-294X.2008.03879.x PMID: 18662230
62. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O. Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol. 2009; 18(24):5101-14. doi: 10.1111/j.1365-294X.2009.04419.x PMID: 19900172
63. DeSalvo MK, Sunagawa S, Voolstra CR, Medina M. Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar Ecol Prog Ser. 2010; 402:97-113. doi: 10.3354/meps08372
64. Fitt WK, Warner ME. Bleaching patterns of four species of Caribbean reef corals. Biol Bull. 1995; 189 (3):298-307. doi: 10.2307/1542147
65. Warner ME, Fitt WK, Schmidt GW. 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. 1996; 19:291-9. doi: 10.1111/j.1365-3040.1996.tb00251.x
66. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change. 2011; 2(2):116-20. doi: 10.1038/nclimate1330
67. Baird AH, Bhagooli R, Ralph PJ, Takahashi S. Coral bleaching: the role of the host. Trends in Ecology & Evolution. 2009; 24(1):16-20. doi: 10.1016/j.tree.2008.09.005
68. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R. Coral bleaching: the winners and the losers. Ecology Letters. 2001; 4(2):122-31. doi: 10.1046/j.1461-0248.2001.00203.x
69. McClanahan TR, Baird AH, Marshall PA, Toscano MA. Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Marine Pollution Bulletin. 2004; 48(3-4):327-35. http://dx.doi.org/10.1016/j.marpolbul.2003.08.024. PMID: 14972585
70. Swiezewska E, Dallner G, Andersson B, Ernster L. Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves. J Biol Chem. 1993; 268(2):1494-9. PMID: 8419349
71. Matus-Ortega MG, Salmerón-Santiago KG, Flores-Herrera O, Guerra-Sánchez G, Martínez F, Rendón JL, et al. The alternative NADH dehydrogenase is present in mitochondria of some animal taxa. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics. 2011; 6(3):256-63. doi: 10.1016/j.cbd.2011.05.002
72. Genova ML, Lenaz G. New developments on the functions of coenzyme Q in mitochondria. Biofactors. 2011; 37(5):330-54. doi: 10.1002/biof.168 PMID: 21989973
73. Arroyo A, Navarro F, Navas P, Villalba JM. Ubiquinol regeneration by plasma membrane ubiquinone reductase. Protoplasma. 1998; 205(1-4):107-13. doi: 10.1007/bf01279300
74. Takahashi T, Yamaguchi T, Shitashige M, Okamoto T, Kishi T. Reduction of ubiquinone in membrane lipids by rat liver cytosol and its involvement in the cellular defence system against lipid peroxidation. Biochem J. 1995; 309(3):883. doi: 10.1042/bj3090883
75. Beyer RE, Segura-Aguilar J, Di Bernardo S, Cavazzoni M, Fato R, Fiorentini D, et al. The role of DTdiaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. Proc Natl Acad Sci U S A. 1996; 93(6):2528-32. doi: 10.1073/pnas.93.6.2528 PMID: 8637908
76. Goldstone J. Environmental sensing and response genes in cnidaria: The chemical defensome in the sea anemone Nematostella vectensis. Cell Biol Toxicol. 2008; 24(6):483-502. doi: 10.1007/s10565-008-9107-5 PMID: 18956243
77. McDonald AE, Vanlerberghe GC, Staples JF. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J Exp Biol. 2009; 212(16):2627-34. doi: 10.1242/jeb.032151
78. Morré DJ, Morré DM. Non-mitochondrial coenzyme Q. Biofactors. 2011; 37(5):355-60. doi: 10.1002/biof.156 PMID: 21674641
79. Bentinger M, Tekle M, Dallner G. Coenzyme Q-biosynthesis and functions. Biochem Biophys Res Commun. 2010; 396(1):74-9. doi: 10.1016/j.bbrc.2010.02.147 PMID: 20494114
80. Rocker MM, Noonan S, Humphrey C, Moya A, Willis BL, Bay LK. Expression of calcification and metabolism-related genes in response to elevated pCO2 and temperature in the reef-building coral Acropora millepora. Marine Genomics. 2015. doi: 10.1016/j.margen.2015.08.001
81. Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Oxford (fourth edition), UK: Oxford University Press; 2007.
82. Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S, Plantivaux A, et al. The symbiotic anthozoan: A physiological chimera between alga and animal. Integrative and Comparative Biology. 2005; 45(4):595-604. doi: 10.1093/icb/45.4.595 PMID: 21676806
83. Yamashita S, Yamamoto Y. Simultaneous detection of ubiquinol and ubiquinone in human plasma as a marker of oxidative stress. Anal Biochem. 1997; 250(1):66-73. PMID: 9234900
84. Flores-Ramírez LA, Liñán-Cabello MA. Relationships among thermal stress, bleaching and oxidative damage in the hermatypic coral, Pocillopora capitata. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2007; 146(1-2):194-202. doi: 10.1016/j.cbpc.2006.09.008
85. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P. Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS Journal. 2006; 273(18):4186-98. doi: 10.1111/j.1742-4658.2006.05414.x PMID: 16907933
86. Császár NBM, Seneca FO, van Oppen MJH. Variation in antioxidant gene expression in the scleractinian coral Acropora millepora under laboratory thermal stress. Mar Ecol Prog Ser. 2009; 392:93-102. doi: 10.3354/meps08194
87. Richier S, Furla P, Plantivaux A, Merle P-L, Allemand D. Symbiosis-induced adaptation to oxidative stress. J Exp Biol. 2005; 208(2):277-85. doi: 10.1242/jeb.01368
88. Dykens JA, Shick JM. Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature. 1982; 297(5867):579-80. doi: 10.1038/297579a0
89. 2, pH and light. Mar Ecol Prog Ser. 1995; 117:159-72.
90. Richier S, Merle PL, Furla P, Pigozzi D, Sola F, Allemand D. Characterization of superoxide dismutases in anoxia-and hyperoxia-tolerant symbiotic cnidarians. BBA-Gen Subjects. 2003; 1621(1):84-91. doi: 10.1016/S0304-4165(03)00049-7
91. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol (Lond). 2003; 552(2):335-44. doi: 10.1113/jphysiol.2003.049478
92. + leak and ROS generation: an odd couple. Free Radic Biol Med. 2005; 38(1):12-23. doi: 10.1016/j.freeradbiomed.2004.10.016 PMID: 15589367
93. Lenaz G, Genova ML. Mobility and function of Coenzyme Q (ubiquinone) in the mitochondrial respiratory chain. BBA-Bioenergetics. 2009; 1787(6):563-73. doi: 10.1016/j.bbabio.2009.02.019 PMID: 19268424
94. Smith DJ, Suggett DJ, Baker NR. Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biology. 2005; 11(1):1-11. doi: 10.1111/j.1529-8817.2003.00895.x
95. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM. Oxidative stress and seasonal coral bleaching. Free Radic Biol Med. 2002; 33(4):533-43. doi: 10.1016/S0891-5849(02)00907-3 PMID: 12160935
96. Lesser MP. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol. 2006; 68:253-78. doi: 10.1146/annurev.physiol.68.040104.110001 PMID: 16460273.
97. Szymańska R, Kruk J. Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant Cell Physiol. 2010; 51(4):537-45. doi: 10.1093/pcp/pcq017 PMID: 20164151
98. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci U S A. 1992; 89(21):10302-5. PMID: 11607337
99. Murata N, Allakhverdiev SI, Nishiyama Y. The mechanism of photoinhibition in vivo: Re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. BBA-Bioenergetics. 2012; 1817(8):1127-33. doi: 10.1016/j.bbabio.2012.02.020 PMID: 22387427
100. Lichtenthaler HK. Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res. 2007; 92 (2):163-79. doi: 10.1007/s11120-007-9204-y PMID: 17634750
101. Eugeni Piller L, Abraham M, Dörmann P, Kessler F, Besagni C. Plastid lipid droplets at the crossroads of prenylquinone metabolism. J Exp Bot. 2012; 63(4):1609-18. doi: 10.1093/jxb/ers016 PMID: 22371323