Sex, Scavengers, and Chaperones: Transcriptome Secrets of Divergent Symbiodinium Thermal Tolerances

Molecular Biology and Evolution

Volumn 33, Issue 9, 2016, Pages 2201-2215

  Levin, Rachel A ^a   Beltran, Victor H ^b   Hill, Ross ^c   Kjelleberg, Staffan ^a,d   McDougald, Diane ^a,d,e   Steinberg, Peter D ^a,f   Van Oppen, Madeleine J H ^b,g  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^f SYDNEY INSTITUTE OF MARINE SCIENCE   (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

acclimation; bleaching; coral; dinoflagellate; Symbiodinium; thermal tolerance; transcriptomics

Indexed keywords

CHAPERONE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTOME;

ARTICLE; BACTERIAL OVERGROWTH; BLEACHING; CLIMATE CHANGE; CORAL REEF; DNA MODIFICATION; DOWN REGULATION; ENVIRONMENTAL STRESS; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ANALYSIS; GENETIC VARIABILITY; HEAT STRESS; HEAT TOLERANCE; MEIOSIS; MICROBIAL COMMUNITY; NONHUMAN; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; POPULATION; PROTEIN BINDING; PROTEIN FOLDING; REPRODUCTION; SEA SURFACE TEMPERATURE; SYMBIODINIUM; TRANSCRIPTOMICS; UPREGULATION; ACCLIMATIZATION; ADAPTATION; ANIMAL; ANTHOZOA; DINOFLAGELLATE; GENETICS; HEAT; METABOLISM; SYMBIOSIS;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTHOZOA; CLIMATE CHANGE; CORAL REEFS; DINOFLAGELLIDA; HOT TEMPERATURE; MOLECULAR CHAPERONES; PHOTOSYNTHESIS; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TRANSCRIPTOME;

EID: 84995529982     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw119     Document Type: Article

References (121)

1. Alavi M, Miller T, Erlandson K, Schneider R, Belas R. 2001. Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environ Microbiol 3:380-396.
2. Arbeitman MN, Furlong EEM, Imam F, Johnson E, Null BH, Baker BS, KrasnowMA, ScottMP, Davis RW, White KP. 2002. Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270-2275.
3. Argueso JL, Wanat J, Gemici Z, Alani E. 2004. Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168:1805-1816.
4. Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, LaJeunesse TC, Voolstra CR. 2014. Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencingbased genotyping of the ITS2 rDNA region. Mol Ecol 23: 4418-4433.
5. Baldi P, Hatfield GW. 2002. DNA microarrays and gene expression: from experiments to data analysis and modeling. Cambridge: Cambridge University Press.
6. Barnes DDJ, Chalker BBE. 1990. Calcification and photosynthesis in reefbuilding corals and algae. In: Dubinsky Z, editor. Ecosystems of the world. Vol. 25 Coral Reefs. Amsterdam: Elsevier. p. 109-131.
7. Barshis DJ, Ladner JT, Oliver TA, Palumbi SR. 2014. Lineage-specific transcriptional profiles of Symbiodinium spp. unaltered by heat stress in a coral host. Mol Biol Evol 31:1343-1352.
8. Baumgarten S, Bayer T, Aranda M, Liew YJ, Carr A, Micklem G, Voolstra CR. 2013. Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reefbuilding corals. BMC Genomics 14:704.
9. Bay RA, Palumbi SR. 2015. Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol Evol 7:1602-1612.
10. Bayer T, Aranda M, Sunagawa S, Yum LK, DeSalvo MK, Lindquist E, Coffroth MA, Voolstra CR, Medina M. 2012. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 7:e35269.
11. Becks L, Agrawal AF. 2012. The evolution of sex is favoured during adaptation to new environments. PLoS Biol 10:e1001317.
12. Bita CE, Gerats T. 2013. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273
13. Bocker T, Barusevicius A, Snowden T, Rasio D, Guerrette S, Robbins D, Schmidt C, Burczak J, Croce CM, Copeland T. 1999. hMSH5 a human MutS homologue that forms a novel heterodimer with hMSH4 and is expressed during spermatogenesis. Cancer Res 59:816-822.
14. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120.
15. Bravo I, Figueroa RI. 2014. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2:11-32.
16. Bruce TJA, Matthes MC, Napier JA, Pickett JA. 2007. Stressful "memories" of plants: evidence and possible mechanisms. Plant Sci 173:603-608.
17. Cao L, Alani E, Kleckner N. 1990. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61:1089-1101.
18. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, De Vantier L. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560-563.
19. Castells-Roca L, Garca-Martnez J, Moreno J, Herrero E, Bell-G, Pérez-Ortn JE. 2011. Heat shock response in yeast involves changes in both transcription rates and mRNA stabilities. PLoS One 6:e17272.
20. Chen Y, Lun ATL, Smyth GK. 2014. Differential expression analysis of complex RNA-seq experiments using edgeR. In: Datta S, Nettleton D, editors. Statistical analysis of next generation sequencing data. New York: Springer. p. 51-74.
21. Chi J, Parrow MW, Dunthorn M. 2014. Cryptic sex in Symbiodinium (Alveolata, Dinoflagellata) is supported by an inventory of meiotic genes. J EukMicrobiol 61:322-327.
22. Chiba Y, Mineta K, Hirai MY, Suzuki Y, Kanaya S, Takahashi H, Onouchi H, Yamaguchi J, Naito S. 2013. Changes inmRNA stability associated with cold stress in Arabidopsis cells. Plant Cell Physiol 54:180-194.
23. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. 2005. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90-93.
24. D'Souza TG, Michiels NK. 2010. The costs and benefits of occasional sex: theoretical predictions and a case study. J Hered 101:S34-S41.
25. De Salvo MK, Sunagawa S, Fisher PL, Voolstra CR, Iglesias-Prieto R, Medina M. 2010. Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol Ecol 19:1174-1186.
26. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM. 2002. Oxidative stress and seasonal coral bleaching. Free Radical Biol Med 33:533-543.
27. Figueroa RI, Rengefors K, Bravo I, Bensch S. 2010. From homothally to heterothally: mating preferences and genetic variation within clones of the dinoflagellate Gymnodinium catenatum. Deep Sea Res Part II: Top Stud Oceanogr 57:190-198.
28. Fitt WK, Brown BE, Warner ME, Dunne RP. 2001. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51-65.
29. Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909-930.
30. Gordon BR, Leggat W. 2010. Symbiodinium-invertebrate symbioses and the role of metabolomics. Mar Drugs 8:2546-2568.
31. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644-652.
32. Granados-Cifuentes C, Neigel J, Leberg P, Rodriguez-Lanetty M. 2015. Genetic diversity of free-living Symbiodinium in the Caribbean: the importance of habitats and seasons. Coral Reefs 34:927-939.
33. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494-1512.
34. Hand SC, Hardewig I. 1996. Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Ann Rev Physiol 58:539-563.
35. Harb A, Krishnan A, Ambavaram MMR, Pereira A. 2010. Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254-1271.
36. Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H. 2007. The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. Plant Cell 19:3090-3099.
37. Hennon GMM, Ashworth J, Groussman RD, Berthiaume C, Morales RL, Baliga NS, Orellana MV, Armbrust EV. 2015. Diatom acclimation to elevated CO2 via cAMP signalling and coordinated gene expression. Nat Clim Change 5:761-765.
38. Her C, Wu X, Griswold MD, Zhou F. 2003. Human MutS homologue MSH4 physically interacts with von Hippel-Lindau tumor suppressor-binding protein 1. Cancer Res 63:865-872.
39. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. 2004. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18:2557-2570.
40. Hill R, Schreiber U, Gademann R, Larkum AWD, Kühl M, Ralph PJ. 2004. Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching conditions in three species of corals. Mar Biol 144:633-640.
41. Hoegh-Guldberg O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshwater Res 50:839-866.
42. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-1742.
43. Hollingsworth NM, Ponte L, Halsey C. 1995. MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but notmismatch repair. Genes Dev 9:1728-1739.
44. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, Van Oppen MJH. 2012. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Change 2:116-120.
45. Huang Y, Niu B, Gao Y, Fu L, Li W. 2010. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680-682.
46. Keeney S. 2007. Spo11 and the formation of DNA double-strand breaks in meiosis. In: Egel R, Lankenau D, editors. Recombination and meiosis. New York: Springer. p. 81-123.
47. Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA doublestrand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375-384.
48. Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM. 2000. Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156:617-630.
49. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou H, Kolodner RD, Kucherlapati R, Pollard JW, Edelmann W. 2000. MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14:1085-1097.
50. Krueger T, Fisher PL, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Davy SK. 2015. Transcriptomic characterization of the enzymatic antioxidants FeSOD, MnSOD, APX and KatG in the dinoflagellate genus Symbiodinium. BMC Evol Biol 15:48.
51. Ladner JT, Barshis DJ, Palumbi SR. 2012. Protein evolution in two cooccurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol Biol 12:217.
52. LaJeunesse TC. 2005. "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570-581.
53. LaJeunesse TC, Thornhill DJ. 2011. Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, evolution through psbA non-coding region genotyping. PLoS One 6:e29013.
54. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW. 2004. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596-603.
55. Leggat W, Seneca F, Wasmund K, Ukani L, Yellowlees D, Ainsworth TD. 2011. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS One 6:e26687.
56. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323.
57. McCarthy DJ, Chen Y, Smyth GK. 2012. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40:4288-4297.
58. McGinty ES, Pieczonka J, Mydlarz LD. 2012. Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000-1007.
59. Modrich P, Lahue R. 1996. Mismatch repair in replication fidelity, genetic recombination, cancer biology. Annu Rev Biochem 65:101-133.
60. Morey JS, Van Dolah FM. 2013. Global analysis ofmRNA half-lives and de novo transcription in a dinoflagellate, Karenia brevis. PLoS One 8:e66347.
61. Muscatine L, Porter JW. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454-460.
62. Novak JE, Ross-Macdonald PB, Roeder GS. 2001. The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158:1013-1025.
63. Nymark M, Valle KC, Brembu T, Hancke K, Winge P, resen K, Johnsen G, Bones AM. 2009. An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS One 4:e7743.
64. Oliver TA, Palumbi SR. 2011. Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241-250.
65. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:418-422.
66. Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, Voolstra CR. 2016. Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium. Genome Biol Evol 8:665-680.
67. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem25:1605-1612.
68. Platt T, Gallegos CL, Harrison WG. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687-701.
69. Putnam HM, Mayfield AB, Fan TY, Chen CS, Gates RD. 2013. The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2. Mar Biol 160:2157-2173.
70. RagniM, Airs RL, Hennige SJ, Suggett DJ, WarnerME, Geider RJ. 2010. PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406:57-70.
71. Ralph P, Gademann R, Larkum A, KühlM. 2002. Spatial heterogeneity in active chlorophyll fluorescence and PSII activity of coral tissues. Mar Biol 141:639-646.
72. Reaka-Kudla ML, Wilson DE, Wilson EO. 1996. Biodiversity II: understanding and protecting our biological resources. Washington (DC): Joseph Henry Press.
73. Ritchie KB. 2012. Bacterial symbionts of corals and Symbiodinium. In: Rosenberg E, Gophna U, editors. Beneficialmicroorganisms inmulticellular life forms. New York: Springer. p. 139-150.
74. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140.
75. Rosic N, Kaniewska P, Chan C-KK, Ling EYS, Edwards D, Dove S, Hoegh-Guldberg O. 2014. Early transcriptional changes in the reef-building coral Acropora aspera in response to thermal and nutrient stress. BMC Genomics 15:1052.
76. Rosic N, Ling EYS, Chan C-KK, Lee HC, Kaniewska P, Edwards D, Dove S, Hoegh-Guldberg O. 2015. Unfolding the secrets of coral-algal symbiosis. ISME J 9:844-856.
77. Rosic NN, Hoegh-Guldberg O. 2010. A method for extracting a highquality RNA from Symbiodinium sp. J Appl Phycol 22:139-146.
78. Rosic NN, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O. 2011. Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chap 16:69-80.
79. Rosic NN, Pernice M, Dunn S, Dove S, Hoegh-Guldberg O. 2010. Differential regulation by heat stress of novel cytochrome P450 genes from the dinoflagellate symbionts of reef-building corals. Appl Environ Microbiol 76:2823-2829.
80. Ross C. 2014. Nitric oxide and heat shock protein 90 co-regulate temperature-induced bleaching in the soft coral Eunicea fusca. Coral Reefs 33:513-522.
81. Ross-Macdonald P, Roeder GS. 1994. Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:1069-1080.
82. Rossouw D, Olivares-Hernandes R, Nielsen J, Bauer FF. 2009. Comparative transcriptomic approach to investigate differences in wine yeast physiology and metabolism during fermentation. Appl Environ Microbiol 75:6600-6612.
83. Roth MS. 2014. The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422.
84. Schmieder R, Edwards R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863-864.
85. Sekine H, Ferreira RC, Pan-Hammarström Q, Graham RR, Ziemba B, De Vries SS, Liu J, Hippen K, Koeuth T, Ortmann W. 2007. Role forMsh5 in the regulation of Ig class switch recombination. Proc Natl Acad Sci USA 104:7193-7198.
86. Shodhan A, Lukaszewicz A, Novatchkova M, Loidl J. 2014. Msh4 and Msh5 function in SC-independent chiasma formation during the streamlined meiosis of Tetrahymena. Genetics 198:983-993.
87. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, FujiwaraM. 2013. Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399-1408.
88. Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210-3212.
89. Singh A, Grover A. 2008. Genetic engineering for heat tolerance in plants. Physiol Mol Biol Plants 14:155-166.
90. Snowden T, Acharya S, Butz C, Berardini M, Fishel R. 2004. hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437-451.
91. Srivastava HS, Singh RP. 1987. Role and regulation of L-glutamate dehydrogenase activity in higher plants. Phytochemistry 26:597-610.
92. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, Wada T, Maxwell A, Roberts K, Sugimoto-Shirasu K. 2006. Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48:206-216.
93. StatM, Bird CE, Pochon X, Chasqui L, Chauka LJ, Concepcion GT, Logan D, Takabayashi M, Toonen RJ, Gates RD. 2011. Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS One 6:e15854.
94. Stat M, Pochon X, Cowie ROM, Gates RD. 2009. Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83-96.
95. Stojic L, Brun R, Jiricny J. 2004. Mismatch repair and DNA damage signalling. DNA Repair 3:1091-1101.
96. Suggett DJ, Goyen S, Evenhuis C, Szab-o M, Pettay DT, Warner ME, Ralph PJ. 2015. Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370-381.
97. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR. 2008. And production of hydrogen peroxide by symbiodinium (Pyrrophyta) phylotypes with different thermal tolerances. J Phycol 44:948-956.
98. Photosynthesis Supek F, Bosnjak M,-Skunca N,-S muc T. 2011. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6:e21800.
99. Takahashi S, Whitney SM, BadgerMR. 2009. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci USA 106:3237-3242.
100. Tamburini BA, Tyler JK. 2005. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 25:4903-4913.
101. Tang L, Kwon S-Y, Kim SH, Kim JS, Choi JS, Cho KY, Sung CK, Kwak SS, Lee HS. 2006. Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep 25:1380-1386.
102. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG. 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531-13535.
103. Tercé-Laforgue T, Clément G, Marchi L, Restivo FM, Lea PJ, Hirel B. 2015. Resolving the role of plant NAD-glutamate dehydrogenase: III. Overexpressing individually or simultaneously the two enzyme subunits under salt stress induces changes in the leaf metabolic profile and increases plant biomass production. Plant Cell Physiol 56:1918-1925.
104. Thompson JD, Gibson T, Higgins DG. 2002. Multiple sequence alignment using ClustalWand ClustalX. Curr Protoc Bioinformatics 231-2322.
105. Tompkins JD, Wu X, Chu Y-L, Her C. 2009. Evidence for a direct involvement of hMSH5 in promoting ionizing radiation induced apoptosis. Exp Cell Res 315:2420-2432.
106. Tonk L, Bongaerts P, Sampayo EM, Hoegh-Guldberg O. 2013. SymbioGBR: a web-based database of Symbiodinium associated with cnidarian hosts on the Great Barrier Reef. BMC Ecol 13:7.
107. Tsubouchi T, Roeder GS. 2005. A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308:870-873.
108. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. 2006. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20:515-524.
109. Van Breusegem F, Slooten L, Stassart J-M, Moens T, Botterman J, Van Montagu M, Inzé D. 1999. Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol 40:515-523.
110. van Oppen MJH, Palstra FP, Piquet AMT, Miller DJ. 2001. Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond B Biol Sci 268:1759-1767.
111. Vierling E. 1991. The roles of heat shock proteins in plants. Annu Rev Plant Biol 42:579-620.
112. Wang Y, Qin J. 2003. MSH2 and ATR form a signaling module and regulate two branches of the damage response to DNAmethylation. Proc Natl Acad Sci USA 100:15387-15392.
113. Warner ME, Fitt WK, Schmidt GW. 1999. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007-8012.
114. Wilkinson SP, Fisher PL, van Oppen MJH, Davy SK. 2015. Intra-genomic variation in symbiotic dinoflagellates: recent divergence or recombination between lineages BMC Evol Biol 15:46.
115. Wilusz CJ, Wilusz J. 2004. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet 20:491-497.
116. Wu L, Fan J, Belasco JG. 2006. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci USA 103:4034-4039.
117. Xiang T, Nelson W, Rodriguez J, Tolleter D, Grossman AR. 2015. Symbiodinium transcriptome and global responses of cells to immediate changes in light intensity when grown under autotrophic or mixotrophic conditions. Plant J 82:67-80.
118. Yamashita H, Koike K. 2013. Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61:68-80.
119. Yampolsky LY, Zeng E, Lopez J, Williams PJ, Dick KB, Colbourne JK, Pfrender ME. 2014. Functional genomics of acclimation and adaptation in response to thermal stress in Daphnia. BMC Genomics 15:859.
120. Young MD, Wakefield MJ, Smyth GK, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14.
121. Method Yuyama I, Harii S, Hidaka M. 2012. Algal symbiont type affects gene expression in juveniles of the coral Acropora tenuis exposed to thermal stress. Mar Environ Res 76:41-47.