Transcriptomic changes in coral holobionts provide insights into physiological challenges of future climate and ocean change

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Kaniewska, Paulina ^a,b   Chan, Chon Kit Kenneth ^b   Kline, David ^b,c   Ling, Edmund Yew Siang ^b   Rosic, Nedeljka ^b   Edwards, David ^b   Hoegh Guldberg, Ove ^b   Dove, Sophie ^b  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BICARBONATE; CALCIUM; WNT PROTEIN; CARBON DIOXIDE; PROTEIN BINDING; SEA WATER; TRANSCRIPTOME;

ACROPORA MILLEPORA; ARTICLE; CALCIUM SIGNALING; CIRCADIAN RHYTHM; CLIMATE; CONTROLLED STUDY; CORAL; CYTOSKELETON; DNA REPAIR; DOWN REGULATION; GENE ONTOLOGY; GENETIC REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; OXIDATIVE STRESS; PH; PHOTOSYNTHESIS; POPULATION DENSITY; PROTEIN INTERACTION; RNA SEQUENCE; SEA; SYMBIODINIUM; TEMPERATURE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANALYSIS OF VARIANCE; ANIMAL; ANTHOZOA; CLIMATE CHANGE; GENE EXPRESSION PROFILING; GENETICS; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION;

ANALYSIS OF VARIANCE; ANIMALS; ANTHOZOA; CARBON DIOXIDE; CLIMATE CHANGE; GENE EXPRESSION PROFILING; GENE ONTOLOGY; OCEANS AND SEAS; PROTEIN BINDING; PROTEIN INTERACTION MAPS; SEAWATER; TEMPERATURE; TRANSCRIPTOME;

EID: 84949883822     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139223     Document Type: Article

References (112)

1. Hoegh-Guldberg O, Bruno JF (2010) The Impact of Climate Change on the World's Marine Ecosystems. Science 328:1523-1528. doi: 10.1126/science.1189930 PMID: 20558709
2. Hoegh-Guldberg O, Cai R, Poloczanska ES, Brewer PG, Sundby S, Hilmi V et al. (2014) The Ocean. In: Barros VR, Field CB, Dokken DJ, Mastrandrea MD, Mach KJet al., editors. Climate Change 2014: Impacts, Adaptation and Vulnerability Part B: Regional Aspects Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press.
3. Hoegh-Guldberg O, Mumby P, Hooten AJ, Steneck RS, Greenfield P, Gomez E et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737-1742. PMID: 18079392
4. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418-422. doi: 10.1126/science.1204794 PMID: 21778392
5. Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecological Economics 29:215-233.
6. Lough JM (2008) 10th Anniversary review: a changing climate for coral reefs. Journal of Environmental Monitoring 10:21-61. doi: 10.1039/b714627m PMID: 18175015
7. Baker AC, Glynn PW, Reigl B (2008) Climate change and coral bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine Coastal and Shelf Science 80:435-471.
8. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C et al. (2003) Climate change, human impacts and the resilience of coral reefs. Science 301:929-933. PMID: 12920289
9. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC et al. (2002) Ecological responses to recent climate change. Nature 416:389-395. PMID: 11919621
10. Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237:133-141.
11. Mendes J, Woodley J (2002) Effect of the 1995-1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band fromation in Montastrea annularis. Marine Ecology Progress Series 235:93-102.
12. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and losers. Ecology Letters 4:122-131.
13. Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspective on ocean acidification. Trends in Ecology & Evolution 25:332-345.
14. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De'ath G et al. (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim Change 1:165-169.
15. Inoue S, Kayanne H, Yamamoto S, Kurihara H (2013) Spatial community shift from hard to soft corals in acidified water. Nature Clim Change 3:683-687.
16. 2 problem. Annual Review of Marine Science 1:169-192. PMID: 21141034
17. Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: where do we draw the line? American Zoologist 39:146-159.
18. Cohen AL, McCorkle DC, De Putron S, Glenn GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochemistry Geophysics Geosystems 10:Q07005.
19. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, et al. (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19:1884-1896. doi: 10.1111/gcb.12179 PMID: 23505245
20. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences of the United States of America 105:17442-17446. doi: 10.1073/pnas.0804478105 PMID: 18988740
21. Munday P, Dixon D, Donelson J, Jones G, Pratchett M, Devitsina G, et al. (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proceeding of the National Academy of Science USA 106:1848.
22. Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Marine Ecology Progress Series 373:203-217.
23. Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, et al. (2012) Major Cellular and Physiological Impacts of Ocean Acidification on a Reef Building Coral. Plos One 7:e34659. doi: 10. 1371/journal.pone.0034659 PMID: 22509341
24. 2 emission scenario. Proceedings of the National Academy of Sciences 110:15342-15347.
25. Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Global Change Biology 18:2173-2183.
26. Rodolfo-Metalpa R, Houlbrèque F, Tambutte E, Boisson F, Baggini C, Patti FP, et al. (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 1:308-312.
27. Yara Y, Vogt M, Fujii M, Yamano H, Hauri C, Steinacher M, et al. (2012) Ocean acidification limits temperatureinduced poleward expansion of coral habitats around Japan. Biogeosciences 9:4955-4968.
28. 2-driven Acidification during the Initiation of Calcification. Molecular Ecology 21:2440-2454. doi: 10.1111/j.1365-294X. 2012.05554.x PMID: 22490231
29. 2-Driven pH Decrease in Corals: New Insights from Transcriptome Analysis. Plos One 8:e58652. doi: 10.1371/journal.pone. 0058652 PMID: 23544045
30. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, et al. (2013) Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences 110:1387-1392.
31. DeSalvo MK, Sunagawa S, Voolstra CR, Medina M (2010) Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Marine Ecology Progress Series 402:97-113.
32. DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Palumbi SR (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952-3971. doi: 10.1111/j.1365-294X.2008.03879.x PMID: 18662230
33. Maor-Landaw K, Karako-Lampert S, Ben-Asher HW, Goffredo S, Falini G, Dubinsky Z, et al. (2014) Gene expression profiles during short-term heat stress in the red sea coral Stylophora pistillata. Global Change Biology 20:3026-3035. doi: 10.1111/gcb.12592 PMID: 24706387
34. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg OVE (2009) Early molecular responses of coral larvae to hyperthermal stress. Molecular Ecology 18:5101-5114. doi: 10.1111/j.1365-294X.2009.04419.x PMID: 19900172
35. 2 and temperature levels projected for the year 2100 AD. Biogeosciences 7:289-300.
36. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. Journal of Experimental Biology 211:3059-3066. doi: 10.1242/jeb.009597 PMID: 18805804
37. Chan NCS, Connolly SR (2012) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Global Change Biology 19:282-290. doi: 10.1111/gcb.12011 PMID: 23504739
38. Harvey B, Gwynn-Jones D, Moore P (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecology and Evolution 3:1016-1030. doi: 10.1002/ece3.516 PMID: 23610641
39. Kroeker K, Kordas R, Crim R, Singh G (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13:1419-1434. doi: 10.1111/j.1461-0248. 2010.01518.x PMID: 20958904
40. Obara M, Szeliga M, Albrecht J (2008) Regulation of pH in the mammalian central nervous system under normal and pathological conditions: Facts and hypotheses. Neurochemistry International 52:905-919. PMID: 18061308
41. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Clim Change 2:623-627.
42. Venn AA, Tambutté E, Lotto S, Zoccola D, Allemand D, Tambutté S (2009) Imaging intracellular pH in a reef coral and symbiotic anemone. Proceedings of the National Academy of Sciences 106:16574-16579.
43. Venn AA, Tambutté E, Holcomb M, Laurent J, Allemand D, Tambutté S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proceedings of the National Academy of Sciences 110:1634-1639.
44. Cohen AL, Holcomb M (2009) Why Corals Care about Ocean Acidification: Uncovering the Mechanism. Oceanography 22:118-127.
45. Cooper TF, Lai M, Ulstrup KE, Saunders SM, Flematti GR, Radford B, et al. (2011) Symbiodinium Genotypic and Environmental Controls on Lipids in Reef Building Corals. Plos One 6:e20434. doi: 10.1371/journal.pone.0020434 PMID: 21637826
46. Fine M, Tchernov D (2007) Scleractinian Coral Species Survive and Recover from Decalcification. Science 315:1811. PMID: 17395821
47. 2 World at Two Temperatures. Plos One 8:e75049. doi: 10. 1371/journal.pone.0075049 PMID: 24146747
48. Ward S (1995) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14:87-90.
49. 2 driven seawater acidification in symbiotic versus non-symbiotic cells. Journal of Experimental Biology 217:1963-1969. doi: 10.1242/jeb.099549
50. Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eliat. Nature 289:172-174.
51. Baroli I, Do AD, Yamane T, Niyogi KK (2003) Zexanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. The Plant Cell 15:992-1008. PMID: 12671093
52. Chaumont D, Thepenier C (1995) Carotenoid content in growing cells of Haematococcus pluvalis during a sunlight cycle. Journal of Applied Phycology 7:529-537.
53. Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, et al. (2004) Photo-oxidative stress in the xanthophyll-deficient mutant of Chlamydomonas. Journal of Biological Chemistry 279:6337-6344. PMID: 14665619
54. Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, et al. (1999) Diurnal changes in photochemical efficiency and xantophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99-105.
55. Muller P, Li XP, Niyogi KK (2001) Non-Photochemical Quenching. A Response to Excess Light Energy. Plant Physiology 125:1558-1566. PMID: 11299337
56. Ulstrup KE, Hill R, Van Oppen MJH, Larkum AWD, Ralph PJ (2008) Seasonal variation in the photophysiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Marine Ecology-Progress Series 361:139-150.
57. Demmig-Adams B, Adams W (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1:21-26.
58. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology 5:355-362. PMID: 17384666
59. Yarden O, Ainsworth TD, Roff G, Leggat W, Fine M, Hoegh Guldberg O (2007) Increased prevalence of ubiquitous ascomycetes in an acropoid coral (Acropora formosa) exhibiting symptoms of brown band syndrome and skeletal eroding band disease. Applied and Environmental Microbiology 73:2755-2757. PMID: 17308192
60. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series 243:1-10.
61. Rosic N, Ling EYS, Chan CKK, Lee HC, Kaniewska P, Edwards D, et al. (2015) Unfolding the secrets of coral-algal symbiosis. ISME J 9:844-856. doi: 10.1038/ismej.2014.182 PMID: 25343511
62. Martin DE, Soulard A, Hall MN (2004) TOR Regulates Ribosomal Protein Gene Expression via PKA and the Forkhead Transcription Factor FHL1. Cell 119:969-979. PMID: 15620355
63. Nozawa Y (2012) Annual Variation in the Timing of Coral Spawning in a High-Latitude Environment: Influence of Temperature. The Biological Bulletin 222:192-202. PMID: 22815368
64. Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biological Reviews 74.
65. Eckel-Mahan K, Sassone-Corsi P (2013) Metabolism and the Circadian Clock Converge. Physiological Reviews 93:107-135. doi: 10.1152/physrev. 00016.2012 PMID: 23303907
66. Adamovich Y, Rousso-Noori L, Zwighaft Z, Neufeld-Cohen A, Golik M, Kraut-Cohen J, et al. (2010) Circadian Clocks and Feeding Time Regulate the Oscillations and Levels of Hepatic Triglycerides. Cell Metabolism 19:319-330.
67. Levy O, Kaniewska P, Alon S, Eisenberg E, Karako-Lampert S, Bay LK, et al. (2011) Complex diel cycles of gene expression in coral-algal symbiosis. Science 331:175. doi: 10.1126/science.1196419 PMID: 21233378
68. Mazzoccoli G, Pazienza V, Vinciguerra M (2012) Clock genes and clock-controlled genes in the regulation of metabolic rhythms. Chronobiology International 29:227-251. doi: 10.3109/07420528.2012. 658127 PMID: 22390237
69. Sha L, MacIntyre L, Machell JA, Kelly MP, Porteous DJ, Brandon NJ, et al. (2012) Transcriptional regulation of neurodevelopmental and metabolic pathways by NPAS3. Mol Psychiatry 17:267-279. doi: 10.1038/mp. 2011.73 PMID: 21709683
70. Kultz D (2005) Molecular and evolutionary basis of the cellular stress response. Annual Review of Physiology 67:225-257. PMID: 15709958
71. Perkins ND (2007) Integrating cell-signalling pathways with NF-[kappa]B and IKK function. Nat Rev Mol Cell Biol 8:49-62. PMID: 17183360
72. Bourne DG, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-assiciated microbial communities during a bleaching event. ISME J 2:350-363. PMID: 18059490
73. Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards R, Angly F, et al. (2009) Metagenomic analysis of stressed coral holobionts. Environmental Microbiology 11:2148-2163. doi: 10.1111/j.1462-2920.2009.01935.x PMID: 19397678
74. Ciechanover A (2005) Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 6:79-87. PMID: 15688069
75. Downs C, Ostrander G, Rougee L, Rongo T, Knutson S, Williams DE, et al. (2012) The use of cellular diagnostics for identifying sub-lethal stress in reef corals. Ecotoxicology 21:768-782. doi: 10.1007/s10646-011-0837-4 PMID: 22215560
76. DeSalvo MK, Estrada A, Sunagawa S, Medina M (2012) Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs 31:215-228.
77. Cui Y, Niziolek PJ, MacDonald BT, Zylstra CR, Alenina N, Robinson DR, et al. (2011) Lrp5 functions in bone to regulate bone mass. Nat Med 17:684-691. doi: 10.1038/nm.2388 PMID: 21602802
78. Bergh J, Shao Y, Puente E, Duncan R, Farach-Carson M (2006) Osteoblast Ca2+ permeability and voltage-sensitive Ca2+ channel expression is temporally regulated by 1, 25-dihydroxyvitamin D3. American Journal of Physiology. Cell Physiology 290:C822. C831. PMID: 16221734
79. Shao Y, Alicknavitch M, Farach-Carson MC (2005) Expression of voltage sensitive calcium channel (VSCC) L-type Cav1.2 (α1C) and T-type Cav3.2 (α1H) subunits during mouse bone development. Developmental Dynamics 234:54-62. PMID: 16059921
80. Allemand D, Tambutte E, Zoccola D, Tambutte S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N, editors. Coral reefs: an ecosystem in transition. London, New York: Springer. pp. 119.150.
81. Furla P, Allemand D, Orsenigo M (2000) Involvement of H+ -ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. American Journal of Physiology: Regulatory Integrative Comparative Physiology 278:R870. R881.
82. Supuran C (2008) Carbonic anhydrases.an overview. Current Pharmaceutical Design 14:603-614. PMID: 18336305
83. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071-1078. doi: 10.1038/nature08467 PMID: 19847258
84. Reyes-Nivia C, Diaz-Pulido G, Kline D, Guldberg O-H, Dove S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Global Change Biology 19:1919-1929. doi: 10.1111/gcb.12158 PMID: 23505093
85. 2 analysis: a method for the certification of total alkalinity. Marine Chemistry 80:185-197.
86. 2 system calculations. In: Carbon Dioxide Information Analysis Center ORNL, US., editor. Oak Ridage, TN: Department of Energy.
87. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18:897-907.
88. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Research 34:1733-1743.
89. Crawley A, Kline DI, Dunn S, Anthony KRN, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biology 15:851-197.
90. Barnes D, Chalker B (1990) Calcification and photosynthesis in reef-building corals and algae. In: D Z., editor. Ecosystems of the World: Vol 25, Coral Reefs. Amsterdam: Elsevier Science. pp. 109-131.
91. Zapata M, Rodriguez F, Garrrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed-phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series 195:29-45.
92. Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. Journal of Experimental Marine Biology and Ecology 153:63-74.
93. Spencer-Davies P (1989) Short-term growth measurements of coral growth using an accurate buoyant weighing technique. Marine Biology 101:389-395.
94. Whitaker JR, Granum PE (1980) An absolute method for protein determination based on differences in absorbance at 235 and 280 nm. Analytical Biochemistry 109:156-159. PMID: 7469012
95. Dunn SR, Thomas MC, Nette GW, Dove SG (2012) A Lipidomic Approach to Understanding Free Fatty Acid Lipogenesis Derived from Dissolved Inorganic Carbon within Cnidarian-Dinoflagellate Symbiosis. Plos One 7:e46801. doi: 10.1371/journal.pone.0046801 PMID: 23115631
96. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11:R25. doi: 10.1186/gb-2010-11-3-r25 PMID: 20196867
97. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protocols 7:562-578. doi: 10.1038/nprot.2012.016 PMID: 22383036
98. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136-138. doi: 10.1093/bioinformatics/btp612 PMID: 19855105
99. Martin JA, Wang Z (2011) Next-generation transcriptome assembly. Nat Rev Genet 12:671-682. doi: 10.1038/nrg3068 PMID: 21897427
100. Rosic N, Kaniewska P, Chan CKK, Ling EYS, Edwards D, Dove S, et al. (2014) Early transcriptional changes in the reef-building coral Acropora aspera in response to thermal and nutrient stress. BMC Genomics 15:1052. doi: 10.1186/1471-2164-15-1052 PMID: 25467196
101. Kurtz S, Narechania A, Stein J, Ware D (2008) A new method to compute K-mer frequencies and its application to annotate large repetitive plant genomes. BMC Genomics 9:517. doi: 10.1186/1471-2164-9-517 PMID: 18976482
102. Marçais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764-770. doi: 10.1093/bioinformatics/btr011 PMID: 21217122
103. Boutet E, Lieberherr D, Tognolli M, Schneider M, Bairoch A (2007) UniProtKB/Swiss-Prot. Methods in molecular biology 406:89-112. PMID: 18287689
104. 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. doi: 10.1371/journal.pone.0026687 PMID: 22039532
105. Rosic N, 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 and Chaperones 16:69-80. doi: 10.1007/s12192-010-0222-x PMID: 20821176
106. Walker NJ (2002) A Technique Whose Time Has Come. Science 296:557-559. PMID: 11964485
107. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple control genes. Genome Biology 3:6906-6914.
108. Meyer E, Aglyamova G, Wang S, Buchanan-Carter J, Abrego D, Colbourne J, et al. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 10:219. doi: 10.1186/1471-2164-10-219 PMID: 19435504
109. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyangi R, et al. (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Current Biology 23:1399-1408. doi: 10.1016/j.cub.2013.05.062 PMID: 23850284
110. Huang DW, Sherman BT, Lempicki RA (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protocols 4:44-57.
111. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37:1-13. doi: 10.1093/nar/gkn923 PMID: 19033363
112. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Research 39:D561-D568. doi: 10.1093/nar/gkq973 PMID: 21045058