Validation of Housekeeping Genes for Gene Expression Studies in Symbiodinium Exposed to Thermal and Light Stress

Marine Biotechnology

Volumn 13, Issue 3, 2011, Pages 355-365

  Rosic, Nedeljka N ^a   Pernice, Mathieu ^a,b   Rodriguez Lanetty, Mauricio ^c   Hoegh Guldberg, Ove ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^c UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

Author keywords

Climate change; Dinoflagellate; Gene expression; Housekeeping genes; Real time RT PCR

Indexed keywords

ACROPORA; CYCLOPHILIN; CYTOCHROME OXIDASE; DATA NORMALIZATION; DINOFLAGELLATE; ELEVATED TEMPERATURE; ENVIRONMENTAL STRESS; EXPRESSION PROFILE; HOUSEKEEPING GENE; LIGHT STRESS; MUTUALISTIC SYMBIOSIS; PHOTOSYNTHETIC ACTIVE RADIATIONS; REAL TIME RT-PCR; RIBOSOMAL PROTEINS; S-ADENOSYL METHIONINES; STABLE EXPRESSION; SYNTHETASES;

AMINO ACIDS; CALMODULIN; CLIMATE CHANGE; THERMAL STRESS; THERMOELASTICITY;

GENE EXPRESSION;

PRIMER DNA;

ALGA; CELL ORGANELLE; CLADISTICS; CLIMATE CHANGE; CORAL; DATA SET; DINOFLAGELLATE; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; GENE EXPRESSION; IDENTIFICATION METHOD; LIGHT EFFECT; MUTUALISM; PHOTOSYNTHESIS; POLYMERASE CHAIN REACTION; RADIATION BALANCE; TEMPERATURE EFFECT;

ARTICLE; BIOLOGY; DINOFLAGELLATE; ESSENTIAL GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEAT; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

COMPUTATIONAL BIOLOGY; DINOFLAGELLIDA; DNA PRIMERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, ESSENTIAL; HOT TEMPERATURE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL;

ACROPORA MILLEPORA; ALGAE; ANTHOZOA; DINOPHYCEAE; SYMBIODINIUM; SYMBIODINIUM SP.;

EID: 79957981213     PISSN: 14362228     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10126-010-9308-9     Document Type: Article

References (95)

1. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem. II. Inactivation, protein damage and turnover. Biochim Biophys Acta Bioenerg 1143: 113-134.
2. Arya R, Mallik M, Lakhotia SC (2007) Heat shock genes-integrating cell survival and death. J Biosci 32: 595-610.
3. Banin E, Israely T, Fine M, Loya Y, Rosenberg E (2001) Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol Lett 199: 33-37.
4. Bay LK, Ulstrup KE, Nielsen HB, Jarmer H, Goffard N, Willis BL, Miller DJ, van Oppen MJH (2009) Microarray analysis reveals transcriptional plasticity in the reef building coral Acropora millepora. Mol Ecol 18: 3062-3075.
5. Bouchard JN, Yamasaki H (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.
6. Bustin SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29: 23-39.
7. Bustin SA, Benes V, Nolan T, Pfaffl MW (2005) Quantitative real-time RT-PCR-a perspective. J Mol Endocrinol 34: 597-601.
8. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156: 19-34.
9. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43: 209-216.
10. de Kok JB, Roelofs RW, Giesendorf BA et al (2005) Normalization of gene expression measurements in tumor tissues: comparison of 13 endogenous control genes. Lab Invest 85: 154-159.
11. DeSalvo MK, Voolstra CR, Sunagawa S et al (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17: 3952-3971.
12. DeSalvo 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.
13. Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Gulberg O (2005) Global assessment of coral bleaching and required rates of adaptation under climate change. Glob Chang Biol 11: 2251-2265.
14. Dove S, Ortiz JC, Enríquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51: 1149-1158.
15. Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM (2000) A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar Biotechnol 2: 533-544.
16. Downs CA, Fauth JE, Robinson CE et al (2005) Cellular diagnostics and coral health: declining coral health in the Florida Keys. Mar Pollut Bull 51: 558-569.
17. Dunn SR, Weis VM (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ Microbiol 11: 268-276.
18. Dunn SR, Thomason JC, Le Tissier MDA, Bythell JC (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.
19. Filby AL, Tyler CR (2007) Appropriate 'housekeeping' genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol Biol 8. doi: 10. 1186/1471-2199-8-10.
20. Fine M, Meroz-Fine E, Hoegh-Guldberg O (2005) Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J Exp Biol 208: 75-81.
21. Fitt WK, Cook CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Mar Biol 139: 507-517.
22. Fu A, He Z, Cho HS et al (2007) A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 15947-15952.
23. Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203: 3445-3457.
24. Gattuso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool 39: 160-183.
25. Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallidal Symbiodinium symbiosis. Limnol Oceanogr 50: 1490-1498.
26. Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 8: 229-239.
27. Gunter HM, Degnan BM (2007) Developmental expression of Hsp90, Hsp70 and HSF during morphogenesis in the vetigastropod Haliotis asinina. Dev Genes Evol 217: 603-612.
28. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshwater Res 50: 839-866.
29. Hoegh-Guldberg O, Salvat B (1995) Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slopes in Moorea French Polynesia. Mar Ecol Prog Ser 21: 81-88.
30. Hoegh-Guldberg O, Smith GJ (1989) 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 129: 279-303.
31. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science (New York, NY) 318: 1737-1742.
32. Hofmann GE, O'Donnell MJ, Todgham AE (2008) Using functional genomics to explore the effects of ocean acidification on calcifying marine organisms. Mar Ecol Prog Ser 373: 219-225.
33. Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalisation; strategies and considerations. Genes Immun 6: 279-284.
34. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89: 10302-10305.
35. Jian B, Liu B, Bi Y et al (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Mol Biol 9.
36. Kampinga HH (2006) Chaperones in preventing protein denaturation in living cells and protecting against cellular stress. Handb Exp Pharmacol 1-42.
37. Karako-Lampert S, Hershkovits G, Stambler N et al (2006) Differential gene expression in Symbiodinium microadriaticum clade B following stress. Mar Biotechnol 8: 268-274.
38. Krone PH, Evans TG, Blechinger SR (2003) Heat shock gene expression and function during zebrafish embryogenesis. Semin Cell Dev Biol 14: 267-274.
39. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48: 2046-2054.
40. Leggat W, Hoegh-Guldberg O, Dove S, Yellowlees D (2007) Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef-building corals. J Phycol 43: 1010-1021.
41. Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41: 271-283.
42. Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300: 217-252.
43. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23: 367-377.
44. Li Z, Srivastava P (2004) Heat-shock proteins. Curr Protoc Immunol Appendix 1, Appendix 1T.
45. Lopez-Legentil S, Song B, McMurray SE, Pawlik JR (2008) Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Mol Ecol 17: 1840-1849.
46. Manchado M, Salas-Leiton E, Infante C et al (2008) Molecular characterization, gene expression and transcriptional regulation of cytosolic HSP90 genes in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 416: 77-84.
47. Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a real-time quantitative polymerase chain reaction protocol for symbiotic anthozoans. Mol Ecol Resour 9: 462-470.
48. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26: 449-457.
49. Mieog JC, van Oppen MJH, Berkelmans R, Stam WT, Olsen JL (2009) Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Resour 9: 74-82.
50. Mitchelmore CL, Schwarz JA, Weis VM (2002) Development of symbiosis-specific genes as biomarkers for the early detection of cnidarian-algal symbiosis breakdown. Mar Environ Res 54: 345-349.
51. Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56: 2907-2914.
52. Odunuga OO, Longshaw VM, Blatch GL (2004) Hop: more than an Hsp70/Hsp90 adaptor protein. BioEssays 26: 1058-1068.
53. Parker R, Flowers TJ, Moore AL, Harpham NVJ (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57: 1109-1118.
54. Pearl LH, Prodromou C, Workman P (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410: 439-453.
55. Perez S, Weis V (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209: 2804-2810.
56. Perez S, Weis V (2008) Cyclophilin and the regulation of symbiosis in Aiptasia pallida. Biol Bull 215: 63-72.
57. Perez SF, Cook CB, Brooks WR (2001) The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 256: 1-14.
58. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38: 20-30.
59. Radonic A, Thulke S, Mackay IM et al (2004) Guideline to reference gene selection for quantitative real-time PCR. Biochem Biophys Res Commun 313: 856-862.
60. Richier S, Rodriguez-Lanetty M, Schnitzler CE, Weis VM (2008) Response of the symbiotic cnidarian Anthopleura elegantissima transcriptome to temperature and UV increase. Comp Biochem Physiol D Genomics Proteomics 3: 283-289.
61. Roberts PC (2008) Gene expression microarray data analysis demystified. Biotechnol Annu Rev 14: 29-61.
62. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42: 568-579.
63. Rodriguez-Lanetty M, Phillips WS, Weis VM (2006) Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7.
64. Rodriguez-Lanetty M, Phillips WS, Dove S, Hoegh-Guldberg O, Weis VM (2008) Analytical approach for selecting normalizing genes from a cDNA microarray platform to be used in q-RT-PCR assays: a cnidarian case study. J Biochem Biophys Meth 70: 985-991.
65. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18: 5101-5114.
66. Rosic NN, Hoegh-Guldberg O (2010) A method for extracting a high-quality RNA from Symbiodinium sp. J Appl Phycol 22: 139-146.
67. 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.
68. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105: 10444-10449.
69. Schmittgen TD, Zakrajsek BA (2000) Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Meth 46: 69-81.
70. Schwarz JA, Brokstein PB, Voolstra C et al. (2008) Erratum: Coral life history and symbiosis: Functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9.
71. Silveira ED, Alves-Ferreira M, Guimaraes LA, da Silva FR, Carneiro VT (2009) Selection of reference genes for quantitative real time PCR expression studies in the apomictic and sexual grass Brachiaria brizantha. BMC Plant Biol 9: 84.
72. Smith-Keune C, Dove S (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Mar Biotechnol 10: 166-180.
73. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts-symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8: 23-43.
74. Strychar KB, Sammarco PW (2009) Exaptation in corals to high seawater temperatures: low concentrations of apoptotic and necrotic cells in host coral tissue under bleaching conditions. J Exp Mar Biol Ecol 369: 31-42.
75. Stürzenbaum SR, Kille P (2001) Control genes in quantitative molecular biological techniques: the variability of invariance. Comp Biochem Physiol B Biochem Mol Biol 130: 281-289.
76. Sunagawa S, DeSalvo MK, Voolstra CR, Reyes-Bermudez A, Medina M (2009) Identification and gene expression analysis of a taxonomically restricted cysteine-rich protein family in reef-building corals. PLoS ONE 4.
77. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13: 178-182.
78. Takahashi S, Whitney S, Itoh S, Maruyama T, Badger M (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.
79. Thellin O, Zorzi W, Lakaye B et al (1999) Housekeeping genes as internal standards: use and limits. J Biotechnol 75: 291-295.
80. Timofeev M, Shatilina Zh M, Bedulina DS, Protopopova MV, Kolesnichenko AV (2008) Application of heat shock proteins as stress markers in aquatic organisms using endemic Baikal amphipods as an example. Prikl Biokhim Mikrobiol 44: 343-346.
81. Toffaletti DL, Del Poeta M, Rude TH, Dietrich F, Perfect JR (2003) Regulation of cytochrome c oxidase subunit 1 (COX1) expression in Cryptococcus neoformans by temperature and host environment. Microbiology 149: 1041-1049.
82. Trapido-Rosenthal HG, Sharp KH, Galloway TS, Morrall CE (2001) Nitric oxide and cnidarian-dinoflagellate symbioses: pieces of a puzzle. Am Zool 41: 247-257.
83. Trapido-Rosenthal H, Zielke S, Owen R et al (2005) Increased zooxanthellae nitric oxide synthase activity is associated with coral bleaching. Biol Bull 208: 3-6.
84. Ulstrup KE, van Oppen MJ (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12: 3477-3484.
85. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15: 3863-3883.
86. Vandesompele J, De Preter K, Pattyn F et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, RESEARCH0034.
87. VanGuilder HD, Vrana KE, Freeman WM (2008) Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques 44: 619-626.
88. Voolstra CR, Schnetzer J, Peshkin L, Randall CJ, Szmant AM, Medina M (2009) Effects of temperature on gene expression in embryos of the coral Montastraea faveolata. BMC Genomics 10.
89. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61: 199-223.
90. Walker NJ (2002) Tech. Sight. A technique whose time has come. Science 296: 557-559.
91. 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.
92. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211: 3059-3066.
93. Wong ML, Medrano JF (2005) Real-time PCR for mRNA quantitation. Biotechniques 39: 75-85.
94. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31: 679-694.
95. Zhang XY, Zhang MZ, Zheng CJ, Liu J, Hu HJ (2009) Identification of two hsp90 genes from the marine crab, Portunus trituberculatus and their specific expression profiles under different environmental conditions. Comp Biochem Physiol C Toxicol Pharmacol 150: 465-473.