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

Volumn 16, Issue 1, 2011, Pages 69-80

  Rosic, Nedeljka N ^a   Pernice, Mathieu ^a,b   Dove, Sophie ^a   Dunn, Simon ^a   Hoegh Guldberg, Ove ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Coral bleaching; Dinoflagellate; Heat stress; HSP; Real time RT PCR; Symbiodinium

Indexed keywords

HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90;

ARTICLE; BLEACHING; CONTROLLED STUDY; CORAL; DINOFLAGELLATE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HEAT ACCLIMATIZATION; HEAT STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTOZOAL GENETICS; SYMBIODINIUM; UNINDEXED SEQUENCE; WATER TEMPERATURE;

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

EID: 79951674462     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-010-0222-x     Document Type: Article

References (76)

1. Arya R, Mallik M, Lakhotia SC (2007) Heat shock genes-integrating cell survival and death. J Biosci 32:595-610 (Pubitemid 46708710)
2. Beissinger M, Buchner J (1998) How chaperones fold proteins. Biol Chem 379:245-259 (Pubitemid 28152087)
3. Berkelmans R (2002) Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Mar. Ecol Prog Ser 229:73-82 (Pubitemid 34305641)
4. Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18:219-228 (Pubitemid 29478081)
5. Bettencourt BR, Feder ME (2001) Hsp70 duplication in the Drosophila melanogaster species group: How and when did two become five? Molecular Biology and Evolution 18:1272-1282 (Pubitemid 32660672)
6. Bijlsma R, Loeschcke V (2005) Environmental stress, adaptation and evolution: an overview. J Evol Biol 18:744-749 (Pubitemid 40968525)
7. Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the Central Red Sea. Science 329:322-325
8. Chen B, Zhong D, Monteiro A (2006) Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics. doi:10.1186/1471-2164-7-156 (Pubitemid 44151610)
9. Cheng L, Hirst K, Piper PW (1992) Authentic temperatureregulation of a heat shock gene inserted into yeast on a high copy number vector. Influences of overexpression of HSP90 protein on high temperature growth and thermotolerance. Biochim Biophys Acta: Gene Struct Expression 1132:26-34
10. Clark MS, Peck LS (2009a) HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: a minireview. Mar. Genom 2:11-18
11. Clark MS, Peck LS (2009b) Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna). Cell Stress Chaperones 14:649-660
12. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19-34 (Pubitemid 40728123)
13. Császár NBM, Ralph PJ, Frankham R, Berkelmans R, van Oppen MJH (2010) Estimating the potential for adaptation of corals to climate warming. PLoS ONE 5: e9751
14. Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79:129-168 (Pubitemid 28380440)
15. DeSalvo MK, Sunagawa S, Fisher PL, Voolstra CR, Iglesias-Prieto R, Medina M (2010a) Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol Ecol 19:1174-1186
16. DeSalvo MK, Sunagawa S, Voolstra CR, Medina M (2010b) Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar. Ecol Prog Ser 402:97-113
17. Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar. Ecol Prog Ser 272:99-116 (Pubitemid 38831286)
18. 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 (Pubitemid 32140026)
19. Fast NM, Xue L, Bingham S, Keeling PJ (2002) Re-examining alveolate evolution using multiple protein molecular phylogenies. J Eukaryot Microbiol 49:30-37 (Pubitemid 34231466)
20. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61:243-282 (Pubitemid 29143171)
21. Felsenstein J (1989) PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5:164-166
22. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar. Biol Ecol 373:102-110
23. Gao Q, Zhao J, Song L, Qiu L, Yu Y, Zhang H, Ni D (2008) Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians. Fish Shellfish Immunol 24:379-385
24. 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
25. 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
26. Gupta RS (1995) Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12:1063-1073
27. 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)
28. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science (New York, NY) 318:1737-1742
29. Hoffman AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Evolutionary genetics and environmental stress: 284
30. Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97:4392-4397 (Pubitemid 30226143)
31. 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
32. IPCC (2007) The Physical Science Basis-Summary for Policymakers. Intergovernmental Panel on Climate Change 2007
33. Iwama GK, Afonso LO, Todgham A, Ackerman P, Nakano K (2004) Are hsps suitable for indicating stressed states in fish? J Exp Biol 207:15-19 (Pubitemid 38069896)
34. Kabani M, Martineau CN (2008) Multiple Hsp70 isoforms in the eukaryotic cytosol: mere redundancy or functional specificity? Curr Genomics 9:338-348
35. Krone PH, Evans TG, Blechinger SR (2003) Heat shock gene expression and function during zebrafish embryogenesis. Semin Cell Dev Biol 14:267-274 (Pubitemid 38160951)
36. 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 (Pubitemid 37207606)
37. 2-terminal threonine residues. J Biol Chem 264:17275-17280 (Pubitemid 19255559)
38. 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 (Pubitemid 47495870)
39. Leignel V, Cibois M, Moreau B, Chenais B (2007) Identification of new subgroup of HSP70 in Bythograeidae (hydrothermal crabs) and Xanthidae. Gene 396:84-92 (Pubitemid 46818781)
40. Lesser MP (2007) Coral reef bleaching and global climate change: can corals survive the next century? Proc Natl Acad Sci USA 104:5259-5260 (Pubitemid 47175667)
41. Li Z, Srivastava P (2004) Heat-shock proteins. Curr Protoc Immunol Appendix 1:Appendix 1T
42. Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chap 6:201-208 (Pubitemid 32912004)
43. Luan W, Li F, Zhang J, Wen R, Li Y, Xiang J (2010) Identification of a novel inducible cytosolic Hsp70 gene in Chinese shrimp Fenneropenaeus chinensis and comparison of its expression with the cognate Hsc70 under different stresses. Cell Stress Chaperones 15:83-93
44. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050-1056 (Pubitemid 351631903)
45. Middlebrook R, Anthony KR, Hoegh-Guldberg O, Dove S (2010) Heating rate and symbiont productivity are key factors determining thermal stress in the reef-building coral Acropora formosa. J Exp Biol 213:1026-1034
46. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, Van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4
47. Pearl LH, Prodromou C, Workman P (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410:439-453 (Pubitemid 351429015)
48. 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 (Pubitemid 41773271)
49. Potts DC, Swart PK (1984) Water temperature as an indicator of environmental variability on a coral reef. Limnol Oceanogr 29:504-516
50. Ramya TNC, Surolia N, Surolia A (2006) 15-Deoxyspergualin modulates Plasmodium falciparum heat shock protein function. Biochem Biophys Res Commun 348:585-592 (Pubitemid 44188604)
51. Richier S, Furla P, Plantivaux A, Merle P-L, Allemand D (2005) Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208:277-285 (Pubitemid 40307231)
52. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18:5101-5114
53. Rosic NN, Hoegh-Guldberg O (2010) A method for extracting a highquality RNA from Symbiodinium sp. J Appl Phycol 22:139-146
54. Rosic NN, Pernice M, Dunn S, Dove S, Hoegh-Guldberg O (2010a) Novel cytochrome P450 genes from the symbiotic dinoflagellates of reef-building corals: differential regulation by heat stress. Appl Environ Microbiol 76:2823-2829
55. Rosic NN, Pernice M, Rodriguez-Lanetty M, Hoegh-Guldberg O (2010b) Validation of housekeeping genes for gene expression studies in Symbiodinium exposed to thermal and light stress. Marine Biotechnology doi:. doi:10.1007/s10126-010-9308-9
56. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336-342 (Pubitemid 28557387)
57. Rutherford S, Hirate Y, Swalla BJ (2007) The Hsp90 capacitor, developmental remodeling, and evolution: the robustness of gene networks and the curious evolvability of metamorphosis. Crit Rev Biochem Mol Biol 42:355-372 (Pubitemid 47537267)
58. Sangster TA, Salathia N, Lee HN, Watanabe E, Schellenberg K, Morneau K, Wang H, Undurraga S, Queitsch C, Lindquist S (2008) HSP90-buffered genetic variation is common in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:2969-2974 (Pubitemid 351723652)
59. Sharp VA, Brown BE, Miller D (1997) Heat shock protein (hsp 70) expression in the tropical reef coral Goniopora djiboutiensis. J Therm Biol 22:11-19 (Pubitemid 27164603)
60. Sorensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025-1037 (Pubitemid 37365491)
61. 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 (Pubitemid 351754358)
62. Takahashi S, Whitney SM, Badger MR (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci USA 106:3237-3242
63. Theodoraki MA, Mintzas AC (2006) cDNA cloning, heat shock regulation and developmental expression of the hsp83 gene in the Mediterranean fruit fly Ceratitis capitata. Ins Mol Biol 15:839-852 (Pubitemid 44952718)
64. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680 (Pubitemid 24354800)
65. 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
66. Van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863-3883 (Pubitemid 44607139)
67. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034. Doi: 10.1186/gb-2002-3-7-research0034
68. Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069-1080 (Pubitemid 351644644)
69. 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 10:627
70. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199-223 (Pubitemid 47513191)
71. Walker NJ (2002) Tech. Sight. A technique whose time has come. Science 296:557-559
72. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059-3066
73. Yamada K, Nishimura M (2008) Cytosolic heat shock protein 90 regulates heat shock transcription factor in Arabidopsis thaliana. Plant Signal Behav 3:660-662
74. Young JC, Moarefi I, Ulrich Hartl F (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154:267-273 (Pubitemid 34286138)
75. Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5:781-791 (Pubitemid 39336272)
76. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94:471-480 (Pubitemid 28391863)