Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Díaz, Noelia ^a,b   Piferrer, Francesc ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

Epigenetics; Gonadal development; Sex ratio; Temperature

Indexed keywords

TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY GROWTH; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIGENETICS; EUROPEAN SEA BASS; FEMALE; GENE EXPRESSION; GONAD; MALE; MICROARRAY ANALYSIS; NONHUMAN; REPRODUCTION; SEX DETERMINATION; SEX DIFFERENTIATION; SEX RATIO; TEMPERATURE SENSITIVITY; UPREGULATION; VALIDATION PROCESS; ANIMAL; BASS; BIOLOGY; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; QUANTITATIVE TRAIT; REPRODUCIBILITY; TEMPERATURE;

ANIMALS; BASS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GONADS; MALE; QUANTITATIVE TRAIT, HERITABLE; REPRODUCIBILITY OF RESULTS; REPRODUCTION; SEX DETERMINATION ANALYSIS; SEX DIFFERENTIATION; SEX RATIO; STRESS, PHYSIOLOGICAL; TEMPERATURE; TRANSCRIPTOME;

EID: 84940770860     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1862-0     Document Type: Article

References (83)

1. Sultan SE. Development in context: the timely emergence of eco-devo. Trends Ecol Evol. 2007;22:575-282.
2. Somero GN. General Principles of Biochemical Adaptations. San Diego: Academic; 2011.
3. Beitinger TL, Lutterschmidt WI. Measures of Thermal Tolerance. In: Farrell AP, Stevens ED, Cech JJ, Richard JG (eds.), Encyclopedia of fish physiology from genome to environment. Oxford, UK: Academic Press; 2011: 1695-1702.
4. Schulte PM, Healy TM, Fangue NA. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol. 2011;51:691-702.
5. Nelson JS. Fishes of the World. New York: Wiley-Interscience; 2006.
6. Devlin RH, Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquacult. 2002;208:191-364.
7. Penman DJ, Piferrer F. Fish gonadogenesis. Part 1. Genetic and environmental mechanisms of sex determination. Rev Fish Sci. 2008;16(Suppl. 1):14-32.
8. Kikuchi K, Hamaguchi S. Novel Sex-determining genes in fish and sex chromosome evolution. Dev Dyn. 2013;242:339-53.
9. Heule C, Salzburger W, Böhne A. Genetics of sexual development: an evolutionary playground for fish. Genetics. 2014;196:579-91.
10. Bull JJ. Evolution of sex determining mechanisms. Menlo Park: Benjamín-Cummings; 1983.
11. Piferrer F, Guiguen G. Fish Gonadogenesis. Part II: Molecular biology and genomics of sex differentiation. Rev Fish Sci. 2008;16(Suppl. 1):35-55.
12. Place AR, Lance VA. The temperature-dependent sex determination drama-same cast, different stars. In: Valenzuela N, Lance VA, editors. Temperature Dependent Sex Determination in Vertebrates. Washingtong: Smithsonian Books; 2004.
13. Liu S, Govoroun M, D'Cotta H, Ricordel MJ, Lareyre JJ, McMeel IM, et al. Expression of cytochrome P45011β (11β-hydroxylase) gene during gonadal sex differentiation and spermatogenesis in rainbow trout, Oncorhynchus mykiss. J Steroid Biochem Mol Biol. 2000;75:291-8.
14. Socorro S, Martins RS, Deloffre L, Mylonas CC, Canario AVM. A cDNA for European sea bass (Dicentrachus labrax) 11 beta-hydroxylase: gene expression during the thermosensitive period and gonadogenesis. Gen Comp Endocrinol. 2007;150:164-73.
15. Wang XG, Orbán L. Anti-Müllerian hormone and 11 β-hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males. Dev Dyn. 2007;236:1329-38.
16. Sreenivasan R, Cai MN, Bartfai R, Wang XG, Christoffels A, Orbán L. Transcriptomic analyses reveal novel genes with sexually dimorphic expression in the zebrafish gonad and brain. PLoS One. 2008;3:e1791.
17. Blázquez M, Navarro-Martin L, Piferrer F. Expression profiles of sex differentiation-related genes during ontogenesis in the European sea bass acclimated to two different temperatures. J Exp Zool B Mol Dev Evol. 2009;312:686-700.
18. Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, et al. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol. 2012;22:1423-8.
19. Luckenbach JA, Early LW, Rowe AH, Borski RJ, Daniels HV, Godwin J. Aromatase cytochrome P450: cloning, intron variation, and ontogeny of gene expression in southern flounder (Paralichthys lethostigma). J Exp Zool A Comp Exp Biol. 2005;303:643-56.
20. Matsuoka MP, van Nes S, Andersen Ø, Benfey TJ, Reith M. Real-time PCR analysis of ovary- and brain-type aromatase gene expression during Atlantic halibut (Hippoglossus hippoglossus) development. Comp Biochem Physiol B Biochem Mol Biol. 2006;144:128-35.
21. Vizziano D, Randuineau G, Baron D, Cauty C, Guiguen Y. Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev Dyn. 2007;236:2198-206.
22. Cutting A, Chue J, Smith CA. Just how conserved is vertebrate sex determination? Dev Dyn. 2013;242:380-7.
23. Volff JN, Nanda I, Schmid M, Schartl M. Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev. 2007;1:85-99.
24. Nagahama Y. Molecular mechanisms of sex determination and gonadal sex differentiation in fish. Fish Physiol Biochem. 2006;31:105-9.
25. Valenzuela N, Lance V. Temperature-dependent sex determination in vertebrates, in Smithsonian Books. Washington D.C; 2004
26. Ospina-Alvárez N, Piferrer F. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One. 2008;3:e2837.
27. Guiguen Y, Fostier A, Piferrer F, Chang CF. Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol. 2010;165:352-66.
28. Somero GN. Proteins and temperature. Annu Rev Physiol. 1995;57:43-68.
29. Gracey AY, Fraser EJ, Li W, Fang Y, Taylor RR, Rogers J, et al. Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. PNAS. 2004;101:16970-5.
30. Podrabsky JE, Somero GN. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol. 2004;207:2237-54.
31. Buckley BA, Gracey AY, Somero GN. The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J Exp Biol. 2006;209:2660-77.
32. Cossins A, Fraser J, Hughes M, Gracey A. Post-genomic approaches to understanding the mechanisms of environmentally induced phenotypic plasticity. J Exp Biol. 2006;209:2328-36.
33. Kassahn KS, Caley MJ, Ward AC, Connolly AR, Stone G, Crozier R. Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish. Mol Ecol. 2007;16:1749-63.
34. Kassahn KS, Crozier RH, Ward AC, Stone G, Caley MJ. From transcriptome to biological function: environmental stress in an ectothermic vertebrate, the coral reef fish Pomacentrus moluccensis. BMC Genomics. 2007;8:358.
35. Chou MY, Hsiao CD, Chen SC, Chen IW, Liu ST, Hwang PP. Effects of hypothermia on gene expression in zebrafish gills: upregulation in differentiation and function of ionocytes as compensatory responses. J Exp Biol. 2008;211:3077-84.
36. Logan CA, Somero GN. Transcriptional responses to thermal acclimation in the eurythermal fish Gillichthys mirabilis (Cooper 1864). Am J Physiol Reg Integr Comp Physiol. 2010;299:R843-52.
37. Logan CA, Somero GN. Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am J Physiol Reg Integr Comp Physiol. 2011;300:R1373-83.
38. Vergauwen L, Benoot D, Blust R, Knapen D. Long-term warm or cold acclimation elicits a specific transcriptional response and affects energy metabolism in zebrafish. Comp Biochem Physiol A Mol Integr Physiol. 2010;157:149-57.
39. Magnanou E, Klopp C, Noirot C, Besseau L, Falcón J. Generation and characterization of the sea bass (Dicentrarchus labrax) brain and liver transcriptomes. Gene. 2014;544:56-66.
40. Ju Z, Dunham RA, Liu Z. Differential gene expression in the brain of channel catfish (Ictalurus punctatus) in response to cold acclimation. Mol Genet Genomics. 2002;268:87-95.
41. Vornanen M, Hassinen M, Koskinen H, Krasnov A. Steady-state effects of temperature acclimation on the transcriptome of the rainbow trout heart. Am J Physiol Reg Integr Comp Physiol. 2005;289:R1177-84.
42. Vandeputte M, Dupont-Nivet M, Chavanne H, Chatain B. A polygenic hypothesis for sex determination in the European sea bass - Dicentrarchus labrax. Genetics. 2007;176:1049-57.
43. Piferrer F, Blázquez M, Navarro-Martín L, González A. Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol. 2005;142:102-10.
44. Blázquez M, Zanuy S, Carillo M, Piferrer F. Effects of rearing temperature on sex differentiation in the European sea bass (Dicentrarchus labrax L.). J Exp Zool. 1998;281:207-16.
45. Saillant E, Fostier A, Haffray P, Menu B, Thimonier J, Chatain B. Temperature effects and genotype-temperature interactions on sex determination in the European sea bass (Dicentrarchus labrax L.). J Exp Zool. 2002;292:494-505.
46. Navarro-Martín L, Blázquez M, Viñas J, Joly S, Piferrer F. Balancing the effects of rearing at low temperature during early development on sex ratios, growth and maturation in the European sea bass (Dicentrarchus labrax). Limitations and opportunities for the production of highly female-biased stocks. Aquacult. 2009;296:347-58.
47. Pavlidis M, Koumoundouros G, Sterioti A, Somarakis S, Divanach P, Kentouri M. Evidence of temperature-dependent sex determination in the European sea bass (Dicentrarchus labrax L.). J Exp Zool. 2000;287:225-32.
48. Koumoundouros G, Pavlidis M, Anezaki L, Kokkari C, Sterioti K, Divanach P, et al. Temperature sex determination in the European sea bass, (Dicentrarchus labrax L., 1758) (Teleostei, Perciformes, Moronidae): critical sensitive ontogenetic phase. J Exp Zool. 2002;92:573-9.
49. Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A, Di Croce L, et al. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet. 2011;7:e1002447.
50. Hattori RS, Fernandino JI, Kishii AI, Kimura H, Kinno T, Oura M, et al. Cortisol-induced masculinization: Does thermal stress affect gonadal fate in Pejerrey, a Teleost fish with temperature-dependent sex determination? PLoS One. 2009;4:e6548.
51. Hayashi Y, Kobira H, Yamaguchi T, Shiraishi E, Yazawa T, Hirai T, et al. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol Reprod Dev. 2010;77:679-86.
52. Choi CY. Environmental stress-related gene expression and blood physiological responses in olive flounder (Paralichthys olivaceus) exposed to osmotic and thermal stress. Anim Cells and Systems. 2010;14:17-23.
53. Fernandino JI, Hattori RS, Moreno Acosta OD, Strüssmann CA, Somoza GM. Environmental stress-induced testis differentiation: androgen as a by-product of cortisol inactivation. Gen Comp Endocrinol. 2013;192:36-44.
54. Piferrer F. Epigenetics of sex determination and gonadogenesis. Dev Dyn. 2013;242:360-70.
55. Blázquez M, González A, Mylonas CC, Piferrer F. Cloning and sequence analysis of a vasa homolog in the European sea bass (Dicentrarchus labrax): Tissue distribution and mRNA expression levels during early development and sex differentiation. Gen Comp Endocrinol. 2011;170:322-33.
56. Stocco CO, Chedrese J, Deis RP. Luteal expression of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, 3beta-hydroxysteroid dehydrogenase, and 20 alpha-hydroxysteroid dehydrogenase genes in late pregnant rats: effect of luteinizing hormone and RU486. Biol Reprod. 2001;65:1114-9.
57. Kusakabe M, Todo T, McQuillan HJ, Goetz FW, Young G. Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinol. 2002;143:2062-70.
58. Ings JS, Van Der Kraak GJ. Characterization of the mRNA expression of StAR and steroidogenic enzymes in zebrafish ovarian follicles. Mol Reprod Dev. 2006;73:943-54.
59. Fabra M, Raldúa D, Power DA, Deen PMT, Cerdà J. Marine fish egg hydration is aquaporin-mediated. Science. 2005;307:545.
60. Piferrer F, Baker IJ, Donaldson EM. Effects of natural, synthetic, aromatizable, and nonaromatizable androgens in inducing male sex differentiation in genotypic female chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol. 1993;91:59-65.
61. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonté B, Szyf M, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12:342-8.
62. Suderman M, McGowan PO, Sasaki A, Huang TCT, Hallett MT, Meaney MJ, et al. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. PNAS. 2012;109:17266-72.
63. Chojnowski J, Braun E. An unbiased approach to identify genes involved in development in a turtle with temperature-dependent sex determination. BMC Genomics. 2012;13:308.
64. Navarro-Martín L, Galay-Burgos M, Sweeney G, Piferrer F. Different sox17 transcripts during sex differentiation in sea bass, Dicentrarchus labrax. Mol Cell Endocrinol. 2009;299:240-51.
65. Tsai CL, Chang SL, Wang LH, Chao TY. Temperature influences the ontogenetic expression of aromatase and oestrogen receptor mRNA in the developing tilapia (Oreochromis mossambicus) brain. J Neuroendocrinol. 2003;15:97-102.
66. Spik A, Oczkowski S, Olszak A, Formanowicz P, Błazewicz J, Jaruzelska J. Human fertility protein PUMILIO2 interacts in vitro with testis mRNA encoding cdc42 effector 3 (CEP3). Reprod Biol. 2006;6:103-13.
67. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, et al. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science. 2007;318:467.
68. Bodoor K, Lontay B, Safi R, Weitzel DH, Loiselle D, Lengyel S, et al. Smoothelin-like 1 Protein Is a Bifunctional Regulator of the Progesterone Receptor during Pregnancy. J Biomech. 2011;286:31839-51.
69. Obinata T, Ono K, Ono S. Troponin I controls ovulatory contraction of non-striated actomyosin networks in the C. elegans somatic gonad. J Cell Sci. 2010;123:1557-66.
70. Sloat MR, Reeves GH. Individual condition, standard metabolic rate, and rearing temperature influence steelhead and rainbow trout (Oncorhynchus mykiss) life histories. Can J Fish Aquat Sci. 2014;71:491-501.
71. Díaz N, Ribas L, Piferrer F. The relationship between growth and sex differentiation in the European sea bass (Dicentrarchus labrax). Aquacult. 2013;408-409:191-202.
72. Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbieri SK. A Standardized terminology for describing reproductive development in fishes. Mar Coast Fish Dynam Manag Ecosys Sci. 2011;3:52-70.
73. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101-8.
74. Hammer Ø, Harper D, Ryan P. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4:1-9.
75. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics. 2007;23:2700-7.
76. Bolstad B. Probe level quantile normalization of high density oligonucleotide array data. [Internet]. Berkeley, CA: University of California. http://bmbolstad.com/stuff/qnorm.pdf . Accessed 20 November 2014
77. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:1544-6115.
78. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57:289-300.
79. Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
80. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S. AmiGO: online access to ontology and annotation data. Bioinformatics. 2009;25:288-9.
81. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674-6.
82. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
83. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc. 2009;4:44-57.