Characterization of the European Sea Bass (Dicentrarchus labrax) Gonadal Transcriptome During Sexual Development

  • L. Ribas
  • B. Crespo
  • N. Sánchez-Baizán
  • D. Xavier
  • H. Kuhl
  • J. M. Rodríguez
  • N. Díaz
  • S. Boltañá
  • S. MacKenzie
  • F. Morán
  • S. Zanuy
  • A. GómezEmail author
  • F. PiferrerEmail author
Original Article


The European sea bass is one of the most important cultured fish in Europe and has a marked sexual growth dimorphism in favor of females. It is a gonochoristic species with polygenic sex determination, where a combination between still undifferentiated genetic factors and environmental temperature determines sex ratios. The molecular mechanisms responsible for gonadal sex differentiation are still unknown. Here, we sampled fish during the gonadal developmental period (110 to 350 days post fertilization, dpf), and performed a comprehensive transcriptomic study by using a species-specific microarray. This analysis uncovered sex-specific gonadal transcriptomic profiles at each stage of development, identifying larger number of differentially expressed genes in ovaries when compared to testis. The expression patterns of 54 reproduction-related genes were analyzed. We found that hsd17β10 is a reliable marker of early ovarian differentiation. Further, three genes, pdgfb, snx1, and nfy, not previously related to fish sex differentiation, were tightly associated with testis development in the sea bass. Regarding signaling pathways, lysine degradation, bladder cancer, and NOD-like receptor signaling were enriched for ovarian development while eight pathways including basal transcription factors and steroid biosynthesis were enriched for testis development. Analysis of the transcription factor abundance showed an earlier increase in females than in males. Our results show that, although many players in the sex differentiation pathways are conserved among species, there are peculiarities in gene expression worth exploring. The genes identified in this study illustrate the diversity of players involved in fish sex differentiation and can become potential biomarkers for the management of sex ratios in the European sea bass and perhaps other cultured species.


Genomics Transcriptomics Reproduction Sex differentiation Gonads Aquaculture 



We would like to thank Dr. Richard Reinhardt for his work on the 454 sequencing of the European sea bass gonads performed at Max Planck Institute for Molecular Genetics, Berlin (Germany).

Funding Information

This work was supported by Spanish Government Consolider-Ingenio 2010 grant “Aquagenomics” (ref. CDS2007-0002) to SMK, FM, SZ and FP. BC was supported by an Aquagenomics contract; LR was supported by Aquagenomics postdoctoral contract; ND was supported by Aquagenomics predoctoral contract. NSB was supported by AGL2016-78710-R.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

10126_2019_9886_MOESM1_ESM.xlsx (2.4 mb)
ESM 1 (XLSX 2476 kb)
10126_2019_9886_MOESM2_ESM.xlsx (85 kb)
ESM 2 (XLSX 85 kb)
10126_2019_9886_MOESM3_ESM.xls (82 kb)
ESM 3 (XLS 82 kb)
10126_2019_9886_MOESM4_ESM.docx (960 kb)
ESM 4 (DOCX 960 kb)


  1. Alexa A, Rahnenfuhrer J (2016) topGO: enrichment analysis for gene ontology. R package version 2.30.0. Available from: Accessed 25 Apr 2018.
  2. Anastasiadi D, Vandeputte M, Sanchez-Baizan N, Allal F, Piferrer F (2018) Dynamic epimarks in sex-related genes predict gonad phenotype in the European sea bass, a fish with mixed genetic and environmental sex determination. Epigenetics 13(9):988–1011PubMedGoogle Scholar
  3. Aref’yev VA (1989) Cytogenetic analysis and nuclear organization of the sea bass Dicentrarchus labrax. J Ichthyol 29:1–12Google Scholar
  4. Bagheri-Fam S, Sinclair AH, Koopman P, Harley VR (2010) Conserved regulatory modules in the Sox9 testis-specific enhancer predict roles for SOX, TCF/LEF, Forkhead, DMRT, and GATA proteins in vertebrate sex determination. Int J Biochem Cell Biol 42(3):472–477PubMedGoogle Scholar
  5. Beltrame L, Bianco L, Fontana P, Cavalieri D (2013) Pathway processor 2.0: a web resource for pathway-based analysis of high-throughput data. Bioinformatics 29(14):1825–1826PubMedGoogle Scholar
  6. Blázquez M, Piferrer F (2005) Sea bass (Dicentrarchus labrax) androgen receptor: cDNA cloning, tissue-specific expression, and mRNA levels during early development and sex differentiation. Mol Cell Endocrinol 237(1–2):37–48PubMedGoogle Scholar
  7. Blázquez M, González A, Papadaki M, Mylonas C, Piferrer F (2008) Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 158(1):95–101PubMedGoogle Scholar
  8. Breton TS, Berlinsky DL (2014) Characterizing ovarian gene expression during oocyte growth in Atlantic cod (Gadus morhua). Comp Biochem Physiol Part D Genomics Proteomics 9:1–10PubMedGoogle Scholar
  9. Budd A, Banh Q, Domingos J, Jerry D (2015) Sex control in fish: approaches, challenges and opportunities for aquaculture. J Mar Sci Eng 3(2):329–355Google Scholar
  10. Cai J, Yang W, Chen D, Zhang Y, He Z, Zhang W, Zhang L (2017) Transcriptomic analysis of the differentiating ovary of the protogynous ricefield eel Monopterus albus. BMC Genomics 18(1):573PubMedGoogle Scholar
  11. Capel B (2017) Vertebrate sex determination: evolutionary plasticity of a fundamental switch. Nat Rev Genet 18(11):675–689PubMedGoogle Scholar
  12. Carlson M (2017) GO.db: a set of annotation maps describing the entire Gene Ontology. R package version 3.5.0 . Available from: Accessed 7 Jul 2018
  13. Carrillo M, Espigares F, Felip A, Escobar S, Moles G, Rodríguez R, Victoria Alvarado M, Gómez A, Zanuy S (2015) Updating control of puberty in male European sea bass: a holistic approach. Gen Comp Endocrinol 221:42–53PubMedGoogle Scholar
  14. Caruso R, Warner N, Inohara N, Nunez G (2014) NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41(6):898–908PubMedGoogle Scholar
  15. Chang GB, Chen R, Xu L, Ma T, Wang HZ, Chen J, Zhang Y, Li ZT, Wan F, Guo XM, Xu Q, Zhao WM, Chen GH (2015) DNA methylation and NF-Y regulate Piwil1 expression during chicken spermatogenesis. Anim Reprod Sci 162:95–103PubMedGoogle Scholar
  16. Chaves-Pozo E, Valero Y, Esteve-Codina A, Gomez-Garrido J, Dabad M, Alioto T, Meseguer J, Esteban MA, Cuesta A (2017) Innate cell-mediated cytotoxic activity of European sea bass leucocytes against nodavirus-infected cells: a functional and RNA-seq study. Sci Rep 7(1):15396PubMedGoogle Scholar
  17. Chawla K, Tripathi S, Thommesen L, Laegreid A, Kuiper M (2013) TFcheckpoint: a curated compendium of specific DNA-binding RNA polymerase II transcription factors. Bioinformatics 29(19):2519–2520PubMedGoogle Scholar
  18. Chen C, Grennan K, Badner J, Zhang D, Gershon E, Jin L, Liu C (2011) Removing batch effects in analysis of expression microarray data: an evaluation of six batch adjustment methods. PLoS One 6(2):e17238PubMedGoogle Scholar
  19. Crespo B, Gómez A, Mazón MJ, Carrillo M, Zanuy S (2013) Isolation and characterization of Ff1 and Gsdf family genes in European sea bass and identification of early gonadal markers of precocious puberty in males. Gen Comp Endocrinol 191(0):155–167PubMedGoogle Scholar
  20. D’Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF (2001) Search for genes involved in the temperature-induced gonadal sex differentiation in the tilapia, Oreochromis niloticus. J Exp Zool 290(6):574–585PubMedGoogle Scholar
  21. Deloffre L, Martins R, Mylonas C, Canario A (2009) Alternative transcripts of DMRT1 in the European sea bass: expression during gonadal differentiation. Aquaculture 293(1–2):89–99Google Scholar
  22. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208(3-4):191–364Google Scholar
  23. Díaz N, Piferrer F (2015) 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 16:679PubMedGoogle Scholar
  24. Díaz N, Piferrer F (2017) Estrogen exposure overrides the masculinizing effect of elevated temperature by a downregulation of the key genes implicated in sexual differentiation in a fish with mixed genetic and environmental sex determination. BMC Genomics 18:973PubMedGoogle Scholar
  25. Díaz N, Ribas L, Piferrer F (2014) Effects of changes in food supply at the time of sex differentiation on the gonadal transcriptome of juvenile fish. Implications for natural and farmed populations. PLoS One 9(10):e111304PubMedGoogle Scholar
  26. Donnem T, Al-Saad S, Al-Shibli K, Busund LT, Bremnes RM (2010) Co-expression of PDGF-B and VEGFR-3 strongly correlates with lymph node metastasis and poor survival in non-small-cell lung cancer. Ann Oncol 21(2):223–231PubMedGoogle Scholar
  27. Du X, Wang B, Liu X, Liu X, He Y, Zhang Q, Wang X (2017) Comparative transcriptome analysis of ovary and testis reveals potential sex-related genes and pathways in spotted knifejaw Oplegnathus punctatus. Gene 637:203–210PubMedGoogle Scholar
  28. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30(1):207–210PubMedGoogle Scholar
  29. Fan ZF, You F, Wang LJ, Weng SD, Wu ZH, Hu JW, Zou YX, Tan XG, Zhang PJ (2014) Gonadal transcriptome analysis of male and female Olive flounder (Paralichthys olivaceus). Biomed Res Int 2014:1–10Google Scholar
  30. Felip A, Piferrer F (2018) State of culture and breeding of European sea bass, Dicentrarchus labrax L. In: Liang, X.F., H.P Wang, H. Liu and R.W. Hardy, eds. World Perch and Bass Culture: Innovation and Industrialization. China Science Press, Beijing, pp. 332–351Google Scholar
  31. Ferraresso S, Milan M, Pellizzari C, Vitulo N, Reinhardt R, Canario AVM, Patarnello T, Bargelloni L (2010) Development of an oligo DNA microarray for the European sea bass and its application to expression profiling of jaw deformity. BMC Genomics 11:354PubMedGoogle Scholar
  32. © FAO 2005-2019. Cultured Aquatic Species Information Programme. Dicentrarchus labrax. Cultured Aquatic Species Information Programme. Text by Bagni, M. In: FAO Fisheries and Aquaculture Department [online]. Rome. Updated 18 February 2005. Available from: Accessed 5 May 2017
  33. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge YC, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang JH (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5(10):R80PubMedGoogle Scholar
  34. Guiguen Y, Fostier A, Piferrer F, Chang CF (2009) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165(3):352–366PubMedGoogle Scholar
  35. Hallen A, Jamie JF, Cooper AJ (2013) Lysine metabolism in mammalian brain: an update on the importance of recent discoveries. Amino Acids 45(6):1249–1272PubMedGoogle Scholar
  36. He X, Yang S (2009) Comments on ‘Significance of developmental expression of amphioxus Branchiostoma belcheri and zebrafish Danio rerio Hsd17b10 in biological and medical research’. J Fish Biol 74(8):1689–1692PubMedGoogle Scholar
  37. Herpin A, Schartl M (2011) Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 278(7):1010–1019PubMedGoogle Scholar
  38. Jacobs SBR, Coss D, McGillivray SM, Mellon PL (2003) Nuclear factor Y and steroidogenic factor 1 physically and functionally interact to contribute to cell-specific expression of the mouse follicle-stimulating hormone-beta gene. Mol Endocrinol 17(8):1470–1483PubMedGoogle Scholar
  39. Jantzen SG, Sanderson DS, von Schalburg KR, Yasuike M, Marass F, Koop BF (2011) A 44K microarray dataset of the changing transcriptome in developing Atlantic salmon (Salmo salar L.). BMC Res Notes 4:88PubMedGoogle Scholar
  40. Jeng SR, Wu GC, Yueh WS, Kuo SF, Dufour S, Chang CF (2018) Gonadal development and expression of sex-specific genes during sex differentiation in the Japanese eel. Gen Comp Endocrinol 257:74–85PubMedGoogle Scholar
  41. Jia Y, Nan P, Zhang W, Wang F, Zhang R, Liang T, Ji X, Du Q, Chang Z (2018) Transcriptome analysis of three critical periods of ovarian development in Yellow River carp (Cyprinus carpio). Theriogenology 105:15–26PubMedGoogle Scholar
  42. Kanamori A, Toyama K, Kitagawa S, Kamehara A, Higuchi T, Kamachi Y, Kinoshita M, Hori H (2008) Comparative genomics approach to the expression of fig alpha, one of the earliest marker genes of oocyte differentiation in medaka (Oryzias latipes). Gene 423(2):180–187PubMedGoogle Scholar
  43. Kim S, Jung D, Kho Y, Choi K (2014) Effects of benzophenone-3 exposure on endocrine disruption and reproduction of Japanese medaka (Oryzias latipes)-a two generation exposure study. Aquat Toxicol 155:244–252PubMedGoogle Scholar
  44. Lagadec C, Vlashi E, Frohnen P, Alhiyari Y, Chan M, Pajonk F (2014) The RNA-binding protein Musashi-1 regulates proteasome subunit expression in breast cancer and glioma-initiating cells. Stem Cells 32(1):135–144PubMedGoogle Scholar
  45. Levavi-Sivan B, Bogerd J, Mananos EL, Gomez A, Lareyre JJ (2010) Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol 165(3):412–437PubMedGoogle Scholar
  46. Li GL, Zhao H, Wang LJ, Wang Y, Guo XQ, Xu BH (2018) The animal nuclear factor Y: an enigmatic and important heterotrimeric transcription factor. Am J Cancer Res 8(7):1106–1125PubMedGoogle Scholar
  47. Matsuoka MP, van Nes S, Andersen O, Benfev TJ, Reith M (2006) 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 144(1):128–135PubMedGoogle Scholar
  48. Mazón MJ, Gómez A, Yilmaz O, Carrillo M, Zanuy S (2014) Administration of follicle-stimulating hormone in vivo triggers testicular recrudescence of juvenile European sea bass (Dicentrarchus labrax). Biol Reprod 90(1):10Google Scholar
  49. Migeon CJ, Wisniewski AB (2000) Human sex differentiation: from transcription factors to gender. Horm Res 53(3):111–119PubMedGoogle Scholar
  50. Millan A, Gomez-Tato A, Fernandez C, Pardo BG, Alvarez-Dios JA, Calaza M, Bouza C, Vazquez M, Cabaleiro S, Martinez P (2010) Design and performance of a turbot (Scophthalmus maximus) oligo-microarray based on ESTs from immune tissues. Mar Biotechnol 12(4):452–465PubMedGoogle Scholar
  51. Mindnich R, Deluca D, Adamski J (2004) Identification and characterization of 17 beta-hydroxysteroid dehydrogenases in the zebrafish, Danio rerio. Mol Cell Endocrinol 215(1–2):19–30PubMedGoogle Scholar
  52. Mitra AP, Datar RH, Cote RJ (2006) Molecular pathways in invasive bladder cancer: new insights into mechanisms, progression, and target identification. J Clin Oncol 24(35):5552–5564PubMedGoogle Scholar
  53. Mitter K, Kotoulas G, Magoulas A, Mulero V, Sepulcre P, Figueras A, Novoa B, Sarropoulou E (2009) Evaluation of candidate reference genes for QPCR during ontogenesis and of immune-relevant tissues of European seabass (Dicentrarchus labrax). Comp Biochem Physiol B Biochem Mol Biol 153(4):340–347PubMedGoogle Scholar
  54. Munger SC, Natarajan A, Looger LL, Ohler U, Capel B (2013) Fine time course expression analysis identifies cascades of activation and repression and maps a putative regulator of mammalian sex determination. PLoS Genet 9(7):e1003630PubMedGoogle Scholar
  55. Nakamura S, Kobayashi K, Nishimura T, Tanaka M (2011) Ovarian germline stem cells in the teleost fish, medaka (Oryzias latipes). Int J Biol Sci 7(4):403–409PubMedGoogle Scholar
  56. Nicol B, Guiguen Y (2011) Expression profiling of wnt signaling genes during gonadal differentiation and gametogenesis in rainbow trout. Sex Dev 5(6):318–329PubMedGoogle Scholar
  57. Palaiokostas C, Bekaert M, Taggart JB, Gharbi K, McAndrew BJ, Chatain B, Penman DJ, Vandeputte M (2015) A new SNP-based vision of the genetics of sex determination in European sea bass (Dicentrarchus labrax). Genet Sel Evol 47:68PubMedGoogle Scholar
  58. Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197(1–4):229–281Google Scholar
  59. Piferrer F, Blázquez M, Navarro L, González A (2005) Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 142(1–2):102–110PubMedGoogle Scholar
  60. Purcell CM, Seetharam AS, Snodgrass O, Ortega-Garcia S, Hyde JR, Severin AJ (2018) Insights into teleost sex determination from the Seriola dorsalis genome assembly. BMC Genomics 19(1):31PubMedGoogle Scholar
  61. R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: Accessed 15 Nov 2017
  62. Ramseyer LJ, Garling DL (1994) Amino acid composition of the ovaries, muscle, and whole body of yellow perch. Prog Fish Cult 56(3):175–179Google Scholar
  63. Ribas L, Robledo D, Gómez-Tato A, Viñas A, Martínez P, Piferrer F (2016) Comprehensive transcriptomic analysis of the process of gonadal sex differentiation in the turbot (Scophthalmus maximus). Mol Cell Endocrinol 422(C):132–149PubMedGoogle Scholar
  64. Ribas L, Liew WC, Díaz N, Sreenivasan R, Orbán L, Piferrer F (2017) Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes. PNAS 114(6):E941–E950PubMedGoogle Scholar
  65. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acid Res 43(7):e47Google Scholar
  66. Rodríguez-Marí A, Postlethwait JH (2011). The role of Fanconi anemia/BRCA genes in zebrafish sex determination. Methods Cell Biol 105:461–490Google Scholar
  67. Rodríguez-Marí A, Canestro C, BreMiller RA, Nguyen-Johnson A, Asakawa K, Kawakami K, Postlethwait JH (2010) Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLoS Genet 6(7):e1001034PubMedGoogle Scholar
  68. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34(2):374–378PubMedGoogle Scholar
  69. Saillant E, Fostier A, Menu B, Haffray P, Chatain B (2001) Sexual growth dimorphism in sea bass Dicentrarchus labrax. Aquaculture 202(3–4):371–387Google Scholar
  70. Sayed AEH, Ismail RF, Mitani H (2018) Oocyte atresia in WT (HdrR) and P53 (-/-) medaka (Oryzias latipes) exposed to UVA. J Photochem Photobiol B Biol 183:57–63Google Scholar
  71. Schaeck M, Reyes-Lopez FE, Vallejos-Vidal E, Van Cleemput J, Duchateau L, Van den Broeck W, Tort L, Decostere A (2017) Cellular and transcriptomic response to treatment with the probiotic candidate Vibrio lentus in gnotobiotic sea bass (Dicentrarchus labrax) larvae. Fish Shellfish Immunol 63:147–156PubMedGoogle Scholar
  72. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108PubMedGoogle Scholar
  73. Shen Z-G, Wang H-P (2014) Molecular players involved in temperature-dependent sex determination and sex differentiation in Teleost fish. Genet Sel Evol 46:26PubMedGoogle Scholar
  74. Shi L, Reid LH, Jones WD, Shippy R, Warrington JA, Baker SC, Collins PJ, de Longueville F, Kawasaki ES, Lee KY, Luo Y, Sun YA, Willey JC, Setterquist RA, Fischer GM, Tong W, Dragan YP, Dix DJ, Frueh FW, Goodsaid FM, Herman D, Jensen RV, Johnson CD, Lobenhofer EK, Puri RK, Scherf U, Thierry-Mieg J, Wang C, Wilson M, Wolber PK, Zhang L, Amur S, Bao W, Barbacioru CC, Lucas AB, Bertholet V, Boysen C, Bromley B, Brown D, Brunner A, Canales R, Cao XM, Cebula TA, Chen JJ, Cheng J, Chu T-M, Chudin E, Corson J, Corton JC, Croner LJ, Davies C, Davison TS, Delenstarr G, Deng X, Dorris D, Eklund AC, X-h F, Fang H, Fulmer-Smentek S, Fuscoe JC, Gallagher K, Ge W, Guo L, Guo X, Hager J, Haje PK, Han J, Han T, Harbottle HC, Harris SC, Hatchwell E, Hauser CA, Hester S, Hong H, Hurban P, Jackson SA, Ji H, Knight CR, Kuo WP, LeClerc JE, Levy S, Li Q-Z, Liu C, Liu Y, Lombardi MJ, Ma Y, Magnuson SR, Maqsodi B, McDaniel T, Mei N, Myklebost O, Ning B, Novoradovskaya N, Orr MS, Osborn TW, Papallo A, Patterson TA, Perkins RG, Peters EH, Peterson R, Philips KL, Pine PS, Pusztai L, Qian F, Ren H, Rosen M, Rosenzweig BA, Samaha RR, Schena M, Schroth GP, Shchegrova S, Smith DD, Staedtler F, Su Z, Sun H, Szallasi Z, Tezak Z, Thierry-Mieg D, Thompson KL, Tikhonova I, Turpaz Y, Vallanat B, Van C, Walker SJ, Wang SJ, Wang Y, Wolfinger R, Wong A, Wu J, Xiao C, Xie Q, Xu J, Yang W, Zhang L, Zhong S, Zong Y, Slikker W Jr, Consortium M (2006) The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat Biotechnol 24(9):1151–1161PubMedGoogle Scholar
  75. Small CM, Carney GE, Mo Q, Vannucci M, Jones AG (2009) A microarray analysis of sex- and gonad-biased gene expression in the zebrafish: evidence for masculinization of the transcriptome. BMC Genomics 10:579PubMedGoogle Scholar
  76. Sreenivasan R, Jiang JH, Wang XG, Bartfai R, Kwan HY, Christoffels A, Orban L (2014) Gonad differentiation in zebrafish is regulated by the canonical wnt signaling pathway. Biol Reprod 90(2):45:41-10PubMedGoogle Scholar
  77. Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K, Shin-I T, Kohara Y, Kuroki Y, Toyoda A, Fujiyama A, Hamaguchi S, Sakaizumi M, Naruse K (2014) Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat Commun 5:4157Google Scholar
  78. Tanaka M (2016) Germline stem cells are critical for sexual fate decision of germ cells. Bioessays 38(12):1227–1233PubMedGoogle Scholar
  79. Tao WJ, Yuan J, Zhou LY, Sun LN, Sun YL, Yang SJ, Li MH, Zeng S, Huang BF, Wang DH (2013) Characterization of gonadal transcriptomes from nile tilapia (Oreochromis niloticus) reveals differentially expressed genes. PLoS One 8(5):e63604PubMedGoogle Scholar
  80. Tine M, Kuhl H, Gagnaire PA, Louro B, Desmarais E, Martins RST, Hecht J, Knaust F, Belkhir K, Klages S, Dieterich R, Stueber K, Piferrer F, Guinand B, Bierne N, Volckaert FAM, Bargelloni L, Power DM, Bonhomme F, Canario AVM, Reinhardt R (2014) European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat Commun 5:5770PubMedGoogle Scholar
  81. Tingaud-Sequeira A, Lozano JJ, Zapater C, Otero D, Kube M, Reinhardt R, Cerda J (2013) A rapid transcriptome response is associated with desiccation resistance in aerially-exposed killifish embryos. PLoS One 8(5):e64410PubMedGoogle Scholar
  82. Tokarz J, Moeller G, de Angelis MH, Adamski J (2015) Steroids in teleost fishes: a functional point of view. Steroids 103:123–144PubMedGoogle Scholar
  83. Vandeputte M, Piferrer F (2019) Genetic and environmental components of sex determination in the European sea bass. In: Wang HP, Piferrer F, Chen SL (eds) Sex Control in Aquaculture. Wiley-Blackwell, Hoboken, pp 307–325Google Scholar
  84. Vandeputte M, Dupont-Nivet M, Chavanne H, Chatain B (2007) A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics 176(2):1049–1057PubMedGoogle Scholar
  85. Vanwert JM, Wolfe SA, Grimes SR (2008) Binding of RFX2 and NF-Y to the testis-specific histone H1t promoter may be required for transcriptional activation in primary spermatocytes. J Cell Biochem 104(3):1087–1101PubMedGoogle Scholar
  86. von Schalburg KR, Rise ML, Brown GD, Davidson WS, Koop BF (2005) A comprehensive survey of the genes involved in maturation and development of the rainbow trout ovary. Biol Reprod 72(3):687–699Google Scholar
  87. Wang XX, Wei JZ, Jiao J, Jiang SY, Yu DH, Li D (2014) Genome-wide DNA methylation and gene expression patterns provide insight into polycystic ovary syndrome development. Oncotarget 5(16):6603–6610PubMedGoogle Scholar
  88. Wang Z, Qiu X, Kong D, Zhou X, Guo Z, Gao C, Ma S, Hao W, Jiang Z, Liu S, Zhang T, Meng X, Wang X (2017) Comparative RNA-Seq analysis of differentially expressed genes in the testis and ovary of Takifugu rubripes. Comp Biochem Physiol Part D Genomics Proteomics 22:50–57PubMedGoogle Scholar
  89. Wang H-P, Piferrer F, Chen SL, Shen ZG (2019) Sex Control in Aquaculture. Wiley, HobokenGoogle Scholar
  90. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M and Venables B (2016) gplots: various R programming tools for plotting data. R package version 3.0.1. Available from: Accessed 4 Nov 2018
  91. Wen HJ, Xie J, Gui JF (2003) cDNA cloning and characterization of a novel SNX gene differentially expressed in previtellogenic oocytes of gibel carp. Comp Biochem Physiol B Biochem Mol Biol 136(3):451–461PubMedGoogle Scholar
  92. Wettenhall JM, Smyth GK (2004) limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20(18):3705–3706PubMedGoogle Scholar
  93. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New YorkGoogle Scholar
  94. Wong TT, Zohar Y (2004) Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 145(11):5210–5220PubMedGoogle Scholar
  95. Wood RK, Seidel JS, Martyniuk CJ (2015) Transcripts involved in steroid biosynthesis and steroid receptor signaling are expressed early in development in the fathead minnow (Pimephales promelas). Comp Biochem Physiol B Biochem Mol Biol 182:64–72PubMedGoogle Scholar
  96. Yamaguchi T, Yamaguchi S, Hirai T, Kitano T (2007) Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem Biophys Res Commun 359(4):935–940PubMedGoogle Scholar
  97. Yang S-Y, He X-Y, Miller D (2007) HSD17B10: a gene involved in cognitive function through metabolism of isoleucine and neuroactive steroids. Mol Genet Metab 92(1–2):36–42PubMedGoogle Scholar
  98. Yang S-Y, He XY, Isaacs C, Dobkin C, Miller D, Philipp M (2014) Roles of 17 beta-hydroxysteroid dehydrogenase type 10 in neurodegenerative disorders. J Steroid Biochem Mol Biol 143:460–472PubMedGoogle Scholar
  99. Yao B, Zhou L, Wang Y, Xia W, Gui J-F (2007) Differential expression and dynamic changes of SOX3 during gametogenesis and sex reversal in protogynous hermaphroditic fish. J Exp Zool A Ecol Genet Physiol 307A(4):207–219Google Scholar
  100. Yasuda T, Oda S, Li Z, Kimori Y, Kamei Y, Ishikawa T, Todo T, Mitani H (2012) Gamma-ray irradiation promotes premature meiosis of spontaneously differentiating testis-ova in the testis of p53-deficient medaka (Oryzias latipes). Cell Death Dis 3:e395PubMedGoogle Scholar
  101. Zeng QF, Liu SK, Yao J, Zhang Y, Yuan ZH, Jiang C, Chen AL, Fu Q, Su BF, Dunham R, Liu ZJ (2016) Ranscriptome display during testicular differentiation of Channel catfish (Ictalurus punctatus) as revealed by RNA-seq analysis. Biol Reprod 95(1):19PubMedGoogle Scholar
  102. Zhang Y, Wang L, Shao M, Li J, Li B, Zhang H (2008) A comparative study on the developmental expression of hadh2 in amphioxus and zebrafish. J Fish Biol 72(5):1215–1222Google Scholar
  103. Zhang XY, Hou JL, Wang GX, Jiang HB, Wang YF, Sun ZH, Jiang XF, Yu QH, Liu HJ (2015) Gonadal transcriptome analysis in sterile double haploid Japanese flounder. PLoS One 10(11):e0143204PubMedGoogle Scholar
  104. Zhao S, Fung-Leung W-P, Bittner A, Ngo K, Liu X (2014) Comparison of RNA-seq and microarray in transcriptome profiling of activated T cells. PLoS One 9(1):e78644PubMedGoogle Scholar
  105. Zhou LY, Wang DS, Senthilkumaran B, Yoshikuni M, Shibata Y, Kobayashi T, Sudhakumari CC, Nagahama Y (2005) Cloning, expression and characterization of three types of 17 beta-hydroxysteroid dehydrogenases from the Nile tilapia, Oreochromis niloticus. J Mol Endocrinol 35(1):103–116PubMedGoogle Scholar
  106. Zschocke J (2012) HSD10 disease: clinical consequences of mutations in the HSD17B10 gene. J Inherit Metab Dis 35(1):81–89PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Marine Sciences (ICM)Spanish National Research Council (CSIC)BarcelonaSpain
  2. 2.Institute of Aquaculture of Torre de la Sal (IATS-CSIC)CastellónSpain
  3. 3.UCL GOS Institute of Child HealthUniversity College LondonLondonUK
  4. 4.Department of Biochemistry and Molecular Biology IComplutense UniversityMadridSpain
  5. 5.Max Planck Institute for Molecular GeneticsBerlinGermany
  6. 6.Department of Ecophysiology and AquacultureLeibniz Institute for Freshwater Ecology and Inland FisheriesBerlinGermany
  7. 7.Spanish National Bioinformatics InstituteMadridSpain
  8. 8.Cardiovascular Proteomics LaboratoryCentro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)MadridSpain
  9. 9.Max Planck Institute for Molecular BiomedicineMuensterGermany
  10. 10.Autonomous University of BarcelonaBarcelonaSpain
  11. 11.Interdisciplinary Center for Aquaculture Research (INCAR), Department of Oceanography, Biotechnology CenterUniversity of ConcepciónConcepciónChile
  12. 12.Institute of AquacultureUniversity of StirlingStirlingUK

Personalised recommendations