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

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Abstract

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.

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Acknowledgments

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

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.

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Author notes

  1. B. Crespo

    Present address: UCL GOS Institute of Child Health, University College London, London, UK

  2. H. Kuhl

    Present address: Department of Ecophysiology and Aquaculture, Leibniz Institute for Freshwater Ecology and Inland Fisheries, Berlin, Germany

  3. J. M. Rodríguez

    Present address: Cardiovascular Proteomics Laboratory, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC), Madrid, Spain

  4. N. Díaz

    Present address: Max Planck Institute for Molecular Biomedicine, Muenster, Germany

  5. S. Boltañá

    Present address: Interdisciplinary Center for Aquaculture Research (INCAR), Department of Oceanography, Biotechnology Center, University of Concepción, Concepción, Chile

  6. S. MacKenzie

    Present address: Institute of Aquaculture, University of Stirling, Stirling, Scotland, UK

  7. L. Ribas and B. Crespo contributed equally to this work.

Authors and Affiliations

  1. Institute of Marine Sciences (ICM), Spanish National Research Council (CSIC), Barcelona, Catalonia, Spain

    L. Ribas, N. Sánchez-Baizán, N. Díaz & F. Piferrer

  2. Institute of Aquaculture of Torre de la Sal (IATS-CSIC), Ribera de Cabanes s/n. Torre la Sal, 12595, Castellón, Spain

    B. Crespo, S. Zanuy & A. Gómez

  3. Department of Biochemistry and Molecular Biology I, Complutense University, Madrid, Spain

    D. Xavier & F. Morán

  4. Max Planck Institute for Molecular Genetics, Berlin, Germany

    H. Kuhl

  5. Spanish National Bioinformatics Institute, Madrid, Spain

    J. M. Rodríguez

  6. Autonomous University of Barcelona, Barcelona, Spain

    S. Boltañá & S. MacKenzie

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  1. L. Ribas
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Correspondence to A. Gómez or F. Piferrer.

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Ribas, L., Crespo, B., Sánchez-Baizán, N. et al. Characterization of the European Sea Bass (Dicentrarchus labrax) Gonadal Transcriptome During Sexual Development. Mar Biotechnol 21, 359–373 (2019). https://doi.org/10.1007/s10126-019-09886-x

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