Cargando…

Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)

BACKGROUND: Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics. These changes are one important ecological consequence, contributing to the risk of extinction in small and inb...

Descripción completa

Detalles Bibliográficos
Autores principales: Hosseini, Shahrbanou, Ha, Ngoc-Thuy, Simianer, Henner, Falker-Gieske, Clemens, Brenig, Bertram, Franke, Andre, Hörstgen-Schwark, Gabriele, Tetens, Jens, Herzog, Sebastian, Sharifi, Ahmad Reza
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6503382/
https://www.ncbi.nlm.nih.gov/pubmed/31060508
http://dx.doi.org/10.1186/s12864-019-5722-1
_version_ 1783416399325036544
author Hosseini, Shahrbanou
Ha, Ngoc-Thuy
Simianer, Henner
Falker-Gieske, Clemens
Brenig, Bertram
Franke, Andre
Hörstgen-Schwark, Gabriele
Tetens, Jens
Herzog, Sebastian
Sharifi, Ahmad Reza
author_facet Hosseini, Shahrbanou
Ha, Ngoc-Thuy
Simianer, Henner
Falker-Gieske, Clemens
Brenig, Bertram
Franke, Andre
Hörstgen-Schwark, Gabriele
Tetens, Jens
Herzog, Sebastian
Sharifi, Ahmad Reza
author_sort Hosseini, Shahrbanou
collection PubMed
description BACKGROUND: Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics. These changes are one important ecological consequence, contributing to the risk of extinction in small and inbred fish populations under natural conditions, due to male-biased sex ratio. Here we investigated the effect of elevated water temperature during embryogenesis on sex ratio and sex-biased gene expression profiles between two different tissues, namely gonad and caudal fin of adult zebrafish males and females, to gain new insights into the molecular mechanisms underlying sex determination (SD) and colour patterning related to sexual attractiveness. RESULTS: Our study demonstrated sex ratio imbalances with 25.5% more males under high-temperature condition, resulting from gonadal masculinization. The result of transcriptome analysis showed a significantly upregulated expression of male SD genes (e.g. dmrt1, amh, cyp11c1 and sept8b) and downregulation of female SD genes (e.g. zp2.1, vtg1, cyp19a1a and bmp15) in male gonads compared to female gonads. Contrary to expectations, we found highly differential expression of colour pattern (CP) genes in the gonads, suggesting the ‘neofunctionalisation’ of those genes in the zebrafish reproduction system. However, in the caudal fin, no differential expression of CP genes was identified, suggesting the observed differences in colouration between males and females in adult fish may be due to post-transcriptional regulation of key enzymes involved in pigment synthesis and distribution. CONCLUSIONS: Our study demonstrates male-biased sex ratio under high temperature condition and support a polygenic SD (PSD) system in laboratory zebrafish. We identify a subset of pathways (tight junction, gap junction and apoptosis), enriched for SD and CP genes, which appear to be co-regulated in the same pathway, providing evidence for involvement of those genes in the regulation of phenotypic sexual dimorphism in zebrafish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5722-1) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6503382
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-65033822019-05-10 Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio) Hosseini, Shahrbanou Ha, Ngoc-Thuy Simianer, Henner Falker-Gieske, Clemens Brenig, Bertram Franke, Andre Hörstgen-Schwark, Gabriele Tetens, Jens Herzog, Sebastian Sharifi, Ahmad Reza BMC Genomics Research Article BACKGROUND: Elevated water temperature, as is expected through climate change, leads to masculinization in fish species with sexual plasticity, resulting in changes in population dynamics. These changes are one important ecological consequence, contributing to the risk of extinction in small and inbred fish populations under natural conditions, due to male-biased sex ratio. Here we investigated the effect of elevated water temperature during embryogenesis on sex ratio and sex-biased gene expression profiles between two different tissues, namely gonad and caudal fin of adult zebrafish males and females, to gain new insights into the molecular mechanisms underlying sex determination (SD) and colour patterning related to sexual attractiveness. RESULTS: Our study demonstrated sex ratio imbalances with 25.5% more males under high-temperature condition, resulting from gonadal masculinization. The result of transcriptome analysis showed a significantly upregulated expression of male SD genes (e.g. dmrt1, amh, cyp11c1 and sept8b) and downregulation of female SD genes (e.g. zp2.1, vtg1, cyp19a1a and bmp15) in male gonads compared to female gonads. Contrary to expectations, we found highly differential expression of colour pattern (CP) genes in the gonads, suggesting the ‘neofunctionalisation’ of those genes in the zebrafish reproduction system. However, in the caudal fin, no differential expression of CP genes was identified, suggesting the observed differences in colouration between males and females in adult fish may be due to post-transcriptional regulation of key enzymes involved in pigment synthesis and distribution. CONCLUSIONS: Our study demonstrates male-biased sex ratio under high temperature condition and support a polygenic SD (PSD) system in laboratory zebrafish. We identify a subset of pathways (tight junction, gap junction and apoptosis), enriched for SD and CP genes, which appear to be co-regulated in the same pathway, providing evidence for involvement of those genes in the regulation of phenotypic sexual dimorphism in zebrafish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5722-1) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-06 /pmc/articles/PMC6503382/ /pubmed/31060508 http://dx.doi.org/10.1186/s12864-019-5722-1 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Hosseini, Shahrbanou
Ha, Ngoc-Thuy
Simianer, Henner
Falker-Gieske, Clemens
Brenig, Bertram
Franke, Andre
Hörstgen-Schwark, Gabriele
Tetens, Jens
Herzog, Sebastian
Sharifi, Ahmad Reza
Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_full Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_fullStr Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_full_unstemmed Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_short Genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (Danio rerio)
title_sort genetic mechanism underlying sexual plasticity and its association with colour patterning in zebrafish (danio rerio)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6503382/
https://www.ncbi.nlm.nih.gov/pubmed/31060508
http://dx.doi.org/10.1186/s12864-019-5722-1
work_keys_str_mv AT hosseinishahrbanou geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT hangocthuy geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT simianerhenner geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT falkergieskeclemens geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT brenigbertram geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT frankeandre geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT horstgenschwarkgabriele geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT tetensjens geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT herzogsebastian geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio
AT sharifiahmadreza geneticmechanismunderlyingsexualplasticityanditsassociationwithcolourpatterninginzebrafishdaniorerio