Sex-specific changes in gene expression in response to estrogen pollution around the onset of sex differentiation in grayling (Salmonidae)

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Abstract

The synthetic 17α-ethinylestradiol (EE2) is a common estrogenic pollutant that has been suspected to affect the demography of river-dwelling salmonids. One possibility is that exposure to EE2 tips the balance during initial steps of sex differentiation, so that male genotypes show female-specific gene expression and gonad formation. Here we study EE2 effects on gene expression around the onset of sex differentiation in a population of European grayling ( Thymallus thymallus) that suffers from sex ratio distortions. We exposed singly-raised embryos to one dose of 1 ng/L EE2, studied gene expression 10 days before hatching, at the day of hatching, and around the end of the yolk-sac stage, and related it to genetic sex (sdY genotype). We found that exposure to EE2 affects expression of a large number of genes, especially around hatching. These effects were strongly sex-dependent. We then raised fish for several months after hatching and found no evidence of sex reversal in the EE2-exposed fish. We conclude that ecologically relevant (i.e. low) levels of EE2 pollution do not cause sex reversal by simply tipping the balance at early stages of sex differentiation, but that they interfere with sex-specific gene expression.

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Why weight? Modelling sample and observational level variability improves power in RNA-seq analyses

Ruijie Liu, Aliaksei Z. Holik, Shian Su … (2015)

Variations in sample quality are frequently encountered in small RNA-sequencing experiments, and pose a major challenge in a differential expression analysis. Removal of high variation samples reduces noise, but at a cost of reducing power, thus limiting our ability to detect biologically meaningful changes. Similarly, retaining these samples in the analysis may not reveal any statistically significant changes due to the higher noise level. A compromise is to use all available data, but to down-weight the observations from more variable samples. We describe a statistical approach that facilitates this by modelling heterogeneity at both the sample and observational levels as part of the differential expression analysis. At the sample level this is achieved by fitting a log-linear variance model that includes common sample-specific or group-specific parameters that are shared between genes. The estimated sample variance factors are then converted to weights and combined with observational level weights obtained from the mean–variance relationship of the log-counts-per-million using ‘voom’. A comprehensive analysis involving both simulations and experimental RNA-sequencing data demonstrates that this strategy leads to a universally more powerful analysis and fewer false discoveries when compared to conventional approaches. This methodology has wide application and is implemented in the open-source ‘limma’ package.

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Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish.

Yann Guiguen, Alexis Fostier, Francesc Piferrer … (2010)

The present review focuses on the roles of estrogens and aromatase (Cyp19a1a), the enzyme needed for their synthesis, in fish gonadal sex differentiation. Based on the recent literature, we extend the already well accepted hypothesis of an implication of estrogens and Cyp19a1a in ovarian differentiation to a broader hypothesis that would place estrogens and Cyp19a1a in a pivotal position to control not only ovarian, but also testicular differentiation, in both gonochoristic and hermaphrodite fish species. This working hypothesis states that cyp19a1a up-regulation is needed not only for triggering but also for maintaining ovarian differentiation and that cyp19a1a down-regulation is the only necessary step for inducing a testicular differentiation pathway. When considering arguments for and against, most of the information available for fish supports this hypothesis since either suppression of cyp19a1a gene expression, inhibition of Cyp19a1a enzymatic activity, or blockage of estrogen receptivity are invariably associated with masculinization. This is also consistent with reports on normal gonadal differentiation, and steroid-modulated masculinization with either androgens, aromatase inhibitors or estrogen receptor antagonists, temperature-induced masculinization and protogynous sex change in hermaphrodite species. Concerning the regulation of fish cyp19a1a during gonadal differentiation, the transcription factor foxl2 has been characterized as an ovarian specific upstream regulator of a cyp19a1a promoter that would co-activate cyp19a1a expression, along with some additional partners such as nr5a1 (sf1) or cAMP. In contrast, upstream factors potentially down-regulating cyp19a1a during testicular differentiation are still hypothetical, such as the dmrt1 gene, but their definitive characterization as testicular repressors of cyp19a1a would strongly strengthen the hypothesis that early testicular differentiation would need active repression of cyp19a1a expression. Copyright 2009 Elsevier Inc. All rights reserved.

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Estrogen masculinizes neural pathways and sex-specific behaviors.

Melody Wu, Devanand S. Manoli, Eleanor J. Fraser … (2009)

Sex hormones are essential for neural circuit development and sex-specific behaviors. Male behaviors require both testosterone and estrogen, but it is unclear how the two hormonal pathways intersect. Circulating testosterone activates the androgen receptor (AR) and is also converted into estrogen in the brain via aromatase. We demonstrate extensive sexual dimorphism in the number and projections of aromatase-expressing neurons. The masculinization of these cells is independent of AR but can be induced in females by either testosterone or estrogen, indicating a role for aromatase in sexual differentiation of these neurons. We provide evidence suggesting that aromatase is also important in activating male-specific aggression and urine marking because these behaviors can be elicited by testosterone in males mutant for AR and in females subjected to neonatal estrogen exposure. Our results suggest that aromatization of testosterone into estrogen is important for the development and activation of neural circuits that control male territorial behaviors.

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Author and article information

Contributors

Claus Wedekind:

ORCID: http://orcid.org/0000-0001-6143-4716

claus.wedekind@unil.ch

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 15 July 2019

Publication date PMC-release: 15 July 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 583

Affiliations

[1 ]ISNI 0000 0001 2165 4204, GRID grid.9851.5, Department of Ecology and Evolution Biophore, , University of Lausanne, ; Lausanne, Switzerland

[2 ]ISNI 0000 0001 2223 3006, GRID grid.419765.8, Swiss Institute of Bioinformatics, ; Lausanne, Switzerland

[3 ]ISNI 0000000121839049, GRID grid.5333.6, Swiss Centre for Applied Ecotoxicology Eawag-EPFL, ; Dübendorf, Switzerland

[4 ]ISNI 0000 0001 2190 4373, GRID grid.7700.0, Aquatic Ecology and Toxicology Group Center of Organismic Studies, , University of Heidelberg, ; Heidelberg, Germany

[5 ]ISNI 0000000121839049, GRID grid.5333.6, Present Address: Swiss Federal Institute of Technology (EPFL), ; 1015 Lausanne, Switzerland

[6 ]ISNI 0000 0004 1937 0642, GRID grid.6612.3, Present Address: Department of Biomedicine, , University of Basel, ; 4031 Basel, Switzerland

[7 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, Present Address: Department of Environmental Sciences, Policy and Management, , University of California, ; Berkeley, CA 94720 USA

Author information

Claus Wedekind http://orcid.org/0000-0001-6143-4716

Article

Publisher ID: 5955

DOI: 10.1186/s12864-019-5955-z

PMC ID: 6631537

PubMed ID: 31307399

SO-VID: 3ee1f61d-fb42-4fb5-8ea0-b1ba75b4c3b6

License:

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.

History

Date received : 24 January 2019

Date accepted : 3 July 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;

Award ID: 31003A_159579

Award ID: 31003A_182265

Award Recipient : Claus Wedekind

Funded by: FundRef http://dx.doi.org/10.13039/501100003338, Bundesamt für Umwelt;

Award ID: none

Award Recipient : Claus Wedekind

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ScienceOpen disciplines: Genetics

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ScienceOpen disciplines: Genetics

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