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Journal articles
Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation
Qiaowei Pan
1, 2
Romain Feron
1, 2
Ayaka Yano
1
René Guyomard
3
Elodie Jouanno
1
Estelle Vigouroux
1
Ming Wen
1
Jean-Mickaël Busnel
4
Julien Bobe
1
Jean-Paul Concordet
5
Hugues Parrinello
6
Laurent Journot
6
Christophe Klopp
7, 8, 9
Jérôme Lluch
10
Céline Roques
10
John Postlethwait
11
Manfred Schartl
12, 13, 14
Amaury Herpin
1
Yann Guiguen
1, *
*
Corresponding author
4
FDPPMA 35 - Fédération d'Ille-et-Vilaine pour la pêche et la protection du milieu aquatique [Rennes]
10
GeT-PlaGe - Génome et Transcriptome - Plateforme Génomique
INRA - Institut National de la Recherche Agronomique : US 1426, GET - Plateforme Génome & Transcriptome
Qiaowei Pan 1, 2
Author
Romain Feron 1, 2
Author IdHAL : romainferon ORCID : https://orcid.org/0000-0001-5893-6184
Ayaka Yano 1
Author
René Guyomard 3
Author
Elodie Jouanno 1
Author Employer institution : Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement IdHAL : elodiejouanno
Estelle Vigouroux 1
Author
Ming Wen 1
Author
Jean-Mickaël Busnel 4
Author
Julien Bobe 1
Author Employer institution : Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement IdHAL : julien-bobe ORCID : https://orcid.org/0000-0002-9355-8227
Jean-Paul Concordet 5
Author
Hugues Parrinello 6
Author
Laurent Journot 6
Author IdHAL : ljournot ResearcherId : http://www.researcherid.com/rid/T-9652-2018 ORCID : https://orcid.org/0000-0003-3499-8887
Christophe C. Klopp 7, 8, 9
Author Employer institution : Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement IdHAL : 0000-0001-7126-5477 ORCID : https://orcid.org/0000-0001-7126-5477
Jérôme Lluch 10
Author
Céline Roques 10
Author
John Postlethwait 11
Author
Manfred Schartl 12, 13, 14
Author
Amaury Herpin 1
Author Employer institution : Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement IdHAL : amaury-herpin ResearcherId : http://www.researcherid.com/rid/B-8950-2011 ORCID : https://orcid.org/0000-0002-0630-4027
Yann Guiguen 1
Correspondent author Employer institution : Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement IdHAL : yann-guiguen ORCID : https://orcid.org/0000-0001-5464-6219
1
LPGP - Laboratoire de Physiologie et Génomique des Poissons (Campus de Beaulieu - Bât. 16A - 35042 RENNES Cedex [France] - France)
- INRA - Institut National de la Recherche Agronomique : UR1037 (France)
- Biosit : Biologie - Santé - Innovation Technologique - Structure Fédérative de Recherche en Biologie et Santé de Rennes (Université Rennes 1 - Campus Santé Villejean - 2, avenue Professeur Léon Bernard 35043 Rennes cedex - France)
2
Department of Ecology and Evolution [Lausanne] (Biophore - CH-1015 Lausanne - Switzerland)
- UNIL - Université de Lausanne (CH-1015 Lausanne - Switzerland)
3
GABI - Génétique Animale et Biologie Intégrative (Domaine de Vilvert F-78252 Jouy-en-Josas - France)
- INRA - Institut National de la Recherche Agronomique : UMR1313 (France)
- AgroParisTech (16 rue Claude Bernard F-75231 Paris Cedex 05 - France)
4
FDPPMA 35 - Fédération d'Ille-et-Vilaine pour la pêche et la protection du milieu aquatique [Rennes] (France)
5
STRING - Structure et Instabilité des Génomes (43 rue Cuvier - Case postale 26 - 75231 Paris Cedex 05 - France)
- MNHN - Muséum national d'Histoire naturelle (57, rue Cuvier - 75231 Paris Cedex 05 - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U1154 (101, rue de Tolbiac, 75013 Paris - France)
- SU - Sorbonne Université (21 rue de l’École de médecine - 75006 Paris - France)
- CNRS - Centre National de la Recherche Scientifique : UMR7196 (France)
6
IGF - Institut de Génomique Fonctionnelle (141, Rue de la Cardonille 34094 Montpellier cedex 5 - France)
- UM - Université de Montpellier (163 rue Auguste Broussonnet - 34090 Montpellier - France)
- UM1 - Université Montpellier 1 (5, boulevard Henri IV - CS 19044 - 34967 Montpellier cedex - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U1191 (101, rue de Tolbiac, 75013 Paris - France)
- UM2 - Université Montpellier 2 - Sciences et Techniques (Place Eugène Bataillon - 34095 Montpellier cedex 5 - France)
- CNRS - Centre National de la Recherche Scientifique : UMR5203 (France)
7
Plateforme Bio-Informatique - Génotoul (France)
9
GenPhySE - Génétique Physiologie et Systèmes d'Elevage (INRA Auzeville -
24, chemin de Borde-Rouge -
Auzeville Tolosane
31326 Castanet Tolosan
- France)
- École nationale supérieure agronomique de Toulouse [ENSAT] (France)
- INRA - Institut National de la Recherche Agronomique : UMR1388 (France)
- ENVT - Ecole Nationale Vétérinaire de Toulouse (23 chemin des Capelles
31076 Toulouse
Cedex - France)
- Toulouse INP - Institut National Polytechnique (Toulouse) (France)
- Université Fédérale Toulouse Midi-Pyrénées (41 Allée Jules Guesde, 31000 Toulouse - France)
- Toulouse INP - Institut National Polytechnique (Toulouse) (France)
10
GeT-PlaGe - Génome et Transcriptome - Plateforme Génomique (Campus INRA
24 chemin de borde rouge - Auzeville
CS 52627
31326 CASTANET-TOLOSAN Cedex - France)
- INRA - Institut National de la Recherche Agronomique : US 1426 (France)
- GET - Plateforme Génome & Transcriptome (Bio5 - INSA 135 Avenue de Rangueil 31077 Toulouse Cedex 04 - France)
- GENOTOUL - Génopole Toulouse Midi-Pyrénées [Auzeville] (Chemin de Borde-Rouge Auzeville - France)
- INSA Toulouse - Institut National des Sciences Appliquées - Toulouse (135, avenue de Rangueil - 31077 Toulouse cedex 4 - France)
- UT3 - Université Toulouse III - Paul Sabatier (118 route de Narbonne - 31062 Toulouse - France)
- Université Fédérale Toulouse Midi-Pyrénées (41 Allée Jules Guesde, 31000 Toulouse - France)
- INRAE - Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (France)
- ENVT - Ecole Nationale Vétérinaire de Toulouse (23 chemin des Capelles
31076 Toulouse
Cedex - France)
- Toulouse INP - Institut National Polytechnique (Toulouse) (France)
- Université Fédérale Toulouse Midi-Pyrénées (41 Allée Jules Guesde, 31000 Toulouse - France)
- Toulouse INP - Institut National Polytechnique (Toulouse) (France)
- Toulouse INP - Institut National Polytechnique (Toulouse) (France)
- Université Fédérale Toulouse Midi-Pyrénées (41 Allée Jules Guesde, 31000 Toulouse - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale (101, rue de Tolbiac, 75013 Paris - France)
- GENOTOUL - Génopole Toulouse Midi-Pyrénées [Auzeville] (Chemin de Borde-Rouge Auzeville - France)
11
Institute of Neuroscience [Eugene, OR, États-Unis] (United States)
- University of Oregon [Eugene] (1585 E 13th Ave. Eugene, OR 97403 - United States)
12
Department of Physiological Chemistry [Würzburg, Allemagne] (Germany)
- University of Würzburg (Sanderring 2 97070 Würzburg - Germany)
- Biocenter [Würzburg, Allemagne] (Germany)
13
Comprehensive Cancer Center Mainfranken [Würzburg, Allemagne] (Germany)
- University Hospital of Würzburg (Germany)
14
Department of Biology [College Station, TX, États-Unis] (United States)
- Hagler Institute for Advanced Study [College Station, TX, États-Unis] (United States)
- Texas A&M University [College Station] (College Station, TX 77843 - United States)
Abstract : Teleost fishes, thanks to their rapid evolution of sex determination mechanisms, provide remarkable opportunities to study the formation of sex chromosomes and the mechanisms driving the birth of new master sex determining (MSD) genes. However, the evolutionary interplay between the sex chromosomes and the MSD genes they harbor is rather unexplored. We characterized a male-specific duplicate of the anti-Müllerian hormone (amh) as the MSD gene in Northern Pike (Esox lucius), using genomic and expression evidence as well as by loss-of-function and gain-of-function experiments. Using RAD-Sequencing from a family panel, we identified Linkage Group (LG) 24 as the sex chromosome and positioned the sex locus in its sub-telomeric region. Furthermore, we demonstrated that this MSD originated from an ancient duplication of the autosomal amh gene, which was subsequently translocated to LG24. Using sex-specific pooled genome sequencing and a new male genome sequence assembled using Nanopore long reads, we also characterized the differentiation of the X and Y chromosomes, revealing a small male-specific insertion containing the MSD gene and a limited region with reduced recombination. Our study reveals an unexpectedly low level of differentiation between a pair of sex chromosomes harboring an old MSD gene in a wild teleost fish population, and highlights both the pivotal role of genes from the amh pathway in sex determination, as well as the importance of gene duplication as a mechanism driving the turnover of sex chromosomes in this clade.
Document type :
Journal articles
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https://www.hal.inserm.fr/inserm-02279967
Contributor : Myriam Bodescot Connect in order to contact the contributor
Submitted on : Thursday, September 5, 2019 - 4:56:23 PM
Last modification on : Friday, October 22, 2021 - 2:48:05 PM
Long-term archiving on: : Thursday, February 6, 2020 - 1:33:42 AM
Contributor : Myriam Bodescot Connect in order to contact the contributor
Submitted on : Thursday, September 5, 2019 - 4:56:23 PM
Last modification on : Friday, October 22, 2021 - 2:48:05 PM
Long-term archiving on: : Thursday, February 6, 2020 - 1:33:42 AM
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journal.pgen.1008013.pdf
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Distributed under a Creative Commons Attribution 4.0 International License
Identifiers
- HAL Id : inserm-02279967, version 1
- DOI : 10.1371/journal.pgen.1008013
- PRODINRA : 482753
- PUBMED : 31437150
- WOS : 000486222200041
Collections
INSERM | INRA | IGF | CNRS | LPGP | BIOSIT | INC-CNRS | AGROPARISTECH | BS | UNIV-MONTPELLIER | SORBONNE-UNIVERSITE | MNHN | SU-SCIENCES | INRAE | SU-TI | GENETIQUE_ANIMALE | GS-BIOSPHERA | UNIV-TLSE3 | INSA-TOULOUSE | PHASE
Citation
Qiaowei Pan, Romain Feron, Ayaka Yano, René Guyomard, Elodie Jouanno, et al.. Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation. PLoS Genetics, Public Library of Science, 2019, 15 (8), pp.e1008013. ⟨10.1371/journal.pgen.1008013⟩. ⟨inserm-02279967⟩
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