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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
1 LPGP - Laboratoire de Physiologie et Génomique des Poissons
2 Department of Ecology and Evolution [Lausanne]
3 GABI - Génétique Animale et Biologie Intégrative
4 FDPPMA 35 - Fédération d'Ille-et-Vilaine pour la pêche et la protection du milieu aquatique [Rennes]
5 STRING - Structure et Instabilité des Génomes
6 IGF - Institut de Génomique Fonctionnelle
7 Plateforme Bioinformatique Genotoul [Castanet-Tolosan]
8 SIGENAE - Système d'Information des GENomes des Animaux d'Elevage
9 GenPhySE - Génétique Physiologie et Systèmes d'Elevage
10 GeT PlaGe - GeT PlaGe, Genotoul
11 Institute of Neuroscience [Eugene, OR, États-Unis]
12 Department of Physiological Chemistry [Würzburg, Allemagne]
13 Comprehensive Cancer Center Mainfranken [Würzburg, Allemagne]
14 Department of Biology [College Station, TX, États-Unis]
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.
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https://www.hal.inserm.fr/inserm-02279967
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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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