Multi-genome comparisons reveal gain-and-loss evolution of anti-Mullerian hormone receptor type 2 as a candidate master sex-determining gene in Percidae.


Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
26 Jun 2024
Historique:
received: 19 01 2024
accepted: 06 06 2024
medline: 27 6 2024
pubmed: 27 6 2024
entrez: 26 6 2024
Statut: epublish

Résumé

The Percidae family comprises many fish species of major importance for aquaculture and fisheries. Based on three new chromosome-scale assemblies in Perca fluviatilis, Perca schrenkii, and Sander vitreus along with additional percid fish reference genomes, we provide an evolutionary and comparative genomic analysis of their sex-determination systems. We explored the fate of a duplicated anti-Mullerian hormone receptor type-2 gene (amhr2bY), previously suggested to be the master sex-determining (MSD) gene in P. flavescens. Phylogenetically related and structurally similar amhr2 duplicates (amhr2b) were found in P. schrenkii and Sander lucioperca, potentially dating this duplication event to their last common ancestor around 19-27 Mya. In P. fluviatilis and S. vitreus, this amhr2b duplicate has been likely lost while it was subject to amplification in S. lucioperca. Analyses of the amhr2b locus in P. schrenkii suggest that this duplication could be also male-specific as it is in P. flavescens. In P. fluviatilis, a relatively small (100 kb) non-recombinant sex-determining region (SDR) was characterized on chromosome 18 using population-genomics approaches. This SDR is characterized by many male-specific single-nucleotide variations (SNVs) and no large duplication/insertion event, suggesting that P. fluviatilis has a male heterogametic sex-determination system (XX/XY), generated by allelic diversification. This SDR contains six annotated genes, including three (c18h1orf198, hsdl1, tbc1d32) with higher expression in the testis than in the ovary. Together, our results provide a new example of the highly dynamic sex chromosome turnover in teleosts and provide new genomic resources for Percidae, including sex-genotyping tools for all three known Perca species.

Sections du résumé

BACKGROUND BACKGROUND
The Percidae family comprises many fish species of major importance for aquaculture and fisheries. Based on three new chromosome-scale assemblies in Perca fluviatilis, Perca schrenkii, and Sander vitreus along with additional percid fish reference genomes, we provide an evolutionary and comparative genomic analysis of their sex-determination systems.
RESULTS RESULTS
We explored the fate of a duplicated anti-Mullerian hormone receptor type-2 gene (amhr2bY), previously suggested to be the master sex-determining (MSD) gene in P. flavescens. Phylogenetically related and structurally similar amhr2 duplicates (amhr2b) were found in P. schrenkii and Sander lucioperca, potentially dating this duplication event to their last common ancestor around 19-27 Mya. In P. fluviatilis and S. vitreus, this amhr2b duplicate has been likely lost while it was subject to amplification in S. lucioperca. Analyses of the amhr2b locus in P. schrenkii suggest that this duplication could be also male-specific as it is in P. flavescens. In P. fluviatilis, a relatively small (100 kb) non-recombinant sex-determining region (SDR) was characterized on chromosome 18 using population-genomics approaches. This SDR is characterized by many male-specific single-nucleotide variations (SNVs) and no large duplication/insertion event, suggesting that P. fluviatilis has a male heterogametic sex-determination system (XX/XY), generated by allelic diversification. This SDR contains six annotated genes, including three (c18h1orf198, hsdl1, tbc1d32) with higher expression in the testis than in the ovary.
CONCLUSIONS CONCLUSIONS
Together, our results provide a new example of the highly dynamic sex chromosome turnover in teleosts and provide new genomic resources for Percidae, including sex-genotyping tools for all three known Perca species.

Identifiants

pubmed: 38926709
doi: 10.1186/s12915-024-01935-9
pii: 10.1186/s12915-024-01935-9
doi:

Substances chimiques

anti-Mullerian hormone receptor 0
Receptors, Peptide 0
Receptors, Transforming Growth Factor beta 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

141

Subventions

Organisme : Agence Nationale de la Recherche
ID : ANR-13-ISV7-0005
Organisme : Agence Nationale de la Recherche
ID : ANR-10-INBS-09
Organisme : Deutsche Forschungsgemeinschaft
ID : KU 3596/1-1
Organisme : Deutsche Forschungsgemeinschaft
ID : project number: 324050651

Informations de copyright

© 2024. The Author(s).

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Auteurs

Heiner Kuhl (H)

Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB (Forschungsverbund Berlin), Müggelseedamm 301/310, D-12587, Berlin, Germany. Heiner.Kuhl@igb-berlin.de.

Peter T Euclide (PT)

Department of Forestry and Natural Resources | Illinois-Indiana Sea Grant, Purdue University, West Lafayette, USA.

Christophe Klopp (C)

Sigenae, Plateforme Bioinformatique, Genotoul, BioinfoMics, UR875 Biométrie et Intelligence Artificielle, INRAE, Castanet-Tolosan, France.

Cédric Cabau (C)

Sigenae, GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet-Tolosan, France.

Margot Zahm (M)

Sigenae, Plateforme Bioinformatique, Genotoul, BioinfoMics, UR875 Biométrie et Intelligence Artificielle, INRAE, Castanet-Tolosan, France.

Céline Lopez-Roques (C)

INRAE, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France.

Carole Iampietro (C)

INRAE, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France.

Claire Kuchly (C)

INRAE, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France.

Cécile Donnadieu (C)

INRAE, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France.

Romain Feron (R)

Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
Swiss Institute of Bioinformatics, Lausanne, Switzerland.

Hugues Parrinello (H)

Montpellier GenomiX (MGX), c/o Institut de Génomique Fonctionnelle, 141 rue de la Cardonille, 34094, Montpellier Cedex 05, France.

Charles Poncet (C)

GDEC Gentyane, INRAE, Université Clermont Auvergne, Clermont-Ferrand, France.

Lydia Jaffrelo (L)

GDEC Gentyane, INRAE, Université Clermont Auvergne, Clermont-Ferrand, France.

Carole Confolent (C)

GDEC Gentyane, INRAE, Université Clermont Auvergne, Clermont-Ferrand, France.

Ming Wen (M)

INRAE, LPGP, 35000, Rennes, France.
State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, China.

Amaury Herpin (A)

INRAE, LPGP, 35000, Rennes, France.

Elodie Jouanno (E)

INRAE, LPGP, 35000, Rennes, France.

Anastasia Bestin (A)

SYSAAF, Station INRAE-LPGP, Campus de Beaulieu, 35042, Rennes Cedex, France.

Pierrick Haffray (P)

SYSAAF, Station INRAE-LPGP, Campus de Beaulieu, 35042, Rennes Cedex, France.

Romain Morvezen (R)

SYSAAF, Station INRAE-LPGP, Campus de Beaulieu, 35042, Rennes Cedex, France.

Taina Rocha de Almeida (TR)

University of Lorraine, INRAE, L2A, Nancy, France.

Thomas Lecocq (T)

University of Lorraine, INRAE, L2A, Nancy, France.

Bérénice Schaerlinger (B)

University of Lorraine, INRAE, L2A, Nancy, France.

Dominique Chardard (D)

University of Lorraine, INRAE, L2A, Nancy, France.

Daniel Żarski (D)

Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, ul. Tuwima 10, 10-748, Olsztyn, Poland.

Wesley A Larson (WA)

National Oceanographic and Atmospheric Administration, National Marine Fisheries Service, Alaska Fisheries Science Center, 17109 Point Lena Loop Road, Auke Bay LaboratoriesJuneau, AK, 99801, USA.

John H Postlethwait (JH)

Institute of Neuroscience, University of Oregon, Eugene, OR, 97403, USA.

Serik Timirkhanov (S)

Sea Biology LLP, Almaty, Kazakhstan.

Werner Kloas (W)

Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB (Forschungsverbund Berlin), Müggelseedamm 301/310, D-12587, Berlin, Germany.

Sven Wuertz (S)

Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB (Forschungsverbund Berlin), Müggelseedamm 301/310, D-12587, Berlin, Germany.

Matthias Stöck (M)

Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB (Forschungsverbund Berlin), Müggelseedamm 301/310, D-12587, Berlin, Germany.

Yann Guiguen (Y)

INRAE, LPGP, 35000, Rennes, France. yann.guiguen@inrae.fr.

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