A 180 My-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

Autor: Emmanuel Bonpunt, Romain Morvezen, Christophe Klopp, Kang Du, Christin Höhne, Pierre Patrice, Elena Santidrian Yebra-Pimentel, Mitica Ciorpac, Radu Suciu, Jörn Gessner, Matthias Stöck, Dunja K. Lamatsch, Dmitry Yu Prokopov, Wibke Kleiner, Pierrick Haffray, Anastasia Bestin, Bastien Debeuf, Heiner Kuhl, Manfred Schartl, Yann Guiguen, Eva Kreuz, Klaus Kohlmann, Sven Wuertz, Daniela Holostenco, Ron P. Dirks, Céline Lopez-Roques, Werner Kloas
Přispěvatelé: Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Laboratoire de Physiologie et Génomique des Poissons (LPGP), Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), University of Würzburg = Universität Würzburg, The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, Plateforme Bio-Informatique - Génotoul, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Future Genomics Technologies, « Danube Delta » National Institute for Research and Development [Tulcea], Academy of Agricultural and Forestry Sciences 'Gheorghe Ionescu-Sisesti' (A.A.F.S.), University of Innsbruck, Siberian Branch of the Russian Academy of Sciences (SB RAS), Syndicat des Sélectionneurs Avicoles et Aquacoles Français (SYSAAF), L’Esturgeonnière, SCEA Sturgeon, This work was funded through COFASP/ERANET (STURGEoNOMICS) by the German Federal Ministry of Food andAgriculture through the Federal Office for Agriculture and Food (grant nos. 2816ERA04G, 2816ERA05G) to M. Stöck,S.W., J.G. and M. Schartl, by the French National Research Agency (grant nos. ANR-16-COFA-0002) to YG, CK and CR,and by the Romanian Executive Agency for Higher Education, Research Development and Innovation Funding(UEFISCDI, contract 3/2017) to RS, MC and DH. This research was also in part supported by the Russian ScienceFoundation (RSF) to DP (grant number 18-44-04-007), by the Deutsche Forschungsgemeinschaft to MSch (DFG SCHA408/14-1), and by a European Maritime and Fisheries Fund to YG (EMFF/FEAMP project SIBERSEX). Research onA.gueldenstaedtii was supported by a European Maritime and Fisheries Fund to YG (EMFF/FEAMP project S’STURGEON)., ANR-16-COFA-0002,STURGEoNOMICS,Genome-based approaches for improvement of aquaculture in two marine sturgeon species: Atlantic sturgeon (Acipenser oxyrinchus) and Beluga (Huso huso)(2016), University of Würzburg, Système d'Information des GENomes des Animaux d'Elevage (SIGENAE), Génome et Transcriptome - Plateforme Génomique ( GeT-PlaGe), Plateforme Génome & Transcriptome (GET), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), This work was funded through COFASP/ERANET (STURGEoNOMICS) by the German Federal Ministry of Food and Agriculture through the Federal Office for Agriculture and Food (grant nos. 2816ERA04G and 2816ERA05G) to M.Stöck, S.W., J.G. and M.Schartl, by the French National Research Agency (grant nos. ANR-16-COFA-0002) to Y.G., C.K. and C.L.R., and by the Romanian Executive Agency for Higher Education, Research Development and Innovation Funding (UEFISCDI, contract 3/2017) to RS, MC and DH. H.K. was funded by the German Research Foundation (DFG) (Eigene Stelle grant no. KU 3596/1-1, Project No. 324050651). This research was also in part supported by the Russian Science Foundation (RSF) to D.P. (grant no. 18-44-04-007), by the Deutsche Forschungsgemeinschaft to MSch (DFG SCHA 408/14-1), and by a European Maritime and Fisheries Fund to Y.G. (EMFF/FEAMP project SIBERSEX). Research on A. gueldenstaedtii was supported by a European Maritime and Fisheries Fund to Y.G. (EMFF/FEAMP project S'STURGEON)., Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3)
Jazyk: angličtina
Rok vydání: 2020
Předmět:
0301 basic medicine
0106 biological sciences
Evolution
[SDV]Life Sciences [q-bio]
Acipenseridae
Sturgeon
Huso
Biology
010603 evolutionary biology
01 natural sciences
Genome
General Biochemistry
Genetics and Molecular Biology

[SDV.BDLR.RS]Life Sciences [q-bio]/Reproductive Biology/Sexual reproduction
Evolution
Molecular

Polyploidy
03 medical and health sciences
Phylogenetics
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]

biology.animal
Sex-determination system
Animals
14. Life underwater
Acipenser ruthenus
Evolution - stars
Clade
Phylogeny
Research Articles
030304 developmental biology
0303 health sciences
Fishes
Chromosome
Vertebrate
Sex chromosomes
Articles
Sex Determination Processes
biology.organism_classification
Female-specific
030104 developmental biology
Evolutionary biology
Female
General Agricultural and Biological Sciences
Zdroj: Philosophical Transactions of the Royal Society B: Biological Sciences
Philosophical Transactions of the Royal Society B: Biological Sciences, Royal Society, The, 2021, 376 (1832), pp.20200089. ⟨10.1098/rstb.2020.0089⟩
ISSN: 0962-8436
1471-2970
DOI: 10.1098/rstb.2020.0089⟩
Popis: Several hypotheses explain the prevalence of undifferentiated sex chromosomes in poikilothermic vertebrates. Turnovers change the master sex determination gene, the sex chromosome or the sex determination system (e.g. XY to WZ). Jumping master genes stay main triggers but translocate to other chromosomes. Occasional recombination (e.g. in sex-reversed females) prevents sex chromosome degeneration. Recent research has uncovered conserved heteromorphic or even homomorphic sex chromosomes in several clades of non-avian and non-mammalian vertebrates. Sex determination in sturgeons (Acipenseridae) has been a long-standing basic biological question, linked to economical demands by the caviar-producing aquaculture. Here, we report the discovery of a sex-specific sequence from sterlet ( Acipenser ruthenus ). Using chromosome-scale assemblies and pool-sequencing, we first identified an approximately 16 kb female-specific region. We developed a PCR-genotyping test, yielding female-specific products in six species, spanning the entire phylogeny with the most divergent extant lineages ( A. sturio, A. oxyrinchus versus A. ruthenus, Huso huso ), stemming from an ancient tetraploidization. Similar results were obtained in two octoploid species ( A. gueldenstaedtii, A. baerii ). Conservation of a female-specific sequence for a long period, representing 180 Myr of sturgeon evolution, and across at least one polyploidization event, raises many interesting biological questions. We discuss a conserved undifferentiated sex chromosome system with a ZZ/ZW-mode of sex determination and potential alternatives. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.
Databáze: OpenAIRE