Sex chromosome and sex locus characterization in goldfish, Carassius auratus (Linnaeus, 1758).


Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
11 Aug 2020
Historique:
received: 08 01 2020
accepted: 29 07 2020
entrez: 13 8 2020
pubmed: 13 8 2020
medline: 15 5 2021
Statut: epublish

Résumé

Goldfish is an important model for various areas of research, including neural development and behavior and a species of significant importance in aquaculture, especially as an ornamental species. It has a male heterogametic (XX/XY) sex determination system that relies on both genetic and environmental factors, with high temperatures being able to produce female-to-male sex reversal. Little, however, is currently known on the molecular basis of genetic sex determination in this important cyprinid model. Here we used sequencing approaches to better characterize sex determination and sex-chromosomes in an experimental strain of goldfish. Our results confirmed that sex determination in goldfish is a mix of environmental and genetic factors and that its sex determination system is male heterogametic (XX/XY). Using reduced representation (RAD-seq) and whole genome (pool-seq) approaches, we characterized sex-linked polymorphisms and developed male specific genetic markers. These male specific markers were used to distinguish sex-reversed XX neomales from XY males and to demonstrate that XX female-to-male sex reversal could even occur at a relatively low rearing temperature (18 °C), for which sex reversal has been previously shown to be close to zero. We also characterized a relatively large non-recombining region (~ 11.7 Mb) on goldfish linkage group 22 (LG22) that contained a high-density of male-biased genetic polymorphisms. This large LG22 region harbors 373 genes, including a single candidate as a potential master sex gene, i.e., the anti-Mullerian hormone gene (amh). However, no sex-linked polymorphisms were detected in the coding DNA sequence of the goldfish amh gene. These results show that our goldfish strain has a relatively large sex locus on LG22, which is likely the Y chromosome of this experimental population. The presence of a few XX males even at low temperature also suggests that other environmental factors in addition to temperature could trigger female-to-male sex reversal. Finally, we also developed sex-linked genetic markers, which will be important tools for future research on sex determination in our experimental goldfish population. However, additional work would be needed to explore whether this sex locus is conserved in other populations of goldfish.

Sections du résumé

BACKGROUND BACKGROUND
Goldfish is an important model for various areas of research, including neural development and behavior and a species of significant importance in aquaculture, especially as an ornamental species. It has a male heterogametic (XX/XY) sex determination system that relies on both genetic and environmental factors, with high temperatures being able to produce female-to-male sex reversal. Little, however, is currently known on the molecular basis of genetic sex determination in this important cyprinid model. Here we used sequencing approaches to better characterize sex determination and sex-chromosomes in an experimental strain of goldfish.
RESULTS RESULTS
Our results confirmed that sex determination in goldfish is a mix of environmental and genetic factors and that its sex determination system is male heterogametic (XX/XY). Using reduced representation (RAD-seq) and whole genome (pool-seq) approaches, we characterized sex-linked polymorphisms and developed male specific genetic markers. These male specific markers were used to distinguish sex-reversed XX neomales from XY males and to demonstrate that XX female-to-male sex reversal could even occur at a relatively low rearing temperature (18 °C), for which sex reversal has been previously shown to be close to zero. We also characterized a relatively large non-recombining region (~ 11.7 Mb) on goldfish linkage group 22 (LG22) that contained a high-density of male-biased genetic polymorphisms. This large LG22 region harbors 373 genes, including a single candidate as a potential master sex gene, i.e., the anti-Mullerian hormone gene (amh). However, no sex-linked polymorphisms were detected in the coding DNA sequence of the goldfish amh gene.
CONCLUSIONS CONCLUSIONS
These results show that our goldfish strain has a relatively large sex locus on LG22, which is likely the Y chromosome of this experimental population. The presence of a few XX males even at low temperature also suggests that other environmental factors in addition to temperature could trigger female-to-male sex reversal. Finally, we also developed sex-linked genetic markers, which will be important tools for future research on sex determination in our experimental goldfish population. However, additional work would be needed to explore whether this sex locus is conserved in other populations of goldfish.

Identifiants

pubmed: 32781981
doi: 10.1186/s12864-020-06959-3
pii: 10.1186/s12864-020-06959-3
pmc: PMC7430817
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

552

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM139635
Pays : United States
Organisme : Agence Nationale de la Recherche
ID : ANR-13-ISV7-0005
Organisme : NIH HHS
ID : R01 OD011116
Pays : United States
Organisme : NIH HHS
ID : R01OD011116
Pays : United States
Organisme : Deutsche Forschungsgemeinschaft
ID : DFG-13-ISV7-0005
Organisme : Agence Nationale de la Recherche
ID : ANR-10-INBS-09
Organisme : NIH HHS
ID : 5R01GM085318
Pays : United States
Organisme : Grant-in-Aid for Scientific Research
ID : 19K22426

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Auteurs

Ming Wen (M)

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

Romain Feron (R)

INRAE, LPGP, 35000, Rennes, France.
Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland.

Qiaowei Pan (Q)

INRAE, LPGP, 35000, Rennes, France.
Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.

Justine Guguin (J)

INRAE, LPGP, 35000, Rennes, France.

Elodie Jouanno (E)

INRAE, LPGP, 35000, Rennes, France.

Amaury Herpin (A)

INRAE, LPGP, 35000, Rennes, France.

Christophe Klopp (C)

Plate-forme bio-informatique Genotoul, Mathématiques et Informatique Appliquées de Toulouse, INRAE, Castanet Tolosan, France.
SIGENAE, GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet Tolosan, France.

Cedric Cabau (C)

SIGENAE, GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet Tolosan, France.

Margot Zahm (M)

SIGENAE, GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet Tolosan, France.

Hugues Parrinello (H)

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

Laurent Journot (L)

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

Shawn M Burgess (SM)

Translational and Functional Genomics Branch, National Human Genome Research Institute, Bethesda, MD, USA.

Yoshihiro Omori (Y)

Laboratory of Functional Genomics, Graduate School of Bioscience, Nagahama Institute of Bioscience and Technology, Nagahama, Shiga, Japan.
Laboratory for Molecular and Developmental Biology, Institute for Protein Research, Osaka University, Suita, Osaka, Japan.

John H Postlethwait (JH)

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

Manfred Schartl (M)

Developmental Biochemistry, Biozentrum, University of Würzburg, Würzburg, Germany.
The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, San Marcos, TX, USA.

Yann Guiguen (Y)

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

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