Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy

International audience Background: Triploidy can occur in many animal species but is often lethal. Among invertebrates, amphibians and fishes, triploids are viable although often sterile or infertile. Most triploids of the Pacific oyster Crassostrea gigas are almost sterile (named ''3nb�...

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Published in:PLoS ONE
Main Authors: Dheilly, Nolwenn, Jouaux, Aude, Boudry, Pierre, Favrel, Pascal, Lelong, Christophe
Other Authors: Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2014
Subjects:
SEX
ACL
Online Access:https://hal.sorbonne-universite.fr/hal-03779108
https://doi.org/10.1371/journal.pone.0112094
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spelling ftnormandieuniv:oai:HAL:hal-03779108v1 2023-05-15T15:58:19+02:00 Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy Dheilly, Nolwenn, Jouaux, Aude Boudry, Pierre Favrel, Pascal Lelong, Christophe Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Biologie des Organismes et Ecosystèmes Aquatiques (BOREA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) 2014-11-06 https://hal.sorbonne-universite.fr/hal-03779108 https://doi.org/10.1371/journal.pone.0112094 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0112094 hal-03779108 https://hal.sorbonne-universite.fr/hal-03779108 doi:10.1371/journal.pone.0112094 http://creativecommons.org/licenses/by/ ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://hal.sorbonne-universite.fr/hal-03779108 PLoS ONE, 2014, 9 (11), pp.e112094. ⟨10.1371/journal.pone.0112094⟩ SEX SPERMATOGENESIS DIFFERENTIATION IDENTIFICATION ACL PERFORMANCE TEMPERATURE GENE-EXPRESSION THUNBERG GROWTH FISH [SDU.OCEAN]Sciences of the Universe [physics]/Ocean Atmosphere [SDV]Life Sciences [q-bio] [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2014 ftnormandieuniv https://doi.org/10.1371/journal.pone.0112094 2023-03-14T23:45:06Z International audience Background: Triploidy can occur in many animal species but is often lethal. Among invertebrates, amphibians and fishes, triploids are viable although often sterile or infertile. Most triploids of the Pacific oyster Crassostrea gigas are almost sterile (named ''3nb'') yet a low but significant proportion show an advanced gametogenesis (named ''3na''). These oysters thus constitute an interesting model to study the effect of triploidy on germ cell development. We used microarrays to compare the gonad transcriptomes of diploid 2n and the abovementioned triploid 3nb and 3na male and female oysters throughout gametogenesis. Results: All triploids displayed an upregulation of genes related to DNA repair and apoptosis and a downregulation of genes associated with cell division. The comparison of 3na and 3nb transcriptomes with 2n revealed the likely involvement of a cell cycle checkpoint during mitosis in the successful but delayed development of gonads in 3na individuals. In contrast, a disruption of sex differentiation mechanisms may explain the sterility of 3nb individuals with 3nb females expressing male-specific genes and 3nb males expressing female-specific genes. Conclusions: The disruption of sex differentiation and mitosis may be responsible for the impaired gametogenesis of triploid Pacific oysters. The function of the numerous candidate genes identified in our study should now be studied in detail in order to elucidate their role in sex determination, mitosis/meiosis control, pachytene cell cycle checkpoint, and the control of DNA repair/apoptosis. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Normandie Université: HAL Pacific PLoS ONE 9 11 e112094
institution Open Polar
collection Normandie Université: HAL
op_collection_id ftnormandieuniv
language English
topic SEX
SPERMATOGENESIS
DIFFERENTIATION
IDENTIFICATION
ACL
PERFORMANCE
TEMPERATURE
GENE-EXPRESSION
THUNBERG
GROWTH
FISH
[SDU.OCEAN]Sciences of the Universe [physics]/Ocean
Atmosphere
[SDV]Life Sciences [q-bio]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle SEX
SPERMATOGENESIS
DIFFERENTIATION
IDENTIFICATION
ACL
PERFORMANCE
TEMPERATURE
GENE-EXPRESSION
THUNBERG
GROWTH
FISH
[SDU.OCEAN]Sciences of the Universe [physics]/Ocean
Atmosphere
[SDV]Life Sciences [q-bio]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Dheilly, Nolwenn,
Jouaux, Aude
Boudry, Pierre
Favrel, Pascal
Lelong, Christophe
Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy
topic_facet SEX
SPERMATOGENESIS
DIFFERENTIATION
IDENTIFICATION
ACL
PERFORMANCE
TEMPERATURE
GENE-EXPRESSION
THUNBERG
GROWTH
FISH
[SDU.OCEAN]Sciences of the Universe [physics]/Ocean
Atmosphere
[SDV]Life Sciences [q-bio]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description International audience Background: Triploidy can occur in many animal species but is often lethal. Among invertebrates, amphibians and fishes, triploids are viable although often sterile or infertile. Most triploids of the Pacific oyster Crassostrea gigas are almost sterile (named ''3nb'') yet a low but significant proportion show an advanced gametogenesis (named ''3na''). These oysters thus constitute an interesting model to study the effect of triploidy on germ cell development. We used microarrays to compare the gonad transcriptomes of diploid 2n and the abovementioned triploid 3nb and 3na male and female oysters throughout gametogenesis. Results: All triploids displayed an upregulation of genes related to DNA repair and apoptosis and a downregulation of genes associated with cell division. The comparison of 3na and 3nb transcriptomes with 2n revealed the likely involvement of a cell cycle checkpoint during mitosis in the successful but delayed development of gonads in 3na individuals. In contrast, a disruption of sex differentiation mechanisms may explain the sterility of 3nb individuals with 3nb females expressing male-specific genes and 3nb males expressing female-specific genes. Conclusions: The disruption of sex differentiation and mitosis may be responsible for the impaired gametogenesis of triploid Pacific oysters. The function of the numerous candidate genes identified in our study should now be studied in detail in order to elucidate their role in sex determination, mitosis/meiosis control, pachytene cell cycle checkpoint, and the control of DNA repair/apoptosis.
author2 Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR)
Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM)
Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)
Biologie des Organismes et Ecosystèmes Aquatiques (BOREA)
Université de Caen Normandie (UNICAEN)
Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
format Article in Journal/Newspaper
author Dheilly, Nolwenn,
Jouaux, Aude
Boudry, Pierre
Favrel, Pascal
Lelong, Christophe
author_facet Dheilly, Nolwenn,
Jouaux, Aude
Boudry, Pierre
Favrel, Pascal
Lelong, Christophe
author_sort Dheilly, Nolwenn,
title Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy
title_short Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy
title_full Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy
title_fullStr Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy
title_full_unstemmed Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy
title_sort transcriptomic profiling of gametogenesis in triploid pacific oysters crassostrea gigas: towards an understanding of partial sterility associated with triploidy
publisher HAL CCSD
publishDate 2014
url https://hal.sorbonne-universite.fr/hal-03779108
https://doi.org/10.1371/journal.pone.0112094
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source ISSN: 1932-6203
EISSN: 1932-6203
PLoS ONE
https://hal.sorbonne-universite.fr/hal-03779108
PLoS ONE, 2014, 9 (11), pp.e112094. ⟨10.1371/journal.pone.0112094⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0112094
hal-03779108
https://hal.sorbonne-universite.fr/hal-03779108
doi:10.1371/journal.pone.0112094
op_rights http://creativecommons.org/licenses/by/
op_doi https://doi.org/10.1371/journal.pone.0112094
container_title PLoS ONE
container_volume 9
container_issue 11
container_start_page e112094
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