Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis

International audience The Pacific oyster, Crassostrea gigas is a successive irregular hermaphrodite mollusc which has an annual breeding cycle. Oysters are naturally diploid organisms, but triploid oysters have been developed for use in shellfish aquaculture, with the aim of obtaining sterile anima...

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Published in:FEBS Open Bio
Main Authors: Maillard, Floriane, Elie, Nicolas, Vilain-Naud, Nadège, Lepoittevin, Mélanie, Martinez, Anne‐sophie, Lelong, Christophe
Other Authors: 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), Interactions Cellules Organismes Environnement (ICORE), Normandie Université (NU)-Normandie Université (NU)-CHU Caen, Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN), Œstrogènes, reproduction, cancer (OeReCa), Normandie Université (NU)-Normandie Université (NU)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2021
Subjects:
Online Access:https://hal.sorbonne-universite.fr/hal-03512046
https://hal.sorbonne-universite.fr/hal-03512046/document
https://hal.sorbonne-universite.fr/hal-03512046/file/FEBS%20Open%20Bio%20-%202021%20-%20Maillard%20-%20Male%20triploid%20oysters%20of%20Crassostrea%20gigas%20exhibit%20defects%20in%20mitosis%20and%20meiosis%20during.pdf
https://doi.org/10.1002/2211-5463.13356
id ftunivantilles:oai:HAL:hal-03512046v1
record_format openpolar
institution Open Polar
collection Université des Antilles (UAG): HAL
op_collection_id ftunivantilles
language English
topic triploid
spermatogenesis
mitosis
meiosis
oysters
Crassostrea gigas
[SDV]Life Sciences [q-bio]
spellingShingle triploid
spermatogenesis
mitosis
meiosis
oysters
Crassostrea gigas
[SDV]Life Sciences [q-bio]
Maillard, Floriane
Elie, Nicolas
Vilain-Naud, Nadège
Lepoittevin, Mélanie
Martinez, Anne‐sophie
Lelong, Christophe
Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
topic_facet triploid
spermatogenesis
mitosis
meiosis
oysters
Crassostrea gigas
[SDV]Life Sciences [q-bio]
description International audience The Pacific oyster, Crassostrea gigas is a successive irregular hermaphrodite mollusc which has an annual breeding cycle. Oysters are naturally diploid organisms, but triploid oysters have been developed for use in shellfish aquaculture, with the aim of obtaining sterile animals with commercial value. However, studies have shown that some triploid oysters are partially able to undergo gametogenesis, with numerous proliferating cells closed to diploids (3n alpha) or a partial one with an accumulation of locked germ cells (3n beta). The aim of our study therefore was to understand the regulation of spermatogenesis in both groups of triploid oysters (alpha and beta) from the beginning of spermatogenesis, during mitosis and meiosis events. Our results demonstrate that the reduced spermatogenesis in triploids results from a deregulation of the development of the germinal lineage and the establishment of the gonadal tract led by a lower number of tubules. Morphological cellular investigation also revealed an abnormal condensation of germ cell nuclei and the presence of clear patches in the nucleoplasm of triploid cells, which were more pronounced in beta oysters. Furthermore, studies of molecular and cellular regulation showed a downregulation of mitotic spindle checkpoint in beta oysters, resulting in disturbance of chromosomal segregation, notably on Spindle Assembly Checkpoint involved in the binding of microtubules to chromosomes. Taken together, our results suggest that the lower reproductive ability of triploid oysters may be due to cellular and molecular events such as impairment of spermatogenesis and disruptions of mitosis and meiosis, occurring early and at various stages of the gametogenetic cycle.
author2 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)
Interactions Cellules Organismes Environnement (ICORE)
Normandie Université (NU)-Normandie Université (NU)-CHU Caen
Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN)
Œstrogènes, reproduction, cancer (OeReCa)
Normandie Université (NU)-Normandie Université (NU)
format Article in Journal/Newspaper
author Maillard, Floriane
Elie, Nicolas
Vilain-Naud, Nadège
Lepoittevin, Mélanie
Martinez, Anne‐sophie
Lelong, Christophe
author_facet Maillard, Floriane
Elie, Nicolas
Vilain-Naud, Nadège
Lepoittevin, Mélanie
Martinez, Anne‐sophie
Lelong, Christophe
author_sort Maillard, Floriane
title Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
title_short Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
title_full Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
title_fullStr Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
title_full_unstemmed Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
title_sort male triploid oysters of crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis
publisher HAL CCSD
publishDate 2021
url https://hal.sorbonne-universite.fr/hal-03512046
https://hal.sorbonne-universite.fr/hal-03512046/document
https://hal.sorbonne-universite.fr/hal-03512046/file/FEBS%20Open%20Bio%20-%202021%20-%20Maillard%20-%20Male%20triploid%20oysters%20of%20Crassostrea%20gigas%20exhibit%20defects%20in%20mitosis%20and%20meiosis%20during.pdf
https://doi.org/10.1002/2211-5463.13356
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source ISSN: 2211-5463
EISSN: 2211-5463
FEBS Open Bio
https://hal.sorbonne-universite.fr/hal-03512046
FEBS Open Bio, 2021, ⟨10.1002/2211-5463.13356⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1002/2211-5463.13356
hal-03512046
https://hal.sorbonne-universite.fr/hal-03512046
https://hal.sorbonne-universite.fr/hal-03512046/document
https://hal.sorbonne-universite.fr/hal-03512046/file/FEBS%20Open%20Bio%20-%202021%20-%20Maillard%20-%20Male%20triploid%20oysters%20of%20Crassostrea%20gigas%20exhibit%20defects%20in%20mitosis%20and%20meiosis%20during.pdf
doi:10.1002/2211-5463.13356
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1002/2211-5463.13356
container_title FEBS Open Bio
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spelling ftunivantilles:oai:HAL:hal-03512046v1 2024-04-14T08:10:37+00:00 Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis Maillard, Floriane Elie, Nicolas Vilain-Naud, Nadège Lepoittevin, Mélanie Martinez, Anne‐sophie Lelong, Christophe 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) Interactions Cellules Organismes Environnement (ICORE) Normandie Université (NU)-Normandie Université (NU)-CHU Caen Normandie Université (NU)-Tumorothèque de Caen Basse-Normandie (TCBN)-Tumorothèque de Caen Basse-Normandie (TCBN) Œstrogènes, reproduction, cancer (OeReCa) Normandie Université (NU)-Normandie Université (NU) 2021-12-22 https://hal.sorbonne-universite.fr/hal-03512046 https://hal.sorbonne-universite.fr/hal-03512046/document https://hal.sorbonne-universite.fr/hal-03512046/file/FEBS%20Open%20Bio%20-%202021%20-%20Maillard%20-%20Male%20triploid%20oysters%20of%20Crassostrea%20gigas%20exhibit%20defects%20in%20mitosis%20and%20meiosis%20during.pdf https://doi.org/10.1002/2211-5463.13356 en eng HAL CCSD Wiley Open Access/Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1002/2211-5463.13356 hal-03512046 https://hal.sorbonne-universite.fr/hal-03512046 https://hal.sorbonne-universite.fr/hal-03512046/document https://hal.sorbonne-universite.fr/hal-03512046/file/FEBS%20Open%20Bio%20-%202021%20-%20Maillard%20-%20Male%20triploid%20oysters%20of%20Crassostrea%20gigas%20exhibit%20defects%20in%20mitosis%20and%20meiosis%20during.pdf doi:10.1002/2211-5463.13356 info:eu-repo/semantics/OpenAccess ISSN: 2211-5463 EISSN: 2211-5463 FEBS Open Bio https://hal.sorbonne-universite.fr/hal-03512046 FEBS Open Bio, 2021, ⟨10.1002/2211-5463.13356⟩ triploid spermatogenesis mitosis meiosis oysters Crassostrea gigas [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2021 ftunivantilles https://doi.org/10.1002/2211-5463.13356 2024-03-21T17:53:07Z International audience The Pacific oyster, Crassostrea gigas is a successive irregular hermaphrodite mollusc which has an annual breeding cycle. Oysters are naturally diploid organisms, but triploid oysters have been developed for use in shellfish aquaculture, with the aim of obtaining sterile animals with commercial value. However, studies have shown that some triploid oysters are partially able to undergo gametogenesis, with numerous proliferating cells closed to diploids (3n alpha) or a partial one with an accumulation of locked germ cells (3n beta). The aim of our study therefore was to understand the regulation of spermatogenesis in both groups of triploid oysters (alpha and beta) from the beginning of spermatogenesis, during mitosis and meiosis events. Our results demonstrate that the reduced spermatogenesis in triploids results from a deregulation of the development of the germinal lineage and the establishment of the gonadal tract led by a lower number of tubules. Morphological cellular investigation also revealed an abnormal condensation of germ cell nuclei and the presence of clear patches in the nucleoplasm of triploid cells, which were more pronounced in beta oysters. Furthermore, studies of molecular and cellular regulation showed a downregulation of mitotic spindle checkpoint in beta oysters, resulting in disturbance of chromosomal segregation, notably on Spindle Assembly Checkpoint involved in the binding of microtubules to chromosomes. Taken together, our results suggest that the lower reproductive ability of triploid oysters may be due to cellular and molecular events such as impairment of spermatogenesis and disruptions of mitosis and meiosis, occurring early and at various stages of the gametogenetic cycle. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Université des Antilles (UAG): HAL Pacific FEBS Open Bio