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

The Pacific oyster, Crassostrea gigas, is a successive irregular hermaphrodite mollusk 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 val...

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Published in:FEBS Open Bio
Main Authors: Maillard, Floriane, Elie, Nicolas, Villain‐Naud, Nadège, Lepoittevin, Mélanie, Martinez, Anne‐Sophie, Lelong, Christophe
Format: Text
Language:English
Published: John Wiley and Sons Inc. 2022
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340784/
http://www.ncbi.nlm.nih.gov/pubmed/34935310
https://doi.org/10.1002/2211-5463.13356
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spelling ftpubmed:oai:pubmedcentral.nih.gov:9340784 2023-05-15T15:58:17+02:00 Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis Maillard, Floriane Elie, Nicolas Villain‐Naud, Nadège Lepoittevin, Mélanie Martinez, Anne‐Sophie Lelong, Christophe 2022-06-21 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340784/ http://www.ncbi.nlm.nih.gov/pubmed/34935310 https://doi.org/10.1002/2211-5463.13356 en eng John Wiley and Sons Inc. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340784/ http://www.ncbi.nlm.nih.gov/pubmed/34935310 http://dx.doi.org/10.1002/2211-5463.13356 © 2021 The Authors. FEBS Open Bio published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. CC-BY FEBS Open Bio Research Articles Text 2022 ftpubmed https://doi.org/10.1002/2211-5463.13356 2022-08-07T00:55:17Z The Pacific oyster, Crassostrea gigas, is a successive irregular hermaphrodite mollusk 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. Text Crassostrea gigas Pacific oyster PubMed Central (PMC) Pacific FEBS Open Bio 12 8 1438 1452
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Articles
spellingShingle Research Articles
Maillard, Floriane
Elie, Nicolas
Villain‐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 Research Articles
description The Pacific oyster, Crassostrea gigas, is a successive irregular hermaphrodite mollusk 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.
format Text
author Maillard, Floriane
Elie, Nicolas
Villain‐Naud, Nadège
Lepoittevin, Mélanie
Martinez, Anne‐Sophie
Lelong, Christophe
author_facet Maillard, Floriane
Elie, Nicolas
Villain‐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 John Wiley and Sons Inc.
publishDate 2022
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340784/
http://www.ncbi.nlm.nih.gov/pubmed/34935310
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 FEBS Open Bio
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340784/
http://www.ncbi.nlm.nih.gov/pubmed/34935310
http://dx.doi.org/10.1002/2211-5463.13356
op_rights © 2021 The Authors. FEBS Open Bio published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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