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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| Format: | Article |
| Language: | English |
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Wiley
2022-08-01
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| Series: | FEBS Open Bio |
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| Online Access: | https://doi.org/10.1002/2211-5463.13356 |
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| author | Floriane Maillard Nicolas Elie Nadège Villain‐Naud Mélanie Lepoittevin Anne‐Sophie Martinez Christophe Lelong |
| author_facet | Floriane Maillard Nicolas Elie Nadège Villain‐Naud Mélanie Lepoittevin Anne‐Sophie Martinez Christophe Lelong |
| author_sort | Floriane Maillard |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-14T07:37:39Z |
| format | Article |
| id | doaj.art-783b0610c3fe4726a5636df54d96069e |
| institution | Directory Open Access Journal |
| issn | 2211-5463 |
| language | English |
| last_indexed | 2024-04-14T07:37:39Z |
| publishDate | 2022-08-01 |
| publisher | Wiley |
| record_format | Article |
| series | FEBS Open Bio |
| spelling | doaj.art-783b0610c3fe4726a5636df54d96069e2022-12-22T02:05:38ZengWileyFEBS Open Bio2211-54632022-08-011281438145210.1002/2211-5463.13356Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesisFloriane Maillard0Nicolas Elie1Nadège Villain‐Naud2Mélanie Lepoittevin3Anne‐Sophie Martinez4Christophe Lelong5Unité de Formation et de Recherches (UFR) des sciences Université de Caen Normandie FranceUnité de Formation et de Recherches (UFR) des sciences Université de Caen Normandie FranceUnité de Formation et de Recherches (UFR) des sciences Université de Caen Normandie FranceUnité de Formation et de Recherches (UFR) des sciences Université de Caen Normandie FranceUnité de Formation et de Recherches (UFR) des sciences Université de Caen Normandie FranceUnité de Formation et de Recherches (UFR) des sciences Université de Caen Normandie FranceThe 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.https://doi.org/10.1002/2211-5463.13356Crassostrea gigasmeiosismitosisoystersspermatogenesistriploid |
| spellingShingle | Floriane Maillard Nicolas Elie Nadège Villain‐Naud Mélanie Lepoittevin Anne‐Sophie Martinez Christophe Lelong Male triploid oysters of Crassostrea gigas exhibit defects in mitosis and meiosis during early spermatogenesis FEBS Open Bio Crassostrea gigas meiosis mitosis oysters spermatogenesis triploid |
| title | 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_short | 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 |
| topic | Crassostrea gigas meiosis mitosis oysters spermatogenesis triploid |
| url | https://doi.org/10.1002/2211-5463.13356 |
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