Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes

Background: The Pacific oyster Crassostrea gigas (Mollusca, Lophotrochozoa) is an alternative and irregular protandrous hermaphrodite: most individuals mature first as males and then change sex several times. Little is known about genetic and phenotypic basis of sex differentiation in oysters, and l...

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Published in:PLoS ONE
Main Authors: Dheilly, Nolwenn, Lelong, Christophe, Huvet, Arnaud, Kellner, Kristell, Dubos, Marie-pierre, Riviere, Guillaume, Boudry, Pierre, Favrel, Pascal
Format: Article in Journal/Newspaper
Language:English
Published: Public Library Science 2012
Subjects:
Online Access:https://archimer.ifremer.fr/doc/00087/19862/17505.pdf
https://doi.org/10.1371/journal.pone.0036353
https://archimer.ifremer.fr/doc/00087/19862/
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spelling ftarchimer:oai:archimer.ifremer.fr:19862 2023-05-15T15:58:26+02:00 Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes Dheilly, Nolwenn Lelong, Christophe Huvet, Arnaud Kellner, Kristell Dubos, Marie-pierre Riviere, Guillaume Boudry, Pierre Favrel, Pascal 2012-05 application/pdf https://archimer.ifremer.fr/doc/00087/19862/17505.pdf https://doi.org/10.1371/journal.pone.0036353 https://archimer.ifremer.fr/doc/00087/19862/ eng eng Public Library Science https://archimer.ifremer.fr/doc/00087/19862/17505.pdf doi:10.1371/journal.pone.0036353 https://archimer.ifremer.fr/doc/00087/19862/ 2012 Dheilly et al. info:eu-repo/semantics/openAccess restricted use Plos One (1932-6203) (Public Library Science), 2012-05 , Vol. 7 , N. 5 text Publication info:eu-repo/semantics/article 2012 ftarchimer https://doi.org/10.1371/journal.pone.0036353 2021-09-23T20:21:00Z Background: The Pacific oyster Crassostrea gigas (Mollusca, Lophotrochozoa) is an alternative and irregular protandrous hermaphrodite: most individuals mature first as males and then change sex several times. Little is known about genetic and phenotypic basis of sex differentiation in oysters, and little more about the molecular pathways regulating reproduction. We have recently developed and validated a microarray containing 31,918 oligomers (Dheilly et al., 2011) representing the oyster transcriptome. The application of this microarray to the study of mollusk gametogenesis should provide a better understanding of the key factors involved in sex differentiation and the regulation of oyster reproduction. Methodology/Principal Findings: Gene expression was studied in gonads of oysters cultured over a yearly reproductive cycle. Principal component analysis and hierarchical clustering showed a significant divergence in gene expression patterns of males and females coinciding with the start of gonial mitosis. ANOVA analysis of the data revealed 2,482 genes differentially expressed during the course of males and/or females gametogenesis. The expression of 434 genes could be localized in either germ cells or somatic cells of the gonad by comparing the transcriptome of female gonads to the transcriptome of stripped oocytes and somatic tissues. Analysis of the annotated genes revealed conserved molecular mechanisms between mollusks and mammals: genes involved in chromatin condensation, DNA replication and repair, mitosis and meiosis regulation, transcription, translation and apoptosis were expressed in both male and female gonads. Most interestingly, early expressed male-specific genes included bindin and a dpy-30 homolog and female-specific genes included foxL2, nanos homolog 3, a pancreatic lipase related protein, cd63 and vitellogenin. Further functional analyses are now required in order to investigate their role in sex differentiation in oysters. Conclusions/Significance: This study allowed us to identify potential markers of early sex differentiation in the oyster C. gigas, an alternative hermaphrodite mollusk. We also provided new highly valuable information on genes specifically expressed by mature spermatozoids and mature oocytes. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Pacific PLoS ONE 7 5 e36353
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
description Background: The Pacific oyster Crassostrea gigas (Mollusca, Lophotrochozoa) is an alternative and irregular protandrous hermaphrodite: most individuals mature first as males and then change sex several times. Little is known about genetic and phenotypic basis of sex differentiation in oysters, and little more about the molecular pathways regulating reproduction. We have recently developed and validated a microarray containing 31,918 oligomers (Dheilly et al., 2011) representing the oyster transcriptome. The application of this microarray to the study of mollusk gametogenesis should provide a better understanding of the key factors involved in sex differentiation and the regulation of oyster reproduction. Methodology/Principal Findings: Gene expression was studied in gonads of oysters cultured over a yearly reproductive cycle. Principal component analysis and hierarchical clustering showed a significant divergence in gene expression patterns of males and females coinciding with the start of gonial mitosis. ANOVA analysis of the data revealed 2,482 genes differentially expressed during the course of males and/or females gametogenesis. The expression of 434 genes could be localized in either germ cells or somatic cells of the gonad by comparing the transcriptome of female gonads to the transcriptome of stripped oocytes and somatic tissues. Analysis of the annotated genes revealed conserved molecular mechanisms between mollusks and mammals: genes involved in chromatin condensation, DNA replication and repair, mitosis and meiosis regulation, transcription, translation and apoptosis were expressed in both male and female gonads. Most interestingly, early expressed male-specific genes included bindin and a dpy-30 homolog and female-specific genes included foxL2, nanos homolog 3, a pancreatic lipase related protein, cd63 and vitellogenin. Further functional analyses are now required in order to investigate their role in sex differentiation in oysters. Conclusions/Significance: This study allowed us to identify potential markers of early sex differentiation in the oyster C. gigas, an alternative hermaphrodite mollusk. We also provided new highly valuable information on genes specifically expressed by mature spermatozoids and mature oocytes.
format Article in Journal/Newspaper
author Dheilly, Nolwenn
Lelong, Christophe
Huvet, Arnaud
Kellner, Kristell
Dubos, Marie-pierre
Riviere, Guillaume
Boudry, Pierre
Favrel, Pascal
spellingShingle Dheilly, Nolwenn
Lelong, Christophe
Huvet, Arnaud
Kellner, Kristell
Dubos, Marie-pierre
Riviere, Guillaume
Boudry, Pierre
Favrel, Pascal
Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
author_facet Dheilly, Nolwenn
Lelong, Christophe
Huvet, Arnaud
Kellner, Kristell
Dubos, Marie-pierre
Riviere, Guillaume
Boudry, Pierre
Favrel, Pascal
author_sort Dheilly, Nolwenn
title Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
title_short Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
title_full Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
title_fullStr Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
title_full_unstemmed Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
title_sort gametogenesis in the pacific oyster crassostrea gigas: a microarrays-based analysis identifies sex and stage specific genes
publisher Public Library Science
publishDate 2012
url https://archimer.ifremer.fr/doc/00087/19862/17505.pdf
https://doi.org/10.1371/journal.pone.0036353
https://archimer.ifremer.fr/doc/00087/19862/
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Plos One (1932-6203) (Public Library Science), 2012-05 , Vol. 7 , N. 5
op_relation https://archimer.ifremer.fr/doc/00087/19862/17505.pdf
doi:10.1371/journal.pone.0036353
https://archimer.ifremer.fr/doc/00087/19862/
op_rights 2012 Dheilly et al.
info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.1371/journal.pone.0036353
container_title PLoS ONE
container_volume 7
container_issue 5
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