A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis
Abstract Background Spermatogenesis appears to be a relatively well-conserved process even among distantly related animal taxa such as invertebrates and vertebrates. Although Hymenopterans share many characteristics with other organisms, their complex haplodiploid reproduction system is still relati...
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| Format: | Article |
| Language: | English |
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BMC
2021-05-01
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| Series: | BMC Ecology and Evolution |
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| Online Access: | https://doi.org/10.1186/s12862-021-01825-6 |
| _version_ | 1818880875977244672 |
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| author | Charlotte Lécureuil Sophie Fouchécourt Rémi Eliautout Vanessa Guérin Kevin Hidalgo Dorian Neutre Géraldine Roux Philippe Monget |
| author_facet | Charlotte Lécureuil Sophie Fouchécourt Rémi Eliautout Vanessa Guérin Kevin Hidalgo Dorian Neutre Géraldine Roux Philippe Monget |
| author_sort | Charlotte Lécureuil |
| collection | DOAJ |
| description | Abstract Background Spermatogenesis appears to be a relatively well-conserved process even among distantly related animal taxa such as invertebrates and vertebrates. Although Hymenopterans share many characteristics with other organisms, their complex haplodiploid reproduction system is still relatively unknown. However, they serve as a complementary insect model to Drosophila for studying functional male fertility. In this study, we used a comparative method combining taxonomic, phenotypic data and gene expression to identify candidate genes that could play a significant role in spermatogenesis in hymenopterans. Results Of the 546 mouse genes predominantly or exclusively expressed in the mouse testes, 36% had at least one ortholog in the fruit fly. Of these genes, 68% had at least one ortholog in one of the six hymenopteran species we examined. Based on their gene expression profiles in fruit fly testes, 71 of these genes were hypothesized to play a marked role in testis function. Forty-three of these 71 genes had an ortholog in at least one of the six hymenopteran species examined, and their enriched GO terms were related to the G2/M transition or to cilium organization, assembly, or movement. Second, of the 379 genes putatively involved in male fertility in Drosophila, 224 had at least one ortholog in each of the six Hymenoptera species. Finally, we showed that 199 of these genes were expressed in early pupal testis in Nasonia vitripennis; 86 exhibited a high level of expression, and 54 displayed modulated expression during meiosis. Conclusions In this study combining phylogenetic and experimental approaches, we highlighted genes that may have a major role in gametogenesis in hymenopterans; an essential prerequisite for further research on functional importance of these genes. |
| first_indexed | 2024-12-19T14:52:56Z |
| format | Article |
| id | doaj.art-b954cf2a1aa94c62942b9029f70b0717 |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-12-19T14:52:56Z |
| publishDate | 2021-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Ecology and Evolution |
| spelling | doaj.art-b954cf2a1aa94c62942b9029f70b07172022-12-21T20:16:47ZengBMCBMC Ecology and Evolution2730-71822021-05-0121111410.1186/s12862-021-01825-6A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennisCharlotte Lécureuil0Sophie Fouchécourt1Rémi Eliautout2Vanessa Guérin3Kevin Hidalgo4Dorian Neutre5Géraldine Roux6Philippe Monget7Institut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS-Université de ToursPRC, CNRS, IFCE, INRAE, Université de ToursInstitut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS-Université de ToursInstitut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS-Université de ToursInstitut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS-Université de ToursInstitut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS-Université de ToursINRAPRC, CNRS, IFCE, INRAE, Université de ToursAbstract Background Spermatogenesis appears to be a relatively well-conserved process even among distantly related animal taxa such as invertebrates and vertebrates. Although Hymenopterans share many characteristics with other organisms, their complex haplodiploid reproduction system is still relatively unknown. However, they serve as a complementary insect model to Drosophila for studying functional male fertility. In this study, we used a comparative method combining taxonomic, phenotypic data and gene expression to identify candidate genes that could play a significant role in spermatogenesis in hymenopterans. Results Of the 546 mouse genes predominantly or exclusively expressed in the mouse testes, 36% had at least one ortholog in the fruit fly. Of these genes, 68% had at least one ortholog in one of the six hymenopteran species we examined. Based on their gene expression profiles in fruit fly testes, 71 of these genes were hypothesized to play a marked role in testis function. Forty-three of these 71 genes had an ortholog in at least one of the six hymenopteran species examined, and their enriched GO terms were related to the G2/M transition or to cilium organization, assembly, or movement. Second, of the 379 genes putatively involved in male fertility in Drosophila, 224 had at least one ortholog in each of the six Hymenoptera species. Finally, we showed that 199 of these genes were expressed in early pupal testis in Nasonia vitripennis; 86 exhibited a high level of expression, and 54 displayed modulated expression during meiosis. Conclusions In this study combining phylogenetic and experimental approaches, we highlighted genes that may have a major role in gametogenesis in hymenopterans; an essential prerequisite for further research on functional importance of these genes.https://doi.org/10.1186/s12862-021-01825-6TestisGenesPhylogenyHymenoptera |
| spellingShingle | Charlotte Lécureuil Sophie Fouchécourt Rémi Eliautout Vanessa Guérin Kevin Hidalgo Dorian Neutre Géraldine Roux Philippe Monget A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis BMC Ecology and Evolution Testis Genes Phylogeny Hymenoptera |
| title | A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis |
| title_full | A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis |
| title_fullStr | A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis |
| title_full_unstemmed | A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis |
| title_short | A comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on Nasonia vitripennis |
| title_sort | comparative genomic approach using mouse and fruit fly data to discover genes involved in testis function in hymenopterans with a focus on nasonia vitripennis |
| topic | Testis Genes Phylogeny Hymenoptera |
| url | https://doi.org/10.1186/s12862-021-01825-6 |
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