Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates
Genes involved in gonadal sex differentiation have been traditionally thought to be fairly conserved across vertebrates, but this has been lately questioned. Here, we performed the first comparative analysis of gonadal transcriptomes across vertebrates, from fish to mammals. Our results unambiguousl...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2024.1328365/full |
| _version_ | 1797348538848378880 |
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| author | Núria Sánchez-Baizán Ignasi Jarne-Sanz Álvaro S. Roco Álvaro S. Roco Manfred Schartl Manfred Schartl Francesc Piferrer |
| author_facet | Núria Sánchez-Baizán Ignasi Jarne-Sanz Álvaro S. Roco Álvaro S. Roco Manfred Schartl Manfred Schartl Francesc Piferrer |
| author_sort | Núria Sánchez-Baizán |
| collection | DOAJ |
| description | Genes involved in gonadal sex differentiation have been traditionally thought to be fairly conserved across vertebrates, but this has been lately questioned. Here, we performed the first comparative analysis of gonadal transcriptomes across vertebrates, from fish to mammals. Our results unambiguously show an extraordinary overall variability in gene activation and repression programs without a phylogenetic pattern. During sex differentiation, genes such as dmrt1, sox9, amh, cyp19a and foxl2 were consistently either male- or female-enriched across species while many genes with the greatest expression change within each sex were not. We also found that downregulation in the opposite sex, which had only been quantified in the mouse model, was also prominent in the rest of vertebrates. Finally, we report 16 novel conserved markers (e.g., fshr and dazl) and 11 signaling pathways. We propose viewing vertebrate gonadal sex differentiation as a hierarchical network, with conserved hub genes such as sox9 and amh alongside less connected and less conserved nodes. This proposed framework implies that evolutionary pressures may impact genes based on their level of connectivity. |
| first_indexed | 2024-03-08T12:07:25Z |
| format | Article |
| id | doaj.art-1e3d6a6bd8054174a3d9d4297f78f401 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-03-08T12:07:25Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-1e3d6a6bd8054174a3d9d4297f78f4012024-01-23T04:40:16ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2024-01-011210.3389/fcell.2024.13283651328365Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebratesNúria Sánchez-Baizán0Ignasi Jarne-Sanz1Álvaro S. Roco2Álvaro S. Roco3Manfred Schartl4Manfred Schartl5Francesc Piferrer6Institut de Ciències del Mar (ICM), Spanish National Research Council (CSIC), Barcelona, SpainInstitut de Ciències del Mar (ICM), Spanish National Research Council (CSIC), Barcelona, SpainDevelopmental Biochemistry, Biocenter, University of Wuerzburg, Wuerzburg, GermanyDepartment of Experimental Biology, Faculty of Experimental Sciences, University of Jaén, Jaén, SpainDevelopmental Biochemistry, Biocenter, University of Wuerzburg, Wuerzburg, GermanyXiphophorus Genetic Stock Center, Texas State University, San Marcos, TX, United StatesInstitut de Ciències del Mar (ICM), Spanish National Research Council (CSIC), Barcelona, SpainGenes involved in gonadal sex differentiation have been traditionally thought to be fairly conserved across vertebrates, but this has been lately questioned. Here, we performed the first comparative analysis of gonadal transcriptomes across vertebrates, from fish to mammals. Our results unambiguously show an extraordinary overall variability in gene activation and repression programs without a phylogenetic pattern. During sex differentiation, genes such as dmrt1, sox9, amh, cyp19a and foxl2 were consistently either male- or female-enriched across species while many genes with the greatest expression change within each sex were not. We also found that downregulation in the opposite sex, which had only been quantified in the mouse model, was also prominent in the rest of vertebrates. Finally, we report 16 novel conserved markers (e.g., fshr and dazl) and 11 signaling pathways. We propose viewing vertebrate gonadal sex differentiation as a hierarchical network, with conserved hub genes such as sox9 and amh alongside less connected and less conserved nodes. This proposed framework implies that evolutionary pressures may impact genes based on their level of connectivity.https://www.frontiersin.org/articles/10.3389/fcell.2024.1328365/fullgonadal developmentgene activationgene repressiongene expression networkstranscriptomicssex determination |
| spellingShingle | Núria Sánchez-Baizán Ignasi Jarne-Sanz Álvaro S. Roco Álvaro S. Roco Manfred Schartl Manfred Schartl Francesc Piferrer Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates Frontiers in Cell and Developmental Biology gonadal development gene activation gene repression gene expression networks transcriptomics sex determination |
| title | Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates |
| title_full | Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates |
| title_fullStr | Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates |
| title_full_unstemmed | Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates |
| title_short | Extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates |
| title_sort | extraordinary variability in gene activation and repression programs during gonadal sex differentiation across vertebrates |
| topic | gonadal development gene activation gene repression gene expression networks transcriptomics sex determination |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2024.1328365/full |
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