Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model

Abstract Background Sex determination is the process whereby the bipotential embryonic gonads become committed to differentiate into testes or ovaries. In genetic sex determination (GSD), the sex determining trigger is encoded by a gene on the sex chromosomes, which activates a network of downstream...

Full description

Bibliographic Details
Main Authors: Susan Wagner, Sarah L. Whiteley, Meghan Castelli, Hardip R. Patel, Ira W. Deveson, James Blackburn, Clare E. Holleley, Jennifer A. Marshall Graves, Arthur Georges
Format: Article
Language:English
Published: BMC 2023-05-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09334-0
_version_ 1827952906752491520
author Susan Wagner
Sarah L. Whiteley
Meghan Castelli
Hardip R. Patel
Ira W. Deveson
James Blackburn
Clare E. Holleley
Jennifer A. Marshall Graves
Arthur Georges
author_facet Susan Wagner
Sarah L. Whiteley
Meghan Castelli
Hardip R. Patel
Ira W. Deveson
James Blackburn
Clare E. Holleley
Jennifer A. Marshall Graves
Arthur Georges
author_sort Susan Wagner
collection DOAJ
description Abstract Background Sex determination is the process whereby the bipotential embryonic gonads become committed to differentiate into testes or ovaries. In genetic sex determination (GSD), the sex determining trigger is encoded by a gene on the sex chromosomes, which activates a network of downstream genes; in mammals these include SOX9, AMH and DMRT1 in the male pathway, and FOXL2 in the female pathway. Although mammalian and avian GSD systems have been well studied, few data are available for reptilian GSD systems. Results We conducted an unbiased transcriptome-wide analysis of gonad development throughout differentiation in central bearded dragon (Pogona vitticeps) embryos with GSD. We found that sex differentiation of transcriptomic profiles occurs at a very early stage, before the gonad consolidates as a body distinct from the gonad-kidney complex. The male pathway genes dmrt1 and amh and the female pathway gene foxl2 play a key role in early sex differentiation in P. vitticeps, but the central player of the mammalian male trajectory, sox9, is not differentially expressed in P. vitticeps at the bipotential stage. The most striking difference from GSD systems of other amniotes is the high expression of the male pathway genes amh and sox9 in female gonads during development. We propose that a default male trajectory progresses if not repressed by a W-linked dominant gene that tips the balance of gene expression towards the female trajectory. Further, weighted gene expression correlation network analysis revealed novel candidates for male and female sex differentiation. Conclusion Our data reveal that interpretation of putative mechanisms of GSD in reptiles cannot solely depend on lessons drawn from mammals.
first_indexed 2024-04-09T14:04:56Z
format Article
id doaj.art-e7e4b9f5aec94ef2900c95e0a7f93f7d
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-04-09T14:04:56Z
publishDate 2023-05-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj.art-e7e4b9f5aec94ef2900c95e0a7f93f7d2023-05-07T11:06:37ZengBMCBMC Genomics1471-21642023-05-0124111810.1186/s12864-023-09334-0Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote modelSusan Wagner0Sarah L. Whiteley1Meghan Castelli2Hardip R. Patel3Ira W. Deveson4James Blackburn5Clare E. Holleley6Jennifer A. Marshall Graves7Arthur Georges8Institute for Applied Ecology, University of CanberraInstitute for Applied Ecology, University of CanberraInstitute for Applied Ecology, University of CanberraGenome Sciences Department. John Curtin School of Medical Research, Australian National UniversityKinghorn Centre for Clinical Genomics, Garvan Institute of Medical ResearchKinghorn Centre for Clinical Genomics, Garvan Institute of Medical ResearchInstitute for Applied Ecology, University of CanberraInstitute for Applied Ecology, University of CanberraInstitute for Applied Ecology, University of CanberraAbstract Background Sex determination is the process whereby the bipotential embryonic gonads become committed to differentiate into testes or ovaries. In genetic sex determination (GSD), the sex determining trigger is encoded by a gene on the sex chromosomes, which activates a network of downstream genes; in mammals these include SOX9, AMH and DMRT1 in the male pathway, and FOXL2 in the female pathway. Although mammalian and avian GSD systems have been well studied, few data are available for reptilian GSD systems. Results We conducted an unbiased transcriptome-wide analysis of gonad development throughout differentiation in central bearded dragon (Pogona vitticeps) embryos with GSD. We found that sex differentiation of transcriptomic profiles occurs at a very early stage, before the gonad consolidates as a body distinct from the gonad-kidney complex. The male pathway genes dmrt1 and amh and the female pathway gene foxl2 play a key role in early sex differentiation in P. vitticeps, but the central player of the mammalian male trajectory, sox9, is not differentially expressed in P. vitticeps at the bipotential stage. The most striking difference from GSD systems of other amniotes is the high expression of the male pathway genes amh and sox9 in female gonads during development. We propose that a default male trajectory progresses if not repressed by a W-linked dominant gene that tips the balance of gene expression towards the female trajectory. Further, weighted gene expression correlation network analysis revealed novel candidates for male and female sex differentiation. Conclusion Our data reveal that interpretation of putative mechanisms of GSD in reptiles cannot solely depend on lessons drawn from mammals.https://doi.org/10.1186/s12864-023-09334-0Sex determinationReptilesSOX9AMHGonad differentiation
spellingShingle Susan Wagner
Sarah L. Whiteley
Meghan Castelli
Hardip R. Patel
Ira W. Deveson
James Blackburn
Clare E. Holleley
Jennifer A. Marshall Graves
Arthur Georges
Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
BMC Genomics
Sex determination
Reptiles
SOX9
AMH
Gonad differentiation
title Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
title_full Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
title_fullStr Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
title_full_unstemmed Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
title_short Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
title_sort gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model
topic Sex determination
Reptiles
SOX9
AMH
Gonad differentiation
url https://doi.org/10.1186/s12864-023-09334-0
work_keys_str_mv AT susanwagner geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT sarahlwhiteley geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT meghancastelli geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT hardiprpatel geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT irawdeveson geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT jamesblackburn geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT clareeholleley geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT jenniferamarshallgraves geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel
AT arthurgeorges geneexpressionofmalepathwaygenessox9andamhduringearlysexdifferentiationinareptiledepartsfromtheclassicalamniotemodel