Response of Candidate Sex-Determining Genes to Changes in Temperature Reveals Their Involvement in the Molecular Network Underlying Temperature-Dependent Sex Determination

Shoemaker, Christina M.; Queen, Joanna H.; Crews, David

doi:10.1210/me.2007-0263

Cited by 100 publications

(99 citation statements)

References 62 publications

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“…Dmrt1 transcript expression in individual embryos was highly temperature dependent between 25 and 33°C, during the sexdetermination period and TSP. The temperature-shift assays showed a rapid response of Dmrt1 to temperature shifts from MPT to FPT or FPT to MPT both in vivo and in vitro, preceding changes in Amh and Sox9, which is consistent with previous reports (Shoemaker-Daly et al, 2010;Shoemaker et al, 2007b). These findings confirm the thermosensitivity of Dmrt1 in T. scripta gonadal cells.…”

Section: Discussionsupporting

confidence: 91%

“…Some genes (or gene networks) involved in GSD systems have been identified in the gonads of TSD species during the thermosensitive period (TSP), and several of those exhibit temperature-dependent expression patterns prior to gonadal sex differentiation (Shoemaker-Daly et al, 2010;Shoemaker et al, 2007b). The idea that TSD and GSD systems share common genetic components is strongly supported by recent transcriptomes of TSD taxa from the red-eared slider turtle (Czerwinski et al, 2016), the painted turtle (Radhakrishnan et al, 2017) and the alligator (Yatsu et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Dmrt1 induces the male pathway in a turtle with temperature-dependent sex determination

Ye²,

Zhang

et al. 2017

Development

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The molecular mechanism underlying temperature-dependent sex determination (TSD) has been a long-standing mystery; in particular, the thermosensitive genetic triggers for gonadal sex differentiation are largely unknown. Here, we have characterized a conserved DM domain gene, Dmrt1, in the red-eared slider turtle Trachemys scripta (T. scripta), which exhibits TSD. We found that Dmrt1 has a temperature-dependent, sexually dimorphic expression pattern, preceding gonadal sex differentiation, and is capable of responding rapidly to temperature shifts and aromatase inhibitor treatment. Most importantly, loss-and gain-of-function analyses provide solid evidence that Dmrt1 is both necessary and sufficient to initiate male development in T. scripta. Furthermore, the DNA methylation dynamics of the Dmrt1 promoter are tightly correlated with temperature and could mediate the impact of temperature on sex determination. Collectively, our findings demonstrate that Dmrt1 is a candidate master male sex-determining gene in this TSD species, consistent with the idea that DM domain genes are conserved during the evolution of sex determination mechanisms.

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Section: Discussionsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Dmrt1 induces the male pathway in a turtle with temperature-dependent sex determination

Ye²,

Zhang

et al. 2017

Development

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“…Additionally, the nuclear localization of SOX9 seems to be essential for its function in male sex determination such that the equilibrium of its nuclear import/export may regulate the repression of female-or the activation of male-specific differentiation [Gasca et al, 2002]. Consistent with the mammalian model, SOX9 expression is upregulated in male embryonic gonads in TSD turtles and crocodilians ( Trachemys scripta [Spotila et al, 1998;Shoemaker et al, 2007a], Lepidochelys olivacea [Moreno-Mendoza et al, 1999;Torres-Maldonado et al, 2001], and alligators [Western et al, 1999b]) but notably, it is upregulated at female-rather than at male-producing temperatures in the TSD leopard gecko Eublepharis macularius [Valleley et al, 2001].…”

Section: Sox9 and Dmrt1mentioning

confidence: 74%

Multivariate Expression Analysis of the Gene Network Underlying Sexual Development in Turtle Embryos with Temperature-Dependent and Genotypic Sex Determination

Valenzuela

2010

Sex Dev

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Sexual development has long been the target of study and despite great advances in our understanding of the composition and regulation of the gene network underlying gonadogenesis, our knowledge remains incomplete. Of particular interest is the relative role that the environment and the genome play in directing gonadal formation, especially the effect of environmental temperature in directing this process in vertebrates. Comparative analyses in closely related taxa with contrasting sex-determining mechanisms should help fill this gap. Here I present a multivariate study of the regulation of the gene network underlying sexual development in turtles with temperature-dependent (TSD; Chrysemys picta) and genotypic sex determination (GSD; Apalone mutica). I combine novel data on SOX9 and DMRT1 from these species with contrasting sex-determining mechanisms for the first time with previously reported data on DAX1, SF-1 (NR5A1), WT1, and aromatase (CYP19A1) from these same taxa. Comparative expression analyses of SOX9 and DMRT1 from these and other species indicate additional elements whose expression has diverged among TSD taxa, further supporting the notion that significant evolutionary changes have accrued in the regulation of the TSD gene network in reptiles. A non-parametric MANOVA revealed that temperature had a significant effect in multivariate gene expression in C. picta that varied during embryonic development, whereas the covariation of gene expression in A. mutica was insensitive to temperature. A phenotypic trajectory analysis (PTA) of gene expression comparing both species directly indicated that the relative covariation in gene expression varied between temperatures in C. picta. Furthermore, the 25°C trajectory of C. picta differed from that of A. mutica in the magnitude of gene expression change. Additional analyses revealed a stronger covariation in gene expression and a more interconnected regulatory network in A. mutica, consistent with the hypothesis that sexual development is a more canalized process in A. mutica, as would be expected if GSD evolved in this lineage through directional selection from its TSD ancestor.

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“…While Sox9 is required for sexual differentiation in eutherians by controlling the development of a testis-specific somatic lineage, in other vertebrates the situation is less clear. Although Sox9 expression is sexually dimorphic in chicken, alligator and turtles, male-specific expression is only evident after the expression of anti-Mül-lerian hormone has been initiated (Oreal et al, 1998;Western et al, 1999;Shoemaker et al, 2007), suggesting that activation of Sox9 is not a primary sex-determining gene in these species. In these non-eutherian vertebrates it is suggested that Sox9 acts to control the correct differentiation of the somatic Sertoli cell lineage rather than its specification (e.g., Smith et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

<i>Sox100B</i>, a <i>Drosophila</i> Group E Sox-domain Gene, Is Required for Somatic Testis Differentiation

Nanda

DeFalco

Loh

et al. 2009

Sex Dev

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Sex determination mechanisms are thought to evolve rapidly and show little conservation among different animal species. For example, the critical gene on the Y chromosome, SRY, that determines sex in most mammals, is not found in other animals. However, a related Sox domain transcription factor, SOX9, is also required for testis development in mammals and exhibits male-specific gonad expression in other vertebrate species. Previously, we found that the Drosophila orthologue of SOX9, Sox100B, is expressed male-specifically during gonad development. We now investigate the function of Sox100B and find, strikingly, that Sox100B is essential for testis development in Drosophila. In Sox100B mutants, the adult testis is severely reduced and fails to interact with other parts of the reproductive tract, which are themselves unaffected. While a testis initially forms in Sox100B mutants, it fails to undergo proper morphogenesis during pupal stages, likely due to defects in the pigment cells. In contrast, no substantive defects are observed in ovary development in Sox100B mutant females. Thus, as is observed in mammals, a Sox9 homolog is essential for sex-specific gonad development in Drosophila, suggesting that the molecular mechanisms regulating sexually dimorphic gonad development may be more conserved than previously suspected.

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Response of Candidate Sex-Determining Genes to Changes in Temperature Reveals Their Involvement in the Molecular Network Underlying Temperature-Dependent Sex Determination

Cited by 100 publications

References 62 publications

Dmrt1 induces the male pathway in a turtle with temperature-dependent sex determination

Dmrt1 induces the male pathway in a turtle with temperature-dependent sex determination

Multivariate Expression Analysis of the Gene Network Underlying Sexual Development in Turtle Embryos with Temperature-Dependent and Genotypic Sex Determination

<i>Sox100B</i>, a <i>Drosophila</i> Group E Sox-domain Gene, Is Required for Somatic Testis Differentiation

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