Just how conserved is vertebrate sex determination?

Cutting, Andrew D.; Chue, Justin; Smith, Craig A.

doi:10.1002/dvdy.23944

Cited by 103 publications

(92 citation statements)

References 96 publications

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“…AMH's role as an essential inducer of male sexual differentiation also predates the Müllerian duct. In some species of fish, AMH regulates the differentiation of the gonads into testes, and putatively determines testicular differentiation in birds (Smith & Sinclair 2004, Morinaga et al 2007, Wu et al 2010, Cutting et al 2013. In mammals, AMH does not affect gonad determination as XY AMH K/K individuals have testes (Behringer et al 1994, Josso et al 2012, although AMH is required for the normal cellular and biochemical development of the mammalian testis (Mishina et al 1996, Wu et al 2005.…”

Section: Amh Is a Gonadal Cytokinementioning

confidence: 99%

Anti-Müllerian hormone is a gonadal cytokine with two circulating forms and cryptic actions

McLennan¹,

Pankhurst²

2015

Journal of Endocrinology

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Anti-Mü llerian hormone (AMH) is a multi-faceted gonadal cytokine. It is present in all vertebrates with its original function in phylogeny being as a regulator of germ cells in both sexes, and as a prime inducer of the male phenotype. Its ancient functions appear to be broadly conserved in mammals, but with this being obscured by its overt role in triggering the regression of the Mü llerian ducts in male embryos. Sertoli and ovarian follicular cells primarily release AMH as a prohormone (proAMH), which forms a stable complex (AMH N,C ) after cleavage by subtilisin/kexin-type proprotein convertases or serine proteinases. Circulating AMH is a mixture of proAMH and AMH N,C , suggesting that proAMH is activated within the gonads and putatively by its endocrine target-cells. The gonadal expression of the cleavage enzymes is subject to complex regulation, and the preliminary data suggest that this influences the relative proportions of proAMH and AMH N,C in the circulation. AMH shares an intracellular pathway with the bone morphogenetic protein (BMP) and growth differentiation factor (GDF) ligands. AMH is male specific during the initial stage of development, and theoretically should produce male biases throughout the body by adding a male-specific amplification of BMP/GDF signalling. Consistent with this, some of the male biases in neuron number and the non-sexual behaviours of mice are dependent on AMH. After puberty, circulating levels of AMH are similar in men and women. Putatively, the function of AMH in adulthood maybe to add a gonadal influence to BMP/GDF-regulated homeostasis.

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Section: Amh Is a Gonadal Cytokinementioning

confidence: 99%

Anti-Müllerian hormone is a gonadal cytokine with two circulating forms and cryptic actions

McLennan¹,

Pankhurst²

2015

Journal of Endocrinology

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“…Sry encodes a transcription factor that upregulates expression of the related HMG box transcription factor gene Sox9 (Sekido and Lovell-Badge, 2008). Unlike Sry, the involvement of Sox9 as a pivotal, early-acting effector of male sex determination has been documented in all vertebrates studied, leading to the prevailing view that the different switch mechanisms that have evolved in different vertebrate taxa all converge on Sox9 (Cutting et al, 2013). …”

Section: Introductionmentioning

confidence: 99%

Female-to-male sex reversal in mice caused by transgenic overexpression of Dmrt1

Zhao

Svingen

et al. 2015

Development

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Genes related to Dmrt1, which encodes a DNA-binding DM domain transcription factor, act as triggers for primary sex determination in a broad range of metazoan species. However, this role is fulfilled in mammals by Sry, a newly evolved gene on the Y chromosome, such that Dmrt1 has become dispensable for primary sex determination and instead maintains Sertoli cell phenotype in postnatal testes. Here, we report that enforced expression of Dmrt1 in XX mouse fetal gonads using a Wt1-BAC transgene system is sufficient to drive testicular differentiation and male secondary sex development. XX transgenic fetal gonads showed typical testicular size and vasculature. Key ovarian markers, including Wnt4 and Foxl2, were repressed. Sertoli cells expressing the hallmark testis-determining gene Sox9 were formed, although they did not assemble into normal testis cords. Other bipotential lineages differentiated into testicular cell types, including steroidogenic fetal Leydig cells and non-meiotic germ cells. As a consequence, male internal and external reproductive organs developed postnatally, with an absence of female reproductive tissues. These results reveal that Dmrt1 has retained its ability to act as the primary testis-determining trigger in mammals, even though this function is no longer normally required. Thus, Dmrt1 provides a common thread in the evolution of sex determination mechanisms in metazoans.

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“…zebrafish | temperature | masculinization | polygenic sex determination | global warming A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1).…”

mentioning

confidence: 99%

“…Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2).…”

mentioning

confidence: 99%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

119

136

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Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2). In addition to fish species with CSD, there are species with polygenic sex determination (PSD), in which sex depends on the combined action of several promale and profemale genetic factors, and species with temperature-dependent sex determination (TSD) (3). Understanding how the environment influences sex ratios in vertebrates is of fundamental importance in the study of the evolution of sex-determining mechanisms (4, 5). It is also of practical relevance in evaluating the effects of climate change and chemical pollution (6, 7).The effects of temperature on gene expression during sex differentiation have been investigated in different teleost species, including the African catfish, Clarias gariepinus (8), European sea bass, Dicentrarchus labrax (9, 10), Japanese flounder, Paralichthys olivaceus (11), pejerrey, Odontesthes...

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Just how conserved is vertebrate sex determination?

Cited by 103 publications

References 96 publications

Anti-Müllerian hormone is a gonadal cytokine with two circulating forms and cryptic actions

Anti-Müllerian hormone is a gonadal cytokine with two circulating forms and cryptic actions

Female-to-male sex reversal in mice caused by transgenic overexpression of Dmrt1

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

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