Sexual Back Talk With Evolutionary Implications: Stimulation of the Drosophila Sex-Determination Gene <i>Sex-lethal</i> by Its Target <i>transformer</i>

Siera, Scott G.; Cline, Thomas W.

doi:10.1534/genetics.108.093898

Cited by 36 publications

(33 citation statements)

References 77 publications

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“…The Drosophila system seems to be a derivative of the ancestral tra-based system in which the key functions, selection and maintenance of the sexual fate, are both delegated to Sxl. It has been proposed that Sxl was initially recruited as an additional coregulator of tra premRNA splicing, thereby establishing a functionally redundant circuit to tra autoregulation (Siera and Cline 2008). In this context, Sxl may have gradually relieved tra from upholding the female mode of its splicing to become eventually the exclusive regulator of tra.…”

Section: Discussionmentioning

confidence: 99%

Molecular Characterization of the Key Switch F Provides a Basis for Understanding the Rapid Divergence of the Sex-Determining Pathway in the Housefly

et al. 2010

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The housefly, Musca domestica, is an excellent model system to study the diversification of the pathway that specifies the sexual fate. A number of different mechanisms have been described in the housefly, which reflects in part the broad diversity of sex-determining strategies used in insects. In this study we present the molecular identification and characterization of F, which acts as the master switch in the housefly pathway. We provide evidence that F corresponds to the transformer ortholog in Musca (Mdtra), which, as a result of alternative processing, expresses functional products only in individuals committed to the female fate. We demonstrate that, once activated, a self-sustaining feedback loop will maintain the female-promoting functions of Mdtra. Absence of Mdtra transcripts in eggs of Arrhenogenic (Ag) mutant females suggests that maternally deployed Mdtra activity initiates this self-sustaining loop in the zygote. When an M factor is paternally transmitted to the zygote, the establishment of the loop is prevented at an early stage before cellularization and splicing of Mdtra shifts irreversibly to the male nonproductive mode. On the basis of the analysis of two mutant alleles we can explain the different sex-determining systems in the housefly largely as deviations at the level of Mdtra regulation. This plasticity in the housefly pathway may provide a suitable framework to understand the evolution of sex-determining mechanisms in other insect species. For instance, while sex determination in a close relative, the tsetse fly Glossina morsitans, differs at the level of the instructive signal, we find that its tra ortholog, Gmtra, is regulated in a mode similar to that of Mdtra.

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Section: Discussionmentioning

confidence: 99%

Molecular Characterization of the Key Switch F Provides a Basis for Understanding the Rapid Divergence of the Sex-Determining Pathway in the Housefly

et al. 2010

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“…In Drosophila, Sxl has been recruited upstream of tra and is female specifically regulated through its own auto regulatory loop. However, Siera and Cline [61 ] showed that tra auto regulation may also be ancestral in Drosophila since a positive feedback loop of tra still operates through Sxl, which in turn regulates tra splicing. Tra regulation by X chromosome dose may occur outside the Drosophilidae but most likely in the absence of Sxl.…”

Section: Doublesexmentioning

confidence: 99%

Insect sex determination: it all evolves around transformer

Verhulst

Zande

Beukeboom

2010

Current Opinion in Genetics & Development

233

225

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“…Sxl orthologs have been identified in insects as diverse as aphids, moths, beetles, and mosquitoes; however, outside of the family Drosophilidae, there seems to be no obvious somatic difference in Sxl expression level or products between the sexes and/or no DNA homologies to the key structural elements in Drosophila Sxl that are responsible for its female-specific functioning (referenced in Traut et al 2006; and see Siera and Cline 2008 for Scaptodrosophila lebanonensis). In most insects, the transformer gene seems to occupy the position of Sxl as the master feminizing switch gene that responds to sex determination signals and epigenetically maintains the sexually determined state through a positive feedback loop on pre-mRNA splicing Gempe et al 2009;Hediger et al 2010;Verhulst et al 2010).…”

Section: T He X Chromosome Counting System Used Bymentioning

confidence: 99%

Evolution of the Drosophila Feminizing Switch Gene Sex-lethal

Cline

Dorsett²,

Sun³

et al. 2010

Genetics

Self Cite

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In Drosophila melanogaster, the gene Sex-lethal (Sxl ) controls all aspects of female development. Since melanogaster males lacking Sxl appear wild type, Sxl would seem to be functionally female specific. Nevertheless, in insects as diverse as honeybees and houseflies, Sxl seems not to determine sex or to be functionally female specific. Here we describe three lines of work that address the questions of how, when, and even whether the ancestor of melanogaster Sxl ever shed its non-female-specific functions. First, to test the hypothesis that the birth of Sxl 's closest paralog allowed Sxl to lose essential ancestral non-femalespecific functions, we determined the CG3056 null phenotype. That phenotype failed to support this hypothesis. Second, to define when Sxl might have lost ancestral non-female-specific functions, we isolated and characterized Sxl mutations in D. virilis, a species distant from melanogaster and notable for the large amount of Sxl protein expression in males. We found no change in Sxl regulation or functioning in the 401 MY since these two species diverged. Finally, we discovered conserved non-sex-specific Sxl mRNAs containing a previously unknown, potentially translation-initiating exon, and we identified a conserved open reading frame starting in Sxl male-specific exon 3. We conclude that Drosophila Sxl may appear functionally female specific not because it lost non-female-specific functions, but because those functions are nonessential in the laboratory. The potential evolutionary relevance of these nonessential functions is discussed.

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Sexual Back Talk With Evolutionary Implications: Stimulation of the Drosophila Sex-Determination Gene Sex-lethal by Its Target transformer

Abstract: We describe a surprising new regulatory relationship between two key genes of the Drosophila sexdetermination gene hierarchy, Sex-lethal (Sxl) and transformer (tra).

Cited by 36 publications

References 77 publications

Molecular Characterization of the Key Switch F Provides a Basis for Understanding the Rapid Divergence of the Sex-Determining Pathway in the Housefly

Molecular Characterization of the Key Switch F Provides a Basis for Understanding the Rapid Divergence of the Sex-Determining Pathway in the Housefly

Insect sex determination: it all evolves around transformer

Evolution of the Drosophila Feminizing Switch Gene Sex-lethal

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