Cooperation of axial and sex specific information controls Drosophila female genitalia growth by regulating the Decapentaplegic pathway

Romero-Pozuelo, Jesús; Foronda, David; Martín, Paloma; Hudry, Bruno; Merabet, Samir; Graba, Yacine; Sánchez‐Herrero, Ernesto

doi:10.1016/j.ydbio.2019.06.014

Cited by 5 publications

(4 citation statements)

References 77 publications

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“…S7, Supplementary Material online). The OD domain is essential for female differentiation in D. melanogaster as it physically binds to Dsx itself, transcription factors, and co-activators ( An and Wensink 1995 ; Erdman et al 1996 ; Ghosh et al 2019 ; Romero-Pozuelo et al 2019 ). Therefore, we hypothesized that the additive region found in D. melanogaster occurred at the evolutionary stage of the common ancestor of Aparaglossata, at which point dsx became essential for female morphogenesis.…”

Section: Resultsmentioning

confidence: 99%

Evolutionary History of Sexual Differentiation Mechanism in Insects

Chikami

Okuno

Toyoda

et al. 2022

Molecular Biology and Evolution

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Alternative splicing underpins functional diversity in proteins and the complexity and diversity of eukaryotes. An example is the doublesex gene, the key transcriptional factor in arthropod sexual differentiation. doublesex is controlled by sex-specific splicing and promotes both male and female differentiation in holometabolan insects, whereas, in hemimetabolan species, doublesex has sex-specific isoforms but is not required for female differentiation. How doublesex evolved to be essential for female development remains largely unknown. Here, we investigate ancestral states of doublesex using Thermobia domestica belonging to Zygentoma, the sister group of Pterygota, i.e., winged insects. We find that, in T. domestica, the doublesex expresses sex-specific isoforms but is only necessary for male differentiation of sexual morphology. This result supports the hypothesis that doublesex initially promoted male differentiation during insect evolution. However, T. domestica doublesex has a short female-specific region and upregulates the expression of vitellogenin homologs in females, suggesting that doublesex may already play some role in female morphogenesis of the common ancestor of Pterygota. Reconstruction of the ancestral sequence and prediction of protein structures show that the female-specific isoform of doublesex has an extended C-terminal disordered region in holometabolan insects but not in non-holometabolan species. We propose that doublesex acquired its function in female morphogenesis through a change in the protein motif structure rather than the emergence of the female-specific exon.

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Section: Resultsmentioning

confidence: 99%

Evolutionary History of Sexual Differentiation Mechanism in Insects

Chikami

Okuno

Toyoda

et al. 2022

Molecular Biology and Evolution

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“…The TFs that directly control dsx expression are unknown in any organism. Genetic analyses in Drosophila showed that Hox and other TFs, including Sex-combs reduced, Abdominal-B, and Caudal 17 , are required for DSX expression in certain contexts, but it is unknown if these TFs directly regulate dsx transcription. On the other hand, ChIP-seq experiments identified binding sites for over 230 different DNA binding proteins within dsx in whole adult Drosophila , chiefly DSX itself (25 sites) 18 .…”

Section: Figmentioning

confidence: 99%

Supergene evolution via gain of auto-regulation

VanKuren,

Sheikh,

Massardo

et al. 2024

Preprint

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The development of complex phenotypes requires the coordinated action of many genes across space and time, yet many species have evolved the ability to develop multiple discrete, alternate phenotypes1–3. Such polymorphisms are often controlled by supergenes, sets of tightly-linked mutations in one or more loci that function together to produce a complex phenotype4. Although theories of supergene evolution are well-established, the mutations that cause functional differences between supergene alleles remain essentially unknown.doublesexis the master regulator of insect sexual differentiation but functions as a supergene in multiplePapilioswallowtail butterflies, where divergentdsxalleles control development of discrete non-mimetic or mimetic female wing color patterns5–7. Here we demonstrate that the functional elements of the mimetic allele inPapilio alphenorare six newcis-regulatory elements (CREs) spread across 150 kb that are bound by DSX itself. Our findings provide experimental support to classic supergene theory and suggest that the evolution of auto-regulation may provide a simple route to supergene origination and to the co-option of pleiotropic genes into new developmental roles.

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“…5). The OD domain is essential for female differentiation in D. melanogaster, as it physically binds to dsx itself, transcription factors, and coactivators (An and Wensink 1995;Erdman 1996;Ghosh et al 2019;Romero-Pozuelo et al 2019). Therefore, we hypothesized that the additive region found in D. melanogaster occurred at the common ancestor of Aparaglossata in which dsx became essential for female morphogenesis.…”

Section: Evolution Of C-terminus Disordered Region Of Dsx Female-typementioning

confidence: 99%

Evolutionary history of sexual differentiation mechanism in insects

Chikami

Okuno

Toyoda

et al. 2021

Preprint

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Gain of alternative splicing gives rise to functional diversity in proteins and underlies the complexity and diversity of biological aspects. However, it is still not fully understood how alternatively spliced genes develop the functional novelty. To this end, we infer the evolutionary history of the doublesex gene, the key transcriptional factor in the sexual differentiation of arthropods. doublesex is controlled by sex-specific splicing and promotes both male and female differentiation in some holometabolan insects. In contrast, doublesex promotes only male differentiation in some hemimetabolan insects. Here, we investigate ancestral states of doublesex using Thermobia domestica belonging to Zygentoma, the sister group of winged insects. We find that doublesex of T. domestica expresses sex-specific isoforms but is only necessary for male differentiation of sexual morphology. This result ensures the hypothesis that doublesex was initially only used to promote male differentiation during insect evolution. However, T. domestica doublesex has a short female-specific region and upregulates the expression of vitellogenin homologs in females, suggesting that doublesex may have already controlled some aspects of feminization in the common ancestor of winged insects. Reconstruction of the ancestral sequence and prediction of the protein structure show that the female-specific isoform of doublesex has a long C-terminal disordered region in holometabolan insects, but not in non-holometabolan species. We propose that doublesex acquired a female-specific isoform and then underwent a change in the protein motif structure, which became essential for female differentiation in sexual dimorphisms.

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Cooperation of axial and sex specific information controls Drosophila female genitalia growth by regulating the Decapentaplegic pathway

Cited by 5 publications

References 77 publications

Evolutionary History of Sexual Differentiation Mechanism in Insects

Evolutionary History of Sexual Differentiation Mechanism in Insects

Supergene evolution via gain of auto-regulation

Evolutionary history of sexual differentiation mechanism in insects

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