Doublesex regulates male-specific differentiation during distinct developmental time windows in a parasitoid wasp

Wang, Yidong; Rensink, Anna H.; Fricke, Ute; Riddle, Megan; Trent, Carol; Zande, Louis van de; Verhulst, Eveline C.

doi:10.1016/j.ibmb.2022.103724

Cited by 10 publications

(7 citation statements)

References 65 publications

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“…However, given that dsx does not affect the development of the head in Ap. mellifera females ( Roth et al 2019 ), leg pigmentation, pheromone synthesis, and wing morphology in females of the parasitoid wasp Nasonia vitripennis ( Wang, Rensink, et al 2022 ; Wang, Sun, et al 2022 ), and female traits in At. rosae ( Mine et al 2017 , 2021 ), it is reasonable to infer for the time being that dsx is nonessential for female morphogenesis during postembryonic development in the common ancestor of Hymenoptera.…”

Section: Resultsmentioning

confidence: 99%

“…Information on the roles of dsx of some species in female morphogenesis is limited to some body parts: body coloration in I. senegalensis ( Takahashi et al 2021 ), leg pigmentation, pheromone synthesis, and wing morphology in Na. vitripenis ( Wang, Rensink, et al 2022 ; Wang, Sun, et al 2022 ), and worker morphology in Ap. mellifera ( Roth et al 2019 ).…”

Section: Resultsmentioning

confidence: 99%

“…In many pterygote insects, dsx is controlled by sex-specific splicing. In Diptera, Coleoptera, Lepidoptera, and Hymenoptera, sex-specific Dsx protein variants are essential for promoting either male or female differentiation (e.g., Hildreth 1965 ; Burtis and Baker 1989 ; Ohbayashi et al 2001 ; Kijimoto et al 2012 ; Shukla and Palli 2012 ; Ito et al 2013 ; Gotoh et al 2016 ; Xu et al 2017 ; Roth et al 2019 ; Wang et al 2022a , 2022b ). For example, in the fruit fly Drosophila melanogaster, dsx is required for sex differentiation, as manifested in external genitalia and foreleg bristle rows, and dsx mutants show an intersexual phenotype in these traits, with both male and female differentiation inhibited ( Hildreth and Lucchesi 1963 ; Hildreth 1965 ).…”

Section: Introductionmentioning

confidence: 99%

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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%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Evolutionary History of Sexual Differentiation Mechanism in Insects

Chikami

Okuno

Toyoda

et al. 2022

Molecular Biology and Evolution

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“…Dsx was first found to produce male- and female-specific proteins via alternative splicing that regulate sex differentiation in Drosophila melanogaster [ 16 ]. Later, dsx homologues were reported to contribute to sexual dimorphism and polymorphism in a number of different insect species, including honey bees, wasps [ 17 , 18 ], flies, mosquitoes [ 19 , 20 , 21 , 22 , 23 ], beetles [ 24 , 25 , 26 ], and butterflies and moths [ 27 , 28 ]. Sexually dimorphic traits in insects include body patterning, body size, abdominal genitalia, and sex-specific physiology [ 29 ].…”

Section: Introductionmentioning

confidence: 99%

“…Functional studies of dsx through genetic approaches have recently been reviewed [ 32 ]. Silencing of dsx by RNA interference led to female-like genitalia development in Nasonia vitripennis males [ 17 ] and disrupted olfaction and reproduction in Aedes aegypti [ 33 ]. Most recently, the CRISPR/Cas9-mediated mutagenesis system was applied to address the functionality of dsx in Lepidoptera.…”

Section: Introductionmentioning

confidence: 99%

CRISPR/Cas9-Mediated Mutagenesis of Sex-Specific Doublesex Splicing Variants Leads to Sterility in Spodoptera frugiperda, a Global Invasive Pest

Wang

et al. 2022

Cells

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Spodoptera frugiperda (J. E. Smith), an emerging invasive pest worldwide, has posed a serious agricultural threat to the newly invaded areas. Although somatic sex differentiation is fundamentally conserved among insects, the sex determination cascade in S. frugiperda is largely unknown. In this study, we cloned and functionally characterized Doublesex (dsx), a “molecular switch” modulating sexual dimorphism in S. frugiperda using male- and female-specific isoforms. Given that Lepidoptera is recalcitrant to RNAi, CRISPR/Cas9-mediated mutagenesis was employed to construct S. frugiperda mutants. Specifically, we designed target sites on exons 2, 4, and 5 to eliminate the common, female-specific, and male-specific regions of S. frugiperda dsx (Sfdsx), respectively. As expected, abnormal development of both the external and internal genitalia was observed during the pupal and adult stages. Interestingly, knocking out sex-specific dsx variants in S. frugiperda led to significantly reduced fecundity and fertility in adults of corresponding sex. Our combined results not only confirm the conserved function of dsx in S. frugiperda sex differentiation but also provide empirical evidence for dsx as a potential target for the Sterile Insect Technique (SIT) to combat this globally invasive pest in a sustainable and environmentally friendly way.

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