A complex gene regulatory architecture underlies the development and evolution of cuticle morphology in Drosophila

Kittelmann, Sebastian; Noon, Ella Preger-Ben; McGregor, Alistair P.; Frankel, Nicolás

doi:10.1016/j.gde.2021.01.003

Cited by 11 publications

(9 citation statements)

References 55 publications

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“…The gene regulatory network underlying trichome development is shared in many body regions, such as in the denticle belts of the larval cuticle and on the surface of the wings and adult cuticle (reviewed in [ 18 , 34 ]). We have shown by the immunostaining of Svb, in situ hybridizations of sha and svb , and the RNA-seq analysis using the developing female genitalia that the svb -regulated pathway is likely to be involved in the formation of the trichomes on the oviprovector membrane.…”

Section: Discussionmentioning

confidence: 99%

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

et al. 2022

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Background The ovipositors of some insects are external female genitalia, which have their primary function to deliver eggs. Drosophila suzukii and its sibling species D. subpulchrella are known to have acquired highly sclerotized and enlarged ovipositors upon their shifts in oviposition sites from rotting to ripening fruits. Inside the ovipositor plates, there are scale-like polarized protrusions termed “oviprovector scales” that are likely to aid the mechanical movement of the eggs. The size and spatial distribution of the scales need to be rearranged following the divergence of the ovipositors. In this study, we examined the features of the oviprovector scales in D. suzukii and its closely related species. We also investigated whether the scales are single-cell protrusions comprised of F-actin under the same conserved gene regulatory network as the well-characterized trichomes on the larval cuticular surface. Results The oviprovector scales of D. suzukii and D. subpulchrella were distinct in size and spatial arrangement compared to those of D. biarmipes and other closely related species. The scale numbers also varied greatly among these species. The comparisons of the size of the scales suggested a possibility that the apical cell area of the oviprovector has expanded upon the elongation of the ovipositor plates in these species. Our transcriptome analysis revealed that 43 out of the 46 genes known to be involved in the trichome gene regulatory network are expressed in the developing female genitalia of D. suzukii and D. subpulchrella. The presence of Shavenbaby (Svb) or svb was detected in the inner cavity of the developing ovipositors of D. melanogaster, D. suzukii, and D. subpulchrella. Also, shavenoid (sha) was expressed in the corresponding patterns in the developing ovipositors and showed differential expression levels between D. suzukii and D. subpulchrella at 48 h APF. Conclusions The oviprovector scales have divergent size and spatial arrangements among species. Therefore, these scales may represent a rapidly diversifying morphological trait of the female reproductive tract reflecting ecological contexts. Furthermore, our results showed that the gene regulatory network underlying trichome formation is also utilized to develop the rapidly evolving trichomes on the oviprovectors of these flies.

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Section: Discussionmentioning

confidence: 99%

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

et al. 2022

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“…The gene regulatory network underlying trichome development is shared in many body regions, such as in the denticle belts of the larval cuticle and on the surface of the wings and adult cuticle (reviewed in [18,34]). We have shown by the immunostaining of Svb and the RNA-seq analysis using the developing female genitalia that the svb-regulated pathway is likely to be involved in the formation of the trichomes on the oviprovector membrane.…”

Section: Discussionmentioning

confidence: 99%

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

Tanaka

Takahashi

Rice

et al. 2022

Preprint

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Background: The ovipositors of some insects are external female genitalia, which have their primary function to deliver eggs. Drosophila suzukii and its sibling species D. subpulchrella are known to have acquired highly sclerotized and enlarged ovipositors upon their shifts in oviposition sites from rotting to ripening fruits. Inside the ovipositor plates, there are scale-like polarized protrusions termed "oviprovector scales" that are likely to aid the mechanical movement of the eggs. The size and spatial distribution of the scales need to be rearranged following the divergence of the ovipositors. In this study, we examined the features of the oviprovector scales in D. suzukii and its closely related species. We also investigated whether the scales are single-cell protrusions comprised of F-actin under the same conserved gene regulatory network as the well-characterized trichomes on the larval cuticular surface. Results: The oviprovector scales of D. suzukii and D. subpulchrella were distinct in size and spatial arrangement compared to those of a closely related species D. biarmipes and D. melanogaster. The comparisons of the size of the scales suggested that the apical cell area of the oviprovector has expanded upon the elongation of the ovipositor plates in these species. Our transcriptome analysis revealed that 43 out of the 46 genes known to be involved in the trichome gene regulatory network are expressed in the developing female genitalia of D. suzukii and D. subpulchrella. An antibody staining depicted the presence of Shavenbaby (Svb) in the inner cavity of the developing ovipositors of D. melanogaster at 44-48 h after puparium formation (APF). Also, shavenoid (sha) was expressed in the corresponding patterns in the developing ovipositors and showed differential expression levels between D. suzukii and D. subpulchrella at 48 h APF. Conclusions: The oviprovector scales have divergent size and spatial arrangements among species. Therefore, these scales may represent a rapidly diversifying morphological trait of the female reproductive tract reflecting ecological contexts. Furthermore, our results showed that the gene regulatory network underlying trichome formation is adopted to develop the rapidly evolving trichomes on the oviprovectors of these flies.

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“…Some enhancers drive svb expression in unique parts of the stripes, whereas a few are redundant and drive svb expression in the same general stripey areas. D. sechellia , a close relative of D. melanogaster , lost its dorsal‐lateral trichomes due to loss of function of some of its enhancers (Frankel et al, 2011; Kittelmann et al, 2021; McGregor et al, 2007; Noon et al, 2018). This suggests that genetic changes in these derived (duplicate) enhancers of svb , presumably more modular than the single hypothetical ancestral pleiotropic enhancer, were targeted by natural selection, which is a prediction of the CRE‐DDC model (Figure 4).…”

Section: Evolution Of Modular Cres Via the Cre‐ddc Modelmentioning

confidence: 99%

Evolution of modular and pleiotropic enhancers

Murugesan

Monteiro

2022

J Exp Zool Pt B

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Cis‐regulatory elements (CREs), or enhancers, are segments of noncoding DNA that regulate the spatial and temporal expression of nearby genes. Sometimes, genes are expressed in more than one tissue, and this can be driven by two main types of CREs: tissue‐specific “modular” CREs, where different CREs drive expression of the gene in the different tissues, or by “pleiotropic” CREs, where the same CRE drives expression in the different tissues. In this perspective, we will discuss some of the ways (i) modular and pleiotropic CREs might originate; (ii) propose that modular CREs might derive from pleiotropic CREs via a process of duplication, degeneration, and complementation (the CRE‐DDC model); and (iii) propose that hotspot loci of evolution are associated with the origin of modular CREs belonging to any gene in a regulatory network.

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A complex gene regulatory architecture underlies the development and evolution of cuticle morphology in Drosophila

Cited by 11 publications

References 55 publications

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

Evolution of modular and pleiotropic enhancers

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