Rewiring of gene interactions during development of serially homologous appendages in male and female Drosophila

ABSTRACT: Arthropod genitalia and walking legs are serially homologous appendages derived from a ventral appendage ‘ground state’ shaped by different Hox inputs. However, there has been little comparison between the downstream gene regulatory networks and how they build and pattern serially homologous appendages differently. In the pre-tarsal region of the developing leg and antennae of Drosophila, a combination of the transcription factors C15, Lim1 homeobox 1 (Lim1), and Al (Aristaless) are required for the development of the terminal structures, the tarsal claws and aristae, respectively, but the role and interactions among these factors as well as other genes known to regulate leg development was not known in the developing genitalia. Here, we explored the expression and function of C15, Lim1, and Al in male and female terminalia (genitalia and analia) development. We found that C15 represses male clasper bristle development but is required for promoting female epiproct bristles. Unlike in the antennae and leg discs, C15, Lim1, and Al are never all co-expressed in any male or female terminal structures, evidencing the interactions among these factors have changed among serially homologous appendages. However, we did infer interactions between C15 and other factors, including bab2 and Dll reflecting similarities between leg and genital development consistent with their homology. Finally, we identified a male-specific clasper enhancer of C15, probably regulated by the Hox gene Abdominal-B, which is not active in the female terminalia or the legs or antennae. This enhancer modularity of C15 may underpin tissue-specific regulatory logic, presumably programmed by different Hox inputs such as Abd-B in the genitalia, and that could have contributed to the diversification of these serially homologous structures from the ‘ground state’ ventral appendage as well as the rapid evolution of terminal morphology among species.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE279524 | GEO | 2024/10/21

REPOSITORIES: GEO