LncRNA modulates Dpp-mediated wing development to influence flight in Aedes aegypti

Area of Science:

• Molecular Biology
• Developmental Biology
• Entomology

Background:

• Aedes aegypti mosquito flight capability is crucial for spreading vector-borne diseases.
• Decapentaplegic (Dpp) signaling is vital for insect development, but its regulation in Ae. aegypti wing and haltere development is not fully understood.

Purpose of the Study:

• To identify novel regulatory mechanisms governing Ae. aegypti wing bud development.
• To elucidate the role of long non-coding RNAs (lncRNAs) in Dpp-mediated morphogenesis and mosquito fitness.

Main Methods:

• Identification of a wing bud/haltere-specific lncRNA, AAEL025449.
• Characterization of the competing endogenous RNA (ceRNA) axis involving AAEL025449, microRNA-281 (miR-281), and Dpp signaling.
• Analysis of the temporal and spatial regulation of Dpp by the ceRNA axis during apoptosis.
• Investigation of the impact of disrupting this axis on wing development, flight capacity, and mating success.

Main Results:

• AAEL025449 functions as a miR-281 sponge, relieving Dpp transcriptional repression in wing buds.
• The lncRNA tunes Dpp dynamics during apoptosis, modulating cell death timing via the c-Jun N-terminal kinase (JNK) pathway.
• Disruption of the AAEL025449-miR-281-Dpp axis leads to shorter wings, reduced flight capacity, and lower mating success.
• Dpp regulates wing bud apoptosis via JNK, with a novel anterior-to-posterior gradient diffusion pattern during critical apoptotic periods.

Conclusions:

• A novel spatiotemporal regulatory mechanism for Ae. aegypti wing bud development involving a lncRNA-ceRNA axis is uncovered.
• This axis links molecular developmental processes to fitness-related traits, providing insights into insect wing evolution.
• The identified ceRNA axis presents potential targets for developing strategies to control mosquito populations and mitigate disease transmission.