AalpiRNA-18529 regulates vitellogenesis of Aedes albopictus via the Gadd45a-mediated JNK-dependent nurse cell apoptosis pathway

Aedes albopictus shows a rapid global expansion and dramatic vectorial capacity for various arboviruses. Mosquitoes display distinct sexual dimorphisms, only adult females consume blood meals to complete ovarian follicle development. Therefore, cyclic reproduction in female mosquitoes serves as a foundation for the transmission of numerous disease-causing pathogens. Aedes have an expansion of the piRNA biogenesis genes, indicated that piRNA may play multiple functional roles in mosquitoes. Although the antiviral function of piRNA pathway in mosquitoes has been extensively studied, the role of piRNAs in mosquito reproduction remain to be further understood. In the present study, we first profiled the characteristics of sex-biased piRNAs in adult Ae.albopictus. Then, we identified a female biased piRNA (Aalpi18529) in adult females, that was highly expressed in ovaries at blood feeding-dependent termination, and depended on PIWI5 and ago3 mediated biogenesis. Aalpi18529 overexpression suppressed ovarian development, and reduced fertility and fecundity in adult females post-bloodmeal. Furthermore, we demonstrated that Aalpi18529 can effectively repress its direct target, growth arrest and DNA-damage-inducible protein 45a (GADD45A), and eventually regulates ovarian development via the Gadd45a-mediated JNK-dependent nurse cell apoptosis pathway. Our study is the first to report an endogenous piRNA, which trigger silencing of an important protein-coding gene by posttranscriptional regulation in mosquitoes, expanding our current understanding of the important and multiple roles of piRNAs in biological processes in Ae. albopictus. Author SummaryHere, we conducted high throughput piRNA sequencing and comprehensive analysis of piRNA sex-based expression profiles in adult females and males of Aedes albopictus. Based on several established universal tools for research, we demonstrate an ovary-enriched endogenous piRNA, Aalpi-18529, is involved in the regulation of the apoptosis of nurse cells during vitellogenesis via the GADD45A/phosphorylated JNK (pJNK) axis and ultimately affects ovarian development. In general, uncovering the biological functions of sex-biased piRNAs in Aedes albopictus will enhance the understanding of piRNA roles in mosquito Sexual dimorphism (SD) and will provide provide more information about the high reproductive capacity of Aedes albopictus, which is essential to find alternative control strategies. Classification: Research Reports