Whole-transcriptome profiling of the fat body identifies aae-miR-283-ApoLp-Ⅱ/Ⅰ regulation associated with lipid transport and ovarian development in Aedes aegypti.

Abstract

Aedes aegypti is a major vector of arboviruses that pose major threats to global public health. In female mosquitoes, the fat body governs nutritional metabolism and vitellogenesis after a blood meal, with its functional state directly determining fecundity. Although endocrine and nutritional signals regulating mosquito reproduction have been widely studied, the role of non-coding RNAs (ncRNAs) and competing endogenous RNA (ceRNA) networks in fat body metabolic homeostasis remains poorly understood. To address this, we performed whole-transcriptome sequencing of fat bodies from sugar-fed and blood-fed females and identified 30 circRNAs, 142 miRNAs, 874 lncRNAs, and 4,362 differentially expressed mRNAs, with significant enrichment in nutrient metabolism, energy homeostasis, and mTOR/MAPK signaling. Based on these data, we constructed ceRNA networks centered on blood-responsive miRNAs. Focusing on the downregulated, high-abundance aae-miR-283, we generated a transgenic overexpression line and found that elevated aae-miR-283 markedly impaired ovarian development, oviposition, and egg hatching. Mechanistically, dual-luciferase reporter assays confirmed that aae-miR-283 directly binds to the 3'UTR of ApoLp-Ⅱ/Ⅰ, supporting ApoLp-Ⅱ/Ⅰ as a direct target of aae-miR-283. The lncRNA MSTRG.88121.1 also showed binding to aae-miR-283 in the dual-luciferase reporter assay, suggesting that it may participate in an aae-miR-283-associated regulatory network. Functional studies revealed that both aae-miR-283 overexpression and ApoLp-Ⅱ/Ⅰ knockdown disrupted lipid homeostasis, increasing triacylglycerol accumulation in the fat body while depleting ovarian lipid stores, supporting a role for aae-miR-283-ApoLp-Ⅱ/Ⅰ regulation in lipid transport from the fat body to the ovaries. Our findings reveal a novel aae-miR-283-centered regulatory mechanism controlling reproductive energy allocation in Ae. aegypti and provide potential molecular targets for metabolic intervention-based vector control strategies.