FoxO directly regulates the expression of TOR/S6K and vitellogenin to modulate the fecundity of the brown planthopper.

As a conserved transcription factor, FoxO plays a crucial role in multiple physiological processes in vivo, including stress resistance, longevity, growth and reproduction. Previous studies on FoxO have focused on human, mouse, Drosophila melanogaster and Caenorhabditis elegans, while there are few reports on agricultural pests and little is known about how FoxO modulates insect fecundity. In Asia, the brown planthopper (BPH) Nilaparvata lugens (Stål) is one of the most serious pests in rice production and high fecundity is the basis of the outbreak of BPH. Here, using the genome-wide ChIP-seq of NlFoxO in BPH, we found that NlFoxO binds to the promoters of ribosomal proteinS6 kinase (NlS6K) and serine/threonine-protein kinase mTOR (NlTOR) and increases their expression levels. We also found that NlFoxO directly binds to the exon of vitellogenin (NlVg) and has a specific inhibitory effect on its expression. In addition, the number of eggs laid and their hatching rate decreased significantly after injection of NlFoxO double-stranded RNA into BPH adults. Our findings provide direct evidence that FoxO modulates insect fecundity through binding to the promoters of NlS6K, NlTOR and the exon of NlVg and affecting their gene expression in the Vg network.