AnInR/mir-9a/NlUbxregulatory cascade regulates wing diphenism in brown planthoppers

Wing polymorphism significantly contributes to the ecological success of some insect species. For example, the brown planthopper (BPH)Nilaparvata lugens, which is one of the most destructive rice pests in Asia, can develop into either highly mobile long-winged or highly fecund short-winged adult morphs. A recent study reported a highly provocative result that theHoxgeneUltrabithorax(Ubx) is expressed in BPH forewings and showed that this wing development gene is differentially expressed in nymphs that develop into long-winged versus short-winged morphs. Here, we found thatUbxmay be amir-9atarget, and used dual luciferase reporter assays and injected micro RNA (miRNA) mimics and inhibitors to confirm the interactions betweenmir-9aandNlUbx. We measured themir-9aandNlUbxexpression profiles in nymphs and found that the expression of these two biomolecules was negatively correlated. By rearing BPH nymphs on host rice plants with different nutritional status, we were able to characterize a regulatory cascade between insulin receptor genes,mir-9a, andNlUbxthat regulate wing length in BPHs. When host quality was low,NlInR1expression in the nymph terga increased andNlInR2expression decreased; this led to a highermir-9alevel, which in turn reduced theNlUbxtranscript level and ultimately resulted in longer wing lengths. Beyond extending our understanding of the interplay between host plant status and genetic events that modulate polymorphism, we demonstrated both the upstream signal and miRNA-based regulatory mechanism that controlUbxexpression in BPH forewings.

Automated summary

Wing polymorphism is crucial for the ecological success of some insect species. The Hox gene Ultrabithorax (Ubx) is expressed in the forewings of the brown planthopper (BPH)Nilaparvata lugens, and interactions between mir-9a and NlUbx regulate the development of short-winged and long-winged morphs. By manipulating the nutritional status of host rice plants, a regulatory cascade involving insulin receptor genes, mir-9a, and NlUbx was characterized to control wing length in BPHs.