Vestigial mediates the effect of insulin signaling pathway on wing-morph switching in planthoppers.

Wing polymorphism is an evolutionary feature found in a wide variety of insects, which offers a model system for studying the evolutionary significance of dispersal. In the wing-dimorphic planthopper Nilaparvata lugens, the insulin/insulin-like growth factor signaling (IIS) pathway acts as a 'master signal' that directs the development of either long-winged (LW) or short-winged (SW) morphs via regulation of the activity of Forkhead transcription factor subgroup O (NlFoxO). However, downstream effectors of the IIS–FoxO signaling cascade that mediate alternative wing morphs are unclear. Here we found that vestigial (Nlvg), a key wing-patterning gene, is selectively and temporally regulated by the IIS–FoxO signaling cascade during the wing-morph decision stage (fifth-instar stage). RNA interference (RNAi)-mediated silencing of Nlfoxo increase Nlvg expression in the fifth-instar stage (the last nymphal stage), thereby inducing LW development. Conversely, silencing of Nlvg can antagonize the effects of IIS activity on LW development, redirecting wing commitment from LW to the morph with intermediate wing size. In vitro and in vivo binding assays indicated that NlFoxO protein may suppress Nlvg expression by directly binding to the first intron region of the Nlvg locus. Our findings provide a first glimpse of the link connecting the IIS pathway to the wing-patterning network on the developmental plasticity of wings in insects, and help us understanding how phenotypic diversity is generated by the modification of a common set of pattern elements. Author summary: Many insects are capable of developing into either long-winged or short-winged adults, but the underlying molecular basis remains largely unknown. Pioneer studies showed that the insulin/insulin-like growth factor signaling pathway acts as a 'master signal' that directs wing buds to develop into long or short wings in the wing-dimorphic planthopper, Nilaparvata lugens. However, downstream effectors mediating the IIS pathway effects are unknown. Our findings highlight that vestigial, a key wing-patterning gene, is a main downstream effector that mediates the IIS activity on the development of alternative wing morphs during the wing-morph decision stage. The molecular mechanism of wing formation, including the function of vestigial, has been studied in great depth in the model insect Drosophila melanogaster. Our data provide a first glimpse of the link connecting the IIS pathway to the wing-patterning network in regulating developmental plasticity of wings in insects. [ABSTRACT FROM AUTHOR]