The maternal vGluT2 and embryonic mGluR3 signaling relay system controls offspring wing dimorphism in pea aphid

Aphid wing dimorphism is a textbook example of transgenerational phenotypic plasticity, but the signaling mechanism from mother to daughter remains unclear. We showed that the physical contact and crowding treatment caused high proportion of winged offspring in the pea aphid Acyrthosiphon pisum. RNA sequencing (RNA-seq) analysis indicated that the expression of brain vesicular glutamate transporter 2 (ApvGluT2) and embryonic metabotropic glutamate receptor 3 (ApmGluR3) were increased by physical contact and crowding treatments. Knockdown of either gene inhibited phosphorylation of ApFoxO in embryos. Furthermore, electrophoretic mobility shift assays (EMSA) showed that dephosphorylated ApFoxO directly bound to the promotor of hedgehog (ApHh) to repress its transcription in stage 20 embryos, causing a lower winged proportion. Our results demonstrated that brain vGluT2 and embryonic mGluR3 coordinately relayed the maternal physical contact signals and control wing development in offspring, showcasing a regulatory mechanism underlying physical contact-dependent, transgenerational wing dimorphism in aphids.