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

Abstract

AbstractTransgenerational phenotypic plasticity (TPP) refers to the phenomenon that environmental conditions experienced by one generation can influence the phenotype of subsequent generations to adapt to the environment without modification of their DNA sequences. Aphid wing dimorphism is a textbook example of TPP by which a maternal aphid perceives the environmental cues to decide the wing morph of her offspring. However, the signaling mechanism from mother to daughter remains unclear. In this study, we showed that the population density and physical contact caused high proportion of winged offspring in the pea aphidAcyrthosiphon pisum. Itsvesicular glutamate transporter 2(ApvGluT2) andmetabotropic glutamate receptor 3(ApmGluR3) were identified by tissue-specific RNA-seq as differentially expressed genes in the head and embryo respectively between solitary and more densely housed maternal aphids. Elevated expression of brainApvGluT2and embryonicApmGluR3led to increases in the winged proportion. Knockdown of either gene inhibited phosphorylation of ApFoxO in embryos. Furthermore, EMSA showed that dephosphorylated ApFoxO directly bound to the promotor ofhedgehog(ApHh), a morphogen gene for wing development, to repress its transcription in stage 20 embryos, causing a lower winged proportion. Our results demonstrated that brainvGluT2and embryonicmGluR3coordinately relayed the maternal physical contact signals and control wing development in offspring, showcasing a novel regulatory mechanism underlying physical contact-dependent, transgenerational wing dimorphism in aphids.SignificanceTransgenerational phenotypic plasticity is a widespread phenomenon that endows organisms and their progenies with abilities to maximize their fitness under different habitats. Aphids exemplify a successful evolutionary strategy through their transgenerational wing dimorphism. We show that transcripts of a vesicular glutamate transportervGluT2in maternal brain and a metabotropic glutamate receptormGluR3in embryo varied in a density-dependent manner and that increased expression ofvGluT2andmGluR3were necessary triggers for signal transduction, leading to production of a high proportion of winged offspring. ThevGluT2-mGluR3cascade increased the phosphorylation of embryonic FoxO, which released its suppression onhedgehogin stage 20 embryos. These findings have brought novel insight into the complicated parent-offspring communications during the wing morph transitions of aphids.