A conserved zona pellucida protein piopio regulates wing morphogenesis via epidermal adhesion

The wings has played a crucial role in the survival and reproduction of insects. The structure of flat insect wings is established through the adhesion of the dorsal and ventral epidermal layers, a process that is contingent upon the dynamics of the basal extracellular matrix (ECM). However, compared with basal ECM, the function of apical ECMs during the wing development remains inadequately understood. In this study, we identified a zona pellucida (ZP) family gene, piopio (pio), as important components of the aECM. This gene exhibited high expression levels in the wing discs of both Bombyx mori and Drosophila melanogaster. Disruption of the gene in these two species resulted in impaired adhesion of the wing layers, leading to the formation of blistered wings. Moreover, the loss-of-function of pio prevented the degradation of the basal ECM, a critical phase required for initial adhesion of wing. Additionally, we observed a similar phenotypic manifestation in two pest species, Tribolium castaneum and Locusta migratoria, thereby confirming the conserved function of the pio gene in the wing development of insects. Our findings not only advance understanding of ZP proteins in insect wing morphogenesis but also propose pio as a potential target for pest control.