Insect cuticles with nano-level structures exhibit functional surface properties such as the photonic nanocrystal of the butterfly wing scale with structural color and the corneal nipple arrays of superhydrophobic compound eye lens. Despite the enormous influence the cuticle has had on biomimetic industrial applications, cellular mechanisms of cuticular nanopatterning remain poorly understood. Drosophila gore-tex/Osiris23 (gox) controls the formation of nanopores, with a molecular filtering function, on the olfactory organs. Here we used 3D electron microscopy imaging of entire hair structures to show that nanopore is formed through a novel process of bidirectional interaction of the ER and the plasma membrane trafficking. ER-resident protein Gox stimulates ER-phagy through regulation of Ref(2)P, the fly counterpart of the autophagy protein p62/SQSTM1, and initiates endocytosis. Dynamin on the plasma membrane completes endocytosis and sustains ER-phagy. The repurposing of ER-phagy for plasma membrane remodeling and the fabrication of nanoscale ECM structures sheds light on the nanopatterning mechanism of insect cuticles and their genetic control.
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