Endoplasmic reticulum patterns insect cuticle nanostructure

Abstract

Insect cuticles with nano-level structures exhibit functional surface properties such as structural color and superhydrophobicity. Despite the enormous influence the cuticle has had on biomimetic industrial applications, molecular and cellular mechanisms of cuticular extracellular matrix (ECM) assembly into nanoscale structures remain poorly understood in insects and other taxa. Ghiradella (1989) described how a crystallin-like lattice of endoplasmic reticulum (ER) prefigures the patterning of the porous cuticle of the butterfly wing scale with structural color1. Building on that insight, we show that the nanopore structure of the olfactory (olf) organs, which serve as molecular filters in Drosophila, is built through a novel process in which ER material is trafficked to the plasma membrane mediated by the autophagy pathway. The process is controlled by the insect-specific protein Gore-tex/Osiris23 (Gox)2, which is localized to the tubular ER of olf hair cells. Gox recruits Ref(2)P, the fly counterpart of mammalian p62/SQSTM13, to initiate ER scission. The excised ER fragments are processed by autophagy to gain access to the plasma membrane and trigger membrane invagination, which plays a role in remodeling the cuticular envelope layer to the nanopore formation. This repurposing of the ER phagy for machinery to support the fabrication of nanoscale ECM by the Gox protein sheds light on the nanopatterning of insect cuticles and their genetic control.