Charting the development of Drosophila leg sensory organs at single-cell resolution

Abstract

To respond to the world around them, animals rely on the input of a network of sensory organs distributed throughout the body. Distinct classes of sensory organ are specialized for the detection of specific stimuli such as strain, pressure, or taste. The features that underlie this specialization relate both to the neurons that innervate sensory organs and the accessory cells that comprise them. This diversity of cell types, both within and between sensory organs, raises two fundamental questions: what makes these cell types distinct from one another, and how is this diversity generated during development? To address these questions, we performed single-cell RNA sequencing on a developing tissue that displays a wide variety of functionally and structurally distinct sensory organs: the first tarsal segment of the pupal male Drosophila melanogaster foreleg. We characterize the cellular landscape in which the sensory organs reside, identify a novel cell type that contributes to the construction of the neural lamella, and characterize the transcriptomic differences among support cells within and between sensory organs. We identify the genes that distinguish between mechanosensory and chemosensory neurons, resolve a combinatorial transcription factor code that defines four distinct classes of gustatory neuron and several types of mechanosensory neuron, and match the expression of sensory receptors to specific neuron classes. Collectively, our work identifies core genetic features of a variety of sensory organs and provides a rich, annotated resource for studying their development and function.