Organizing the Drosophila olfactory circuits by interacting Ig superfamily adhesion molecules
Authors: Qichen Duan; Scott Barish; Allison Carson; Rachel Estrella; Pelin Volkan
Affiliation: Department of Biology, Duke University, Durham, NC
Keywords: a. axon guidance; r. cell-cell interactions
The Drosophila olfactory system provides an excellent model to study how complex neuronal circuits are assembled. In Drosophila, each olfactory receptor neuron (ORN) class exclusively expresses a unique olfactory receptor (OR) gene and target each class-specific and uniquely positioned glomerulus in the antennal lobe. How ORN axon terminals are organized into these dedicated structural compartments is not well understood. Through transcriptome profiling of the antennal tissues during development and RNAi screen, we identified two protein subfamilies belonging to the Immunoglobulin Superfamily, Beats and their heterophilic binding partners Sides, as novel regulators of ORN glomerular organization. Many Beats and Sides are expressed at low levels at early pupal stages but increase their expression levels later. Beats and Sides are also differentially expressed across ORN classes, making them good candidates for encoding the ORN class-specific cell surface codes to mediate neuron-neuron recognition. Perturbing the functions of many Beats and Sides in all or a subset of ORNs at later stages leads to diverse local defects of ORN glomerular organization, associated with the expanding, split, or flipped glomerular morphology. Binding Beat-Side pairs are co-expressed in the same class of ORNs and knockdown of either member of these interacting pairs could lead to similar ORN axonal disorganization. These defects are not likely to be resulted from synaptic mismatching, but rather the loss of axonal adhesion. Furthermore, OR function regulates the expression of Beats and Sides, as some of these genes show altered expression levels in OR mutants. Our data suggest the context-dependent control of ORN glomerular organization by Beat/Side combinatorial codes, and bring new insights into how diverse neuronal populations are coordinated into hardwired circuits.