Chemoreceptor co-expression in <i>Drosophila melanogaster</i> olfactory neurons.

Abstract

<i>Drosophila melanogaster</i> olfactory neurons have long been thought to express only one chemosensory receptor gene family. There are two main olfactory receptor gene families in <i>Drosophila</i>, the odorant receptors (ORs) and the ionotropic receptors (IRs). The dozens of odorant-binding receptors in each family require at least one co-receptor gene in order to function: <i>Orco</i> for ORs, and <i>Ir25a</i>, <i>Ir8a</i>, and <i>Ir76b</i> for IRs. Using a new genetic knock-in strategy, we targeted the four co-receptors representing the main chemosensory families in <i>D. melanogaster</i> (<i>Orco, Ir8a, Ir76b, Ir25a</i>). Co-receptor knock-in expression patterns were verified as accurate representations of endogenous expression. We find extensive overlap in expression among the different co-receptors. As defined by innervation into antennal lobe glomeruli, <i>Ir25a</i> is broadly expressed in 88% of all olfactory sensory neuron classes and is co-expressed in 82% of Orco+ neuron classes, including all neuron classes in the maxillary palp. <i>Orco</i>, <i>Ir8a</i>, and <i>Ir76b</i> expression patterns are also more expansive than previously assumed. Single sensillum recordings from Orco-expressing <i>Ir25a</i> mutant antennal and palpal neurons identify changes in olfactory responses. We also find co-expression of <i>Orco</i> and <i>Ir25a</i> in <i>Drosophila sechellia</i> and <i>Anopheles coluzzii</i> olfactory neurons. These results suggest that co-expression of chemosensory receptors is common in insect olfactory neurons. Together, our data present the first comprehensive map of chemosensory co-receptor expression and reveal their unexpected widespread co-expression in the fly olfactory system.