Advantage of the Highly Restricted Odorant Receptor Expression Pattern in Chemosensory Neurons of Drosophila

Abstract

A fundamental molecular feature of olfactory systems is that individual neurons express only one receptor from a large odorant receptor gene family. While numerous theories have been proposed, the functional significance and evolutionary advantage of generating a sophisticated one-receptor-per neuron expression pattern is not well understood. Using the genetically tractable Drosophila melanogaster as a model, we demonstrate that the breakdown of this highly restricted expression pattern of an odorant receptor in neurons leads to a deficit in the ability to exploit new food sources. We show that animals with ectopic co-expression of odorant receptors also have a competitive disadvantage in a complex environment with limiting food sources. At the level of the olfactory system, we find changes in both the behavioral and electrophysiological responses to odorants that are detected by endogenous receptors when an olfactory receptor is broadly misexpressed in chemosensory neurons. Taken together these results indicate that restrictive expression patterns and segregation of odorant receptors to individual neuron classes are important for sensitive odor-detection and appropriate olfactory behaviors.

Cis-Regulatory Mechanisms for Robust Olfactory Sensory Neuron Class-restricted Odorant Receptor Gene Expression in Drosophila

“…OSNs expressing the same OR project their axons to the same glomerulus in the brain and create a functional unit, the OSN class, that exists in both insects and mammals [ 6 ]. The restriction of OR expression to a single OSN class is crucial for the perception of odors as changes in OR expression pattern produce a mix of ORs in each OSN class, distorting the response properties of the class and thereby impairing odor detection [ 7 ].…”

Complex and non-redundant signals from individual odor receptors that underlie chemotaxis behavior in Drosophila melanogaster larvae

“…In a recent analysis of larval behavior, ectopic expression of Or42a in multiple sensory neurons affected behavioral responses to both 3-octanol and anisole. The proposed explanation for these results was that ectopic Or42a expression was affecting receptor function in non-native sensory neurons ( Tharadra et al, 2013 ). A second explanation, consistent with the data presented here, is that modest electrophysiological responses of Or42a to these odors is altering gain control, thereby altering behavioral responses.…”