Chemoreceptor co-expression in Drosophila melanogaster olfactory neurons

Abstract

Drosophila melanogaster olfactory neurons have long been thought to express only one chemosensory receptor gene family. There are two main olfactory receptor gene families in Drosophila, 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: Orco for ORs, and Ir25a, Ir8a, and Ir76b for IRs. Using a new genetic knock-in strategy, we targeted the four co-receptors representing the main chemosensory families in D. melanogaster (Orco, Ir8a, Ir76b, Ir25a). 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, Ir25a 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. Orco, Ir8a, and Ir76b expression patterns are also more expansive than previously assumed. Single sensillum recordings from Orco-expressing Ir25a mutant antennal and palpal neurons identify changes in olfactory responses. We also find co-expression of Orco and Ir25a in Drosophila sechellia and Anopheles coluzzii 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.

A spatial map of antennal-expressed olfactory ionotropic receptors in the malaria mosquito

“…Tuning IRs form a functional complex with at least 1 or more co-receptors (Abuin et al, 2011; Ai et al, 2013), which might influence their functional properties (Task et al, 2022). To examine this, we utilized two probe whole mount fluorescent in situs to identify which IR co-receptors were co-expressed in the same cells as the 4 highly expressed tuning IRs.…”

No functional contribution of the gustatory receptor, Gr64b, co-expressed in olfactory sensory neurons of Drosophila melanogaster

“…Taken together, our results suggest that Gr64b plays no significant role in modulating odor sensitivity or specificity in Or47aexpressing OSNs even though they are co-expressed in the very same neurons. (Task et al, 2022) and also in Aedes aegypti (Younger et al, 2022). Both of these studies demonstrated co-expression of the olfactory co-receptor (Orco) and multiple ionotropic co-receptors, Ir8a, Ir76b and Ir25a, in multiple OSN classes in the antenna and maxillary palps.…”

“…However, surprisingly, it was in the recent study by Task et al (2022) observed that a few Orco and Ir25a positive neurons also innervate the V glomerulus sparsely, pointing to a wider possibility of overlap between these three gene families, but which could be revealed only after using more effective expression systems (Task et al, 2022). Similarly, the VM6 glomerulus, which was earlier considered a singular entity, was shown to be innervated by subpopulations of (Vulpe et al, 2021) and also by Ir25a positive OSNs (Task et al, 2022). Further, it was shown that the VA6 glomerulus (corresponding to Or82a) was innervated by OSNs expressing multiple coreceptors, including Orco, Ir25a, Ir8a and Ir76b, while, interestingly, the DM3 (corresponding to Or47a and Or33b) was innervated only by Orco positive neurons.…”

“…Labeling of neurons using binary expression systems greatly depend on the construction of the transgenic line (positional effect). It is thus possible that some essential regulatory elements for the expression could have been replaced during the genetic insertion (Yavuz et al, 2014; Task et al, 2022). This is specifically true in case of GRs from the GR64 cluster due to the complex arrangement of regulatory elements, sometimes also within the locus (Fujii et al, 2015).…”

“…In other combinations, it has been reported that detection of sour taste via tarsal gustatory sensory neurons (GSNs) was mediated via co-expressed IRs (Chen and Amrein, 2017). Two recent studies also demonstrated overlapping expression of multiple gene families, with emphasis on IRs and ORs in the D. melanogaster antenna (Task et al, 2022) and in the yellow fever mosquito, Aedes aegypti (Younger et al, 2022). These studies are particularly important in demonstrating a functional role of IRs and ORs co-expressed in the OSNs.…”