Abstract
Two large families of olfactory receptors, the Odorant Receptors (ORs) and Ionotropic Receptors (IRs), mediate responses to most odors in the insect olfactory system. Individual odorant binding “tuning” OrX receptors are expressed by olfactory neurons in basiconic and trichoid sensilla and require the co-receptor Orco. The situation for IRs is more complex. Different tuning IrX receptors are expressed by olfactory neurons in coeloconic sensilla and rely on either the Ir25a or Ir8a co-receptors; some evidence suggests that Ir76b may also act as a co-receptor, but its function has not been systematically examined. Surprisingly, recent data indicate that nearly all coeloconic olfactory neurons co-express Ir25a, Ir8a, and Ir76b. Here, we demonstrate that Ir76b and Ir25a function together in all amine-sensing olfactory receptor neurons. In most neurons, loss of either co-receptor abolishes amine responses. In contrast, amine responses persist in the absence of Ir76b or Ir25a in ac1 sensilla but are lost in a double mutant. We show that responses mediated by acid-sensing neurons do not require Ir76b, despite their expression of this co-receptor. Our study also demonstrates that one population of coeloconic olfactory neurons exhibits Ir76b/Ir25a-dependent and Orco-dependent responses to distinct odorants. Together, our data establish the role of Ir76b as a bona fide co-receptor, which acts in partnership with Ir25a. Given that these co-receptors are among the most highly conserved olfactory receptors and are often co-expressed in chemosensory neurons, our data suggest Ir76b and Ir25a also work in tandem in other insects.
Highlights
A vast number of different volatile molecules can be detected as odorants by both vertebrate and invertebrate animals
This suggests that only Ir25a and Ir76b are necessary for the proper functioning of these amine receptors, despite co-expression of Ir8a in these neurons
This study clarifies the roles of Ionotropic Receptors (IRs) co-receptors in olfactory neurons in Drosophila
Summary
A vast number of different volatile molecules can be detected as odorants by both vertebrate and invertebrate animals. Most odorants are detected by receptors in one of two large gene families, the Odorant Receptors (ORs) and the Ionotropic Receptors (IRs; Vosshall and Stocker, 2007; Rytz et al, 2013). These receptors are found on the dendrites of olfactory receptor neurons (ORNs) housed in antennal olfactory sensilla. IRs are distantly related to well-characterized ionotropic glutamate receptors, such as AMPA and NMDA receptors (Benton et al, 2009) Like those receptors, IRs form ligandgated non-selective cation channels, which are likely tetrameric complexes (Abuin et al, 2011). These complexes contain both IrX tuning subunits as well as highly conserved co-receptors that are required for the formation of functional receptors and trafficking of IrX to olfactory neuron dendrites (Abuin et al, 2011, 2019)
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