Most insect species rely on the detection of olfactory cues for critical behaviors for the survival of the species, e.g., finding food, suitable mates and appropriate egg-laying sites. Although insects show a diverse array of molecular receptors dedicated to the detection of sensory cues, two main types of molecular receptors have been described as responsible for olfactory reception in Drosophila, the odorant receptors (ORs) and the ionotropic receptors (IRs). Although both receptor families share the role of being the first chemosensors in the insect olfactory system, they show distinct evolutionary origins and several distinct structural and functional characteristics. While ORs are seven-transmembrane-domain receptor proteins, IRs are related to the ionotropic glutamate receptor (iGluR) family. Both types of receptors are expressed on the olfactory sensory neurons (OSNs) of the main olfactory organ, the antenna, but they are housed in different types of sensilla, IRs in coeloconic sensilla and ORs in basiconic and trichoid sensilla. More importantly, from the functional point of view, they display different odorant specificity profiles. Research advances in the last decade have improved our understanding of the molecular basis, evolution and functional roles of these two families, but there are still controversies and unsolved key questions that remain to be answered. Here, we present an updated review on the advances of the genetic basis, evolution, structure, functional response and regulation of both types of chemosensory receptors. We use a comparative approach to highlight the similarities and differences among them. Moreover, we will discuss major open questions in the field of olfactory reception in insects. A comprehensive analysis of the structural and functional convergence and divergence of both types of receptors will help in elucidating the molecular basis of the function and regulation of chemoreception in insects.
In many species, olfactory transduction is triggered by odorant molecules that interact with olfactory receptors coupled to heterotrimeric G-proteins. The role of G-protein-linked transduction in the olfaction of Drosophila is currently under study. Here, we supply a thorough description of the expression in the olfactory receptor organs (antennae and maxillary palps) of all known Drosophila melanogaster genes that encode for G-proteins. Using RT-polymerase chain reaction, we analyzed 6 Galpha (G(s), G(i), G(q), G(o), G(f), and concertina), 3 Gbeta (G(beta5), G(beta13F), and G(beta76C)), and 2 Ggamma genes (G(gamma1) and G(gamma30A)). We found that all Galpha protein-encoding genes showed expression in both olfactory organs, but G(f) mRNA was not detected in palps. Moreover, all the Gbeta and Ggamma genes are expressed in antennae and palps, except for G(beta76C). To gain insight into the hypothesis of different G-protein subunits mediating differential signaling in olfactory receptor neurons (ORNs), we performed immunohistochemical studies to observe the expression of several Galpha and Gbeta proteins. We found that Gs, Gi, Gq, and G(beta13F) subunits displayed generalized expression in the antennal tissue, including ORNs support cells and glial cells. Finally, complete coexpression was found between Gi and Gq, which are mediators of the cyclic adenosine monophosphate and IP3 transduction cascades, respectively.
1. Amplitude as well as time course of the electroantennogram (EAG) in Drosophila has been used for describing electrical changes produced in the antenna in response to odorous stimulation. 2. Maximal amplitude of response appears to be directly correlated to stimulus concentration but, after achieving a maximum value, is independent of stimulation duration. 3. Rise time and fall time constants have been quantified for describing kinetics of response. The rise time constant decreases, but the fall time constant increases when increasing concentrations of odorant are supplied. 4. Variation among individuals for these EAG parameters is small enough to uncover even partial defects affecting the first sensory step. This fact combined with the possibility of obtaining mutants with defects in any intermediate process producing the electrical response makes the EAG of Drosophila a very useful tool for dissecting the components of the capture and transduction processes in the olfactory sense. 5. This kind of quantitative study of the EAG has been used in a new Drosophila mutant, od A, for localizing peripheral expression of the mutation. od A has been isolated as a behavioral mutant with an abnormally enhanced olfactory response to ethyl acetate. 6. The mutant's EAG in response to this odorant displays a normal amplitude but abnormal kinetics. Rise time as well as fall time show slower kinetics than normal, suggesting some defective step in the capture and transduction process.
Two main second messenger systems depending on IP3 and cAMP have been related to olfaction in vertebrates as well as invertebrates. In Drosophila melanogaster, the availability of mutations affecting one or the other pathway (rdgB and norpA or rut and dnc, respectively) allowed showing of abnormal olfactory behavior phenotypes associated with olfactory transduction in complete living animals. However, because rut and dnc genes showed ubiquitous expression at olfactory receptor organs and some brain locations, the mutant behavior cannot be assigned exclusively to olfactory reception. In this report, overexpression of the dnc gene directed specifically to different olfactory receptor neuron subsets was used to produce dominant mutants. Abnormal olfactory behavior was found in 62.5% of the 8 lines studied in response to some odorants, depending on the affected neuronal subset. These results suggest that even for a small number of tested odorants (5), cAMP cascade is involved in olfactory reception to an important extent.
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