Functional properties of insect olfactory receptors: ionotropic receptors and odorant receptors

Wicher, Dieter; Miazzi, Fabio

doi:10.1007/s00441-020-03363-x

Cited by 114 publications

(87 citation statements)

References 119 publications

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“…3 ). Without Orco , the correct localization of all ORs is compromised, preventing the OR-signaling while maintaining other chemosensory pathways unharmed 26 , 27 , 29 , 30 . This knockout system allowed us to evaluate the contribution of OR and IR olfactory receptor families on C .…”

Section: Discussionmentioning

confidence: 99%

Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly

Paulo

Junqueira

Arp

et al. 2021

Sci Rep

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The evolution of obligate ectoparasitism in blowflies (Diptera: Calliphoridae) has intrigued scientists for over a century, and surprisingly, the genetics underlying this lifestyle remain largely unknown. Blowflies use odors to locate food and oviposition sites; therefore, olfaction might have played a central role in niche specialization within the group. In insects, the coreceptor Orco is a required partner for all odorant receptors (ORs), a major gene family involved in olfactory-evoked behaviors. Hence, we characterized the Orco gene in the New World screwworm, Cochliomyia hominivorax, a blowfly that is an obligate ectoparasite of warm-blooded animals. In contrast, most of the closely related blowflies are scavengers that lay their eggs on dead animals. We show that the screwworm Orco orthologue (ChomOrco) is highly conserved within Diptera, showing signals of strong purifying selection. Expression of ChomOrco is broadly detectable in chemosensory appendages, and is related to morphological, developmental, and behavioral aspects of the screwworm biology. We used CRISPR/Cas9 to disrupt ChomOrco and evaluate the consequences of losing the OR function on screwworm behavior. In two-choice assays, Orco mutants displayed an impaired response to floral-like and animal host-associated odors, suggesting that OR-mediated olfaction is involved in foraging and host-seeking behaviors in C. hominivorax. These results broaden our understanding of the chemoreception basis of niche occupancy by blowflies.

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Section: Discussionmentioning

confidence: 99%

Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly

Paulo

Junqueira

Arp

et al. 2021

Sci Rep

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“…Different from other OSNs, Gr-dependent CO 2 receptor neurons undergo constant receptor-ligand interaction due to the atmospheric/ambient existence of CO 2 , making it challenging to differentiate stimulation-evoked from spontaneous activity. Spontaneous activity appears to be a characteristic of olfactory receptor neurons in Drosophila (Wilson, 2013;Wicher and Miazzi, 2021) and various internal (Andrea Yao and Carlson, 2010) and external (Joseph et al, 2012;Cao et al, 2017) factors can change the rate. For instance, increases in temperature increase the basal firing rate, while decreases in temperature decrease it baseline spiking in insect ORNs (Joseph et al, 2012;Cao et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Flies Avoid Current Atmospheric CO2 Concentrations

Üçpunar

Kadow

2021

Front. Physiol.

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CO2 differs from most other odors by being ubiquitously present in the air animals inhale. CO2 levels of the atmosphere, however, are subject to change. Depending on the landscape, temperature, and time of the year, CO2 levels can change even on shortest time scales. In addition, since the 18th century the CO2 baseline keeps increasing due to the intensive fossil fuel usage. However, we do not know whether this change is significant for animals, and if yes whether and how animals adapt to this change. Most insects possess olfactory receptors to detect the gaseous molecule, and CO2 is one of the key odorants for insects such as the vinegar fly Drosophila melanogaster to find food sources and to warn con-specifics. So far, CO2 and its sensory system have been studied in the context of rotting fruit and other CO2-emitting sources to investigate flies’ response to significantly elevated levels of CO2. However, it has not been addressed whether flies detect and potentially react to atmospheric levels of CO2. By using behavioral experiments, here we show that flies can detect atmospheric CO2 concentrations and, if given the choice, prefer air with sub-atmospheric levels of the molecule. Blocking the synaptic release from CO2 receptor neurons abolishes this choice. Based on electrophysiological recordings, we hypothesize that CO2 receptors, similar to ambient temperature receptors, actively sample environmental CO2 concentrations close to atmospheric levels. Based on recent findings and our data, we hypothesize that Gr-dependent CO2 receptors do not primarily serve as a cue detector to find food sources or avoid danger, instead they function as sensors for preferred environmental conditions.

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“…A tremendous breadth of questions remains to be answered. Functionally, do Drosophila support cell activities influence classic neuronal properties such as adaptation and sensitization (Wicher and Miazzi, 2021), for example in their ability to discriminate transient, repeated, sustained or excessive cues, perhaps by switching rates of odor clearance from the sensillum lymph through adjustable release of enzymes or pinocytosis? Do support cells vary heterogeneously and phenotypically between sensilla within or between organisms, beyond that of known differential expression of OBPs?…”

Section: Future Perspectivesmentioning

confidence: 99%

Functional interaction between Drosophila olfactory sensory neurons and their support cells

Prelic

Mahadevan

Venkateswaran

et al. 2021

Preprint

Self Cite

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Insects detect volatile chemicals using antennae, which house a vast variety of olfactory sensory neurons (OSNs) that innervate hair-like structures called sensilla where odor detection takes place. In addition to OSNs, the antenna also hosts various support cell types. These include the triad of trichogen, tormogen and thecogen support cells that lie adjacent to their respective OSNs. The arrangement of OSN supporting cells occurs stereotypically for all sensilla and is widely conserved in evolution. While insect chemosensory neurons have received considerable attention, little is known about the functional significance of the cells that support them. For instance, it remains unknown whether support cells play an active role in odor detection, or only passively contribute to homeostasis, e.g. by maintaining sensillum lymph composition. To investigate the functional interaction between OSNs and support cells, we used optical and electrophysiological approaches in Drosophila. First, we characterized the distribution of various supporting cells using genetic markers. By means of an ex vivo antennal preparation and genetically-encoded Ca2+ and K+ indicators, we then studied the activation of these auxiliary cells during odor presentation in adult flies. We observed acute responses and distinct differences in Ca2+ and K+ fluxes between support cell types. Finally, we observed alterations in OSN responses upon thecogen cell ablation in mature adults. Upon inducible ablation of thecogen cells, we notice a gain in mechanical responsiveness to mechanical stimulations during single-sensillum recording, but a lack of change to neuronal resting activity. Taken together, these results demonstrate that support cells play a more active and responsive role during odor processing than previously thought. Our observations thus reveal that support cells functionally interact with OSNs and may be important for the extraordinary ability of insect olfactory systems to dynamically and sensitively discriminate between odors in the turbulent sensory landscape of insect flight.

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Functional properties of insect olfactory receptors: ionotropic receptors and odorant receptors

Cited by 114 publications

References 119 publications

Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly

Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly

Flies Avoid Current Atmospheric CO2 Concentrations

Functional interaction between Drosophila olfactory sensory neurons and their support cells

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