Recent Advances in Physiology of Insect Olfaction

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Physiology, Reproduction and Development".

Deadline for manuscript submissions: closed (1 March 2022) | Viewed by 29691

Special Issue Editors

Department of Animal Physiology, Institute of Biology/Zoology, Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany
Interests: chemoreception in insects; physiology of olfactory systems; primary processes of odorant detection and signal transduction; reception and coding of pheromone signals
Department of Animal Physiology, Institute of Biology/Zoology, Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany
Interests: olfaction; olfactory transduction; chemoreceptors; pheromone detection

Special Issue Information

Dear colleagues,

The sense of smell is of pivotal importance to insects. Odorants originating from food, conspecifics, oviposition sites, or predators initiate and control a variety of insect behaviors essential for survival and reproduction. Insects use sophisticated olfactory systems to constantly screen their environment for olfactory cues and are able to detect behaviorally relevant odorants with remarkable sensitivity and precision. 

This Special Issue aims at highlighting new research on the physiology of insect olfaction with a focus on the olfactory elements and processes that underly the peripheral detection of odorants, the central coding of odors and odor-guided behavior. We invite colleagues to submit original articles, short communications, or reviews that report newest findings or update our understanding of insect olfaction.

Prof. Dr. Jürgen Krieger
Dr. Jörg Fleischer
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Insects is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • olfaction
  • odorant reception
  • pheromone detection
  • olfactory proteins
  • odorant coding
  • odor-guided behavior

Published Papers (10 papers)

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Research

Jump to: Review

20 pages, 3077 KiB  
Article
The Sensilla-Specific Expression and Subcellular Localization of SNMP1 and SNMP2 Reveal Novel Insights into Their Roles in the Antenna of the Desert Locust Schistocerca gregaria
by Sina Cassau, Doreen Sander, Thomas Karcher, Michael Laue, Gerd Hause, Heinz Breer and Jürgen Krieger
Insects 2022, 13(7), 579; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13070579 - 25 Jun 2022
Cited by 4 | Viewed by 1658
Abstract
Insect olfactory sensilla house olfactory sensory neurons (OSNs) and supports cells (SCs). The olfactory sensory processes require, besides the odorant receptors (ORs), insect-specific members of the CD36 family, named sensory neuron membrane proteins (SNMPs). While SNMP1 is considered to act as a coreceptor [...] Read more.
Insect olfactory sensilla house olfactory sensory neurons (OSNs) and supports cells (SCs). The olfactory sensory processes require, besides the odorant receptors (ORs), insect-specific members of the CD36 family, named sensory neuron membrane proteins (SNMPs). While SNMP1 is considered to act as a coreceptor in the OR-mediated detection of pheromones, SNMP2 was found to be expressed in SCs; however, its function is unknown. For the desert locust, Schistocerca gregaria, we previously visualized mRNA for SNMP1 in OSNs and SNMP2 mRNA in cells associated with OSN clusters. Towards an understanding of their functional implication, it is imperative to explore the cellular and the subcellular localization the SNMP proteins. Therefore, we have generated polyclonal antibodies against SNMP1 and SNMP2 and used fluorescence immunohistochemistry (FIHC) to visualize the SNMP proteins. We found SNMP1 in the somata and respective dendrites of all OSNs in trichoid sensilla and in subsets of OSNs in basiconic sensilla. Notably, SNMP1 was also detected in SCs of these sensilla types. In contrast, SNMP2 protein was only visualized in SCs of basiconic and coeloconic sensilla, but not of trichoid sensilla. Exploring the subcellular localization by electron microscopy using anti-SNMP1-ab and anti-SNMP2-ab revealed an immunogold labelling of SC microvilli bordering the sensillum lymph. Together our findings suggest a dual role of SNMP1 in the antenna of S. gregaria, in some OSN subpopulations in odor detection as well as in functions of some SCs, whereas the role of SNMP2 is limited to the functions of support cells. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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16 pages, 13896 KiB  
Article
Surface Properties and Architectures of Male Moth Trichoid Sensilla Investigated Using Atomic Force Microscopy
by Thomas Charles Baker, Qiong Zhou, Charles E. Linn, James Y. Baker and Timothy B. Tighe
Insects 2022, 13(5), 423; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13050423 - 30 Apr 2022
Viewed by 1743
Abstract
The surfaces of trichoid sensilla on male moth antennae have been sculpted over evolutionary time to capture pheromone odorant molecules emitted by the females of their species and transport the molecules in milliseconds into the binding protein milieu of the sensillum lumen. The [...] Read more.
The surfaces of trichoid sensilla on male moth antennae have been sculpted over evolutionary time to capture pheromone odorant molecules emitted by the females of their species and transport the molecules in milliseconds into the binding protein milieu of the sensillum lumen. The capture of pheromone molecules likely has been optimized by the topographies and spacings of the numerous ridges and pores on these sensilla. A monolayer of free lipids in the outer epicuticle covers the sensillar surfaces and must also be involved in optimal pheromone odorant capture and transport. Using electro-conductive atomic force microscopy probes, we found that electrical surface potentials of the pores, ridges and flat planar areas between ridges varied in consistent ways, suggesting that there is a heterogeneity in the distribution of surface lipid mixtures amongst these structures that could help facilitate the capture and transport of pheromone molecules down through the pores. We also performed experiments using peak force atomic force microscopy in which we heated the sensilla to determine whether there is a temperature-related change of state of some of the surface lipid exudates such as the prominent domes covering many of the pores. We found that these exudates were unaffected by heating and did not melt or change shape significantly under high heat. Additionally, we measured and compared the topographies of the trichoid sensilla of five species of moths, including the distributions, spacings, heights and diameters of ridges, pores and pore exudates. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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11 pages, 1815 KiB  
Article
An Odorant Receptor from the Proboscis of the Cotton Bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) Narrowly Tuned to Indole
by Mengbo Guo, Xueting Ren, Yang Liu and Guirong Wang
Insects 2022, 13(4), 385; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13040385 - 13 Apr 2022
Cited by 4 | Viewed by 2093
Abstract
Helicoverpa armigera is a serious agricultural pest with polyphagous diets, widespread distribution, and causing severe damage. Among sixty-five candidate ORs in H. armigera, the co-receptor HarmOrco and three specific ORs with partial sequences were identified to be expressed in the proboscis by [...] Read more.
Helicoverpa armigera is a serious agricultural pest with polyphagous diets, widespread distribution, and causing severe damage. Among sixty-five candidate ORs in H. armigera, the co-receptor HarmOrco and three specific ORs with partial sequences were identified to be expressed in the proboscis by our previous work, whereas their exact function is not known yet. In this study, we first confirmed the expression of these ORs in the proboscis by full-length cloning, which obtained the complete coding region of HarmOrco, OR24, and OR30. We then performed functional identification of HarmOR24 and OR30 by co-expressing them respectively with HarmOrco in Xenopus oocytes eukaryotic expression system combined with two-electrode voltage-clamp physiology. By testing the response of HarmOR24/OR30-expressing oocytes against eighty structural-divergent compounds, respectively, HarmOR30 was characterized to narrowly tune to indole and showed a specific tuning spectrum compared to its ortholog in Spodoptera littoralis. As indole is a distinctive herbivore-induced plant volatile and floral scent component, HarmOR30 might play roles in foraging and mediating the interactions between H. armigera with its surrounding environment. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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10 pages, 1092 KiB  
Article
Homeostasis of Mitochondrial Ca2+ Stores Is Critical for Signal Amplification in Drosophila melanogaster Olfactory Sensory Neurons
by Eric Wiesel, Sabine Kaltofen, Bill S. Hansson and Dieter Wicher
Insects 2022, 13(3), 270; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13030270 - 09 Mar 2022
Cited by 3 | Viewed by 1980
Abstract
Insects detect volatile chemosignals with olfactory sensory neurons (OSNs) that express olfactory receptors. Among them, the most sensitive receptors are the odorant receptors (ORs), which form cation channels passing Ca2+. OSNs expressing different groups of ORs show varying optimal odor concentration [...] Read more.
Insects detect volatile chemosignals with olfactory sensory neurons (OSNs) that express olfactory receptors. Among them, the most sensitive receptors are the odorant receptors (ORs), which form cation channels passing Ca2+. OSNs expressing different groups of ORs show varying optimal odor concentration ranges according to environmental needs. Certain types of OSNs, usually attuned to high odor concentrations, allow for the detection of even low signals through the process of sensitization. By increasing the sensitivity of OSNs upon repetitive subthreshold odor stimulation, Drosophila melanogaster can detect even faint and turbulent odor traces during flight. While the influx of extracellular Ca2+ has been previously shown to be a cue for sensitization, our study investigates the importance of intracellular Ca2+ management. Using an open antenna preparation that allows observation and pharmacological manipulation of OSNs, we performed Ca2+ imaging to determine the role of Ca2+ storage in mitochondria. By disturbing the mitochondrial resting potential and induction of the mitochondrial permeability transition pore (mPTP), we show that effective storage of Ca2+ in the mitochondria is vital for sensitization to occur, and release of Ca2+ from the mitochondria to the cytoplasm promptly abolishes sensitization. Our study shows the importance of cellular Ca2+ management for sensitization in an effort to better understand the underlying mechanics of OSN modulation. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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10 pages, 2015 KiB  
Article
Aphid Odorant-Binding Protein 9 Is Narrowly Tuned to Linear Alcohols and Aldehydes of Sixteen Carbon Atoms
by Chiara D’Onofrio, Wolfgang Knoll and Paolo Pelosi
Insects 2021, 12(8), 741; https://0-doi-org.brum.beds.ac.uk/10.3390/insects12080741 - 18 Aug 2021
Cited by 9 | Viewed by 2426
Abstract
Aphid odorant-binding protein 9 is almost exclusively expressed in antennae and is well conserved between different aphid species. In order to investigate its function, we have expressed this protein and measured ligand-binding affinities to a number of common natural compounds. The best ligands [...] Read more.
Aphid odorant-binding protein 9 is almost exclusively expressed in antennae and is well conserved between different aphid species. In order to investigate its function, we have expressed this protein and measured ligand-binding affinities to a number of common natural compounds. The best ligands are long-chain aldehydes and alcohols, in particular Z9-hexadecenal and Z11-hexadecenal, as well as 1-hexadecanol and Z11-1-hexadecenol. A model of this protein indicated Lys37 as the residue that is likely to establish strong interactions with the ligands, probably a Schiff base with aldehydes and a hydrogen bond with alcohols. Indeed, when we replaced this lysine with a leucine, the mutated protein lost its affinity to both long aldehydes and alcohols, while the binding of other volatiles was unaffected. Long-chain linear alcohols are common products of molds and have been reported as aphid antifeedants. Corresponding aldehydes, instead, are major components of sex pheromones for several species of Lepidoptera. We speculate that aphids might use OBP9 to avoid mold-contaminated plants as well as competition with lepidopteran larvae. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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16 pages, 3557 KiB  
Article
Evidence of the Involvement of a Plus-C Odorant-Binding Protein HparOBP14 in Host Plant Selection and Oviposition of the Scarab Beetle Holotrichia parallela
by Yafei Qu, Xiangyu Liu, Xu Zhao, Jianhui Qin, Yazhong Cao, Kebin Li, Jing-Jiang Zhou, Senshan Wang and Jiao Yin
Insects 2021, 12(5), 430; https://0-doi-org.brum.beds.ac.uk/10.3390/insects12050430 - 10 May 2021
Cited by 5 | Viewed by 2036
Abstract
Holotrichia parallela is one of the agriculturally important scarab beetle pests in China. In this study, HparOBP14 was cloned, which is the most abundantly expressed among the OBP genes in the legs of female H. parallela adults. Sequence comparison and phylogenetic analysis showed [...] Read more.
Holotrichia parallela is one of the agriculturally important scarab beetle pests in China. In this study, HparOBP14 was cloned, which is the most abundantly expressed among the OBP genes in the legs of female H. parallela adults. Sequence comparison and phylogenetic analysis showed that HparOBP14 has a Plus-C structure motif. The expression profile analysis revealed that HparOBP14 expression was the highest in the female antennae and then in the legs. The fluorescence competitive binding experiment of the recombinant HparOBP14 protein showed that HparOBP14 had an affinity with 6-methyl-5-heptene-2-one (plant volatile), 3-methylindole, p-cymene, methanol, formaldehyde, α-pinene, and geraniol (organic fertilizer volatile). Knockdown HparOBP14 expression decreased significantly the EAG response of the injected female adults to p-cymene, methanol, formaldehyde, α-pinene, and geraniol. Similarly, the injected female adults were significantly less attracted to geraniol and methanol. Therefore, HparOBP14 might bind organic matter volatiles during oviposition. These results are not only helpful to analyze the olfactory recognition mechanism of female adult H. parallela when choosing suitable oviposition sites, but also to provide target genes for green prevention and control of H. parallela in the future. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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Review

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20 pages, 1917 KiB  
Review
Olfactory Strategies in the Defensive Behaviour of Insects
by Kavitha Kannan, C. Giovanni Galizia and Morgane Nouvian
Insects 2022, 13(5), 470; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13050470 - 18 May 2022
Cited by 11 | Viewed by 6303
Abstract
Most animals must defend themselves in order to survive. Defensive behaviour includes detecting predators or intruders, avoiding them by staying low-key or escaping or deterring them away by means of aggressive behaviour, i.e., attacking them. Responses vary across insect species, ranging from individual [...] Read more.
Most animals must defend themselves in order to survive. Defensive behaviour includes detecting predators or intruders, avoiding them by staying low-key or escaping or deterring them away by means of aggressive behaviour, i.e., attacking them. Responses vary across insect species, ranging from individual responses to coordinated group attacks in group-living species. Among different modalities of sensory perception, insects predominantly use the sense of smell to detect predators, intruders, and other threats. Furthermore, social insects, such as honeybees and ants, communicate about danger by means of alarm pheromones. In this review, we focus on how olfaction is put to use by insects in defensive behaviour. We review the knowledge of how chemical signals such as the alarm pheromone are processed in the insect brain. We further discuss future studies for understanding defensive behaviour and the role of olfaction. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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20 pages, 17002 KiB  
Review
Enantiomeric Discrimination in Insects: The Role of OBPs and ORs
by Cassie Sims, Michael A. Birkett and David M. Withall
Insects 2022, 13(4), 368; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13040368 - 08 Apr 2022
Cited by 12 | Viewed by 2929
Abstract
Olfaction is a complex recognition process that is critical for chemical communication in insects. Though some insect species are capable of discrimination between compounds that are structurally similar, little is understood about how this high level of discrimination arises. Some insects rely on [...] Read more.
Olfaction is a complex recognition process that is critical for chemical communication in insects. Though some insect species are capable of discrimination between compounds that are structurally similar, little is understood about how this high level of discrimination arises. Some insects rely on discriminating between enantiomers of a compound, demonstrating an ability for highly selective recognition. The role of two major peripheral olfactory proteins in insect olfaction, i.e., odorant-binding proteins (OBPs) and odorant receptors (ORs) has been extensively studied. OBPs and ORs have variable discrimination capabilities, with some found to display highly specialized binding capability, whilst others exhibit promiscuous binding activity. A deeper understanding of how odorant-protein interactions induce a response in an insect relies on further analysis such as structural studies. In this review, we explore the potential role of OBPs and ORs in highly specific recognition, specifically enantiomeric discrimination. We summarize the state of research into OBP and OR function and focus on reported examples in the literature of clear enantiomeric discrimination by these proteins. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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12 pages, 1154 KiB  
Review
Time-Dependent Odorant Sensitivity Modulation in Insects
by Hao Guo and Dean P. Smith
Insects 2022, 13(4), 354; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13040354 - 02 Apr 2022
Cited by 4 | Viewed by 2454
Abstract
Insects use olfaction to detect ecologically relevant chemicals in their environment. To maintain useful responses over a variety of stimuli, olfactory receptor neurons are desensitized to prolonged or high concentrations of stimuli. Depending on the timescale, the desensitization is classified as short-term, which [...] Read more.
Insects use olfaction to detect ecologically relevant chemicals in their environment. To maintain useful responses over a variety of stimuli, olfactory receptor neurons are desensitized to prolonged or high concentrations of stimuli. Depending on the timescale, the desensitization is classified as short-term, which typically spans a few seconds; or long-term, which spans from minutes to hours. Compared with the well-studied mechanisms of desensitization in vertebrate olfactory neurons, the mechanisms underlying invertebrate olfactory sensitivity regulation remain poorly understood. Recently, using a large-scale functional screen, a conserved critical receptor phosphorylation site has been identified in the model insect Drosophila melanogaster, providing new insight into the molecular basis of desensitization in insects. Here, we summarize the progress in this area and provide perspectives on future directions to determine the molecular mechanisms that orchestrate the desensitization in insect olfaction. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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21 pages, 620 KiB  
Review
Multimodal Information Processing and Associative Learning in the Insect Brain
by Devasena Thiagarajan and Silke Sachse
Insects 2022, 13(4), 332; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13040332 - 28 Mar 2022
Cited by 10 | Viewed by 4757
Abstract
The study of sensory systems in insects has a long-spanning history of almost an entire century. Olfaction, vision, and gustation are thoroughly researched in several robust insect models and new discoveries are made every day on the more elusive thermo- and mechano-sensory systems. [...] Read more.
The study of sensory systems in insects has a long-spanning history of almost an entire century. Olfaction, vision, and gustation are thoroughly researched in several robust insect models and new discoveries are made every day on the more elusive thermo- and mechano-sensory systems. Few specialized senses such as hygro- and magneto-reception are also identified in some insects. In light of recent advancements in the scientific investigation of insect behavior, it is not only important to study sensory modalities individually, but also as a combination of multimodal inputs. This is of particular significance, as a combinatorial approach to study sensory behaviors mimics the real-time environment of an insect with a wide spectrum of information available to it. As a fascinating field that is recently gaining new insight, multimodal integration in insects serves as a fundamental basis to understand complex insect behaviors including, but not limited to navigation, foraging, learning, and memory. In this review, we have summarized various studies that investigated sensory integration across modalities, with emphasis on three insect models (honeybees, ants and flies), their behaviors, and the corresponding neuronal underpinnings. Full article
(This article belongs to the Special Issue Recent Advances in Physiology of Insect Olfaction)
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