Olfactory Neurons and Brain Centers Directing Oviposition Decisions in Drosophila

Chin, Sonia G.; Maguire, Sarah E.; Huoviala, Paavo; Jefferis, Gregory S.X.E.; Potter, Christopher J.

doi:10.1016/j.celrep.2018.07.018

Cited by 49 publications

(45 citation statements)

References 73 publications

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“…Strikingly, the innervation patterns of the projection neurons downstream of olfactory neurons detecting the aversive odors geosmin and iridomyrmecin overlap strongly and target the same regions of the mushroom body calyx and lateral horn (Ebrahim et al, 2015a;Huoviala et al, 2018). Furthermore, additional projection neurons downstream of olfactory sensory neurons involved in oviposition also send some axonal segments to the same ventral-posterior region of the lateral horn (Chin et al, 2018).…”

Section: Oviposition Decisions Are Complex Context-dependent Sensorymentioning

confidence: 96%

A short guide to insect oviposition: when, where and how to lay an egg

Cury

Prud’homme

Gompel

2019

Journal of Neurogenetics

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Egg-laying behavior is one of the most important aspects of female behavior, and has a profound impact on the fitness of a species. As such, it is controlled by several layers of regulation. Here, we review recent advances in our understanding of insect neural circuits that control when, where and how to lay an egg. We also outline outstanding open questions about the control of egg-laying decisions, and speculate on the possible neural underpinnings that can drive the diversification of oviposition behaviors through evolution.

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Section: Oviposition Decisions Are Complex Context-dependent Sensorymentioning

confidence: 96%

A short guide to insect oviposition: when, where and how to lay an egg

Cury

Prud’homme

Gompel

2019

Journal of Neurogenetics

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“…Physiology. To activate Orco-positive ORNs in the presence of human odor, we used 'olfactogenetics,' a technique whereby a specific volatile odorant is used to activate a defined set of OR-expressing neurons (14). To accomplish this, an Or with known response properties is ectopically expressed in ORNs of interest through the use of a binary expression system, such as the Q-system (15) or the UAS-Gal4 system.…”

Section: Ectopically Expressing Agor2 In Orco-positive Neurons Impairmentioning

confidence: 99%

“…Ectopically expressing an Or in Drosophila ORNs causes the expressing neuron to activate in the presence of the introduced OR's odor ligand (14,16,(18)(19)(20). One possibility as to why Orco>AgOr2 cells in the mosquito did not respond to benzaldehyde or indole was because the AgOr2 sequence used to create the transgenic QUAS-AgOr2 line was perhaps acting in a dominant-negative manner to disrupt ORCO/OR X ion channels.…”

Section: Olfactogenetics Impairs Anopheles But Not Drosophila Orco-pomentioning

confidence: 99%

A Feedback Mechanism RegulatesOdorant ReceptorExpression in the Malaria Mosquito,Anopheles gambiae

Maguire

Afify

Goff

et al. 2020

Preprint

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Mosquitoes locate and approach humans (‘host-seek’) when specific Olfactory Neurons (ORNs) in the olfactory periphery activate a specific combination of glomeruli in the mosquito Antennal Lobe (AL). We hypothesize that dysregulating proper glomerular activation in the presence of human odor will prevent host-seeking behavior. In experiments aimed at ectopically activating most ORNs in the presence of human odor, we made a surprising finding: ectopic expression of an AgOr (AgOr2) in Anopheles gambiae ORNs dampens the activity of the expressing neuron. This contrasts studies in Drosophila melanogaster, the typical insect model of olfaction, in which ectopic expression of non-native ORs in ORNs confers ectopic neuronal responses without interfering with native olfactory physiology. To gain insight into this dysfunction in mosquitoes, RNA-seq analyses were performed comparing wild-type antennae to those ectopically expressing AgOr2 in ORNs. Remarkably, almost all Or transcripts were significantly downregulated (except for AgOr2), and additional experiments suggest that it is AgOR2 protein rather than mRNA that mediates this downregulation. Our study shows that ORNs of Anopheles mosquitoes (in contrast to Drosophila) employ a currently unexplored regulatory mechanism of OR expression, which may be adaptable as a vector-control strategy.SIGNIFICANCE STATEMENTStudies in Drosophila melanogaster suggest that insect Olfactory Receptor Neurons (ORNs) do not contain mechanisms by which Odorant Receptors (ORs) regulate OR expression. This has proved useful in studies where ectopic expression of an OR in Drosophila ORNs confers responses to the odorants that activate the newly expressed OR. In experiments in Anopheles gambiae mosquitoes, we found that ectopic expression of an OR in most Anopheles ORNs dampened the activity of the expressing neurons. RNA-seq analyses demonstrated that ectopic OR expression in Anopheles ORNs leads to downregulation of endogenous Or transcripts. Additional experiments suggest that this downregulation required ectopic expression of a functional OR protein. These findings reveal that Anopheles mosquitoes, in contrast to Drosophila, contain a feedback mechanism to regulate OR expression. Mosquito ORNs might employ regulatory mechanisms of OR expression previously thought to occur only in non-insect olfactory systems.

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“…Of these receptors, homologs of Or67d detect the Drosophila pheromone 11-cis-vaccenyl acetate (27) and likely function in intraspecific communication in Scaptomyza, Or63a is only expressed in larvae (28), and the Or98a-like genes found in Scaptomyza have no D. melanogaster homologs and are functionally uncharacterized. In contrast, Or67b is expressed in adults and modulates oviposition behavior (29), suggesting that it is a good candidate for further study. In a previous study, branch-site tests were also consistent with episodic positive selection acting on Or67b paralogs from S. flava (19).…”

Section: Phylogenetic Analysis Identified Or67b Paralogs As Candidatementioning

confidence: 99%

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Matsunaga

Reisenman

Goldman-Huertas

et al. 2019

Preprint

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248): 21 Plant toxins are effective defenses because they are aversive to most insects. The same 22 molecules, however, are co-opted as host-finding cues by specialist herbivores. Although such 23 behavioral shifts are central to our understanding of herbivorous insect diversification, it is not 24 well understood how these behaviors evolve. We addressed this in Scaptomyza flava, a 25 herbivorous drosophilid fly within a lineage that shifted to feeding on toxic mustard plants 26 (Brassicales) less than 10 million years ago. S flava lost the ancestral attraction to yeast volatiles 27 and the attendant chemoreceptors used to detect these odors. Here we report that S. flava, but not 28 its close microbe-feeding relatives Drosophila melanogaster and S. pallida, is attracted to 29 mustard host-plant odors, including volatile mustard oils (isothiocyanates or ITCs). Our genomic 30 analysis uncovered three S. flava paralogs of an olfactory receptor gene (Or67b) that likely 31 experienced recent positive selection. We then tested whether these chemoreceptors could 32 underlie the observed attraction to volatile ITCs. Our in vivo recordings revealed that two of the 33 S. flava Or67b proteins (Or67b1 and Or67b3) -but not the homologous Ors from microbe-34 feeding relatives -responded selectively and sensitively to volatile ITCs. These Ors are the first 35 ITC chemoreceptors other than TRP channel family (e.g., the TrpA1 'wasabi' receptor) known 36 from any animal. Remarkably, S. flava Or67b3 was sufficient to drive olfactory attraction toward 37 butyl ITC when expressed in an attractive olfactory circuit. Our study illuminates that ancestrally 38 aversive chemicals can be co-opted as attractants through gene duplication, leading to the origin 39 of hedonic valence shifts in herbivorous insects. 40 41 42Significance Statement (120) 43 Plant toxins trigger aversive olfactory (volatile-mediated) and gustatory (contact-mediated) 44 responses in animals. Paradoxically, toxic plants are often colonized by specialist insects that co-45 opt these toxins as host-plant finding cues. The mechanisms underlying these behavioral shifts, 46 from indifference or repulsion to plant chemicals, to attraction, remain unclear. To address this, 47 we used a fly lineage, Scaptomyza, that switched from yeast-feeding to feeding on mustard plants 48 less than 10 million years ago. We found that S. flava is attracted to mustard-plant odors and 49 volatile mustard oils (isothiocyanates or ITCs) such as 'wasabi', a behavior enabled by the 50 evolution of genes encoding odorant receptors highly sensitive to ITCs. Our study illuminates 51 how insects colonize toxic host plants through duplication and ecological repurposing of genes 52 encoding pre-existing chemoreceptors. 53 54 55 56 57 Many plant compounds used in food, agriculture and medicine originally evolved as 58 toxins that deter and repel enemies (1). Among the most well-known compounds are those 59 reactive electrophiles that induce the sensation of pain, such as diallyl disulfide a...

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Olfactory Neurons and Brain Centers Directing Oviposition Decisions in Drosophila

Cited by 49 publications

References 73 publications

A short guide to insect oviposition: when, where and how to lay an egg

A short guide to insect oviposition: when, where and how to lay an egg

A Feedback Mechanism RegulatesOdorant ReceptorExpression in the Malaria Mosquito,Anopheles gambiae

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

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