Analysis of natural variation reveals neurogenetic networks for<i>Drosophila</i>olfactory behavior

Swarup, Shilpa; Huang, Wen; Mackay, Trudy F. C.; Anholt, Robert R. H.

doi:10.1073/pnas.1220168110

Cited by 97 publications

(114 citation statements)

References 55 publications

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“…One interpretation of our results is that the ORN expressing Or42b, which is activated by acetal, and the ORN expressing Or33b, which is activated by 2,5-dimethylpyrazine, do not belong to a single equivalence class; that is, they may play distinguishable roles in driving olfactory behavior. Although our results support a model in which many ORNs can activate an attraction response, their connectivity may not be functionally identical (43). Different ORNs may contribute differently to the modulation of the runs and turns of navigation behavior or to feeding decisions.…”

Section: Discussioncontrasting

confidence: 87%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

107

184

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The ability of an animal to detect, discriminate, and respond to odors depends on the function of its olfactory receptor neurons (ORNs), which in turn depends ultimately on odorant receptors. To understand the diverse mechanisms used by an animal in olfactory coding and computation, it is essential to understand the functional diversity of its odor receptors. The larval olfactory system of Drosophila melanogaster contains 21 ORNs and a comparable number of odorant receptors whose properties have been examined in only a limited way. We systematically screened them with a panel of ∼500 odorants, yielding >10,000 receptor-odorant combinations. We identify for each of 19 receptors an odorant that excites it strongly. The responses elicited by each of these odorants are analyzed in detail. The odorants elicited little cross-activation of other receptors at the test concentration; thus, low concentrations of many of these odorants in nature may be signaled by a single ORN. The receptors differed dramatically in sensitivity to their cognate odorants. The responses showed diverse temporal dynamics, with some odorants eliciting supersustained responses. An intriguing question in the field concerns the roles of different ORNs and receptors in driving behavior. We found that the cognate odorants elicited behavioral responses that varied across a broad range. Some odorants elicited strong physiological responses but weak behavioral responses or weak physiological responses but strong behavioral responses.T he olfactory system of the Drosophila larva achieves remarkable function with minimal structure. It detects and responds to spatial and temporal gradients of odorants, transforming chemical information into navigation via an elegant repertoire of head sweeps, runs, and turns (1-3). Its sophisticated function is based on the activities of 21 olfactory receptor neurons (ORNs), which innervate the dorsal organ of the head and send axons to the antennal lobe of the brain (4). The activities of the ORNs are in turn based on the responses of odor receptors (Ors). Thus, to understand the molecular basis of larval olfactory navigation, it is necessary to understand the function of the receptors.ORNs together express 25 members of the Or family of odor receptors and the Orco coreceptor (5-8). In each ORN, an Or and Orco together form a ligand-gated ion channel (9-11). Most ORNs express a single Or, although one ORN coexpresses Or94a and Or94b and another ORN coexpresses Or33b and Or47a (7). The significance of this coexpression remains speculative, but the response profiles of some coexpressed adult Ors are additive (12).The responses of the larval Or repertoire to a limited odorant panel was previously examined in an in vivo expression system known as the empty neuron system (8, 13). With the use of this system, 21 of the larval Ors were found to be functional. However, studies of the larval Or repertoire have been limited not only in the number of odorants examined, but also in their consideration of receptor sensitivity, tempor...

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Section: Discussioncontrasting

confidence: 87%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

107

184

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“…To test this, we generated various Drosophila flies with mutations in PKC genes rather than in Orco itself. PKC53E and PKCδ are genes that could be involved in OSN signal transduction (Swarup et al, 2013;Arya et al, 2015). Here, we found that null mutations of both conventional PKC53E and novel PKCδ or suppression of PKC53E and PKCδ genes using RNAi shifted the concentration-response of the OSNs to higher odour concentrations compared with wild-type (P<0.05; Fig.…”

Section: Pkc Increases Osn Sensitivity To Brief and Intermittent Odoumentioning

confidence: 67%

“…Insect olfactory systems express diverse calcium-and cyclic nucleotide-activated kinases (Schaeffer et al, 1989;Chintapalli et al, 2007;Tunstall et al, 2012), yet any role in signal transduction is unknown. Members of the protein kinase C family (PKCs), in particular, are network genes found to play a role in insect signal transduction, neural connectivity and natural variation in olfactory behaviour (Swarup et al, 2013;Arya et al, 2015). Here, we propose that PKC-mediated intracellular signalling in the recently evolved ORs offers a mechanistic advantage to detect and respond to the brief and intermittent odour information received while tracking plume information in flight.…”

Section: Introductionmentioning

confidence: 99%

Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

Getahun

Thoma

Lavista-Llanos

et al. 2016

Journal of Experimental Biology

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Flying insects are well known for airborne odour tracking and have evolved diverse chemoreceptors. While ionotropic receptors (IRs) are found across protostomes, insect odorant receptors (ORs) have only been identified in winged insects. We therefore hypothesized that the unique signal transduction of ORs offers an advantage for odour localization in flight. Using Drosophila, we found expression and increased activity of the intracellular signalling protein PKC in antennal sensilla following odour stimulation. Odour stimulation also enhanced phosphorylation of the OR co-receptor Orco in vitro, while site-directed mutation of Orco or mutations in PKC subtypes reduced the sensitivity and dynamic range of OR-expressing neurons in vivo, but not IR-expressing neurons. We ultimately show that these mutations reduce competence for odour localization of flies in flight. We conclude that intracellular regulation of OR sensitivity is necessary for efficient odour localization, which suggests a mechanistic advantage for the evolution of the OR complex in flying insects.

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“…The effects of Drosophila mutations (33) and natural variants (37) on aggression depend on genetic background, a phenomenon also observed for mutations in neuronal nitric oxide synthase (38) and Nr2e1 (16) in mice. Analysis of naturally segregating variation can leverage polymorphisms at many loci to explore the contribution of epistatic interactions to genetic variation for complex traits (39)(40)(41).…”

mentioning

confidence: 99%

Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior

Shorter

Couch

Huang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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130

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Aggression is an evolutionarily conserved complex behavior essential for survival and the organization of social hierarchies. With the exception of genetic variants associated with bioamine signaling, which have been implicated in aggression in many species, the genetic basis of natural variation in aggression is largely unknown. Drosophila melanogaster is a favorable model system for exploring the genetic basis of natural variation in aggression. Here, we performed genome-wide association analyses using the inbred, sequenced lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and replicate advanced intercross populations derived from the most and least aggressive DGRP lines. We identified genes that have been previously implicated in aggressive behavior as well as many novel loci, including gustatory receptor 63a (Gr63a), which encodes a subunit of the receptor for CO 2 , and genes associated with development and function of the nervous system. Although genes from the two association analyses were largely nonoverlapping, they mapped onto a genetic interaction network inferred from an analysis of pairwise epistasis in the DGRP. We used mutations and RNAi knock-down alleles to functionally validate 79% of the candidate genes and 75% of the candidate epistatic interactions tested. Epistasis for aggressive behavior causes cryptic genetic variation in the DGRP that is revealed by changing allele frequencies in the outbred populations derived from extreme DGRP lines. This phenomenon may pertain to other fitness traits and species, with implications for evolution, applied breeding, and human genetics.Drosophila Genetic Reference Panel | genome-wide association mapping | extreme QTL mapping | advanced intercross population | epistasis A ggression is a near-universal animal behavior, important for securing food resources, defense against predators, gaining access to mating partners and, among social animals, creating and maintaining dominance hierarchies. Aggressive behavior is a typical quantitative trait, with natural variation attributable to segregating variants at multiple interacting loci, the effects of which are sensitive to the physical and social environments to which the individuals are exposed (1). Sociopathic and violent behaviors place a significant socioeconomic burden on human societies. However, disentangling the relative genetic and environmental contributions to aggressive behavior in natural populations is challenging due to its low heritability, and, in humans, because of the difficulty in accounting for social and other environmental influences, precisely quantifying aggression, and comorbidity with other psychological disorders.These challenges can be overcome using animal models. Numerous studies have highlighted the evolutionary conservation of neural pathways affecting aggression (2-4). Genes affecting bioamine signaling affect aggressive behavior in humans (4, 5), mice (6-8), and Drosophila (9-15). The nuclear receptor subfamily 2, group E, member 1 gene Nr2e1 affects aggressiv...

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Analysis of natural variation reveals neurogenetic networks forDrosophilaolfactory behavior

Cited by 97 publications

References 55 publications

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior

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