Farnesol-detecting olfactory neurons in Drosophila.
ABSTRACT We set out to deorphanize a subset of putative Drosophila odorant receptors expressed in trichoid sensilla using a transgenic in vivo misexpression approach. We identified farnesol as a potent and specific activator for the orphan odorant receptor Or83c. Farnesol is an intermediate in juvenile hormone biosynthesis, but is also produced by ripe citrus fruit peels. Here, we show that farnesol stimulates robust activation of Or83c-expressing olfactory neurons, even at high dilutions. The CD36 homolog Snmp1 is required for normal farnesol response kinetics. The neurons expressing Or83c are found in a subset of poorly characterized intermediate sensilla. We show that these neurons mediate attraction behavior to low concentrations of farnesol and that Or83c receptor mutants are defective for this behavior. Or83c neurons innervate the DC3 glomerulus in the antennal lobe and projection neurons relaying information from this glomerulus to higher brain centers target a region of the lateral horn previously implicated in pheromone perception. Our findings identify a sensitive, narrowly tuned receptor that mediates attraction behavior to farnesol and demonstrates an effective approach to deorphanizing odorant receptors expressed in neurons located in intermediate and trichoid sensilla that may not function in the classical "empty basiconic neuron" system.
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ABSTRACT: Dietary antioxidants play an important role in preventing oxidative stress. Whether animals in search of food or brood sites are able to judge the antioxidant content, and if so actively seek out resources with enriched antioxidant content, remains unclear. We show here that the vinegar fly Drosophila melanogaster detects the presence of hydroxycinnamic acids (HCAs)-potent dietary antioxidants abundant in fruit-via olfactory cues. Flies are unable to smell HCAs directly but are equipped with dedicated olfactory sensory neurons detecting yeast-produced ethylphenols that are exclusively derived from HCAs. These neurons are housed on the maxillary palps, express the odorant receptor Or71a, and are necessary and sufficient for proxy detection of HCAs. Activation of these neurons in adult flies induces positive chemotaxis, oviposition, and increased feeding. We further demonstrate that fly larvae also seek out yeast enriched with HCAs and that larvae use the same ethylphenol cues as the adults but rely for detection upon a larval unique odorant receptor (Or94b), which is co-expressed with a receptor (Or94a) detecting a general yeast volatile. We also show that the ethylphenols act as reliable cues for the presence of dietary antioxidants, as these volatiles are produced-upon supplementation of HCAs-by a wide range of yeasts known to be consumed by flies. For flies, dietary antioxidants are presumably important to counteract acute oxidative stress induced by consumption or by infection by entomopathogenic microorganisms. The ethylphenol pathway described here adds another layer to the fly's defensive arsenal against toxic microbes. Copyright © 2015 Elsevier Ltd. All rights reserved.Current biology : CB. 01/2015;
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ABSTRACT: Many insect vectors of disease detect their hosts through olfactory cues, and thus it is of great interest to understand better how odors are encoded. However, little is known about the molecular underpinnings that support the unique function of coeloconic sensilla, an ancient and conserved class of sensilla that detect amines and acids, including components of human odor that are cues for many insect vectors. Here, we generate antennal transcriptome databases both for wild type Drosophila and for a mutant that lacks coeloconic sensilla. We use these resources to identify genes whose expression is highly enriched in coeloconic sensilla, including many genes not previously implicated in olfaction. Among them, we identify an ammonium transporter gene that is essential for ammonia responses in a class of coeloconic olfactory receptor neurons (ORNs), but is not required for responses to other odorants. Surprisingly, the transporter is not expressed in ORNs, but rather in neighboring auxiliary cells. Thus, our data reveal an unexpected non-cell autonomous role for a component that is essential to the olfactory response to ammonia. The defective response observed in a Drosophila mutant of this gene is rescued by its Anopheles ortholog, and orthologs are found in virtually all insect species examined, suggesting that its role is conserved. Taken together, our results provide a quantitative analysis of gene expression in the primary olfactory organ of Drosophila, identify molecular components of an ancient class of olfactory sensilla, and reveal that auxiliary cells, and not simply ORNs, play an essential role in the coding of an odor that is a critical host cue for many insect vectors of human disease.PLoS Genetics 11/2014; 10(11):e1004810. · 8.17 Impact Factor
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ABSTRACT: Most naturally occurring olfactory signals do not consist of monomolecular odorants but, rather, are mixtures whose composition and concentration ratios vary. While there is ample evidence for the relevance of complex odor blends in ecological interactions and for interactions of chemicals in both peripheral and central neuronal processing, a fine-scale analysis of rules governing the innate behavioral responses of Drosophila melanogaster towards odor mixtures is lacking. In this study we examine whether the innate valence of odors is conserved in binary odor mixtures. We show that binary mixtures of attractants are more attractive than individual mixture constituents. In contrast, mixing attractants with repellents elicits responses which are lower than the responses towards the corresponding attractants. This decrease in attraction is repellent-specific, independent of the identity of the attractant and more stereotyped across individuals than responses towards the repellent alone. Mixtures of repellents are either less attractive than the individual mixture constituents or these mixtures represent an intermediate. Within the limits of our data set, most mixture responses are quantitatively predictable on the basis of constituent responses. In summary, the valence of binary odor mixtures is predictable on the basis of valences of mixture constituents. Our findings will further our understanding of innate behavior towards ecologically relevant odor blends and will serve as a powerful tool for deciphering the olfactory valence code.Journal of Experimental Biology 09/2014; · 3.00 Impact Factor