Ionotropic Receptors Mediate Drosophila Oviposition Preference through Sour Gustatory Receptor Neurons

Abstract

Summary Carboxylic acids are present in many foods, being especially abundant in fruits. Yet, relatively little is known about how acids are detected by the gustatory systems, whether they have a potential role in nutrition or provide other health benefits. Here, we identify sour gustatory receptor neurons (GRNs) in tarsal taste sensilla of Drosophila melanogaster. We find that most tarsal sensilla harbor a sour GRN that is specifically activated by carboxylic and mineral acids, but does not respond to sweet and bitter-tasting chemicals or salt. One pair of taste sensilla features two GRNs that respond only to a subset of carboxylic acids and high concentrations of salt. All sour GRNs prominently express two Ionotropic Receptor (IR) genes, IR76b and IR25a, and we show that both these genes are necessary for the detection of acids. Furthermore, we establish that IR25a and IR76b are essential in sour GRNs of females for oviposition preference on acid containing food. Our investigations reveal that acids activate a unique set of taste cells largely dedicated to sour taste, and they indicate that both pH/proton concentration and the structure of carboxylic acids contribute to sour GRN activation. Together, our studies provide new insights into the cellular and molecular basis of sour taste.

The olfactory co-receptor IR8a governs larval-frass mediated competition avoidance in a hawkmoth

“…One gram of frass from caterpillars raised on either D. wrightii or N. attenuata were put into a 500-mL plastic container. A circular filter paper (diameter: 12 mm Whatman, Sigma-Aldrich USA) loaded with 10 µL of diluted bromodecane (1:10 4 in hexane) was used as an internal standard. Through a hole in the lid of the container, a SPME fiber (50 µm Divinylbenzene / Carboxen / Polydimethylsiloxane coating; Supelco) was exposed to the container headspace for 30 min at room temperature without agitation, and then introduced into the injector inlet for 2 min at 250°C in split-less mode.…”

“…Therefore, gravid females must carefully examine the environment prior to selecting the oviposition site. For this, they utilize visual 1, 2 , gustatory 3, 4 , mechanosensory 5 , as well as olfactory 6, 7 cues. Among these modalities, olfaction plays a pivotal role in an insect’s life, as it provides information not only about oviposition sites but also about other biologically relevant resources such as food and mating partners 8 .…”

In vivo assembly and trafficking of olfactory Ionotropic Receptors

“…Moreover, transcriptomic and in situ expression analyses in a range of animals indicate that Ir genes are expressed in peripheral, rather than central, neurons [5][6][7][8][9]. Functional analyses of IRs, in particular in Drosophila melanogaster, have shown that these receptors have diverse roles in environmental sensing, including in olfaction [6,[10][11][12], gustation [13][14][15][16][17][18][19][20][21], hygrosensation [22][23][24] and thermosensation [25,26].…”

Dedicated acetic acid preference coded by broad spectrum ionotropic receptors in a moth species

“…Many of these compounds are acids, which exist widely in nature as common products of plants [5,6]. In Drosophila , acetic acid is sensed to assess food, oviposition medium, and mating [7–10]. Many other insect species, including armyworms, can be trapped by acetic acid-containing lures [11–15].…”

“…Furthermore, Ir75a is also used by D. melanogaster and D. sechellia to smell acetic acid and propionic acid [29,30]. Ir76b mediates oviposition preference in female Drosophila by sensing acetic acid and citric acid through gustatory reception [10]. Meanwhile, reports on lepidopteran species have also revealed glomeruli based coding for feeding behaviors which were elicited by acidity components [31].…”