Acid sensing by sweet and bitter taste neurons in Drosophila melanogaster

Charlu, Sandhya; Wisotsky, Zev; Medina, Adriana; Dahanukar, Anupama

doi:10.1038/ncomms3042

Cited by 76 publications

(119 citation statements)

References 53 publications

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“…For example, bitter chemicals inhibit sugar detection in insects of different groups (Morita, 1959;Dethier, 1980Dethier, , 1987Schoonhoven, 1982;Dethier andBowdan, 1989, 1992;Chapman et al, 1991;Schoonhoven and Liner, 1994), including Drosophila (Meunier et al, 2003a; Lee et al, , 2012Sellier and Marion-Poll, 2011;Jeong et al, 2013) in which other interactions were described recently, such as between sugars and acids (Charlu et al, 2013;Chen and Amrein, 2014). Whereas the molecular basis of bitter suppression of sugar detection is still under scrutiny and may involve odorant binding proteins (OBPs;Jeong et al, 2013;Swarup et al, 2014), the behavioral role of such interactions have been considered rarely (König et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Dual Mechanism for Bitter Avoidance inDrosophila

et al. 2015

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In flies and humans, bitter chemicals are known to inhibit sugar detection, but the adaptive role of this inhibition is often overlooked. At best, this inhibition is described as contributing to the rejection of potentially toxic food, but no studies have addressed the relative importance of the direct pathway that involves activating bitter-sensitive cells versus the indirect pathway represented by the inhibition of sugar detection. Using toxins to selectively ablate or inactivate populations of bitter-sensitive cells, we assessed the behavioral responses of flies to sucrose mixed with strychnine (which activates bitter-sensitive cells and inhibits sugar detection) or with L-canavanine (which only activates bitter-sensitive cells). As expected, flies with ablated bitter-sensitive cells failed to detect L-canavanine mixed with sucrose in three different feeding assays (proboscis extension responses, capillary feeding, and two-choice assays). However, such flies were still able to avoid strychnine mixed with sucrose. By means of electrophysiological recordings, we established that bitter molecules differ in their potency to inhibit sucrose detection and that sugar-sensing inhibition affects taste cells on the proboscis and the legs. The optogenetic response of sugar-sensitive cells was not reduced by strychnine, thus suggesting that this inhibition is linked directly to sugar transduction. We postulate that sugar-sensing inhibition represents a mechanism in insects to prevent ingesting harmful substances occurring within mixtures.

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Section: Introductionmentioning

confidence: 99%

Dual Mechanism for Bitter Avoidance inDrosophila

et al. 2015

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“…Each GRN can express several different types of receptors, each sensitive to different tastant chemicals (Liman et al, 2014). In Drosophila, GRNs have been shown to respond to only some, but not all, tastants drawn from a basic taste category (Dahanukar et al, 2007;Weiss et al, 2011;Miyamoto et al, 2012), as well as to some, but not all, tastants from multiple categories (Wisotsky et al, 2011;Charlu et al, 2013;Jeong et al, 2013;Masek and Keene, 2013). Further, many GRNs respond to chemicals not readily associated with any of the basic tastes, such as fatty acids (Cartoni et al, 2010;Masek and Keene, 2013), carbon dioxide , water (Cameron et al, 2010), and contact pheromones (Lacaille et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…To date, studies of gustatory coding in both insects and vertebrates have nearly always been interpreted in terms of basic tastes (Caicedo and Roper, 2001;Caicedo et al, 2002;Dahanukar et al, 2007;Lacaille et al, 2007;Cameron et al, 2010;Chen et al, 2011;Weiss et al, 2011;Wilson et al, 2012;Charlu et al, 2013;Jeong et al, 2013;Masek and Keene, 2013;Oka et al, 2013). In light of our new results, though, these earlier findings appear more consistent with a framework in which individual tastes are encoded.…”

Section: Discussionmentioning

confidence: 99%

Spatiotemporal Coding of Individual Chemicals by the Gustatory System

et al. 2015

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Four of the five major sensory systems (vision, olfaction, somatosensation, and audition) are thought to use different but partially overlapping sets of neurons to form unique representations of vast numbers of stimuli. The only exception is gustation, which is thought to represent only small numbers of basic taste categories. However, using new methods for delivering tastant chemicals and making electrophysiological recordings from the tractable gustatory system of the moth Manduca sexta, we found chemical-specific information is as follows: (1) initially encoded in the population of gustatory receptor neurons as broadly distributed spatiotemporal patterns of activity; (2) dramatically integrated and temporally transformed as it propagates to monosynaptically connected second-order neurons; and (3) observed in tastant-specific behavior. Our results are consistent with an emerging view of the gustatory system: rather than constructing basic taste categories, it uses a spatiotemporal population code to generate unique neural representations of individual tastant chemicals.

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“…Nevertheless, efforts to elucidate the role of IR8a on carboxylic acid-triggered behavioral avoidance produced contradictory results (Silbering et al, 2011;Ai et al, 2013). In the gustatory system, it was recently shown that high concentrations of carboxylic acids activate a subset of bitter neurons while they inhibit the activity of sweet neurons (Charlu et al, 2013). At the same time, another study demonstrated that carboxylic acids suppress bitter neuron activity when presented in dietary relevant concentrations (Chen and Amrein, 2014).…”

Section: Chemoreceptors and Sexual Behavior: Relevance Of Pheromone Amentioning

confidence: 99%

Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila

2015

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Insects encounter a vast repertoire of chemicals in their natural environment, which can signal positive stimuli like the presence of a food source, a potential mate, or a suitable oviposition site as well as negative stimuli such as competitors, predators, or toxic substances reflecting danger. The presence of specialized chemoreceptors like taste and olfactory receptors allows animals to detect chemicals at short and long distances and accordingly, trigger proper behaviors toward these stimuli. Since the first description of olfactory and taste receptors in Drosophila melanogaster 15 years ago, our knowledge on the identity, properties, and function of specific chemoreceptors has increased exponentially. In the last years, multidisciplinary approaches combining genetic tools with electrophysiological techniques, behavioral recording, evolutionary analysis, and chemical ecology studies are shedding light on our understanding on the ecological relevance of specific chemoreceptors for the survival of Drosophila in their natural environment. In this review we discuss the current knowledge on chemoreceptors of both the olfactory and taste systems of the fruitfly. We focus on the relevance of particular receptors for the detection of ecologically relevant cues such as pheromones, food sources, and toxic compounds, and we comment on the behavioral changes that the detection of these chemicals induce in the fly. In particular, we give an updated outlook of the chemical communication displayed during one of the most important behaviors for fly survival, the courtship behavior. Finally, the ecological relevance of specific chemicals can vary depending on the niche occupied by the individual. In that regard, in this review we also highlight the contrast between adult and larval systems and we propose that these differences could reflect distinctive requirements depending on the change of ecological niche occupied by Drosophila along its life cycle.

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Acid sensing by sweet and bitter taste neurons in Drosophila melanogaster

Cited by 76 publications

References 53 publications

Dual Mechanism for Bitter Avoidance inDrosophila

Dual Mechanism for Bitter Avoidance inDrosophila

Spatiotemporal Coding of Individual Chemicals by the Gustatory System

Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila

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