A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging

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In the gustatory systems of mammals and flies, different populations of sensory cells recognize different taste modalities, such that there are cells that respond selectively to sugars and others to bitter compounds. This organization readily allows animals to distinguish compounds of different modalities but may limit the ability to distinguish compounds within one taste modality. Here, we developed a behavioral paradigm in Drosophila melanogaster to evaluate directly the tastes that a fly distinguishes. These studies reveal that flies do not discriminate among different sugars, or among different bitter compounds, based on chemical identity. Instead, flies show a limited ability to distinguish compounds within a modality based on intensity or palatability. Taste associative learning, similar to olfactory learning, requires the mushroom bodies, suggesting fundamental similarities in brain mechanisms underlying behavioral plasticity. Overall, these studies provide insight into the discriminative capacity of the Drosophila gustatory system and the modulation of taste behavior.chemosensory | gustatory | neurobiology T he gustatory system allows animals to detect chemical compounds in the environment and determine their value as potential food sources. To make this assessment, animals detect two different features of taste stimuli with the gustatory system: the concentration and the quality of a taste compound. In humans, taste concentration is perceived as intensity and taste quality as a component of flavor. Determining how these two features of taste stimuli are encoded by the nervous system and used to direct behavior is central for the neural basis of taste perception.Mammals are thought to detect five different general taste qualities or modalities: sugars, bitter compounds, salt, acids, and amino acids (1). Each taste modality is detected by a unique taste cell population in the periphery, such that the activation of different taste cells provides a simple mechanism to encode modality. In addition, taste cells show dose-dependent activation, providing the potential to encode different concentrations.Although taste cell activity readily allows for modality and concentration discrimination, does it allow for finer discrimination of individual taste compounds? Animals distinguish sugars from bitter compounds, but do they distinguish compounds within a single modality? In principle, different sugars could activate slightly different taste cell populations or activate the same population with different temporal properties, and these differences could be exploited to allow for the discrimination of individual compounds. Alternatively, different taste compounds could activate the same taste cell population with a different efficacy and lead to a perceived difference in sugar concentration or intensity rather than quality.The Drosophila gustatory system provides an attractive model for studies of taste discrimination because it is an experimentally tractable system that retains similarities to mammalian taste. Like ...

Section: Resultsmentioning

confidence: 99%

Limited taste discrimination in Drosophila

Mašek¹,

Scott

2010

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“…Our understanding of the molecular components required for contact chemosensation in insects is limited primarily to the identification of a series of gustatory receptors (18)(19)(20)(21)(22)(23)(24)(25). Currently, the channels required for contact chemosensation in insects are not known.…”

mentioning

confidence: 99%

Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons

Kim

Lee

Akitake

et al. 2010

Self Cite

166

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Mammalian sweet, bitter, and umami taste is mediated by a single transduction pathway that includes a phospholipase C (PLC)β and one cation channel, TRPM5. However, in insects such as the fruit fly, Drosophila melanogaster, it is unclear whether different tastants, such as bitter compounds, are sensed in gustatory receptor neurons (GRNs) through one or multiple ion channels, as the cation channels required in insect GRNs are unknown. Here, we set out to explore additional sensory roles for the Drosophila TRPA1 channel, which was known to function in thermosensation. We found that TRPA1 was expressed in GRNs that respond to aversive compounds. Elimination of TRPA1 had no impact on the responses to nearly all bitter compounds tested, including caffeine, quinine, and strychnine. Rather, we found that TRPA1 was required in a subset of avoidance GRNs for the behavioral and electrophysiological responses to aristolochic acid. TRPA1 did not appear to be activated or inhibited directly by aristolochic acid. We found that elimination of the same PLC that leads to activation of TRPA1 in thermosensory neurons was also required in the TRPA1-expressing GRNs for avoiding aristolochic acid. Given that mammalian TRPA1 is required for responding to noxious chemicals, many of which cause pain and injury, our analysis underscores the evolutionarily conserved role for TRPA1 channels in chemical avoidance.

“…Gr5a is expressed in most sugar-responsive GRNs (7-9, 11, 12). Gr64a is essential for the detection of multiple other sugars, including sucrose, glucose, and maltose (13,14). A third receptor, Gr64f, is a coreceptor, which is broadly required for the detection of most sugars (15).…”

mentioning

confidence: 99%

Multiple gustatory receptors required for the caffeine response in Drosophila

Lee

Moon

Montell³

2009

Self Cite

229

214

The ability of insects to detect and avoid ingesting naturally occurring repellents and insecticides is essential for their survival. Nevertheless, the gustatory receptors enabling them to sense toxic botanical compounds are largely unknown. The only insect gustatory receptor shown to be required for avoiding noxious compounds is the Drosophila caffeine receptor, Gr66a. However, this receptor is not sufficient for the caffeine response, suggesting that Gr66a may be a subunit of a larger receptor. Here, we report that mutations in the gene encoding the gustatory receptor, Gr93a, result in a phenotype identical to that caused by mutations in Gr66a. This includes an inability to avoid caffeine or the related methylxanthine present in tea, theophylline. Caffeine-induced action potentials were also eliminated in Gr93a-mutant animals, while the flies displayed normal responses to other aversive compounds or to sugars. The Gr93a protein was coexpressed with Gr66a in avoidance-gustatory receptor neurons (GRNs), and functioned in the same GRNs as Gr66a. However, misexpression of both receptors in GRNs that normally do not express either Gr93a or Gr66a does not confer caffeine sensitivity to these GRNs. Because Gr93a-and Gr66a-mutant animals exhibit the identical phenotypes and function in the same cells, we propose that they may be caffeine coreceptors. In contrast to mammalian and Drosophila olfactory receptors and mammalian taste receptors, which are monomeric or dimeric receptors, we propose that Drosophila taste receptors that function in avoidance of bitter compounds are more complex and require additional subunits that remain to be identified.Gr93a ͉ gustatory receptor neuron ͉ taste ͉ repellent ͉ chemosensation