Abstract
Evaluation of food compounds by chemosensory cells is essential for animals to make appropriate feeding decisions. In the fruit fly Drosophila melanogaster, structurally diverse chemicals are detected by multimeric receptors composed of members of a large family of Gustatory receptor (Gr) proteins. Putative sugar and bitter receptors are expressed in distinct subsets of Gustatory Receptor Neurons (GRN) of taste sensilla, thereby assigning distinct taste qualities to sugars and bitter tasting compounds, respectively. Here we report a Ca2+ imaging method that allows association of ligand-mediated responses to a single GRN. We find that different sweet neurons exhibit distinct response profiles when stimulated with various sugars, and likewise, different bitter neurons exhibit distinct response profiles when stimulated with a set of bitter chemicals. These observations suggest that individual neurons within a taste modality are represented by distinct repertoires of sweet and bitter taste receptors, respectively. Furthermore, we employed this novel method to identify glucose as the primary ligand for the sugar receptor Gr61a, which is not only expressed in sweet sensing neurons of classical chemosensory sensilla, but also in two supersensitive neurons of atypical taste sensilla. Thus, single cell Ca2+ imaging can be employed as a powerful tool to identify ligands for orphan Gr proteins.
Highlights
Taste is a sensory modality found in virtually all animals
The ‘‘sweet’’ neuron is tuned to sugar compounds, the ‘‘bitter/high salt’’ neuron responds to solutions containing high concentration of salt (.400 mM) and a diverse group of bitter tasting chemicals, the ‘‘low salt’’ neuron is activated by solutions containing low concentration of salt (,200 mM) and the ‘‘water’’ neuron is stimulated by solutions of low osmolarity [5]
The molecular basis for several of these taste modalities is known: sweet and bitter compounds are detected by Gustatory receptor (Gr) proteins which are thought to form multimeric complexes that interact with sugars and diverse organic chemicals, respectively [6,7,8,9,10,11], while water and salt sensing is mediated by members of the Degenerin/epithelial sodium channel family (Deg/ENaC) of proteins [12,13,14]
Summary
Taste is a sensory modality found in virtually all animals. Chemicals are detected by specialized sensory cells in the tongue of vertebrates and labial palps and legs of insects, respectively [1]. The molecular basis for several of these taste modalities is known: sweet and bitter compounds are detected by Gustatory receptor (Gr) proteins which are thought to form multimeric complexes that interact with sugars and diverse organic chemicals (alkaloids, terpenoids etc), respectively [6,7,8,9,10,11], while water and salt sensing is mediated by members of the Degenerin/epithelial sodium channel family (Deg/ENaC) of proteins [12,13,14]. Especially bitter tasting compounds, are structurally diverse, and the number of receptors detecting these chemicals is predictably large. Gr66a and Gr93a were shown to be necessary for sensing caffeine, while Gr33a is required for detecting a wide range of bitter tasting chemicals that include lobeline, quinine and denatonium [7,19,20]
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