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

ABSTRACT: In Drosophila, detection of tastants is thought to be mediated by members of a family of 68 gustatory receptors (Grs). However, only one receptor, Gr5a, has been associated with a sugar, and it appears to be activated specifically by trehalose. It is unclear whether other sugar receptors are activated by single or multiple sugars. Currently, no Grs are known to colocalize with Gr5a. Such Grs would be candidate sugar receptors because Gr5a-expressing cells function in the responses to attractive tastants. Here we use an "mRNA tagging" approach to identify Gr RNAs that are coexpressed with Gr5a. We found that all seven Grs most related to Gr5a (Gr64a-f and Gr61a) were expressed in Gr5a-expressing cells, whereas none of the other Grs examined were enriched in these Gr neurons (GRNs). We characterized the role of one Gr5a-related receptor, Gr64a, and found that it was required for the behavioral responses to glucose, sucrose, and maltose. Gr64a was required for GRN function because action potentials induced by these sugars were dependent on expression of Gr64a in GRNs. These data demonstrate that multiple Grs are coexpressed with Gr5a and that Drosophila Gr64a is required for the responses to multiple sugars.

SUBMITTER: Jiao Y

PROVIDER: S-EPMC1955822 | biostudies-other | 2007 Aug

REPOSITORIES: biostudies-other

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

Jiao Yuchen Y Moon Seok Jun SJ Montell Craig C

Proceedings of the National Academy of Sciences of the United States of America 20070822 35

In Drosophila, detection of tastants is thought to be mediated by members of a family of 68 gustatory receptors (Grs). However, only one receptor, Gr5a, has been associated with a sugar, and it appears to be activated specifically by trehalose. It is unclear whether other sugar receptors are activated by single or multiple sugars. Currently, no Grs are known to colocalize with Gr5a. Such Grs would be candidate sugar receptors because Gr5a-expressing cells function in the responses to attractive ...[more]

PMID: 17715294

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Project description:Although the gustatory system provides animals with sensory cues important for food choice and other critical behaviors, little is known about neural circuitry immediately following gustatory sensory neurons (GSNs). Here, we identify and characterize a bilateral pair of gustatory second-order neurons (G2Ns) in Drosophila. Previous studies identified GSNs that relay taste information to distinct subregions of the primary gustatory center (PGC) in the gnathal ganglia (GNG). To identify candidate G2Ns, we screened ∼5,000 GAL4 driver strains for lines that label neural fibers innervating the PGC. We then combined GRASP (GFP reconstitution across synaptic partners) with presynaptic labeling to visualize potential synaptic contacts between the dendrites of the candidate G2Ns and the axonal terminals of Gr5a-expressing GSNs, which are known to respond to sucrose. Results of the GRASP analysis, followed by a single-cell analysis by FLP-out recombination, revealed a pair of neurons that contact Gr5a axon terminals in both brain hemispheres and send axonal arborizations to a distinct region outside the PGC but within the GNG. To characterize the input and output branches, respectively, we expressed fluorescence-tagged acetylcholine receptor subunit (Dα7) and active-zone marker (Brp) in the G2Ns. We found that G2N input sites overlaid GRASP-labeled synaptic contacts to Gr5a neurons, while presynaptic sites were broadly distributed throughout the neurons' arborizations. GRASP analysis and further tests with the Syb-GRASP method suggested that the identified G2Ns receive synaptic inputs from Gr5a-expressing GSNs, but not Gr66a-expressing GSNs, which respond to caffeine. The identified G2Ns relay information from Gr5a-expressing GSNs to distinct regions in the GNG, and are distinct from other, recently identified gustatory projection neurons, which relay information about sugars to a brain region called the antennal mechanosensory and motor center (AMMC). Our findings suggest unexpected complexity for taste information processing in the first relay of the gustatory system.

Dataset Information

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

Publications

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

Similar Datasets

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