June 22, 2004 DURHAM, N.C. -- The first sensory map of the fly equivalent of a tongue suggests that insects have discriminating taste -- perhaps trumping that of mammals in the ability to differentiate among bitter flavors. The findings could ultimately prove useful in the development of improved pest repellants, said the Duke University Medical Center researchers.
According to the team's analysis, specialized cells in the fruit fly's primary taste organ, the labellum -- a structure on the fly's head that looks like a pair of lips covered in bristles -- respond to either sweet or bitter flavors, much like cells of the human tongue. However, while earlier work suggested mammalian bitter tasting cells are all alike, the Duke researchers found that different sets of bitter-sensitive nerve cells on the fly "tongue" bear distinct combinations of taste receptors, the Duke team found. Receptors are the protein switches that trigger the nerve cells to send signals to the brain's taste-processing centers in response to particular food items or other chemicals.
The unique coding of the flies' tasting cells raises the possibility that insects can discern among different bitter tastes more precisely than can humans or other mammals, said Hubert Amrein, Ph.D., assistant professor of genetics and lead author of the study. Amrein and his colleagues reported their findings in the June 22, 2004, issue of Current Biology. The work was supported by the National Institutes of Health.
"Our findings suggest that the sensory systems for taste in insects and mammals are set up in a remarkably similar manner, despite the fact that the structure of the taste organs are so different and that the genes involved bear no relationship to one another," Amrein said.
The fly's potentially more discriminating sensitivity to bitter tastes -- generally associated with unpalatable food or toxins -- might allow them to select the best food item among multiple suboptimal choices, Amrein speculates. For example, he said, a fruit fly landing on spoiled apples infected with different bacteria could select those less likely to cause harm when ingested.
In mammals, taste receptors on the tongue can detect five primary flavors: sweet, bitter, sour, salty and umami -- a savory or meaty taste. The sense of taste plays an important role in mammals' decisions about what to eat and what to avoid, and scientists have identified many of the underlying genes and their functions.
In the Drosophila fruit fly, taste receptors are found all over the insect body -- on taste bristles and pegs at the tip of the insect labellum, and in clusters of taste cells in the pharynx. Still other taste sensors are found on the fly's legs and along the margin of the wings. Each tasting bristle or peg contains chemosensory nerve cells bearing receptor proteins that respond to particular compounds.
Geneticists have proposed that many if not most of the tasting abilities in the insect are enabled by receptor proteins coded for by the gustatory receptor (Gr) gene family, consisting of 60 related genes, Amrein said. "But little is known about how insects examine food and decide what to eat," he added.
The team's earlier research indicated that the receptor produced by one Gr gene detects pheromones important in sexual behavior and mating. A research group at another university also has found that a second receptor senses the sugar trehalose, a metabolic component of yeast and major part of the fruit fly diet.
In the current study, Amrein's team mapped the location on the fly's labellum and body of cells that produce proteins encoded by eight of the Gr genes, including the earlier identified trehalose receptor.
The researchers linked individual taste receptor genes with their functions by disabling specific taste cells and observing the feeding behavior of the resulting mutant flies. For example, flies that lacked taste cells containing the trehalose receptor would largely ignore food containing the trehalose sugar that they would otherwise feast on.
The seven previously undescribed Gr proteins were found to trigger an avoidance response to caffeine, a bitter compound. And consistent with earlier findings, the team linked the trehalose receptor to the flies' normal feeding behavior elicited by that sugar.
The researchers found that the bitter and sweet receptor proteins mapped to distinct classes of neurons, suggesting that separate nerve cells trigger the avoidance and feeding responses, the researchers reported. Neurons bearing the bitter versus sweet taste proteins also connected to different areas of the fly brain.
Furthermore, the team found, the seven identified bitter receptors appear in distinct combinations in different sets of avoidance neurons -- such that some receptors are present on many bitter tasting cells while others appear only in a few. The differences in receptor composition among the bitter-sensing taste cells suggest that the fly might have a unique ability to pick and choose among unpalatable substances having distinct health consequences when ingested, Amrein said. The team will conduct research to further unravel those details and to identify the function of the remaining Gr receptors.
As researchers uncover the key molecular components underlying insects' senses of taste and smell, the findings might be applied to the development of improved insect repellants, Amrein said. For example, compounds that specifically block proteins underlying insects' feeding response or trigger an avoidance response might offer targeted repellants for human and agricultural uses, he added.
Collaborators on the research include Natasha Thorne, Caroline Chromey and Steve Bray, all of Duke.
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