Editors' ChoiceNeuroscience

Sensing the Bitter in the Sweet

Science Signaling  27 Aug 2013:
Vol. 6, Issue 290, pp. ec199
DOI: 10.1126/scisignal.2004680

Most foods have complex flavors, and food preferences are decided by integrating the taste and olfactory sensations produced. Fruit flies serve as a model system for studying odorant or tastant perception. Fruit flies are attracted to sweet and repelled by bitter, which are detected by distinct neurons and receptors in the gustatory sensilla (cells of the taste organ). The extracellular fluid of the sensilla contains secreted proteins, including a class called odorant-binding proteins (OBPs), one of which functions as a pheromone-binding protein and is necessary for detection of this chemical (see Lvovskaya and Smith). Jeong et al. investigated the molecular mechanism by which bitter chemicals can inhibit the attraction to a sweet chemical (sugar) when presented to flies in a mixture. By analyzing solution preferences of transgenic flies in which each of the four most highly expressed OBP-encoding genes in the sensilla were knocked out, OBP49a was identified as necessary for avoidance of sugar solutions containing one of several bitter compounds. Electrophysiological recording of the gustatory organ showed that inhibition of sugar-induced action potentials by bitter chemicals was reduced in the mutant flies compared with wild-type flies. The inhibitory response was rescued by transgenic expression of Obp49a in the thecogen cell, an accessory cell in which it was expressed in wild-type animals, or by expression of a membrane-tethered engineered form in the sugar-activated neuron. Surface plasmon resonance assays showed that OBP49a directly bound several bitter chemicals in a dose-dependent manner. A fluorescent protein complementation assay indicated that OBP49a and the gustatory receptor GR64a were in close proximity, a finding that was consistent with the membrane-tethered rescue experiments. Thus, OBP49a appears to function as a bitter chemical-binding protein that directly inhibits the activity of the sugar-activated gustatory receptor to mediate avoidance of mixtures of sweet and bitter chemicals.

Y. T. Jeong, J. Shim, S. R. Oh, H. I . Yoon, C. H. Kim, S. J. Moon, C. Montell, An odorant-binding protein required for suppression of sweet taste by bitter chemicals. Neuron 79, 725–737 (2013). [Abstract]

S. Lvovskaya, D. P. Smith, A spoonful of bitter helps the sugar response go down. Neuron 79, 612–614 (2013). [Abstract]