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Molecular and cellular basis of acid taste sensation in Drosophila


Authors:
Ting-Wei Mi 1; John Mack 1; Christopher Lee 2; Yali Zhang 1,3

Affiliations:
1) Monell Chemical Senses Center, Philadelphia, PA; 2) Department of Biology, University of Pennsylvania, Philadelphia, PA; 3) Department of Physiology, The Diabetes Research Center, University of Pennsylvania, Perelman School of Medicine, Philadelphia, PA

Keywords:
k. feeding behavior; k. feeding behavior

Sour taste is one of the five commonly accepted basic taste modalities, alongside four other fundamental taste: bitter, sweet, salty, and umami. This taste sensation is evoked by acidic foods such as vinegar or certain fruits, and allows organisms to avoid consuming unripe or spoiled, or fermented foods. Species from insects to mammals are attracted by slightly acidic foods, but repulsed to highly acidic foods. However, the molecular and cellular mechanism of how animals distinguish low from high acid foods is still largely unknown. Here, we use the fruit fly (Drosophila melanogaster) as a model organism to address this question. Firstly, we show that fruit flies employ two competing taste sensory pathways to discriminate low from high acidity, which trigger attractive or aversive behavior respectively. Secondly, we identify Otopetrin-like a (OtopLa), a member of an evolutionarily conserved gene family, as a proton channel in fruit flies expressed in bipolar type gustatory receptor neurons (GRNs) in the proboscis with central projection patterns in the subesophageal zone (SEZ), which receives taste input from the peripheral taste organs. Loss of otopla impairs flies’ acid sensation, causing an imbalance in the competing taste pathways leading to an abnormal aversive response to low acid. In summary, our behavioral, anatomical, and electrophysiological data strongly suggest that flies display a competing acid-sensing mechanism to distinguish between high and low acid, and the proton channel OtopLa is required for low acid sensation. This sensing mechanism that may be evolutionarily conserved between insects and mammals, given the similarity in their taste preferences for acid and homologous functions of Otop genes.