Response of Drosophila to Wasabi Is Mediated by painless, the Fly Homolog of Mammalian TRPA1/ANKTM1

SummaryA number of repellent compounds produced by plants elicit a spicy or pungent sensation in mammals 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15 and 16. In several cases, this has been found to occur through activation of ion channels in the transient receptor potential (TRP) family 1, 2, 3, 4, 5, 6 and 7. We report that isothiocyanate (ITC), the pungent ingredient of wasabi, is a repellent to the insect Drosophila melanogaster, and that the painless gene, previously known to be required for larval nociception, is required for this avoidance behavior. A painless reporter gene is expressed in gustatory receptor neurons of the labial palpus, tarsus, and wing anterior margin, but not in olfactory receptor neurons, suggesting a gustatory role. Indeed, painless expression overlaps with a variety of gustatory-receptor gene reporters. Some, such as Gr66a, are known to be expressed in neurons that mediate gustatory repulsion 8, 9 and 10. painless mutants are not taste blind; they show normal aversive gustatory behavior with salt and quinine and attractive responses to sugars and capsaicin. The painless gene is an evolutionary homolog of the mammalian “wasabi receptor” TRPA1/ANKTM1 [6], also thought to be involved in nociception. Our results suggest that the stinging sensation of isothiocyanate is caused by activation of an evolutionarily conserved molecular pathway that is also used for nociception.