A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila

Abstract

Behavioral responses to temperature are critical for survival, and animals from insects to humans show strong preferences for specific temperatures1, 2. Preferred temperature selection promotes avoidance of adverse thermal environments in the short-term and maintenance of optimal body temperatures over the long-term1, 2, but its molecular and cellular basis is largely unknown. Recent studies have yielded conflicting views of thermal preference in Drosophila, attributing importance to either internal3 or peripheral4 warmth sensors. Here we reconcile these views by demonstrating that thermal preference is not a singular response, but involves multiple systems relevant in different contexts. We previously found that the Transient Receptor Potential (TRP) channel TRPA1 acts internally to control the slowly developing preference response of flies exposed to a shallow thermal gradient3. Here we find that the rapid response of flies exposed to a steep warmth gradient does not require TRPA1; rather, the Gustatory receptor (Gr) Gr28b(D) drives this behavior via peripheral thermosensors. Grs are a large gene family widely studied in insect gustation and olfaction and implicated in host-seeking by insect disease vectors5–7, but not previously implicated in thermosensation. At the molecular level, Gr28b(D) misexpression confers thermosensitivity upon diverse cell types, suggesting it is a warmth sensor. These data reveal a new type of thermosensory molecule and uncover a functional distinction between peripheral and internal warmth sensors in this tiny ectotherm reminiscent of thermoregulatory systems in larger, endothermic animals2. The use of multiple, distinct molecules to respond to a given temperature, as observed here, may facilitate independent tuning of an animal’s distinct thermosensory responses.

Drosophila Ionotropic Receptor 25a mediates circadian clock resetting by temperature

“…Our data indicating that IR25a contributes to temperature sensing within ChO extend the roles of IR's beyond chemoreception, reminiscent of the requirement for the "gustatory receptor" Gr28b in warmth-avoidance 22 . Although we show that IR25a-expressing leg neurons are capable of sensing temperature and mediating temperature entrainment, it is possible that this receptor has a similar role elsewhere in the peripheral nervous system.…”

A decision underlies phototaxis in an insect

“…We also combined trpa1 1 and gr28b MB , abolishing thermosensation completely. It is worth mentioning that the TrpA1 channel also mediates chemical avoidance via gustatory neurons [51,52], and Gr28b is expressed in HC neurons located in the same portion of the antennae damaged with our manipulation [50]. The wings-intact mutants all showed a positive photopreference (figure 4m), indicating that photopreference is not automatically affected when any sensory modality is knocked out.…”

Drosophila circadian rhythms in seminatural environments: Summer afternoon component is not an artifact and requires TrpA1 channels

“…We also examined the effect of mutations in genes known to contribute to temperature sensing in the 25-40°C range (Right panels of Fig. 3), including the Trp channels TrpA1 (12), painless (13), and pyrexia (14); the temperature entrainment mutant nocte (15); and the gustatory receptor paralogue Gr28b required for rapid negative thermotaxis (16). The most dramatic differences observed involved pyrexia, in which the M and E components were significantly suppressed compared with A and TrpA1 mutants in which the A component was largely eliminated (Fig.…”