Function of Rhodopsin in Temperature Discrimination in Drosophila

Abstract

Many animals, including the fruit fly, are sensitive to small differences in ambient temperature. The ability of Drosophila larvae to choose their ideal temperature (18°C) over other comfortable temperatures (19° to 24°C) depends on a thermosensory signaling pathway that includes a heterotrimeric guanine nucleotide-binding protein (G protein), a phospholipase C, and the transient receptor potential TRPA1 channel. We report that mutation of the gene (ninaE) encoding a classical G protein-coupled receptor (GPCR), Drosophila rhodopsin, eliminates thermotactic discrimination in the comfortable temperature range. This role for rhodopsin in thermotaxis toward 18°C was light-independent. Introduction of mouse melanopsin restored normal thermotactic behavior in ninaE mutant larvae. We propose that rhodopsins represent a class of evolutionarily conserved GPCRs that are required for initiating thermosensory signaling cascades.

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

“…Neurons that are required for thermotaxis had not yet been identified. Several proteins-TRP, TRP-like, and Rhodopsin-have been suggested to have roles in thermotaxis by affecting the setpoint of the larva's preferred temperature (12,18). Another member of the TRP family of cation channels-inactive, which is largely expressed in the chordotonal organs along the larva's body (Fig.…”

“…In addition, dTRPA1-expressing neurons in the central brain function as internal temperature sensors that also contribute to warm avoidance (10). Several genes that can affect the range of preferred temperatures in larvae have been identified, which include transient receptor potential (trp) channels and rhodopsin (11,12). However, none of these genes are required for driving larval movement toward preferred temperatures.…”

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

“…The ortholog of a key gene in the rhodopsin biosynthesis pathway santa-maria, Dvir\GJ17608, was up-regulated in both species in response to cold acclimation. Rhodopsin has long been known to be the primary pigment for phototransduction (see Katz and Minke (2009) for a review), however recently it has been shown that the rhodopsin signalling pathway also has a several additional lightindependent roles including hearing (Senthilan et al, 2012) and thermosensory signalling (Shen et al, 2011). Shen et al (2011) showed that by knocking out santa-maria in D. melanogaster, flies were unable to discriminate between differences in temperature.…”

“…Rhodopsin has long been known to be the primary pigment for phototransduction (see Katz and Minke (2009) for a review), however recently it has been shown that the rhodopsin signalling pathway also has a several additional lightindependent roles including hearing (Senthilan et al, 2012) and thermosensory signalling (Shen et al, 2011). Shen et al (2011) showed that by knocking out santa-maria in D. melanogaster, flies were unable to discriminate between differences in temperature. Our finding that Dvir\GJ17608 is upregulated in both species is intriguing as it suggests the rhodopsin pathway may act to detect changes in temperature and thus may cue the cold acclimation response.…”

Fever-like temperature modification differentially affects in vitro signaling of bradykinin B1 and B2 receptors

“…Interestingly, it is worth mentioning that GPCRs cannot only be affected in their signaling properties by the surrounding temperature as shown herein, but may even act as a temperature sensor as has recently been reported for the GPCR rhodopsin in Drosophila larvae (Shen et al, 2011).…”