Drosophila photoreceptors respond to oscillating light of high frequency (∼100 Hz), while the detected maximal frequency is modulated by the light rearing conditions, thus maintaining high sensitivity to light and high temporal resolution. However, the molecular basis for this adaptive process is unclear. Here, we report that dephosphorylation of the light-activated Transient Receptor Potential (TRP) ion channel at S936 is a fast, graded, light-, and Ca2+-dependent process that is partially modulated by the rhodopsin phosphatase Retinal Degeneration C (RDGC). Electroretinogram (ERG) measurements of the frequency response to oscillating lights in vivo revealed that dark-reared flies expressing wild type TRP exhibited a detection limit of oscillating light at relatively low frequencies, which was shifted to higher frequencies upon light adaptation. Strikingly, preventing phosphorylation of the S936-TRP site by alanine substitution in transgenic Drosophila (trpS936A) abolished the difference in frequency response between dark- and light-adapted flies, resulting in high frequency response also in dark adapted flies. In contrast, inserting a phosphomimetic mutation by substituting the S936-TRP site to aspartic acid (trpS936D) set the frequency response of light-adapted flies to low frequencies typical of dark-adapted flies. Light-adapted rdgC mutant flies showed relatively high S936-TRP phosphorylation levels and light-dark phosphorylation dynamics. These findings suggest that RDGC is one but not the only phosphatase involved in pS936-TRP dephosphorylation. Together, this study indicates that TRP channel dephosphorylation is a regulatory process that affects the detection limit of oscillating light according to the light rearing condition, thus adjusting dynamic processing of visual information under varying light conditions.
Drosophila photoreceptors exhibit high temporal resolution as manifested in frequency response to oscillating light of high frequency (up to ∼100 Hz). The detected maximal frequency is modulated by the light rearing conditions, thus maintaining high sensitivity to light and high temporal resolution via unclear mechanisms. Here, we show by combination of biochemistry and in vivo electrophysiology that TRP channel dephosphorylation at a specific site is a fast, light-activated and Ca2+-dependent regulatory process. TRP dephosphorylation affects the detection limit of oscillating light according to the adaptation state of the photoreceptor cells by shifting the detection limit to higher frequencies upon light adaptation. This novel mechanism thus adjusts dynamic processing of visual information under varying light conditions.
The authors declare no competing financial interests.
We thank Drs. Moshe Parnas, Shahar Frechter and Shirley Weiss for useful comments on the manuscript. We also thank Mr. Anatoly Shapochnikov for the construction of the stimulating light source of variable frequencies and Katherina Beck for help with generating transgenic flies. This research was supported by grants from the National Eye Institute (NEI, R01 EY 03529), the Israel Science Foundation (ISF) and the Deutsch-lsraelische Projektkooperation (DIP) to B.M. and by grants from the Deutsche Forschungsgemeinschaft (Vo 1741/1-1, Hu 839/2-6, Hu 839/7-1). Dr. Ben Katz was a post doctoral fellow of Teva NNE and ELSC.