The Phosphorylation State of theDrosophilaTRP Channel Modulates the Frequency Response to Oscillating LightIn Vivo.
Drosophilaphotoreceptors respond to oscillating light of high frequency (∼100 Hz), while the detected maximal frequency is modulated by the light rearing conditions, thus enabling 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-dependent, and Ca2+-dependent process that is partially modulated by the rhodopsin phosphatase retinal degeneration C (RDGC). Electroretinogram measurements of the frequency response to oscillating lightsin vivorevealed 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 transgenicDrosophila(trpS936A) abolished the difference in frequency response between dark-adapted 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-adaptedrdgCmutant 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.SIGNIFICANCE STATEMENTDrosophilaphotoreceptors exhibit high temporal resolution as manifested in frequency response to oscillating light of high frequency (≤∼100 Hz). Light rearing conditions modulate the maximal frequency detected by photoreceptors, thus enabling them to maintain high sensitivity to light and high temporal resolution. However, the precise mechanisms for this process are not fully understood. Here, we show by combination of biochemistry andin vivoelectrophysiology that transient receptor potential (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.
Department of Biosensorics, Institute of Physiology, University of Hohenheim, 70599 Stuttgart, Germany, and.
Olaf
0000-0002-8697-5866
O
Voolstra
Department of Medical Neurobiology, Faculty of Medicine and the Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91120, Israel.
Elisheva
E
Rhodes-Mordov
Department of Medical Neurobiology, Faculty of Medicine and the Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91120, Israel.
Ben
B
Katz
Department of Biosensorics, Institute of Physiology, University of Hohenheim, 70599 Stuttgart, Germany, and.
Jonas-Peter
0000-0002-0055-5706
JP
Bartels
Department of Biosensorics, Institute of Physiology, University of Hohenheim, 70599 Stuttgart, Germany, and.
Claudia
C
Oberegelsbacher
Department of Biosensorics, Institute of Physiology, University of Hohenheim, 70599 Stuttgart, Germany, and.
Susanne Katharina
0000-0001-5727-0296
SK
Schotthöfer
Department of Medical Neurobiology, Faculty of Medicine and the Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91120, Israel.
Bushra
B
Yasin
Department of Medical Neurobiology, Faculty of Medicine and the Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91120, Israel.
Hanan
H
Tzadok
Department of Biosensorics, Institute of Physiology, University of Hohenheim, 70599 Stuttgart, Germany, and.
Armin
A
Huber
Department of Medical Neurobiology, Faculty of Medicine and the Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem 91120, Israel baruchm@ekmd.huji.ac.il.
Baruch
B
Minke
D000221:Adaptation, Ocular / Q000502:physiology*; D000818:Animals; D030801:Animals, Genetically Modified; D029721:Drosophila Proteins / Q000378:metabolism*; D004331:Drosophila melanogaster; D004596:Electroretinography / Q000379:methods; D005260:Female; D008297:Male; D010766:Phosphorylation / Q000502:physiology; D010775:Photic Stimulation / Q000379:methods*; D017956:Photoreceptor Cells, Invertebrate / Q000378:metabolism*; D050051:Transient Receptor Potential Channels / Q000378:metabolism*
D029721:Drosophila Proteins; D050051:Transient Receptor Potential Channels; C063169:trp protein, Drosophila
Drosophila; TRP channel; TRP phosphorylation; frequency response; photoreceptor; phototransduction