Light-induced remodeling of the Drosophila phosphoproteome regulates visual adaptation through the Trp channel

Light is an important environmental stimulus that is necessary for vision and circadian entrainment. Here, we present a system-wide analysis of the kinase-mediated light response in Drosophila using optimized data-independent acquisition mass spectrometry (DIA-MS) for quantitative phosphoproteomics analysis. Exposure to standard white light or high-intensity blue light induced a widespread increase in phosphorylation relative to dark-adapted flies. The light-sensitive phosphoproteins were part of multiple pathways, including phototransduction, circadian control, lipid metabolism, and synapse organization, and exhibited distinct phosphorylation signatures under dark adaptation or white or blue light. The Ca²⁺-permeable transient receptor potential (Trp) channel was differentially phosphorylated at multiple sites in a white and blue light-dependent manner, and phosphorylation stoichiometric analysis identified Thr⁸⁴⁹ in Trp as a pivotal functional switch. It was entirely unphosphorylated in the dark, but 80% of the Trp molecules were phosphorylated in either light condition. This phosphorylation event was mediated in part by the eye-specific protein kinase C InaC and regulated the eye's electrophysiological response to oscillating light. Thus, our results show that light remodels the Drosophila phosphoproteome, establishing a crucial mechanism for sensory adaptation to a changing light-dark environment.