Light Adaptation of Rod Photoreceptor Synapses by a Transducin-Complexin-SNARE Complex Interaction

Adaptation of photoreceptor sensitivity to varying light intensities is a fundamental requirement for retinal function and thus for vision. Photoreceptors transduce light into neuronal signals, which they transmit at their synapses to postsynaptic neurons. To optimize visual information transfer, photoreceptors are equipped with a highly specialized chemical synapse, the ribbon synapse, whose output is continuously adjusted to the light intensity. Cplx3 and Cplx4, SNARE-complex-regulators of the Complexin family, were proposed to be involved in the light adaptation of ribbon synapses by throttling synaptic vesicle (SV) recruitment and fusion, but how this Cplx effect might be exerted is unknown. We performed an unbiased quantitative proteomic study to identify proteins that specifically interact with the Cplx4-SNARE complex at rod photoreceptor ribbon synapses and identified the G protein Transducin as an interaction partner. Imaging and in situ proximity ligation assays demonstrated a light-dependent interplay between Transducin and Cplx4-SNARE complexes. In bright light, the presence of Cplx4 and Transducin reduces the number of readily releasable SVs, enhancing light signaling at the rod photoreceptor ribbon synapse, whereas the absence of Cplx4 and the consequent perturbation of the Transducin-Cplx4-SNARE complex desensitizes light signaling. Our findings provide evidence for a presynaptic mechanism that involves Transducin-Cplx4-SNARE complexes and facilitates the adaptation of synaptic transmission to light at rod photoreceptor ribbon synapses.