Light-mediated planar polarization of cone photoreceptorcilia contributes to visual acuity in mammals

The coordinated spatial arrangement of organelles within a tissue plane, generally referred to as Planar Cell Polarity (PCP), is critical for various processes ranging from organogenesis to sensory detection. Mechanistically, planar cell polarity is typically set-up by gradients of morphogens and their receptors, but whether non-molecular cues, akin to phototropism in plants, might play a part in setting up PCP in animals remains unknown. Here we report that the basal body of newborn photoreceptor cells in the mouse retina is centrally positioned, but then moves laterally around the first post-natal week, thereby generating cell-intrinsic asymmetry. During the second postnatal week, when eyes open, the basal bodies of cone photoreceptor cilia, but not rods, become coordinated across the tissue plane to face the center of the retina. Mechanistically, we show that light is required during a critical window in development, triggering a non-canonical cascade whereby cone transducin interacts with the G- protein signaling modulator protein 2 (GPSM2), which is in turn necessary for cone PCP. This work uncovers a non-canonical PCP pathway initiated by light.