Photoreceptor calyceal processes accompany the developing outer segment, adopting a stable length despite a dynamic core

Abstract

Vertebrate photoreceptors detect light through a large cilium-based outer segment, which is filled with photopigment-laden membranous discs. Surrounding the base of the outer segment are microvilli-like calyceal processes (CPs). While CP disruption has been associated with altered outer segment morphology and photoreceptor degeneration, the role of the processes remains elusive. Here, we used zebrafish as a model to characterize CPs. We quantified CP parameters and report a strong disparity in outer segment coverage between photoreceptor subtypes. CP length is stable across light and dark conditions, while heat shock inducible expression of tagged actin revealed rapid turnover of the CP actin core. Detailed imaging of the embryonic retina uncovered substantial remodeling of the developing photoreceptor apical surface, including a transition from dynamic tangential processes to vertically-oriented CPs immediately prior to outer segment formation. Remarkably, we also found a direct connection between apical extensions of the Muller glia and retinal pigment epithelium, arranged as bundles around the ultraviolet sensitive cones. In summary, our data characterize the structure, development, and surrounding environment of photoreceptor microvilli in the zebrafish retina.