Development and characteristics of photoreceptor actin-based apical processes in zebrafish (Danio rerio)

Abstract

AbstractVertebrate 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 calyceal processes (CPs), actin-based microvilli-like protrusions extending from the apical surface of the adjacent inner segment. 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 length, number, and diameter, and report a strong disparity in outer segment coverage between different photoreceptor subtypes. CP length was stable across light and dark conditions, while heat shock inducible expression of tagged actin revealed rapid turnover of the CP actin core and of the actin roots extending into the inner segment. Detailed imaging of the larval zebrafish retina revealed the presence of dynamic tangential processes extending from the photoreceptor progenitor apical surface up until the emergence of an actin dome over the growing inner segment. As the tangential processes retracted, CPs emerged just prior to outer segment formation. CPs did not accompany the emerging outer segment cilium but immediately aligned with the nascent outer segment discs. Remarkably, we also found a direct connection between apical extensions of the Müller glia and retinal pigment epithelium, arranged as bundles around the CP encircled outer segments of the ultraviolet sensitive cones. In summary, our data characterizes CP structure, development, and surrounding environment in the zebrafish retina.