The photoreceptors and pigment epithelium of the larval Xenopus retina: morphogenesis and outer segment renewal.

Abstract

Light microscopic autoradiography and electron microscopy were used to examine outer segment renewal and the development of photoreceptors and pigment epithelium in the larvalXenopusretina. Following the injection of [3H]-leucine at stages 37/38–40 (when outer segments first develop) or 53–54 (when rod outer segments (r. o. s.) attain adult length), a band of label accumulated at the base of r. o. s. and was displaced sclerally with time, whereas label was diffusely distributed in cone outer segments (c. o. s.). By taking into account the change in shape of r. o. s. from conical to cylindrical around stage 46, and calculating outer segment growth (determined from the rate of band displacement) asvolumeof material added with time, we found a constant rate of membrane addition (1.59 μm/day) from the time of initial outer segment formation. The changes observed in r. o. s. length therefore indicate variations in the rate of disk shedding and phagocytosis, which is minimal before stage 46 and rises to 1.19 μm/day after stages 53–54. Ultrastructural observation showed that although all photoreceptor outer segments form by the repeated evagination of the plasma membrane of the connecting cilium, r. o. s. and c. o. s. are distinguishable by differences in membrane appearance even before they develop divergent membrane topologies. Fibrous granules near the basal body of young receptors may be precursors to the elongating ciliary microtubules. Clusters of cisternae observed near the ciliary base in photoreceptor inner segments may represent a stage in the transport of newly-synthesized opsin to the outer segment base.