Light microscopic autoradiography and electron microscopy were used to examine outer segment renewal and the development of photoreceptors and pigment epithelium in the larval Xenopus retina. Following the injection of [ 3 H]-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) as volume of 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.
Histological examination of the retinae of Xenopus tadpoles undergoing the extensive transformations of metamorphic climax revealed a progressive and dramatic decrease in the length of rod outer segments (r. o. s.) (by 1.22 µm/day), which was reversed after the completion of metamorphosis, when r. o. s. grew longer (by 1.11 µm/day). The rate of r. o. s. disk addition during these two periods was determined by examining the incorporation of [ 3 H]-leucine by light microscopic autoradiography. The band of labelled protein in r. o. s. was displaced sclerally at a rate of 1.70 µm/day during the first half of metamorphic climax, and of 1.56 µm/day in young juveniles during the second month after metamorphosis. The similarity of the rate of band displacement at these times indicates that the changes in r. o. s. length associated with metamorphosis result from major changes in the rate of disk shedding and/or phagocytosis, which was about 2.92 µm/day pre-metamorphically and 0.45 µm/day post-metamorphically. E. m. observation at these stages and during the final stages of metamorphic climax revealed no significant alterations in the cellular organization or ultrastructure of rods or pigment epithelium, even though some r. o. s. were only 3 µm long. This large change in r. o. s. length undoubtedly influences the animal’s scotopic sensitivity and the relative mesopic activity of its rods and cones, and may have important effects on the animal’s visual physiology.
Outer segment renewal and the fine structure of photoreceptors and pigment epithelium (p. e.) were studied in the adult Xenopus retina by light microscopic autoradiography and electron microscopy. Following the injection of [ 3 H]leucine, the pattern of labelling observed in receptor outer segments was typical of that reported in other adult retinae: only diffuse labelling was found in cones, but in rods a discrete band of label accumulated at the base of the outer segment and migrated sclerally with time. The rate of band displacement and thus disk addition in Xenopus rods was 1.86 μm/day (or 78 disks/day), which is more than twice that reported for red rods in Rana under similar experimental conditions, although these species have similar metabolic rates. Average rod outer segment (r. o. s.) length did not change, demonstrating a balance between disk addition and shedding. R. o. s. renewal time was about 24 days, corresponding to the time when labelled phagosomes were first found in the p. e. Ultrastructurally, one kind of (red) rod and one kind of cone were found whose outer segments differed in membrane topology. Although microfilaments were found in the apical processes of the p. e. and its cytoplasm contained both pigment granules and myeloid bodies, pigment granules did not migrate into these processes during light adaptation. In addition to possible morphological evidence for phagosomes of cone origin, both large and small rod phagosomes were observed in the p. e. The latter appear to represent small stacks of partial disks shed from individual r. o. s. scallops.
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