Changes in length and disk shedding rate of Xenopus rod outer segments associated with metamorphosis

Abstract

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.

Metamorphosis of the amphibian eye

“…The authors suggest that the extreme hyperopia late in metamorphosis indicates that vision is not critical in the animals' behavior during these stages. Such a proposal gains support from the observation that some anurans complete metamorphic changes while remaining in mud at the pond floor (Nieuwkoop andFaber, 1956 in Kinney andFisher, 1978).…”

“…Although there is no reason at present to link these disparate results, they suggest that thyroid hormone might bring about diverse different effects in different target tissues during metamorphosis by inducing the synthesis of factors whose receptors are differentially distributed in target tissues. Thus the previously described effect of thyroid hormone on photoreceptors (Kinney and Fisher, 1978) might be mediated through thyroid hormone induction of growth hormone and growth hormone induction of IGFl. A similar involvement in retinal develapment during metamorphosis could be proposed for acidic and/or basic fibroblast growth factor (FGF).…”

“…The lengths of rod outer segments, and the rate at which they are shed, also change during mctamorphosis, with a substantial increase in the rate of disk shedding and/or phagocytosis during metamorphic climax and a decrease after metamorphosis is complete (Kinney and Fisher, 1978). Because longer rods absorb more light and thus confer higher scotopic sensitivity (Witkovsky et al, 1976), the shorter rod outer segments during metamorphosis presumably decrease visual sensitivity during this period.…”