Outer segment growth and periciliary vesicle turnover in developing photoreceptors of Xenopus laevis

Abstract

It has been proposed that periciliary vesicles in the photoreceptor inner segment represent newly synthesized membrane en route to the outer segment, and that membrane is delivered to the outer segment via fusion of these vesicles with the plasma membrane at the base of the connecting cilium and sclerad flow of the ciliary membrane. The present research was undertaken to test the periciliary vesicle hypothesis and clarify the dynamics of membrane flow in vertebrate photoreceptors. Light- and electron-microscopic measurements on developing photoreceptors in the retina of Xenopus laevis were used to determine the amount of membrane in outer segments and in periciliary vesicles. No significant diurnal variations were found in outer segment growth rate or size of the periciliary vesicle population. In all rods and in cones at the end of the experiment, the area of periciliary vesicle membrane was proportional to the rate at which membrane was added to the outer segment. Thus, the turnover time for the periciliary vesicle population was similar in rods and cones, supporting the periciliary vesicle hypothesis. Quantification of periciliary vesicle membrane in inner segments provides a method for determining the rate at which membrane is added to outer segments, heretofore not possible for cones.