Disc morphogenesis in vertebrate photoreceptors

Abstract

Electron microscopic examination of the bases of adult rod and cone outer segments (rhesus monkey, ground squirrel, and grey squirrel) has led to a new model of disc morphogenesis. In this model the disc surfaces and disc rims develop by separate mechanisms and from separate regions of the membrane of the inner face of the cilium. This membrane is alternately specified into regions that will form either the disc surfaces or the disc rims. The disc surfaces develop by an evagination or outpouching of the ciliary membrane. The two surfaces of an evagination, scleral and vitreal, each form one of the surfaces of adjacent discs. The disc rim is initially specified as a region of ciliary membrane between adjacent disc-surface evaginations. This region grows bilaterally around the circumferences of adjacent discs, zippering together the apposed surfaces to form the rim and completed disc. At the same time it seals the plasma-membrane edges of the evaginations, which have become detached from the surfaces. Incisures form in rod discs by infolding of the rim and surfaces together, and they begin to form before the rim is completed around the disc perimeter. When a number of new discs are developing simultaneously the ciliary membrane at the base of an outer segment consists of a stack of rim forming and surface forming growth points. This model provides, in addition, for the continuous renewal of outer-segment plasma membrane. It also establishes a developmental basis for the structural uniqueness of the disc rim. Finally, it indicates an evolutionary relationship between the discs of vertebrate visual cells and the membrane specializations of invertebrate visual cells.