Cone-like rectification properties of cGMP-gated channels in transmutated retinal photoreceptors of nocturnal geckoes

Abstract

Photoreceptors of nocturnal geckoes are scotopic, with rod-shaped outer segments, and sensitivities to light similar to the one of retinal rods from other species of lower vertebrates. However, these cells are not rods, but they originated from cones of ancestral diurnal geckoes with pure-cone retinas, after being forced to adapt to a nocturnal behavior. Several interesting adaptations of these rod-like cones have been studied to date; molecular biology and functional studies confirmed that several proteins of the phototransductive cascade display structural and functional properties that indicate their origin from cones rather than from rods. In this paper, we investigate, with whole cell voltage clamp in the photoreceptor detached outer segment preparation, the voltage rectification properties of cGMP-gated channels in three species, Gekko gecko, Tarentola mauritanica, and Hemidactylus frenatus. We show that the current-voltage properties in the physiological voltage range are reminiscent of the ones of cGMP-gated channels from cones rather than from rods of other cold-blooded vertebrates. The origin and the relevance of the mechanisms investigated are discussed.

Figure 1

cGMP-gated current amplitude during voltage step protocol. Typical whole cell voltage clamp recording of a gecko photoreceptor detached outer segment (Tarentola mauritanica) performed in the dark. Upon exposure to bright light, most current disappeared and only a negligible amount of leakage current remained. Arrow indicates the time (50 ms after voltage change) when current amplitude was measured to obtain the I-V plot, before any time-dependent change of cGMP-gated current occurred. Further details in text.

Figure 2

I-V relationship of light-sensitive (cGMP-gated) current recorded from gecko photoreceptor DOS. (a) I-V relationship of cGMP-gated current in a single, representative DOS from the nocturnal geckos Gekko gecko (black squares), Tarentola mauritanica (white circles), and Hemidactylus frenatus (grey triangles). Each curve shows a single trial from a single DOS. Data were fitted with (1) (continuous lines). Average parameters obtained are in Table 1. (b) Numerical simulation according to (1) of the I-V behavior of the cGMP-gated current in amphibian rods (dotted line), in catfish cones (dashed line), and in nocturnal geckos (solid line).