Abstract
We examined the genes encoding the proteins that mediate the Ca-feedback regulatory system in vertebrate rod and cone phototransduction. These proteins comprise four families: recoverin/visinin, the guanylyl cyclase activating proteins (GCAPs), the guanylyl cyclases (GCs) and the sodium/calcium-potassium exchangers (NCKXs). We identified a paralogon containing at least 36 phototransduction genes from at least fourteen families, including all four of the families involved in the Ca-feedback loop (recoverin/visinin, GCAPs, GCs and NCKXs). By combining analyses of gene synteny with analyses of the molecular phylogeny for each of these four families of genes for Ca-feedback regulation, we have established the likely pattern of gene duplications and losses underlying the expansion of isoforms, both before and during the two rounds of whole-genome duplication (2R WGD) that occurred in early vertebrate evolution. Furthermore, by combining our results with earlier evidence on the timing of duplication of the visual G-protein receptor kinase genes, we propose that specialization of proto-vertebrate photoreceptor cells for operation at high and low light intensities preceded the emergence of rhodopsin, which occurred during 2R WGD.
Highlights
The rod and cone photoreceptors of the vertebrate duplex retina, used, respectively, for night and day vision, employ distinct protein isoforms for many of the components of the transduction cascade
In searching for synteny among the genes encoding the proteins of the calcium feedback loop, we were struck by the close proximity of many sets of phototransduction genes to each other
The occurrence of multiple families of genes, with paralogues arranged in a closely similar sequence across four chromosomes, is a signature of the remnants of a quartet that arose during the two rounds of whole-genome duplication (2R WGD) that occurred very early in vertebrate evolution [1]
Summary
The rod and cone photoreceptors of the vertebrate duplex retina, used, respectively, for night and day vision, employ distinct protein isoforms for many of the components of the transduction cascade. These cells represent a unique evolutionary system, where the same process (detection of light) uses a distinct set of genes in different classes of cell. A series of studies from Larhammar’s group [2,3,4,5,6,7] reported evidence for extensive expansion of phototransduction gene isoforms during 2R WGD. We confirmed the importance of 2R WGD in establishing distinct rod/cone isoforms in both the activation and the shut-off steps in the phototransduction cascade, and we presented likely
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