Evolution of the calcium feedback steps of vertebrate phototransduction

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.

Mechanosensitivity is an essential component of phototransduction in vertebrate rods

“…Likewise, the distance from TRPC5 to GC-F (= GUCY2F) is <1 Mb in spotted gar ( Fig 6A) and <2.5 Mb in human ( Fig 6B); in the other 2 species, the loss of the gene for GC-F precludes this comparison (S8 Fig). Furthermore, as shown previously [30], in several cases members of the other 3 families of phototransduction genes are close to each other; for example, GRK1B, GC-E, and ARRB2 are close to each other in spotted gar (Fig 6A). Such proximity in extant chromosomes is an important telltale sign of ancient proximity because of the very low likelihood that random chromosomal rearrangements could bring so many genes into mutual proximity; instead, random rearrangements are likely to obscure any proximity that originally occurred.…”

Selective Gene Loss of Visual and Olfactory Guanylyl Cyclase Genes Following the Two Rounds of Vertebrate-Specific Whole-Genome Duplications

“…Vertebrate species predating 2R WGD had one common ancestor of GC-D/E/F. The GC-E and GC-F/D split seems to have occurred before the vertebrate-specific WGD as studies in lamprey and hagfish have demonstrated ( Lamb and Hunt 2018 ). Initially, following a WGD event, the exon–intron structure of the duplicated genes is indistinguishable.…”

“…2016 ; Lamb and Kraft 2016 ; Lamb et al. 2018 ; Lamb and Hunt 2018 ). Nevertheless, the fate of phototransduction gene ohnologs in different vertebrate lineages following the 2R WGD has not been systematically investigated.…”

“…Nevertheless, functionally there might also be some relation between these two groups of cyclases as GC-D expression in the retina of some basal fish species has recently been described ( Lamb and Hunt 2018 ). In general, GC-D expression is restricted to some special cells in the olfactory epithelium (OE), where their signaling represents an alternative to the cAMP signaling.…”

The Binding Properties and Physiological Functions of Recoverin

“…Like other family members, it contains four EF hand motifs and a myristoyl chain on the N-terminus. Only two of the EF hands (EF2 and EF3) bind Ca 2+ across species (Senin et al, 2002; Lamb and Hunt, 2018). Rcv undergoes a conformational change upon Ca 2+ binding in darkness and subsequently attaches to the disc membrane in photoreceptor outer segment (Tanaka et al, 1995; Ames et al, 1997).…”