Abstract
Different isoforms of the genes involved in phototransduction are expressed in vertebrate rod and cone photoreceptors, providing a unique example of parallel evolution via gene duplication. In this study, we determine the molecular phylogeny of the proteins underlying the shut-off steps of phototransduction in the agnathan and jawed vertebrate lineages. For the G-protein receptor kinases (GRKs), the GRK1 and GRK7 divisions arose prior to the divergence of tunicates, with further expansion during the two rounds of whole-genome duplication (2R); subsequently, jawed and agnathan vertebrates retained different subsets of three isoforms of GRK. For the arrestins, gene expansion occurred during 2R. Importantly, both for GRKs and arrestins, the respective rod isoforms did not emerge until the second round of 2R, just prior to the separation of jawed and agnathan vertebrates. For the triplet of proteins mediating shut-off of the G-protein transducin, RGS9 diverged from RGS11, probably at the second round of 2R, whereas Gβ5 and R9AP appear not to have undergone 2R expansion. Overall, our analysis provides a description of the duplications and losses of phototransduction shut-off genes that occurred during the transition from a chordate with only cone-like photoreceptors to an ancestral vertebrate with both cone- and rod-like photoreceptors.
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
We suggest that the following two rules apply to all jawed vertebrate species that have been studied: (i) if the GRK1A isoform exists in a species, it is expressed in the rod photoreceptors; (ii) if the GRK7 isoform exists, it is expressed in the cone photoreceptors
We propose that the multiple classes of photoreceptor in descendent organisms generally inherited the property of coexpression of one GRK1 and one GRK7, though in some cases the ability to express one member of the pair was lost, and, in other cases, one of the genes was lost
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. The rapid shut-off of activated visual pigment (rhodopsin or its cone equivalent) is a two-step process that first involves phosphorylation by a G-protein receptor kinase (GRK), and capping of the phosphorylated pigment by a visual arrestin Both of these proteins have distinct rod and cone isoforms, GRK1 and GRK7, and Arr-S and Arr-C. Jawed vertebrate genomes typically possess four arrestin genes— SAG (retinal S-antigen), ARR3, ARRB1 and ARRB2—that encode proteins that we denote, respectively, as Arr-S (expressed in rods), Arr-C (in cones), Arr-B1 and Arr-B2. These last two are often referred to as b-arrestins, though they are by no means restricted to the b-adrenergic system, and instead are widely distributed.
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