Light adaptation and the evolution of vertebrate photoreceptors

Abstract

The earliest vertebrates were agnathans - fish-like organisms without jaws, which first appeared near the end of the Cambrian radiation. One group of agnathans became cyclostomes, which include lamprey and hagfish. Other agnathans gave rise to jawed vertebrates or gnathostomes, the group including all other existing vertebrate species. Because cyclostomes diverged from other vertebrates 500 million years ago, it may be possible to infer some of the properties of the retina of early vertebrate progenitors by comparing lamprey to other vertebrates. We have previously shown that rods and cones in lamprey respond to light much like photoreceptors in other vertebrates and have a similar sensitivity. We now show that these affinities are even closer. Both rods and cones adapt to background light and to bleaches in a manner almost identical to other vertebrate photoreceptors. The operating range in darkness is nearly the same in lamprey and in amphibian or mammalian rods and cones; moreover background light shifts response-intensity curves downward and to the right over a similar range of ambient intensities. Rods show increment saturation at about the same intensity as mammalian rods, and cones never saturate. Bleaches decrease sensitivity in part by loss of quantum catch and in part by opsin activation of transduction. These correspondences are so numerous and pervasive that they are unlikely to result from convergent evolution but argue instead that early vertebrate progenitors of both cyclostomes and mammals had photoreceptors much like our own.

The N termini of the inhibitory γ-subunits of phosphodiesterase-6 (PDE6) from rod and cone photoreceptors differentially regulate transducin-mediated PDE6 activation

“…We chose to root our phylogeny in the most evolutionarily parsimonious manner, which places P␥ sequences from the hagfish Eptatretus stoutii at the base of both the rod and cone clades. However, we note that electrophysiological evidence for cyclostome photoreceptor light responsiveness exists only for the lamprey (17,21,22), and other rootings for the P␥ phylogenetic tree could change the affinity of the hagfish P␥ sequences.…”

“…The rod and cone P␥ genes (PDE6G and PDE6H) appear to have evolved with our earliest vertebrate ancestors at the same time when PDE6 catalytic subunit genes arose (14,15) with their unique catalytic and regulatory properties (3). It is noteworthy that the sea lamprey (Petromyzon marinus), a cyclostome that diverged from other vertebrate lineages about 500 million years ago, has a duplex retina in which rod and cone photoreceptors show similar physiological differences to light, as observed with mammalian photoreceptors (16,17). Interestingly, lamprey rods and cones express the same PDE6 catalytic subunit along with distinct rod-and cone-specific P␥ isoforms (18).…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…D, E), likely via gap junctions similar to the contacts between mammalian rods and cones (Asteriti, Gargini & Cangiano, ). Furthermore, short photoreceptors saturate in bright light, similar to rods but not to cones (Morshedian & Fain, ). Taken together, these findings suggest homology between short photoreceptors in lampreys and rods in gnathostomes.…”

Pathways and disease-causing alterations in visual chromophore production for vertebrate vision

“…The visual cycle as well as visual opsin evolution are thought to have been driven by a change in visual ecology as vertebrate predecessors began to occupy deep waters where light-driven 11-cis-retinal production became a non-viable pathway (Freeman et al, 2012). The visual opsins evolved to become more photosensitive and achieve greater efficiency in activating G proteins while at the same time losing their ability to remain covalently link in the binding pocket in cis and trans configurations (Kojima et al, 2017;Morshedian and Fain, 2017). Support for this timeline comes from biochemical and phylogenic studies on the presence of RPE65 and LRAT activities, the two essential enzymes of the classical visual cycle, found in amphioxus and in the early branching cyclostome vertebrate lineage represented by sea lampreys (Poliakov et al, 2012).…”