The molecular mechanism for the spectral shifts between vertebrate ultraviolet- and violet-sensitive cone visual pigments

Abstract

The short-wave-sensitive (SWS) visual pigments of vertebrate cone photoreceptors are divided into two classes on the basis of molecular identity, SWS1 and SWS2. Only the SWS1 class are present in mammals. The SWS1 pigments can be further subdivided into violet-sensitive (VS), with lambda(max) (the peak of maximal absorbance) values generally between 400 and 430 nm, and ultraviolet-sensitive (UVS), with a lambda(max)<380 nm. Phylogenetic evidence indicates that the ancestral pigment was UVS and that VS pigments have evolved separately from UVS pigments in the different vertebrate lineages. In this study, we have examined the mechanism of evolution of VS pigments in the mammalian lineage leading to present day ungulates (cow and pig). Amino acid sequence comparisons of the UVS pigments of teleost fish, amphibia, reptiles and rodents show that site 86 is invariably occupied by Phe but is replaced in bovine and porcine VS pigments by Tyr. Using site-directed mutagenesis of goldfish UVS opsin, we have shown that a Phe-86-->Tyr substitution is sufficient by itself to shift the lambda(max) of the goldfish pigment from a wild-type value of 360 nm to around 420 nm, and the reverse substitution of Tyr-86-Phe into bovine VS opsin produces a similar shift in the opposite direction. The substitution of this single amino acid is sufficient to account therefore for the evolution of bovine and porcine VS pigments. The replacement of Phe with polar Tyr at site 86 is consistent with the stabilization of Schiff-base protonation in VS pigments and the absence of protonation in UVS pigments.

Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus)

“…The presence of a UVS SWS1 pigment is therefore confirmed; this pigment retains Phe86 as proposed for the ancestral vertebrate SWS1 pigment (Hunt et al 2004 and contrasts with the VS SWS1 pigment of the Tamar wallaby (Deeb et al 2003). This latter pigment has Tyr86 as found in the VS pigments of the cow, pig (Cowing et al 2002) and squirrel (Carvalho et al 2006), and represents therefore convergent evolution in the generation of violet sensitivity in metatherian and eutherian mammals.…”

“…The SWS1 pigment of both marsupial species also has Phe86, consistent therefore with a l max in the UV. By contrast, the Tamar wallaby has a VS pigment with Phe86 replaced by Tyr, as found in the bovine and porcine pigments (Cowing et al 2002).…”

How a small change in retinal leads to G‐protein activation: Initial events suggested by molecular dynamics calculations

“…In particular, the results strongly underlie the importance of the protein cavity in forming a part of the solvation environment dictating the type of conformational change that will be determined by the light-activated retinal. 15,[100][101][102][103][104][105][106][107][108] In that sense, the nature of these sidechain and main chain interactions drive a preference for a particular type of excited state and a particular type of relaxation response. Experimental work that shifts the nature of retinal further supports this type of thinking.…”

Evolutionary replacement of UV vision by violet vision in fish

“…However, to achieve these goals, we are faced with two major problems. First, certain amino acid changes at 13 sites are known to shift the max s of SWS1 pigments to date (5,(9)(10)(11)(12)(13)(14), but it is a daunting task to identify other critical amino acid changes because their effects on the max -shift are often not detectible when they are studied individually (9,15,16). Second, and perhaps more disturbingly, no violet-sensitive SWS1 pigment has been isolated from fish (17).…”