Mechanisms of spectral tuning in the mouse green cone pigment

Abstract

Diversification of cone pigment spectral sensitivities during evolution is a prerequisite for the development of color vision. Previous studies have identified two naturally occurring mechanisms that produce variation among vertebrate pigments by red-shifting visual pigment absorbance: addition of hydroxyl groups to the putative chromophore binding pocket and binding of chloride to a putative extracellular loop. In this paper we describe the use of two blue-shifting mechanisms during the evolution of rodent long-wave cone pigments. The mouse green pigment belongs to the long-wave subfamily of cone pigments, but its absorption maximum is 508 nm, similar to that of the rhodopsin subfamily of visual pigments, but blue-shifted 44 nm relative to the human red pigment, its closest homologue. We show that acquisition of a hydroxyl group near the retinylidene Schiff base and loss of the chloride binding site mentioned above fully account for the observed blue shift. These data indicate that the chloride binding site is not a universal attribute of long-wave cone pigments as generally supposed, and that, depending upon location, hydroxyl groups can alter the environment of the chromophore to produce either red or blue shifts.Visual pigments differ between species and between different photoreceptor cells within the same species in their wavelengths of maximal absorption. This diversity of visual pigment absorption spectra is determined by interactions between the 11-cis-retinal chromophore and the particular opsin to which it binds, or in rare instances by the alternate use of an 11-cis-dehydroretinal chromophore (1). Among vertebrate visual pigments that use 11-cis-retinal, absorption maxima have been identified throughout the wavelength interval from 360 nm (2, 3) to 570 nm (4). Sequencing of visual pigments from diverse species shows a limited range of wavelengths of maximal absorption among members of each of the three major branches of the visual pigment family: the short-wave subfamily absorbs maximally at wavelengths less than 500 nm, the rhodopsin subfamily absorbs maximally at wavelengths near 500 nm, and the long-wave subfamily absorbs at wavelengths greater than 500 nm (5-7).Experiments with retinal and its derivatives in solution have led to a number of plausible mechanisms for spectral tuning in visual pigments (8-11). The two photochemical properties of retinal that are most relevant are the shift in absorption maximum from 360 nm to 440 nm upon formation of a protonated Schiff base (12, 13) and the increase in -electron delocalization and the concomitant change in dipole moment that accompanies photoexcitation (14,15). Therefore, amino acids from the apoprotein that alter the polarity, polarizability, or charge density around either the conjugated -electron system or the retinylidene Schiff base would be expected to shift the absorption spectrum of the pigment. In keeping with these models, sequence comparisons and spectroscopic studies of site-directed mutants have identified a glutamate counterio...

Phototransduction in transgenic mice after targeted deletion of the rod transducin α-subunit

“…About 3% of the photoreceptors in the mouse retina are cones that resemble rods at the light-microscopic level (25). However, UV-and mid-wavelength-sensitive cones have spectral maxima at 355-359 nm and 508-511 nm, respectively (16,26,27), whereas the murine rod is maximally sensitive at 502-503 nm. Also, mammalian rods express only a single type of pigment, but at least some cones contain a pigment mixture (16,28).…”

Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi

“…Several mutation analysis studies targeting positions 83 and 292 have been conducted. S292A in RH1 pigments in coelacanth or a replacement at the corresponding position in mammalian red and green pigments shifts the max values 8-28 nm toward red (32,50,51), although the reverse mutation in human pigment did not cause any change (52). It was also reported that D83N in bovine RH1 pigment shifts the max values 6 nm toward blue (53).…”

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

“…The identity of these sequences as orthologues of the LWS sequences in other vertebrate species was obtained by phylogenetic analysis where both form a clade with other LWS sequences (figure 2b). The l max values of LWS pigments across different mammalian species vary from 508 nm in the mouse, Mus musculus (Sun et al 1997), to approximately 565 nm in primates (Bowmaker et al 1991). Since the separate MWS and LWS classes of cone photoreceptors that have been identified by MSP in the retinae of both the honey possum and the fat-tailed dunnart show a similar range with the l max values at 505 and 557 nm for the honey possum, and at 509 and 535 nm for the fat-tailed dunnart, in vitro expression of the fat-tailed dunnart sequence was used to determine the l max of the encoded opsin.…”

“…The LWS pigment in the mouse, M. musculus, has a l max at 508 nm, which is similar to the l max values of the marsupial MWS pigments. This shortwave shift in the mouse pigment arises from a Ser rather than the more usual Ala residue at site 308 combined with the loss of chloride binding arising from a His197Tyr substitution in the chloride-binding site (Sun et al 1997). A genomic fragment that encompasses intron 4 of 776 bp and the flanking regions of exons 3 and 4, the latter including the coding region for His197, was PCR amplified from the fattailed dunnart genomic DNA using the primer pair LWSDC and LWSEK listed in table 1.…”