Molecular genetics and the evolution of ultraviolet vision in vertebrates

Abstract

Despite the biological importance of UV vision, its molecular bases are not well understood. Here, we present evidence that UV vision in vertebrates is determined by eight specific amino acids in the UV pigments. Amino acid sequence analyses show that contemporary UV pigments inherited their UV sensitivities from the vertebrate ancestor by retaining most of these eight amino acids. In the avian lineage, the ancestral pigment lost UV sensitivity, but some descendants regained it by one amino acid change. Our results also strongly support the hypothesis that UV pigments have an unprotonated Schiff base-linked chromophore. It is now clear that, counter to the traditional view, many vertebrates use UV vision for such basic behaviors as foraging, social signaling, and mating (1-5). UV vision is achieved by the pigments that absorb light maximally ( max ) at Ϸ360 nm, but the mechanisms of the spectral tuning in these UV pigments remain mostly as an area of speculation. In general, visual pigments consist of an apoprotein, opsin, and an 11-cis-retinal chromophore that is bound to opsin by a Schiff base linkage to the lysine residue in the center of the seventh transmembrane (TM) helix (6). The Schiff base of 11-cis-retinal is usually protonated by the glutamate counterion in the third TM helix (7-9). The protonated Schiff base has a max at 440 nm in solution (10). Through the interaction with an opsin, however, the Schiff base-linked chromophore in a visual pigment can have a max ranging from 360 to 635 nm (11). Interestingly, the unprotonated Schiff base-linked chromophore in solution has a max at 365 nm (12). Thus, it has been proposed that UV pigments may have an unprotonated Schiff base-linked chromophore (13-17), but this hypothesis has not been experimentally tested.Recently, it has been shown that some avian species have acquired UV vision by one amino acid change (17,18). It is also proposed that five amino acid sites regulate the absorption spectra of UV pigments in nonavian species (19). This evolutionary approach, however, lacks rigor in identifying all amino acids involved in the spectral tuning in the UV pigments. Here, to study the molecular bases of UV vision, we first determine the mechanisms of the spectral tuning in the mouse UV pigment. The general molecular bases of UV vision in vertebrates are then studied by considering the mouse UV pigment and other orthologous pigments, often referred to as short-wavelengthsensitive type 1 (SWS1) pigments (20,21). Using the mouse UV pigment, we also examine the effects of the glutamate counterion on the spectral sensitivities of visual pigments. Materials and Methods Construction of Chimeric Pigments and Site-Directed Mutagenesis.The UV opsin cDNA clone of the mouse (Mus musculus) has been subcloned into an expression vector, pMT5 (22). The human blue opsin cDNA clone is a gift from Jeremy Nathans (Johns Hopkins Univ., Baltimore). To subclone the human blue opsin cDNA into pMT5, the cDNA clone was amplified by PCR by using primers: 5Ј-AGGGTGGAATTCCACCATG-AGAAAAA...

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