Haplotype diversity in the human red and green opsin genes: evidence for frequent sequence exchange in exon 3

Abstract

We studied polymorphisms in the coding sequences of the human red and green opsin genes of 133 Caucasian males. Eleven polymorphic sites were discovered in the red opsin gene, seven of which were in exon 3, three in exon 4 and one in exon 5. Polymorphisms at 8 of these sites resulted in amino acid substitutions which generated a total of 18 unique red opsins in the population. The substitutions at three (S180A, I230T, and A233S) of the 8 sites involve hydroxyl-bearing to non-polar amino acid residues, and are therefore likely to alter spectral characteristics of the red pigment. Eight polymorphic sites were observed in the green opsin coding sequences, six of which were in exon 3, one in exon 2 and one in exon 5. Five of the eight involved amino acid substitutions which generated 15 unique green opsins in the population. Substitutions at two of these sites involve hydroxyl-bearing vs. non-polar residues. Six polymorphisms, all of which are located in exon 3, are shared between the red and green opsin genes, essentially making it difficult to assign this exon to either of these genes. Markers in exon 3 are in partial linkage disequilibrium with those in exons 4 and 5, whereas the latter two are in strong linkage disequilibrium with each other. Furthermore, markers in the 5' region of exon 3 are also in only partial (54%) disequilibrium with those in the 3' region. The above results strongly suggest a history of frequent gene conversion, mainly localized to exon 3, in the lineages leading to the human red and green opsin genes.(ABSTRACT TRUNCATED AT 250 WORDS)

Neofunctionalization of Duplicated Genes Under the Pressure of Gene Conversion

“…The sequences of the red and green genes are very similar to each other, indicating that the two genes are undergoing concerted evolution. There are a very limited number of fixed differences between the two genes (Nathans et al 1986;Winderickx et al 1993;Hayashi et al 2001), at least three of which are known to be responsible for the difference in color sensitivity. Particularly, two of the three are closely located in exon 5 (amino acids 277 and 283), and these two account for .80% of the functional difference (measure by l max , a peak value of the light absorption spectrum) between the red and green pigments (Neitz et al 1991).…”

Richer color experience in observers with multiple photopigment opsin genes

“…Neitz & Jacobs, 1986;J. Neitz, M. Neitz, & Jacobs, 1993;Winderickx, Battisti, Hibiya, Motulsky, & Deeb, 1993).…”

“…Although larger sample sizes are needed to accurately assess the population frequency of the serine-180 shift versus the alanine-180 shift, some investigations suggest that the general Caucasian populationshows a~56% occurrence for the "normal" serine 180 and a~44% occurrence of a polymorphic mutation alanine 180 for the red pigment gene. By comparison, the frequency of occurrence for the green pigment gene is~96% "normal" alanine 180 and~4% polymorphic serine 180 (Winderickx et al, 1993). Asenjo et al (1994), M. Neitz and J. , and , show that the serine amino acid at codon 180 is primarily linked to the normal red gene, whereas the presence of alanine at codon 180 can indicate the presence of a polymorphic (shifted) red photopigmentgene, the presence of a normal green gene, or the presence of both a shifted red and a normal green gene.…”

“…On the basis of existing findings (Asenjo et al 1994;Winderickx et al, 1993;Winderickx et al 1992), presence of codon 180 amino acid variants for either the red or the green gene allows several possible phenotypesto be expressed.These are summarized as follows:…”

Minimal Effect of Ectopic Gene Conversion Among Recent Duplicates in Four Mammalian Genomes

“…This pattern has been demonstrated, for example, in the rDNA gene family (Arnheim et al 1980) and visual pigment genes in Old World monkeys (e.g., Winderickx et al 1993;Zhou and Li 1996). Conversely, it has been suggested that gene conversion may generate diversity among paralogs through reassortment of genetic variation in the major histocompatibility complex gene family (e.g., Weiss et al 1983;Ohta 1997;Martinsohn et al 1999).…”