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On the other hand, much less is known about a regulatory network governing expression of the middle-wavelength–sensitive opsin genes, sws2 and rh2, which have been lost in most mammalian species. Another transcription factor, T-box 2b (Tbx2b), plays an essential role in sws1 opsin expression in zebrafish ( 16). With regard to cone subtypes, thyroid hormone receptor beta (Thrb) is a master transcriptional regulator for expression of lws opsin and responsible for differential expression between lws and sws opsins in mice ( 13), zebrafish ( 14), and human ( 15). A rod master regulator, neural retina leucine zipper (NRL), and its downstream factor, nuclear receptor 2E3 (Nr2e3), enhance rod-specific gene expression and repress sws1 expression ( 11, 12). Cone-rod homeobox (Crx) is an upstream transcriptional regulator for both rod and cone photoreceptors ( 10). In the later process, transcription factors regulate photoreceptor-specific gene expression. Retinal progenitor cells differentiate into all types of retinal neurons in a temporal order, conserved among many species ( 8, 9). This fact supports the idea that the last common ancestor of vertebrates should have had color vision based on the four cone opsin subfamilies ( 4, 7).
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A full set of genes encoding the four cone opsins is present in the Southern Hemisphere lamprey, a jawless vertebrate belonging to the earliest-branching vertebrate group ( 6). Most vertebrates retain the tetrachromatic visual system organized by the four cone opsin subfamilies. Color discrimination is established by a combination of spectrally distinct cone subtypes, each expressing a single cone opsin out of four subfamilies: ultraviolet-sensitive, blue-sensitive (SWS2, λ max: 400 to 470 nm), green-sensitive (RH2, λ max: 460 to 510 nm), and red-sensitive opsins (LWS, λ max: 510 to 560 nm) ( 4, 5). In contrast, cones show a relatively lower sensitivity without saturating in brighter light and mediate photopic vision under a daylight condition. Rods with a higher light-sensitivity respond to single photons and mediate scotopic vision under twilight conditions at night. Most vertebrates have highly developed camera-type eyes with duplex retinas equipped with rod and cone photoreceptor cells ( 1– 3).
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We propose that Foxq2-dependent sws2 expression is a prevalent regulatory mechanism that was acquired at the early stage of vertebrate evolution. A wide range of vertebrate species retain both foxq2 and sws2 genes.
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Foxq2 has dual functions acting as an activator of sws2 transcription and as a suppressor of UV ( sws1) opsin transcription in blue cones. Here, we pursued loss-of-function studies on transcription factors expressed predominantly in zebrafish cone photoreceptors and identified Foxq2 as a blue cone–specific factor driving sws2 gene expression. The blue cone identity is ensured by selective expression of blue ( sws2) opsin, and the mechanism is poorly understood because sws2 gene has been lost in mammalian species such as mouse, whose visual system has been extensively studied. Most vertebrate lineages retain a tetrachromatic visual system, which is supported by a functional combination of spectrally distinct multiple cone photoreceptors, ultraviolet (UV), blue, green, and red cones.