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1
Kojima, Keiichi, Takahiro Yamashita, Yasushi Imamoto, Takehiro G. Kusakabe, Motoyuki Tsuda, and Yoshinori Shichida. "Evolutionary steps involving counterion displacement in a tunicate opsin." Proceedings of the National Academy of Sciences 114, no. 23 (May 22, 2017): 6028–33. http://dx.doi.org/10.1073/pnas.1701088114.
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Ci-opsin1 is a visible light-sensitive opsin present in the larval ocellus of an ascidian, Ciona intestinalis. This invertebrate opsin belongs to the vertebrate visual and nonvisual opsin groups in the opsin phylogenetic tree. Ci-opsin1 contains candidate counterions (glutamic acid residues) at positions 113 and 181; the former is a newly acquired position in the vertebrate visual opsin lineage, whereas the latter is an ancestral position widely conserved among invertebrate opsins. Here, we show that Glu113 and Glu181 in Ci-opsin1 act synergistically as counterions, which imparts molecular properties to Ci-opsin1 intermediate between those of vertebrate- and invertebrate-type opsins. Synergy between the counterions in Ci-opsin1 was demonstrated by E113Q and E181Q mutants that exhibit a pH-dependent spectral shift, whereas only the E113Q mutation in vertebrate rhodopsin yields this spectral shift. On absorbing light, Ci-opsin1 forms an equilibrium between two intermediates with protonated and deprotonated Schiff bases, namely the MI-like and MII-like intermediates, respectively. Adding G protein caused the equilibrium to shift toward the MI-like intermediate, indicating that Ci-opsin1 has a protonated Schiff base in its active state, like invertebrate-type opsins. Ci-opsin1’s G protein activation efficiency is between the efficiencies of vertebrate- and invertebrate-type opsins. Interestingly, the E113Y and E181S mutations change the molecular properties of Ci-opsin1 into those resembling invertebrate-type or bistable opsins and vertebrate ancient/vertebrate ancient-long or monostable opsins, respectively. These results strongly suggest that acquisition of counterion Glu113 changed the molecular properties of visual opsin in a vertebrate/tunicate common ancestor as a crucial step in the evolution of vertebrate visual opsins.
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Zhang, Tao, Li-Hui Cao, Sandeep Kumar, Nduka O. Enemchukwu, Ning Zhang, Alyssia Lambert, Xuchen Zhao, et al. "Dimerization of visual pigments in vivo." Proceedings of the National Academy of Sciences 113, no. 32 (July 26, 2016): 9093–98. http://dx.doi.org/10.1073/pnas.1609018113.
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It is a deeply engrained notion that the visual pigment rhodopsin signals light as a monomer, even though many G protein-coupled receptors are now known to exist and function as dimers. Nonetheless, recent studies (albeit all in vitro) have suggested that rhodopsin and its chromophore-free apoprotein, R-opsin, may indeed exist as a homodimer in rod disk membranes. Given the overwhelmingly strong historical context, the crucial remaining question, therefore, is whether pigment dimerization truly exists naturally and what function this dimerization may serve. We addressed this question in vivo with a unique mouse line (S-opsin+Lrat−/−) expressing, transgenically, short-wavelength–sensitive cone opsin (S-opsin) in rods and also lacking chromophore to exploit the fact that cone opsins, but not R-opsin, require chromophore for proper folding and trafficking to the photoreceptor’s outer segment. In R-opsin’s absence, S-opsin in these transgenic rods without chromophore was mislocalized; in R-opsin’s presence, however, S-opsin trafficked normally to the rod outer segment and produced functional S-pigment upon subsequent chromophore restoration. Introducing a competing R-opsin transmembrane helix H1 or helix H8 peptide, but not helix H4 or helix H5 peptide, into these transgenic rods caused mislocalization of R-opsin and S-opsin to the perinuclear endoplasmic reticulum. Importantly, a similar peptide-competition effect was observed even in WT rods. Our work provides convincing evidence for visual pigment dimerization in vivo under physiological conditions and for its role in pigment maturation and targeting. Our work raises new questions regarding a potential mechanistic role of dimerization in rhodopsin signaling.
3
Upton, Brian A., Nicolás M. Díaz, Shannon A. Gordon, Russell N. Van Gelder, Ethan D. Buhr, and Richard A. Lang. "Evolutionary Constraint on Visual and Nonvisual Mammalian Opsins." Journal of Biological Rhythms 36, no. 2 (March 25, 2021): 109–26. http://dx.doi.org/10.1177/0748730421999870.
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Animals have evolved light-sensitive G protein–coupled receptors, known as opsins, to detect coherent and ambient light for visual and nonvisual functions. These opsins have evolved to satisfy the particular lighting niches of the organisms that express them. While many unique patterns of evolution have been identified in mammals for rod and cone opsins, far less is known about the atypical mammalian opsins. Using genomic data from over 400 mammalian species from 22 orders, unique patterns of evolution for each mammalian opsins were identified, including photoisomerases, RGR-opsin (RGR) and peropsin (RRH), as well as atypical opsins, encephalopsin (OPN3), melanopsin (OPN4), and neuropsin (OPN5). The results demonstrate that OPN5 and rhodopsin show extreme conservation across all mammalian lineages. The cone opsins, SWS1 and LWS, and the nonvisual opsins, OPN3 and RRH, demonstrate a moderate degree of sequence conservation relative to other opsins, with some instances of lineage-specific gene loss. Finally, the photoisomerase, RGR, and the best-studied atypical opsin, OPN4, have high sequence diversity within mammals. These conservation patterns are maintained in human populations. Importantly, all mammalian opsins retain key amino acid residues important for conjugation to retinal-based chromophores, permitting light sensitivity. These patterns of evolution are discussed along with known functions of each atypical opsin, such as in circadian or metabolic physiology, to provide insight into the observed patterns of evolutionary constraint.
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Liénard, Marjorie A., Gary D. Bernard, Andrew Allen, Jean-Marc Lassance, Siliang Song, Richard Rabideau Childers, Nanfang Yu, et al. "The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies." Proceedings of the National Academy of Sciences 118, no. 6 (February 5, 2021): e2008986118. http://dx.doi.org/10.1073/pnas.2008986118.
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Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate Gq protein-coupled opsins function in a novel or convergent way compared to vertebrate Gt opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple Gq opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation.
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PORTER, MEGAN L., MICHAEL J. BOK, PHYLLIS R. ROBINSON, and THOMAS W. CRONIN. "Molecular diversity of visual pigments in Stomatopoda (Crustacea)." Visual Neuroscience 26, no. 3 (May 2009): 255–65. http://dx.doi.org/10.1017/s0952523809090129.
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AbstractStomatopod crustaceans possess apposition compound eyes that contain more photoreceptor types than any other animal described. While the anatomy and physiology of this complexity have been studied for more than two decades, few studies have investigated the molecular aspects underlying the stomatopod visual complexity. Based on previous studies of the structure and function of the different types of photoreceptors, stomatopod retinas are hypothesized to contain up to 16 different visual pigments, with 6 of these having sensitivity to middle or long wavelengths of light. We investigated stomatopod middle- and long-wavelength-sensitive opsin genes from five species with the hypothesis that each species investigated would express up to six different opsin genes. In order to understand the evolution of this class of stomatopod opsins, we examined the complement of expressed transcripts in the retinas of species representing a broad taxonomic range (four families and three superfamilies). A total of 54 unique retinal opsins were isolated, resulting in 6–15 different expressed transcripts in each species. Phylogenetically, these transcripts form six distinct clades, grouping with other crustacean opsins and sister to insect long-wavelength visual pigments. Within these stomatopod opsin groups, intra- and interspecific clusters of highly similar transcripts suggest that there has been rampant recent gene duplication. Some of the observed molecular diversity is also due to ancient gene duplication events within the stem crustacean lineage. Using evolutionary trace analysis, 10 amino acid sites were identified as functionally divergent among the six stomatopod opsin clades. These sites form tight clusters in two regions of the opsin protein known to be functionally important: six in the chromophore-binding pocket and four at the cytoplasmic surface in loops II and III. These two clusters of sites indicate that stomatopod opsins have diverged with respect to both spectral tuning and signal transduction.
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Dalton, Brian E., Ellis R. Loew, Thomas W. Cronin, and Karen L. Carleton. "Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field." Proceedings of the Royal Society B: Biological Sciences 281, no. 1797 (December 22, 2014): 20141980. http://dx.doi.org/10.1098/rspb.2014.1980.
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Vision frequently mediates critical behaviours, and photoreceptors must respond to the light available to accomplish these tasks. Most photoreceptors are thought to contain a single visual pigment, an opsin protein bound to a chromophore, which together determine spectral sensitivity. Mechanisms of spectral tuning include altering the opsin, changing the chromophore and incorporating pre-receptor filtering. A few exceptions to the use of a single visual pigment have been documented in which a single mature photoreceptor coexpresses opsins that form spectrally distinct visual pigments, and in these exceptions the functional significance of coexpression is unclear. Here we document for the first time photoreceptors coexpressing spectrally distinct opsin genes in a manner that tunes sensitivity to the light environment. Photoreceptors of the cichlid fish, Metriaclima zebra , mix different pairs of opsins in retinal regions that view distinct backgrounds. The mixing of visual pigments increases absorbance of the corresponding background, potentially aiding the detection of dark objects. Thus, opsin coexpression may be a novel mechanism of spectral tuning that could be useful for detecting prey, predators and mates. However, our calculations show that coexpression of some opsins can hinder colour discrimination, creating a trade-off between visual functions.
7
ISAYAMA, T., Y. CHEN, M. KONO, W. J. DEGRIP, J. X. MA, R. K. CROUCH, and C. L. MAKINO. "Differences in the pharmacological activation of visual opsins." Visual Neuroscience 23, no. 6 (November 2006): 899–908. http://dx.doi.org/10.1017/s0952523806230256.
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Opsins, like many other G-protein-coupled receptors, sustain constitutive activity in the absence of ligand. In partially bleached rods and cones, opsin's activity closes cGMP-gated channels and produces a state of “pigment adaptation” with reduced sensitivity to light and accelerated flash response kinetics. The truncated retinal analogue, β-ionone, further desensitizes partially bleached green-sensitive salamander rods, but enables partially bleached red-sensitive cones to recover dark-adapted physiology. Structural differences between rod and cone opsins were proposed to explain the effect. Rods and cones, however, also contain different transducins, raising the possibility that G-protein type determines the photoreceptor-specific effects of β-ionone. To test the two hypotheses, we applied β-ionone to partially bleached blue-sensitive rods and cones of salamander, two cells that couple the same cone-like opsin to either rod or cone transducin, respectively. Immunocytochemistry confirmed that all salamander rods contain one form of transducin, whereas all cones contain another. β-Ionone enhanced pigment adaptation in blue-sensitive rods, but it also did so in blue- and UV-sensitive cones. Furthermore, all recombinant salamander rod and cone opsins, with the exception of the red-sensitive cone opsin, activated rod transducin upon the addition of β-ionone. Thus opsin structure determines the identity of β-ionone as an agonist or an inverse agonist and in that respect distinguishes the red-sensitive cone opsin from all others.
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Musilova, Zuzana, Fabio Cortesi, Michael Matschiner, Wayne I. L. Davies, Jagdish Suresh Patel, Sara M. Stieb, Fanny de Busserolles, et al. "Vision using multiple distinct rod opsins in deep-sea fishes." Science 364, no. 6440 (May 9, 2019): 588–92. http://dx.doi.org/10.1126/science.aav4632.
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Vertebrate vision is accomplished through light-sensitive photopigments consisting of an opsin protein bound to a chromophore. In dim light, vertebrates generally rely on a single rod opsin [rhodopsin 1 (RH1)] for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their RH1 gene repertoires. Among these, the silver spinyfin (Diretmus argenteus) stands out as having the highest number of visual opsins in vertebrates (two cone opsins and 38 rod opsins). Spinyfins express up to 14 RH1s (including the most blueshifted rod photopigments known), which cover the range of the residual daylight as well as the bioluminescence spectrum present in the deep sea. Our findings present molecular and functional evidence for the recurrent evolution of multiple rod opsin–based vision in vertebrates.
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FASICK, JEFFRY I., THOMAS W. CRONIN, DAVID M. HUNT, and PHYLLIS R. ROBINSON. "The visual pigments of the bottlenose dolphin (Tursiops truncatus)." Visual Neuroscience 15, no. 4 (April 1998): 643–51. http://dx.doi.org/10.1017/s0952523898154056.
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To assess the dolphin's capacity for color vision and determine the absorption maxima of the dolphin visual pigments, we have cloned and expressed the dolphin opsin genes. On the basis of sequence homology with other mammalian opsins, a dolphin rod and long-wavelength sensitive (LWS) cone opsin cDNAs were identified. Both dolphin opsin cDNAs were expressed in mammalian COS-7 cells. The resulting proteins were reconstituted with the chromophore 11-cis-retinal resulting in functional pigments with absorption maxima (λmax) of 488 and 524 nm for the rod and cone pigments respectively. These λmax values are considerably blue shifted compared to those of many terrestrial mammals. Although the dolphin possesses a gene homologous to other mammalian short-wavelength sensitive (SWS) opsins, it is not expressed in vivo and has accumulated a number of deletions, including a frame-shift mutation at nucleotide position 31. The dolphin therefore lacks the common dichromatic form of color vision typical of most terrestrial mammals.
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VIHTELIC, THOMAS S., CHRISTOPHER J. DORO, and DAVID R. HYDE. "Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins." Visual Neuroscience 16, no. 3 (May 1999): 571–85. http://dx.doi.org/10.1017/s0952523899163168.
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Zebrafish (Danio rerio) represents an excellent genetic model for vertebrate visual system studies. Because the opsin proteins are ideal markers of specific photoreceptor cell types, we cloned six different zebrafish opsin cDNAs. Based on pairwise alignments and phylogenetic comparisons between the predicted zebrafish opsin amino acid sequences and other vertebrate opsins, the cDNAs encode rhodopsin, two different green opsins (zfgr1 and zfgr2), a red, a blue, and an ultraviolet opsin. Phylogenetic analysis indicates the zfgr1 protein occupies a well-resolved dendrogram branch separate from the other green opsins examined, while zebrafish ultraviolet opsin is closely related to the human blue- and chicken violet-sensitive proteins. Polyclonal antisera were generated against individual bacterial fusion proteins containing either the red, blue, or ultraviolet amino termini or the rod or green opsin carboxyl termini. Immunolocalization on adult zebrafish frozen sections demonstrates the green and red opsins are each expressed in different members of the double cone cell pair, the blue opsin is detected in long single cones, and the ultraviolet opsin protein is expressed in the short single cones. In 120-h postfertilization wholemounts, green, red, blue, and ultraviolet opsin-positive cells are detected in an orderly arrangement throughout the entire retina. The antibodies' photoreceptor-type specificity indicates they will be useful for characterizing both wild-type and mutant zebrafish retinas.
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Zhang, Sufang, Xiangbo Kong, Fu Liu, and Zhen Zhang. "Identification and Expression Patterns of Opsin Genes in a Forest Insect, Dendrolimus punctatus." Insects 11, no. 2 (February 11, 2020): 116. http://dx.doi.org/10.3390/insects11020116.
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Dendrolimus punctatus walker (Lepidoptera: Lasiocampidae) is the most serious coniferous forest defoliator in China. This species has long life history, and shows different activity rhythms and light response behaviors at larval and adult stages. Insect vision system play important roles for survival and reproduction, and disturbance of photoreception may help us to control this pest. However, we know little about the visual system of D. punctatus. As opsins are the most important genes determining photoreceptor sensitivity of insects, we identified opsins of D. punctatus and analyzed their expression patterns at different development stages in this study. Four opsin genes were identified based on our transcriptome data. Phylogenetic analysis showed that there are three classical ultraviolet (UV), blue, and long-wavelength (LW) light sensitive opsin genes, and another UV-like opsin as homolog of a circadian photoreceptor, Rh7, in Drosophila melanogaster and other insects. Expression analysis indicated that the UV and UV-like opsins expression levels only fluctuated slightly during whole life stages of D. punctatus, while Blue and LW opsins were up-regulated many times at adult stage. Interestingly, the ratio of UV-opsin was much higher in eggs and larvae stages, and lower in pupa and adult stages; reversely, LW-opsin showed extremely high relative ratio in pupa and adult stages. High expression level of LW opsin in the adult stage may correlate to the nocturnal lifestyles of this species at adult stage, and different ratios of UV and LW opsins in larval and adult stages may help to explain the different visual ecologies of these two development stages of D. punctatus. This work is the foundation for further research of opsin functions and vision mechanisms of D. punctatus.
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Porter, Megan L., Hiroko Awata, Michael J. Bok, and Thomas W. Cronin. "Exceptional diversity of opsin expression patterns in Neogonodactylus oerstedii (Stomatopoda) retinas." Proceedings of the National Academy of Sciences 117, no. 16 (April 2, 2020): 8948–57. http://dx.doi.org/10.1073/pnas.1917303117.
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Stomatopod crustaceans possess some of the most complex animal visual systems, including at least 16 spectrally distinct types of photoreceptive units (e.g., assemblages of photoreceptor cells). Here we fully characterize the set of opsin genes expressed in retinal tissues and determine expression patterns of each in the stomatopod Neogonodactylus oerstedii. Using a combination of transcriptome and RACE sequencing, we identified 33 opsin transcripts expressed in each N. oerstedii eye, which are predicted to form 20 long-wavelength–sensitive, 10 middle-wavelength–sensitive, and three UV-sensitive visual pigments. Observed expression patterns of these 33 transcripts were highly unusual in five respects: 1) All long-wavelength and short/middle-wavelength photoreceptive units expressed multiple opsins, while UV photoreceptor cells expressed single opsins; 2) most of the long-wavelength photoreceptive units expressed at least one middle-wavelength–sensitive opsin transcript; 3) the photoreceptors involved in spatial, motion, and polarization vision expressed more transcripts than those involved in color vision; 4) there is a unique opsin transcript that is expressed in all eight of the photoreceptive units devoted to color vision; and 5) expression patterns in the peripheral hemispheres of the eyes suggest visual specializations not previously recognized in stomatopods. Elucidating the expression patterns of all opsin transcripts expressed in the N. oerstedii retina reveals the potential for previously undocumented functional diversity in the already complex stomatopod eye and is a first step toward understanding the functional significance of the unusual abundance of opsins found in many arthropod species’ visual systems.
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Neal, S., D. M. de Jong, and E. C. Seaver. "CRISPR/CAS9 mutagenesis of a single r-opsin gene blocks phototaxis in a marine larva." Proceedings of the Royal Society B: Biological Sciences 286, no. 1904 (June 5, 2019): 20182491. http://dx.doi.org/10.1098/rspb.2018.2491.
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Many marine animals depend upon a larval phase of their life cycle to locate suitable habitat, and larvae use light detection to influence swimming behaviour and dispersal. Light detection is mediated by the opsin genes, which encode light-sensitive transmembrane proteins. Previous studies suggest that r-opsins in the eyes mediate locomotory behaviour in marine protostomes, but few have provided direct evidence through gene mutagenesis. Larvae of the marine annelid Capitella teleta have simple eyespots and are positively phototactic, although the molecular components that mediate this behaviour are unknown. Here, we characterize the spatio-temporal expression of the rhabdomeric opsin genes in C. teleta and show that a single rhabdomeric opsin gene, Ct-r-opsin1 , is expressed in the larval photoreceptor cells. To investigate its function, Ct-r-opsin1 was disrupted using CRISPR/CAS9 mutagenesis. Polymerase chain reaction amplification and DNA sequencing demonstrated efficient editing of the Ct-r-opsin1 locus. In addition, the pattern of Ct-r-opsin1 expression in photoreceptor cells was altered. Notably, there was a significant decrease in larval phototaxis, although the eyespot photoreceptor cell and associated pigment cell formed normally and persisted in Ct-r-opsin1 -mutant animals. The loss of phototaxis owing to mutations in Ct-r-opsin1 is similar to that observed when the entire photoreceptor and pigment cell are deleted, demonstrating that a single r-opsin gene is sufficient to mediate phototaxis in C. teleta . These results establish the feasibility of gene editing in animals like C. teleta , and extend previous work on the development, evolution and function of the C. teleta visual system . Our study represents one example of disruption of animal behaviour by gene editing through CRISPR/CAS9 mutagenesis, and has broad implications for performing genome editing studies in a wide variety of other understudied animals.
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Bloch, Natasha I. "Evolution of opsin expression in birds driven by sexual selection and habitat." Proceedings of the Royal Society B: Biological Sciences 282, no. 1798 (January 7, 2015): 20142321. http://dx.doi.org/10.1098/rspb.2014.2321.
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Theories of sexual and natural selection predict coevolution of visual perception with conspecific colour and/or the light environment animals occupy. One way to test these theories is to focus on the visual system, which can be achieved by studying the opsin-based visual pigments that mediate vision. Birds vary greatly in colour, but opsin gene coding sequences and associated visual pigment spectral sensitivities are known to be rather invariant across birds. Here, I studied expression of the four cone opsin genes ( Lws, Rh2, Sws2 and Sws1 ) in 16 species of New World warblers (Parulidae). I found levels of opsin expression vary both across species and between the sexes. Across species, female, but not male Sws2 expression is associated with an index of sexual selection, plumage dichromatism. This fits predictions of classic sexual selection models, in which the sensory system changes in females, presumably impacting female preference, and co-evolves with male plumage. Expression of the opsins at the extremes of the light spectrum, Lws and Uvs, correlates with the inferred light environment occupied by the different species. Unlike opsin spectral tuning, regulation of opsin gene expression allows for fast adaptive evolution of the visual system in response to natural and sexual selection, and in particular, sex-specific selection pressures.
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Chinen, Akito, Takanori Hamaoka, Yukihiro Yamada, and Shoji Kawamura. "Gene Duplication and Spectral Diversification of Cone Visual Pigments of Zebrafish." Genetics 163, no. 2 (February 1, 2003): 663–75. http://dx.doi.org/10.1093/genetics/163.2.663.
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Abstract Zebrafish is becoming a powerful animal model for the study of vision but the genomic organization and variation of its visual opsins have not been fully characterized. We show here that zebrafish has two red (LWS-1 and LWS-2), four green (RH2-1, RH2-2, RH2-3, and RH2-4), and single blue (SWS2) and ultraviolet (SWS1) opsin genes in the genome, among which LWS-2, RH2-2, and RH2-3 are novel. SWS2, LWS-1, and LWS-2 are located in tandem and RH2-1, RH2-2, RH2-3, and RH2-4 form another tandem gene cluster. The peak absorption spectra (λmax) of the reconstituted photopigments from the opsin cDNAs differed markedly among them: 558 nm (LWS-1), 548 nm (LWS-2), 467 nm (RH2-1), 476 nm (RH2-2), 488 nm (RH2-3), 505 nm (RH2-4), 355 nm (SWS1), 416 nm (SWS2), and 501 nm (RH1, rod opsin). The quantitative RT-PCR revealed a considerable difference among the opsin genes in the expression level in the retina. The expression of the two red opsin genes and of three green opsin genes, RH2-1, RH2-3, and RH2-4, is significantly lower than that of RH2-2, SWS1, and SWS2. These findings must contribute to our comprehensive understanding of visual capabilities of zebrafish and the evolution of the fish visual system and should become a basis of further studies on expression and developmental regulation of the opsin genes.
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DALAL, JASBIR S., ROBERT N. JINKS, CHELSIE CACCIATORE, ROBERT M. GREENBERG, and BARBARA-ANNE BATTELLE. "Limulus opsins: Diurnal regulation of expression." Visual Neuroscience 20, no. 5 (September 2003): 523–34. http://dx.doi.org/10.1017/s095252380320506x.
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Much has been learned from studies of Limulus photoreceptors about the role of the circadian clock and light in the removal of photosensitive membrane. However, little is known in this animal about mechanisms regulating photosensitive membrane renewal, including the synthesis of proteins in, and associated with, the photosensitive membrane. To begin to understand renewal, this study examines diurnal changes in the levels of mRNAs encoding opsin, the integral membrane protein component of visual pigment, and the relative roles of light and the circadian clock in producing these changes. We show that at least two distinct opsin genes encoding very similar proteins are expressed in both the lateral and ventral eyes, and that during the day and night in the lateral eye, the average level of mRNA encoding opsin1 is consistently higher than that encoding opsin2. Northern blot assays showed further that total opsin mRNA in the lateral eyes of animals maintained under natural illumination increases during the afternoon (9 & 12 h after sunrise) in the light and falls at night in the dark. This diurnal change occurs whether or not the eyes receive input from the circadian clock, but it is eliminated in eyes maintained in the dark. Thus, it is regulated by light and darkness, not by the circadian clock, with light stimulating an increase in opsin mRNA levels. The rise in opsin mRNA levels observed under natural illumination was seasonal; it occurred during the summer but not the spring and fall. However, a significant increase in opsin mRNA levels could be achieved in the fall by exposing lateral eyes to 3 h of natural illumination followed by 9 h of artificial light. The diurnal regulation of opsin mRNA levels contrasts sharply with the circadian regulation of visual arrestin mRNA levels (Battelle et al., 2000). Thus, in Limulus, distinctly different mechanisms regulate the levels of mRNA encoding two proteins critical for the photoresponse.
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Makino, C. L., and R. L. Dodd. "Multiple visual pigments in a photoreceptor of the salamander retina." Journal of General Physiology 108, no. 1 (July 1, 1996): 27–34. http://dx.doi.org/10.1085/jgp.108.1.27.
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Although a given retina typically contains several visual pigments, each formed from a retinal chromophore bound to a specific opsin protein, single photoreceptor cells have been thought to express only one type of opsin. This design maximizes a cell's sensitivity to a particular wavelength band and facilitates wavelength discrimination in retinas that process color. We report electrophysiological evidence that the ultraviolet-sensitive cone of salamander violates this rule. This cell contains three different functional opsins. The three opsins could combine with the two different chromophores present in salamander retina to form six visual pigments. Whereas rods and other cones of salamander use both chromophores, they appear to express only one type of opsin per cell. In visual pigment absorption spectra, the bandwidth at half-maximal sensitivity increases as the pigment's wavelength maximum decreases. However, the bandwidth of the UV-absorbing pigment deviates from this trend; it is narrow like that of a red-absorbing pigment. In addition, the UV-absorbing pigment has a high apparent photosensitivity when compared with that of red- and blue-absorbing pigments and rhodopsin. These properties suggest that the mechanisms responsible for spectrally tuning visual pigments separate two absorption bands as the wavelength of maximal sensitivity shifts from UV to long wavelengths.
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Kefalov, Vladimir J., M. Carter Cornwall, and Rosalie K. Crouch. "Occupancy of the Chromophore Binding Site of Opsin Activates Visual Transduction in Rod Photoreceptors." Journal of General Physiology 113, no. 3 (March 1, 1999): 491–503. http://dx.doi.org/10.1085/jgp.113.3.491.
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The retinal analogue β-ionone was used to investigate possible physiological effects of the noncovalent interaction between rod opsin and its chromophore 11-cis retinal. Isolated salamander rod photoreceptors were exposed to bright light that bleached a significant fraction of their pigment, were allowed to recover to a steady state, and then were exposed to β-ionone. Our experiments show that in bleach-adapted rods β-ionone causes a decrease in light sensitivity and dark current and an acceleration of the dim flash photoresponse and the rate constants of guanylyl cyclase and cGMP phosphodiesterase. Together, these observations indicate that in bleach-adapted rods β-ionone activates phototransduction in the dark. Control experiments showed no effect of β-ionone in either fully dark-adapted or background light-adapted cells, indicating direct interaction of β-ionone with the free opsin produced by bleaching. We speculate that β-ionone binds specifically in the chromophore pocket of opsin to produce a complex that is more catalytically potent than free opsin alone. We hypothesize that a similar reaction may occur in the intact retina during pigment regeneration. We propose a model of rod pigment regeneration in which binding of 11-cis retinal to opsin leads to activation of the complex accompanied by a decrease in light sensitivity. The subsequent covalent attachment of retinal to opsin completely inactivates opsin and leads to the recovery of sensitivity. Our findings resolve the conflict between biochemical and physiological data concerning the effect of the occupancy of the chromophore binding site on the catalytic potency of opsin. We show that binding of β-ionone to rod opsin produces effects opposite to its previously described effects on cone opsin. We propose that this distinction is due to a fundamental difference in the interaction of rod and cone opsins with retinal, which may have implications for the different physiology of the two types of photoreceptors.
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Helvik, Jon Vidar, Øyvind Drivenes, Torstein Harboe, and Hee-Chan Seo. "Topography of different photoreceptor cell types in the larval retina of Atlantic halibut (Hippoglossus hippoglossus)." Journal of Experimental Biology 204, no. 14 (July 15, 2001): 2553–59. http://dx.doi.org/10.1242/jeb.204.14.2553.
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SUMMARY The identities of single cone cells in the retina of Atlantic halibut (Hippoglossus hippoglossus) larvae were studied by in situ hybridisation using RNA probes for the five different halibut opsins. Four different cone opsins (ultraviolet-, blue-, green- and red-sensitive) are expressed in Atlantic halibut at the end of the yolk-sac period, whereas rod opsin is expressed later in development. Photoreceptor cells expressing ultraviolet-sensitive opsin are found only in the ventral retina, presumably to optimise detection of the downwelling ultraviolet light. The majority of the photoreceptors (approximately 90%) in the retina express green-sensitive opsin and its distribution shows no regional differences. In contrast, blue- and red-sensitive opsins are expressed much less frequently (in approximately 10% of photoreceptors), although these two opsins are also found over the entire retina. The expression patterns of the different visual pigments indicate some form of mosaic expression in the single-coned larval retina, and this is reminiscent of the square mosaic expression found in post-metamorphic Atlantic halibut. These findings suggest plasticity in green-opsin-expressing cells during development, resulting in a square mosaic expression pattern.
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Veldhoen, Kathy, Luc Beaudet, John Runions, Sansar Sharma, and Craig Hawryshyn. "Antibody labeling of the blue-sensitive cones in the retinae of teleost fishes." Canadian Journal of Zoology 77, no. 11 (December 1, 1999): 1733–39. http://dx.doi.org/10.1139/z99-120.
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Characterization of visual opsins can be achieved with the use of specific polyclonal or monoclonal antibodies. In this study, antiserum was raised against a conjugate protein including an N-terminal sequence of the short wavelength sensitive (SWS, commonly referred to as blue-sensitive) visual pigment opsin in goldfish (Carrasius auratus). The antiserum showed immunoreactivity to retinae of phylogenetically distant teleosts, including the goldfish, rainbow trout (Oncorhynchus mykiss), and bluehead wrasse (Thalassoma bisasciatum). Complementary DNA (cDNA) was synthesized from goldfish retinal messenger RNA. An N-terminal sequence of the SWS opsin was PCR-amplified from the cDNA and subsequently cloned into an expression vector. Expressed protein was purified by metal chelate affinity chromatography and used to immunize New Zealand white rabbits. Immune serum was collected and used in immunocytochemical assays, which revealed that the antiserum contains antibodies specific for an opsin that resides in single-cone photoreceptors of the goldfish, rainbow trout, and bluehead wrasse. The results confirm those from earlier studies of goldfish in which short-wavelength sensitivity was localized to single cones, and suggest that the association between short-wavelength sensitivity and single cones may be a feature common to many teleosts. The production of antiserum specific for SWS opsins provides a useful tool in the characterization of opsin expression within teleost retinae.
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Srinivas, Maya, Lily Ng, Hong Liu, Li Jia, and Douglas Forrest. "Activation of the Blue Opsin Gene in Cone Photoreceptor Development by Retinoid-Related Orphan Receptor β." Molecular Endocrinology 20, no. 8 (August 1, 2006): 1728–41. http://dx.doi.org/10.1210/me.2005-0505.
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Abstract Color vision requires the expression of opsin photopigments with different wavelength sensitivities in retinal cone photoreceptors. The basic color visual system of mammals is dichromatic, involving differential expression in the cone population of two opsins with sensitivity to short (S, blue) or medium (M, green) wavelengths. However, little is known of the factors that directly activate these opsin genes and thereby contribute to the S or M opsin identity of the cone. We report that the orphan nuclear receptor RORβ (retinoid-related orphan receptor β) activates the S opsin gene (Opn1sw) through binding sites upstream of the gene. RORβ lacks a known physiological ligand and activates the Opn1sw promoter modestly alone but strongly in synergy with the retinal cone-rod homeobox factor (CRX), suggesting a cooperative means of enhancing RORβ activity. Comparison of wild-type and mutant lacZ reporter transgenes showed that the RORβ-binding sites in Opn1sw are required for expression in mouse retina. RORβ-deficient mice fail to induce S opsin appropriately during postnatal cone development. Photoreceptors in these mice also lack outer segments, indicating additional functions for RORβ in photoreceptor morphological maturation. The results identify Opn1sw as a target gene for RORβ and suggest a key role for RORβ in regulating opsin expression in the color visual system.
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Chung, Wen-Sung, and N. Justin Marshall. "Comparative visual ecology of cephalopods from different habitats." Proceedings of the Royal Society B: Biological Sciences 283, no. 1838 (September 14, 2016): 20161346. http://dx.doi.org/10.1098/rspb.2016.1346.
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Previous investigations of vision and visual pigment evolution in aquatic predators have focused on fish and crustaceans, generally ignoring the cephalopods. Since the first cephalopod opsin was sequenced in late 1980s, we now have data on over 50 cephalopod opsins, prompting this functional and phylogenetic examination. Much of this data does not specifically examine the visual pigment spectral absorbance position ( λ max ) relative to environment or lifestyle, and cephalopod opsin functional adaptation and visual ecology remain largely unknown. Here we introduce a new protocol for photoreceptor microspectrophotometry (MSP) that overcomes the difficulty of bleaching the bistable visual pigment and that reveals eight coastal coleoid cephalopods to be monochromatic with λ max varying from 484 to 505 nm. A combination of current MSP results, the λ max values previously characterized using cephalopod retinal extracts (467–500 nm) and the corresponding opsin phylogenetic tree were used for systematic comparisons with an end goal of examining the adaptations of coleoid visual pigments to different light environments. Spectral tuning shifts are described in response to different modes of life and light conditions. A new spectral tuning model suggests that nine amino acid substitution sites may determine the direction and the magnitude of spectral shifts.
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CHENG, CHRISTIANA L., and IÑIGO NOVALES FLAMARIQUE. "Photoreceptor distribution in the retina of adult Pacific salmon: Corner cones express blue opsin." Visual Neuroscience 24, no. 3 (May 2007): 269–76. http://dx.doi.org/10.1017/s0952523807070137.
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The retina of salmonid fishes has two types of cone photoreceptors: single and double cones. At the nuclear level, these cones are distributed in a square mosaic such that the double cones form the sides of the square and the single cones occupy positions at the centre and at the corners of the square. Double cones consist of two members, one having visual pigment protein maximally sensitive to green light (RH2 opsin), the other maximally sensitive to red light (LWS opsin). Single cones can have opsins maximally sensitive to ultraviolet (UV) or blue light (SWS1 and SWS2 opsins, respectively). In Pacific salmonids, all single cones express UV opsin at hatching. Around the time of yolk sac absorption, single cones start switching opsin expression from UV to blue, in an event that proceeds from the ventral to the dorsal retina. This transformation is accompanied by a loss of single corner cones such that the large juvenile shows corner cones and UV opsin expression in the dorsal retina only. Previous research has shown that adult Pacific salmon have corner cones over large areas of retina suggesting that these cones may be regenerated and that they may express UV opsin. Here we used in-situ hybridization with cRNA probes and RT-PCR to show that: (1) all single cones in non-growth zone areas of the retina express blue opsin and (2) double cone opsin expression alternates around the square mosaic unit. Our results indicate that single cone driven UV sensitivity in adult salmon must emanate from stimulation of growth zone areas.
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Kawamura, Shoji, Nathan S. Blow, and Shozo Yokoyama. "Genetic Analyses of Visual Pigments of the Pigeon (Columba livia)." Genetics 153, no. 4 (December 1, 1999): 1839–50. http://dx.doi.org/10.1093/genetics/153.4.1839.
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AbstractWe isolated five classes of retinal opsin genes rh1Cl, rh2Cl, sws1Cl, sws2Cl, and lwsCl from the pigeon; these encode RH1Cl, RH2Cl, SWS1Cl, SWS2Cl, and LWSCl opsins, respectively. Upon binding to 11-cis-retinal, these opsins regenerate the corresponding photosensitive molecules, visual pigments. The absorbance spectra of visual pigments have a broad bell shape with the peak, being called λmax. Previously, the SWS1Cl opsin cDNA was isolated from the pigeon retinal RNA, expressed in cultured COS1 cells, reconstituted with 11-cis-retinal, and the λmax of the resulting SWS1Cl pigment was shown to be 393 nm. In this article, using the same methods, the λmax values of RH1Cl, RH2Cl, SWS2Cl, and LWSCl pigments were determined to be 502, 503, 448, and 559 nm, respectively. The pigeon is also known for its UV vision, detecting light at 320–380 nm. Being the only pigments that absorb light below 400 nm, the SWS1Cl pigments must mediate its UV vision. We also determined that a nonretinal PCl pigment in the pineal gland of the pigeon has a λmax value at 481 nm.
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Wada, Seiji, Baoguo Shen, Emi Kawano-Yamashita, Takashi Nagata, Masahiko Hibi, Satoshi Tamotsu, Mitsumasa Koyanagi, and Akihisa Terakita. "Color opponency with a single kind of bistable opsin in the zebrafish pineal organ." Proceedings of the National Academy of Sciences 115, no. 44 (October 15, 2018): 11310–15. http://dx.doi.org/10.1073/pnas.1802592115.
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Lower vertebrate pineal organs discriminate UV and visible light. Such color discrimination is typically considered to arise from antagonism between two or more spectrally distinct opsins, as, e.g., human cone-based color vision relies on antagonistic relationships between signals produced by red-, green-, and blue-cone opsins. Photosensitive pineal organs contain a bistable opsin (parapinopsin) that forms a signaling-active photoproduct upon UV exposure that may itself be returned to the signaling-inactive “dark” state by longer-wavelength light. Here we show the spectrally distinct parapinopsin states (with antagonistic impacts on signaling) allow this opsin alone to provide the color sensitivity of this organ. By using calcium imaging, we show that single zebrafish pineal photoreceptors held under a background light show responses of opposite signs to UV and visible light. Both such responses are deficient in zebrafish lacking parapinopsin. Expressing a UV-sensitive cone opsin in place of parapinopsin recovers UV responses but not color opponency. Changes in the spectral composition of white light toward enhanced UV or visible wavelengths respectively increased vs. decreased calcium signal in parapinopsin-sufficient but not parapinopsin-deficient photoreceptors. These data reveal color opponency from a single kind of bistable opsin establishing an equilibrium-like mixture of the two states with different signaling abilities whose fractional concentrations are defined by the spectral composition of incident light. As vertebrate visual color opsins evolved from a bistable opsin, these findings suggest that color opponency involving a single kind of bistable opsin might have been a prototype of vertebrate color opponency.
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Byun, Jun-Hwan, Ji-Yeon Hyeon, Eun-Su Kim, Byeong-Hoon Kim, Hiroshi Miyanishi, Hirohiko Kagawa, Yuki Takeuchi, Se-Jae Kim, Akihiro Takemura, and Sung-Pyo Hur. "Gene expression patterns of novel visual and non-visual opsin families in immature and mature Japanese eel males." PeerJ 8 (February 27, 2020): e8326. http://dx.doi.org/10.7717/peerj.8326.
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This study was carried out to identify and estimate physiological function of a new type of opsin subfamily present in the retina and whole brain tissues of Japanese eel using RNA–Seq transcriptome method. A total of 18 opsin subfamilies were identified through RNA–seq. The visual opsin family included Rh2, SWS2, FWO, DSO, and Exo-Rhod. The non-visual opsin family included four types of melanopsin subfamily (Opn4x1, Opn4x2, Opn4m1, and Opn4m2), peropsin, two types of neuropsin subfamily (Opn5-like, Opn5), Opn3, three types of TMT opsin subfamily (TMT1, 2, 3), VA-opsin, and parapinopsin. In terms of changes in photoreceptor gene expression in the retina of sexually mature and immature male eels, DSO mRNA increased in the maturation group. Analysis of expression of opsin family gene in male eel brain before and after maturation revealed that DSO and SWS2 expression in terms of visual opsin mRNA increased in the sexually mature group. In terms of non-visual opsin mRNA, parapinopsin mRNA increased whereas that of TMT2 decreased in the fore-brain of the sexually mature group. The mRNA for parapinopsin increased in the mid-brain of the sexually mature group, whereas those of TMT1 and TMT3 increased in the hind-brain of the sexually mature group. DSO mRNA also increased in the retina after sexual maturation, and DSO and SWS2 mRNA increased in whole brain part, suggesting that DSO and SWS2 are closely related to sexual maturation.
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Fontinha, Bruno M., Theresa Zekoll, Mariam Al-Rawi, Miguel Gallach, Florian Reithofer, Alison J. Barker, Maximilian Hofbauer, et al. "TMT-Opsins differentially modulate medaka brain function in a context-dependent manner." PLOS Biology 19, no. 1 (January 7, 2021): e3001012. http://dx.doi.org/10.1371/journal.pbio.3001012.
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Vertebrate behavior is strongly influenced by light. Light receptors, encoded by functional opsin proteins, are present inside the vertebrate brain and peripheral tissues. This expression feature is present from fishes to human and appears to be particularly prominent in diurnal vertebrates. Despite their conserved widespread occurrence, the nonvisual functions of opsins are still largely enigmatic. This is even more apparent when considering the high number of opsins. Teleosts possess around 40 opsin genes, present from young developmental stages to adulthood. Many of these opsins have been shown to function as light receptors. This raises the question of whether this large number might mainly reflect functional redundancy or rather maximally enables teleosts to optimally use the complex light information present under water. We focus on tmt-opsin1b and tmt-opsin2, c-opsins with ancestral-type sequence features, conserved across several vertebrate phyla, expressed with partly similar expression in non-rod, non-cone, non-retinal-ganglion-cell brain tissues and with a similar spectral sensitivity. The characterization of the single mutants revealed age- and light-dependent behavioral changes, as well as an impact on the levels of the preprohormone sst1b and the voltage-gated sodium channel subunit scn12aa. The amount of daytime rest is affected independently of the eyes, pineal organ, and circadian clock in tmt-opsin1b mutants. We further focused on daytime behavior and the molecular changes in tmt-opsin1b/2 double mutants, and found that—despite their similar expression and spectral features—these opsins interact in part nonadditively. Specifically, double mutants complement molecular and behavioral phenotypes observed in single mutants in a partly age-dependent fashion. Our work provides a starting point to disentangle the highly complex interactions of vertebrate nonvisual opsins, suggesting that tmt-opsin-expressing cells together with other visual and nonvisual opsins provide detailed light information to the organism for behavioral fine-tuning. This work also provides a stepping stone to unravel how vertebrate species with conserved opsins, but living in different ecological niches, respond to similar light cues and how human-generated artificial light might impact on behavioral processes in natural environments.
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Hart, Nathan S., Trevor D. Lamb, Hardip R. Patel, Aaron Chuah, Riccardo C. Natoli, Nicholas J. Hudson, Scott C. Cutmore, Wayne I. L. Davies, Shaun P. Collin, and David M. Hunt. "Visual Opsin Diversity in Sharks and Rays." Molecular Biology and Evolution 37, no. 3 (November 26, 2019): 811–27. http://dx.doi.org/10.1093/molbev/msz269.
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Abstract The diversity of color vision systems found in extant vertebrates suggests that different evolutionary selection pressures have driven specializations in photoreceptor complement and visual pigment spectral tuning appropriate for an animal’s behavior, habitat, and life history. Aquatic vertebrates in particular show high variability in chromatic vision and have become important models for understanding the role of color vision in prey detection, predator avoidance, and social interactions. In this study, we examined the capacity for chromatic vision in elasmobranch fishes, a group that have received relatively little attention to date. We used microspectrophotometry to measure the spectral absorbance of the visual pigments in the outer segments of individual photoreceptors from several ray and shark species, and we sequenced the opsin mRNAs obtained from the retinas of the same species, as well as from additional elasmobranch species. We reveal the phylogenetically widespread occurrence of dichromatic color vision in rays based on two cone opsins, RH2 and LWS. We also confirm that all shark species studied to date appear to be cone monochromats but report that in different species the single cone opsin may be of either the LWS or the RH2 class. From this, we infer that cone monochromacy in sharks has evolved independently on multiple occasions. Together with earlier discoveries in secondarily aquatic marine mammals, this suggests that cone-based color vision may be of little use for large marine predators, such as sharks, pinnipeds, and cetaceans.
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Gutierrez, Eduardo de A., Ryan K. Schott, Matthew W. Preston, Lívia O. Loureiro, Burton K. Lim, and Belinda S. W. Chang. "The role of ecological factors in shaping bat cone opsin evolution." Proceedings of the Royal Society B: Biological Sciences 285, no. 1876 (April 4, 2018): 20172835. http://dx.doi.org/10.1098/rspb.2017.2835.
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Bats represent one of the largest and most striking nocturnal mammalian radiations, exhibiting many visual system specializations for performance in light-limited environments. Despite representing the greatest ecological diversity and species richness in Chiroptera, Neotropical lineages have been undersampled in molecular studies, limiting the potential for identifying signatures of selection on visual genes associated with differences in bat ecology. Here, we investigated how diverse ecological pressures mediate long-term shifts in selection upon long-wavelength ( Lws ) and short-wavelength ( Sws1 ) opsins, photosensitive cone pigments that form the basis of colour vision in most mammals, including bats. We used codon-based likelihood clade models to test whether ecological variables associated with reliance on visual information (e.g. echolocation ability and diet) or exposure to varying light environments (e.g. roosting behaviour and foraging habitat) mediated shifts in evolutionary rates in bat cone opsin genes. Using additional cone opsin sequences from newly sequenced eye transcriptomes of six Neotropical bat species, we found significant evidence for different ecological pressures influencing the evolution of the cone opsins. While Lws is evolving under significantly lower constraint in highly specialized high-duty cycle echolocating lineages, which have enhanced sonar ability to detect and track targets, variation in Sws1 constraint was significantly associated with foraging habitat, exhibiting elevated rates of evolution in species that forage among vegetation. This suggests that increased reliance on echolocation as well as the spectral environment experienced by foraging bats may differentially influence the evolution of different cone opsins. Our study demonstrates that different ecological variables may underlie contrasting evolutionary patterns in bat visual opsins, and highlights the suitability of clade models for testing ecological hypotheses of visual evolution.
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Fleming, James F., Reinhardt Møbjerg Kristensen, Martin Vinther Sørensen, Tae-Yoon S. Park, Kazuharu Arakawa, Mark Blaxter, Lorena Rebecchi, et al. "Molecular palaeontology illuminates the evolution of ecdysozoan vision." Proceedings of the Royal Society B: Biological Sciences 285, no. 1892 (December 5, 2018): 20182180. http://dx.doi.org/10.1098/rspb.2018.2180.
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Colour vision is known to have arisen only twice—once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35–71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.
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Chang, Chia-Hao, Julian Catchen, Rachel L. Moran, Angel G. Rivera-Colón, Yu-Chun Wang, and Rebecca C. Fuller. "Sequence Analysis and Ontogenetic Expression Patterns of Cone Opsin Genes in the Bluefin Killifish (Lucania goodei)." Journal of Heredity 112, no. 4 (April 9, 2021): 357–66. http://dx.doi.org/10.1093/jhered/esab017.
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Abstract Sensory systems allow for the transfer of environmental stimuli into internal cues that can alter physiology and behavior. Many studies of visual systems focus on opsins to compare spectral sensitivity among individuals, populations, and species living in different lighting environments. This requires an understanding of the cone opsins, which can be numerous. The bluefin killifish is a good model for studying the interaction between environments and visual systems as they are found in both clear springs and tannin-stained swamps. We conducted a genome-wide screening and demonstrated that the bluefin killifish has 9 cone opsins: 1 SWS1 (354 nm), 2 SWS2 (SWS2B: 359 nm, SWS2A: 448 nm), 2 RH2 (RH2-2: 476 nm, RH2-1: 537 nm), and 4 LWS (LWS-1: 569 nm, LWS-2: 524 nm, LWS-3: 569 nm, LWS-R: 560 or 569 nm). These 9 cone opsins were located on 4 scaffolds. One scaffold contained the 2 SWS2 and 3 of the 4 LWS opsins in the same syntenic order as found in other cyprinodontoid fishes. We also compared opsin expression in larval and adult killifish under clear water conditions, which mimic springs. Two of the newly discovered opsins (LWS-2 and LWS-3) were expressed at low levels (<0.2%). Whether these opsins make meaningful contributions to visual perception in other contexts (i.e., swamp conditions) is unclear. In contrast, there was an ontogenetic change from using LWS-R to LWS-1 opsin. Bluefin killifish adults may be slightly more sensitive to longer wavelengths, which might be related to sexual selection and/or foraging preferences.
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Futahashi, Ryo, Ryouka Kawahara-Miki, Michiyo Kinoshita, Kazutoshi Yoshitake, Shunsuke Yajima, Kentaro Arikawa, and Takema Fukatsu. "Extraordinary diversity of visual opsin genes in dragonflies." Proceedings of the National Academy of Sciences 112, no. 11 (February 23, 2015): E1247—E1256. http://dx.doi.org/10.1073/pnas.1424670112.
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Dragonflies are colorful and large-eyed animals strongly dependent on color vision. Here we report an extraordinary large number of opsin genes in dragonflies and their characteristic spatiotemporal expression patterns. Exhaustive transcriptomic and genomic surveys of three dragonflies of the family Libellulidae consistently identified 20 opsin genes, consisting of 4 nonvisual opsin genes and 16 visual opsin genes of 1 UV, 5 short-wavelength (SW), and 10 long-wavelength (LW) type. Comprehensive transcriptomic survey of the other dragonflies representing an additional 10 families also identified as many as 15–33 opsin genes. Molecular phylogenetic analysis revealed dynamic multiplications and losses of the opsin genes in the course of evolution. In contrast to many SW and LW genes expressed in adults, only one SW gene and several LW genes were expressed in larvae, reflecting less visual dependence and LW-skewed light conditions for their lifestyle under water. In this context, notably, the sand-burrowing or pit-dwelling species tended to lack SW gene expression in larvae. In adult visual organs: (i) many SW genes and a few LW genes were expressed in the dorsal region of compound eyes, presumably for processing SW-skewed light from the sky; (ii) a few SW genes and many LW genes were expressed in the ventral region of compound eyes, probably for perceiving terrestrial objects; and (iii) expression of a specific LW gene was associated with ocelli. Our findings suggest that the stage- and region-specific expressions of the diverse opsin genes underlie the behavior, ecology, and adaptation of dragonflies.
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NEWMAN, LUCY A., and PHYLLIS R. ROBINSON. "Cone visual pigments of aquatic mammals." Visual Neuroscience 22, no. 6 (November 2005): 873–79. http://dx.doi.org/10.1017/s0952523805226159.
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It has long been hypothesized that the visual systems of animals are evolutionarily adapted to their visual environment. The entrance many millions of years ago of mammals into the sea gave these new aquatic mammals completely novel visual surroundings with respect to light availability and predominant wavelengths. This study examines the cone opsins of marine mammals, hypothesizing, based on previous studies [Fasick et al. (1998) and Levenson & Dizon (2003)], that the deep-dwelling marine mammals would not have color vision because the pressure to maintain color vision in the dark monochromatic ocean environment has been relaxed. Short-wavelength-sensitive (SWS) and long-wavelength-sensitive (LWS) cone opsin genes from two orders (Cetacea and Sirenia) and an additional suborder (Pinnipedia) of aquatic mammals were amplified from genomic DNA (for SWS) and cDNA (for LWS) by PCR, cloned, and sequenced. All animals studied from the order Cetacea have SWS pseudogenes, whereas a representative from the order Sirenia has an intact SWS gene, for which the corresponding mRNA was found in the retina. One of the pinnipeds studied (harp seal) has an SWS pseudogene, while another species (harbor seal) appeared to have an intact SWS gene. However, no SWS cone opsin mRNA was found in the harbor seal retina, suggesting a promoter or splice site mutation preventing transcription of the gene. The LWS opsins from the different species were expressed in mammalian cells and reconstituted with the 11-cis-retinal chromophore in order to determine maximal absorption wavelengths (λmax) for each. The deeper dwelling Cetacean species had blue shifted λmax values compared to shallower-dwelling aquatic species. Taken together, these findings support the hypothesis that in the monochromatic oceanic habitat, the pressure to maintain color vision has been relaxed and mutations are retained in the SWS genes, resulting in pseudogenes. Additionally, LWS opsins are retained in the retina and, in deeper-dwelling animals, are blue shifted in λmax.
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Sakai, Yusuke, Shoji Kawamura, and Masakado Kawata. "Genetic and plastic variation in opsin gene expression, light sensitivity, and female response to visual signals in the guppy." Proceedings of the National Academy of Sciences 115, no. 48 (November 12, 2018): 12247–52. http://dx.doi.org/10.1073/pnas.1706730115.
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According to the sensory drive model, variation in visual properties can lead to diverse female preferences, which in turn results in a range of male nuptial colors by way of sexual selection. However, the cause of variation in visual properties and the mechanism by which variation drives female response to visual signals remain unclear. Here, we demonstrate that both differences in the long-wavelength–sensitive 1 (LWS-1) opsin genotype and the light environment during rearing lead to variation in opsin gene expression. Opsin expression variation affects the visual sensitivity threshold to long wavelengths of light. Moreover, a behavioral assay using digitally modified video images showed that the expression of multiple opsin genes is positively correlated with the female responsiveness to images of males with luminous orange spots. The findings suggest that genetic polymorphisms and light environment in habitats induce variations in opsin gene expression levels. The variations may facilitate variations in visual sensitivity and female responsiveness to male body colors within and among populations.
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Gerrard, Elliot, Eshita Mutt, Takashi Nagata, Mitsumasa Koyanagi, Tilman Flock, Elena Lesca, Gebhard F. X. Schertler, Akihisa Terakita, Xavier Deupi, and Robert J. Lucas. "Convergent evolution of tertiary structure in rhodopsin visual proteins from vertebrates and box jellyfish." Proceedings of the National Academy of Sciences 115, no. 24 (May 23, 2018): 6201–6. http://dx.doi.org/10.1073/pnas.1721333115.
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Box jellyfish and vertebrates are separated by >500 million years of evolution yet have structurally analogous lens eyes that employ rhodopsin photopigments for vision. All opsins possess a negatively charged residue—the counterion—to maintain visible-light sensitivity and facilitate photoisomerization of their retinaldehyde chromophore. In vertebrate rhodopsins, the molecular evolution of the counterion position—from a highly conserved distal location in the second extracellular loop (E181) to a proximal location in the third transmembrane helix (E113)—is established as a key driver of higher fidelity photoreception. Here, we use computational biology and heterologous action spectroscopy to determine whether the appearance of the advanced visual apparatus in box jellyfish was also accompanied by changes in the opsin tertiary structure. We found that the counterion in an opsin from the lens eye of the box jellyfish Carybdea rastonii (JellyOp) has also moved to a unique proximal location within the transmembrane bundle—E94 in TM2. Furthermore, we reveal that this Schiff base/counterion system includes an additional positive charge—R186—that has coevolved with E94 to functionally separate E94 and E181 in the chromophore-binding pocket of JellyOp. By engineering this pocket—neutralizing R186 and E94, or swapping E94 with the vertebrate counterion E113—we can recreate versions of the invertebrate and vertebrate counterion systems, respectively, supporting a relatively similar overall architecture in this region of animal opsins. In summary, our data establish the third only counterion site in animal opsins and reveal convergent evolution of tertiary structure in opsins from distantly related species with advanced visual systems.
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Taylor, John S., and Thomas E. Reimchen. "Opsin gene repertoires in northern archaic hominids." Genome 59, no. 8 (August 2016): 541–49. http://dx.doi.org/10.1139/gen-2015-0164.
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The Neanderthals’ northern distribution, hunting techniques, and orbit breadths suggest that they were more active in dim light than modern humans. We surveyed visual opsin genes from four Neanderthals and two other archaic hominids to see if they provided additional support for this hypothesis. This analysis was motivated by the observation that alleles responsible for anomalous trichromacy in humans are more common in northern latitudes, by data suggesting that these variants might enhance vision in mesopic conditions, and by the observation that dim light active species often have fewer opsin genes than diurnal relatives. We also looked for evidence of convergent amino acid substitutions in Neanderthal opsins and orthologs from crepuscular or nocturnal species. The Altai Neanderthal, the Denisovan, and the Ust’-Ishim early modern human had opsin genes that encoded proteins identical to orthologs in the human reference genome. Opsins from the Vindija Cave Neanderthals (three females) had many nonsynonymous substitutions, including several predicted to influence colour vision (e.g., stop codons). However, the functional implications of these observations were difficult to assess, given that “control” loci, where no substitutions were expected, differed from humans to the same extent. This left unresolved the test for colour vision deficiencies in Vindija Cave Neanderthals.
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Rhim, Issac, Gabriela Coello-Reyes, Hee-Kyoung Ko, and Ian Nauhaus. "Maps of cone opsin input to mouse V1 and higher visual areas." Journal of Neurophysiology 117, no. 4 (April 1, 2017): 1674–82. http://dx.doi.org/10.1152/jn.00849.2016.
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Studies in the mouse retina have characterized the spatial distribution of an anisotropic ganglion cell and photoreceptor mosaic, which provides a solid foundation to study how the cortex pools from afferent parallel color channels. In particular, the mouse’s retinal mosaic exhibits a gradient of wavelength sensitivity along its dorsoventral axis. Cones at the ventral extreme mainly express S opsin, which is sensitive to ultraviolet (UV) wavelengths. Then, moving toward the retina’s dorsal extreme, there is a transition to M-opsin dominance. Here, we tested the hypothesis that the retina’s opsin gradient is recapitulated in cortical visual areas as a functional map of wavelength sensitivity. We first identified visual areas in each mouse by mapping retinotopy with intrinsic signal imaging (ISI). Next, we measured ISI responses to stimuli along different directions of the S- and M-color plane to quantify the magnitude of S and M input to each location of the retinotopic maps in five visual cortical areas (V1, AL, LM, PM, and RL). The results illustrate a significant change in the S:M-opsin input ratio along the axis of vertical retinotopy that is consistent with the gradient along the dorsoventral axis of the retina. In particular, V1 populations encoding the upper visual field responded to S-opsin contrast with 6.1-fold greater amplitude than to M-opsin contrast. V1 neurons encoding lower fields responded with 4.6-fold greater amplitude to M- than S-opsin contrast. The maps in V1 and higher visual areas (HVAs) underscore the significance of a wavelength sensitivity gradient for guiding the mouse’s behavior. NEW & NOTEWORTHY Two elements of this study are particularly novel. For one, it is the first to quantify cone inputs to mouse visual cortex; we have measured cone input in five visual areas. Next, it is the first study to identify a feature map in the mouse visual cortex that is based on well-characterized anisotropy of cones in the retina; we have identified maps of opsin selectivity in five visual areas.
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McDonald, Brandon, Bryce Geiger, and Sarah Vrla. "Ultraviolet vision in Ord’s kangaroo rat (Dipodomys ordii)." Journal of Mammalogy 101, no. 5 (August 18, 2020): 1257–66. http://dx.doi.org/10.1093/jmammal/gyaa083.
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Abstract Knowledge of a species’ visual system has far reaching implications that affect our understanding of a species’ ecology and evolutionary history. As a model taxon, the heteromyid rodent genus Dipodomys has been valuable in elucidating patterns and mechanisms in biomechanics, ecology, adaptive physiology, biogeography, and more. Although studied extensively, the visual system of Dipodomys has not been described beyond anecdotal mention of their large eyes. Here, the transmittance parameters of the cornea and lens of Ord’s kangaroo rat (Dipodomys ordii) were analyzed and photoreceptor proteins (opsins) expressed in the retina were identified with immunohistochemical (IHC) labeling. Retina maps were constructed to illustrate the relative densities of photoreceptor cells expressing short wavelength (SWS1) opsins, middle/long wavelength (MW/LW) opsins, and rhodopsin (RH1). The retina of D. ordii has variable densities of SWS1 opsin with the highest density being ventral to the optic nerve, high density of MW/LW opsin, and uniform distribution and high density of RH1 across the retina. Our results suggest that D. ordii has a UV-sensitive visual system. Composition and densities of MW/LW- and SWS1-expressing cells resemble that of a crepuscular/diurnal species thereby supporting previous authors who have reported such activity patterns. Uniform retinal distribution of RH1 indicates visual acuity at night, also confirming the paradigm of D. ordii as primarily a nocturnal species and suggesting visual acuity at all times of the day in the species. These results demonstrate not only that the species is capable of UV vision and has a retina characteristic of a diurnal mammal, but that many previously unknown photic niche selective advantages likely have shaped the evolution and ecology of this model taxon.
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Chase, M. R., R. R. Bennett, and R. H. White. "Three opsin-encoding cDNAS from the compound eye of Manduca sexta." Journal of Experimental Biology 200, no. 18 (September 1, 1997): 2469–78. http://dx.doi.org/10.1242/jeb.200.18.2469.
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Three distinct opsin-encoding cDNAs, designated MANOP1, MANOP2 and MANOP3, were isolated from the retina of the sphingid moth Manduca sexta. MANOP1 codes for a protein with 377 amino acid residues. It is similar in sequence to members of a phylogenetic group of long-wavelength-sensitive arthropod photopigments, most closely resembling the opsins of ants, a praying mantis, a locust and the honeybee. MANOP2 and MANOP3 opsins have 377 and 384 residues respectively. They belong to a related group of insect visual pigments that include the ultraviolet-sensitive rhodopsins of flies as well as other insect rhodopsins that are also thought to absorb at short wavelengths. The retina of Manduca sexta contains three rhodopsins, P520, P450 and P357, with absorbance peaks, respectively, at green, blue and ultraviolet wavelengths. There is evidence that MANOP1 encodes the opsin of P520. We suggest that MANOP2 encodes P357 and that MANOP3, representing a class of blue-sensitive insect photopigments, encodes P450.
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Saito, Kazuma, Kazuhiko Horiguchi, Battsetseg Buyandalai, Ayaka Nishikido, Takashi Okamura, Akiko Toki, Emi Ishida, et al. "Maternal Hypothyroidism Delayed Retinal Opsin-Development in the Neonatal Period: Analysis of TRH-Deficient Mice." Journal of the Endocrine Society 5, Supplement_1 (May 1, 2021): A851—A852. http://dx.doi.org/10.1210/jendso/bvab048.1738.
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Abstract Introduction: Retinal cone photoreceptor cells contain short (S) and medium (M) wavelength opsins, which are light-sensitive substances involved in color vision and visual acuity by sensing lights of different wavelengths. Thyroid hormones promote M-opsin expression and suppress S-opsin expression during the differentiation of cone photoreceptors. It was previously reported that M-opsin expression was delayed and S-opsin expression increased in TSH receptor-deficient mice and methimazole-induced hypothyroid mice. In addition, no M-opsin expression and increased S-opsin expression were observed in thyroid hormone receptor (TR) β2-deficient mice (Ng L et al, Nature Genetics. 2001; 27(1): 94-98.). This suggested that impaired thyroid function affects opsin development. We therefore examined retinal development in TRH-deficient mice, which are a model of central hypothyroidism established in our laboratory. Methods: We performed HE staining of the retina at postnatal 30 days and electroretinography at postnatal 10 weeks using TRH-/- and wild-type (WT) mice. We also examined expression levels of S/M opsin mRNA in WT, TRH-/- and TRH-/- pups born from TRH-/- dams at postnatal 12,17 and 30 days, and TRβΔ337T knock-in mice (TRβmut/mut) at postnatal 30 days. Furthermore, we performed immunohistochemistry to examine S/M opsin protein expression in these mice. Results: The retinal structures by HE staining and retinal functions by electroretinography in TRH-/- mice were unchanged compared with those in WT mice. Although M-opsin expression was not detected and S-opsin expression was higher in TRβmut/mut mice than in WT mice, the mRNA and protein expression levels of S/M-opsin did not significantly differ between TRH-/- pups born from TRH+/- dams and WT pups at all postnatal days. TRH-/- pups born from TRH-/- dams exposed to maternal hypothyroidism had similar serum total T4 levels to TRH-/- pups born from TRH+/- with normal maternal thyroid function. In contrast, the mRNA expression level of M-opsin was significantly lower (1.00±0.06 vs 0.64±0.05: mean ± SE, p<0.01) and the protein expression level was lower in TRH-/- pups born from TRH-/- dams than in WT pups at postnatal 12 days. However, these differences disappeared after postnatal 17 days, and there was no difference in M-opsin expression in TRH-/- pups born from TRH-/- dams compared with WT pups. Conclusions: Although no delay in opsin development was observed in TRH-/- pups born from TRH+/- dams, TRH-/- pups born from central hypothyroid dams exhibited delayed opsin development, suggesting that maternal hypothyroidism affects the development of retinal opsin in the neonatal period.
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Simon, Noah, Suguru Fujita, Megan Porter, and Masato Yoshizawa. "Expression of extraocular opsin genes and light-dependent basal activity of blind cavefish." PeerJ 7 (December 17, 2019): e8148. http://dx.doi.org/10.7717/peerj.8148.
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Background Animals living in well-lit environments utilize optical stimuli for detecting visual information, regulating the homeostatic pacemaker, and controlling patterns of body pigmentation. In contrast, many subterranean animal species without optical stimuli have evolved regressed binocular eyes and body pigmentation. Interestingly, some fossorial and cave-dwelling animals with regressed eyes still respond to light. These light-dependent responses may be simply evolutionary residuals or they may be adaptive, where negative phototaxis provides avoidance of predator-rich surface environments. However, the relationship between these non-ocular light responses and the underlying light-sensing Opsin proteins has not been fully elucidated. Methods To highlight the potential functions of opsins in a blind subterranean animal, we used the Mexican cave tetra to investigate opsin gene expression in the eyes and several brain regions of both surface and cave-dwelling adults. We performed database surveys, expression analyses by quantitative reverse transcription PCR (RT-qPCR), and light-dependent locomotor activity analysis using pinealectomized fish, one of the high-opsin expressing organs of cavefish. Results Based on conservative criteria, we identified 33 opsin genes in the cavefish genome. Surveys of available RNAseq data found 26 of these expressed in the surface fish eye as compared to 24 expressed in cavefish extraocular tissues, 20 of which were expressed in the brain. RT-qPCR of 26 opsins in surface and cavefish eye and brain tissues showed the highest opsin-expressing tissue in cavefish was the pineal organ, which expressed exo-rhodopsin at 72.7% of the expression levels in surface fish pineal. However, a pinealectomy resulted in no change to the light-dependent locomotor activity in juvenile cavefish and surface fish. Therefore, we conclude that, after 20,000 or more years of evolution in darkness, cavefish light-dependent basal activity is regulated by a non-pineal extraocular organ.
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Robinson, Judith, Ellen A. Schmitt, and John E. Dowling. "Temporal and spatial patterns of opsin gene expression in zebrafish (Danio rerio)." Visual Neuroscience 12, no. 5 (September 1995): 895–906. http://dx.doi.org/10.1017/s0952523800009457.
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AbstractIn zebrafish, the first class of cone photoreceptor to become morphologically distinct is the ultraviolet-sensitive short single cone, at 4 days postfertilization, whereas the last class, the red- and green-sensitive double cone, becomes distinct at 10 days postfertilization. We have examined the time course of visual pigment gene expression in zebrafish using whole-mount in situ hybridization. Within the retina, opsins may be detected as early as 40 h postfertilization with the ultraviolet and rod visual pigments being expressed before the blue- (48 h) and red- (60 h) sensitive pigments. In the pineal, red-sensitive opsin is expressed at 48 h postfertilization. Visual pigment expression provides a useful tool for investigations of early cell fate in zebrafish.
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Sandkam, Benjamin A., Laura Campello, Conor O’Brien, Sri Pratima Nandamuri, William J. Gammerdinger, Matthew A. Conte, Anand Swaroop, and Karen L. Carleton. "Tbx2a Modulates Switching of RH2 and LWS Opsin Gene Expression." Molecular Biology and Evolution 37, no. 7 (March 19, 2020): 2002–14. http://dx.doi.org/10.1093/molbev/msaa062.
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Abstract Sensory systems are tuned by selection to maximize organismal fitness in particular environments. This tuning has implications for intraspecies communication, the maintenance of species boundaries, and speciation. Tuning of color vision largely depends on the sequence of the expressed opsin proteins. To improve tuning of visual sensitivities to shifts in habitat or foraging ecology over the course of development, many organisms change which opsins are expressed. Changes in this developmental sequence (heterochronic shifts) can create differences in visual sensitivity among closely related species. The genetic mechanisms by which these developmental shifts occur are poorly understood. Here, we use quantitative trait locus analyses, genome sequencing, and gene expression studies in African cichlid fishes to identify a role for the transcription factor Tbx2a in driving a switch between long wavelength sensitive (LWS) and Rhodopsin-like (RH2) opsin expression. We identify binding sites for Tbx2a in the LWS promoter and the highly conserved locus control region of RH2 which concurrently promote LWS expression while repressing RH2 expression. We also present evidence that a single change in Tbx2a regulatory sequence has led to a species difference in visual tuning, providing the first mechanistic model for the evolution of rapid switches in sensory tuning. This difference in visual tuning likely has important roles in evolution as it corresponds to differences in diet, microhabitat choice, and male nuptial coloration.
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Sakamoto, K., O. Hisatomi, F. Tokunaga, and E. Eguchi. "Two opsins from the compound eye of the crab Hemigrapsus sanguineus." Journal of Experimental Biology 199, no. 2 (February 1, 1996): 441–50. http://dx.doi.org/10.1242/jeb.199.2.441.
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The primary structures of two opsins from the brachyuran crab Hemigrapsus sanguineus were deduced from the cDNA nucleotide sequences. Both deduced proteins were composed of 377 amino acid residues and included residues highly conserved in visual pigments of other species, and the proteins were 75 % identical to each other. The distribution of opsin transcripts in the compound eye, determined by in situ hybridization, suggested that the mRNAs of the two opsins were expressed simultaneously in all of the seven retinular cells (R1-R7) forming the main rhabdom in each ommatidium. Two different visual pigments may be present in one photoreceptor cell in this brachyuran crab. The spectral sensitivity of the compound eye was also determined by recording the electroretinogram. The compound eye was maximally sensitive at about 480 nm. These and previous findings suggest that both opsins of this brachyuran crab produce visual pigments with maximal absorption in the blue-green region of the spectrum. Evidence is presented that crustaceans possess multiple pigment systems for vision.
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Hárosi, Ferenc I., and Jochen Kleinschmidt. "Visual pigments in the sea lamprey, Petromyzon marinus." Visual Neuroscience 10, no. 4 (July 1993): 711–15. http://dx.doi.org/10.1017/s0952523800005411.
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AbstractWe present microspectrophotometric evidence for the existence of two distinct visual pigments residing in two different morphological types of photoreceptor of the sea lamprey. In the upstream migrant Petromyzon marinus, the pigment found in short receptors has a wavelength of peak absorbance (λmax) of 525 nm, whereas the pigment located in long receptors has a λmax of 600 nm. Although the former appears to be pure porphyropsin, the latter is akin to visual pigments found in the red-absorbing cones of amphibian and teleost retinae. The kinship is more than superficial pertaining to λmax of the a–band absorbance to its native maximum value. The presence of an anion-sensitive and an anion-insensitive pigment in a retina implies the expression of two distinct opsin genes. We infer this from several examples of correlation between anion sensitivity and opsin sequence groupings. Moreover, the presence of two distinct opsin genes expressed throughout six vertebrate classes implies their existence in a common ancestor to all.
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Kasagi, Satoshi, Kanta Mizusawa, and Akiyoshi Takahashi. "Molecular evolution of flounder visual opsin genes." Electrophoresis Letters 63, no. 1 (2019): 15–18. http://dx.doi.org/10.2198/electroph.63.15.
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Butler, Julie M., and Karen P. Maruska. "Opsin Expression Varies with Reproductive State in the Cichlid Fish Astatotilapia burtoni." Integrative and Comparative Biology 61, no. 1 (July 1, 2021): 240–48. http://dx.doi.org/10.1093/icb/icab058.
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Synopsis Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared with non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g., sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared with mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.
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Cortesi, Fabio, Zuzana Musilová, Sara M. Stieb, Nathan S. Hart, Ulrike E. Siebeck, Martin Malmstrøm, Ole K. Tørresen, et al. "Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes." Proceedings of the National Academy of Sciences 112, no. 5 (December 29, 2014): 1493–98. http://dx.doi.org/10.1073/pnas.1417803112.
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Single-gene and whole-genome duplications are important evolutionary mechanisms that contribute to biological diversification by launching new genetic raw material. For example, the evolution of animal vision is tightly linked to the expansion of the opsin gene family encoding light-absorbing visual pigments. In teleost fishes, the most species-rich vertebrate group, opsins are particularly diverse and key to the successful colonization of habitats ranging from the bioluminescence-biased but basically dark deep sea to clear mountain streams. In this study, we report a previously unnoticed duplication of the violet-blue short wavelength-sensitive 2 (SWS2) opsin, which coincides with the radiation of highly diverse percomorph fishes, permitting us to reinterpret the evolution of this gene family. The inspection of close to 100 fish genomes revealed that, triggered by frequent gene conversion between duplicates, the evolutionary history of SWS2 is rather complex and difficult to predict. Coincidentally, we also report potential cases of gene resurrection in vertebrate opsins, whereby pseudogenized genes were found to convert with their functional paralogs. We then identify multiple novel amino acid substitutions that are likely to have contributed to the adaptive differentiation between SWS2 copies. Finally, using the dusky dottyback Pseudochromis fuscus, we show that the newly discovered SWS2A duplicates can contribute to visual adaptation in two ways: by gaining sensitivities to different wavelengths of light and by being differentially expressed between ontogenetic stages. Thus, our study highlights the importance of comparative approaches in gaining a comprehensive view of the dynamics underlying gene family evolution and ultimately, animal diversification.
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Kitamoto, J., K. Sakamoto, K. Ozaki, Y. Mishina, and K. Arikawa. "Two visual pigments in a single photoreceptor cell: identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus." Journal of Experimental Biology 201, no. 9 (May 1, 1998): 1255–61. http://dx.doi.org/10.1242/jeb.201.9.1255.
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This paper describes the localization of newly identified visual pigment opsins in the tiered retina of the Japanese yellow swallowtail Papilio xuthus. We first cloned three cDNAs encoding visual pigment opsins, PxRh1, PxRh2 and PxRh3, and then carried out histological in situ hybridization to localize their mRNAs in the retina. By combining the present data with our previous electrophysiological results, we concluded that both PxRh1 and PxRh2 correspond to visual pigments expressed in photoreceptor cells sensitive in the green wavelength region (green receptors), whereas PxRh3 corresponds to a pigment in red receptors. The in situ hybridization studies showed that some photoreceptor cells express two opsin mRNAs. In the ventral half of the eye, all green receptors in the distal tier were labelled by both PxRh1 and PxRh2 probes. The labelling by the PxRh2 and PxRh3 probes was detected throughout the eye in the proximal tier; in 18 % of ommatidia, the probes labelled the same photoreceptor cell. These results suggest that the possible co-localization of two different visual pigments will broaden the sensitivity spectrum of the photoreceptor cells.
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Mackin, Robert D., Ruth A. Frey, Carmina Gutierrez, Ashley A. Farre, Shoji Kawamura, Diana M. Mitchell, and Deborah L. Stenkamp. "Endocrine regulation of multichromatic color vision." Proceedings of the National Academy of Sciences 116, no. 34 (August 5, 2019): 16882–91. http://dx.doi.org/10.1073/pnas.1904783116.
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Vertebrate color vision requires spectrally selective opsin-based pigments, expressed in distinct cone photoreceptor populations. In primates and in fish, spectrally divergent opsin genes may reside in head-to-tail tandem arrays. Mechanisms underlying differential expression from such arrays have not been fully elucidated. Regulation of human red (LWS) vs. green (MWS) opsins is considered a stochastic event, whereby upstream enhancers associate randomly with promoters of the proximal or distal gene, and one of these associations becomes permanent. We demonstrate that, distinct from this stochastic model, the endocrine signal thyroid hormone (TH) regulates differential expression of the orthologous zebrafish lws1/lws2 array, and of the tandemly quadruplicated rh2-1/rh2-2/rh2-3/rh2-4 array. TH treatment caused dramatic, dose-dependent increases in abundance of lws1, the proximal member of the lws array, and reduced lws2. Fluorescent lws reporters permitted direct visualization of individual cones switching expression from lws2 to lws1. Athyroidism increased lws2 and reduced lws1, except within a small ventral domain of lws1 that was likely sustained by retinoic acid signaling. Changes in lws abundance and distribution in athyroid zebrafish were rescued by TH, demonstrating plasticity of cone phenotype in response to this signal. TH manipulations also regulated the rh2 array, with athyroidism reducing abundance of distal members. Interestingly, the opsins encoded by the proximal lws gene and distal rh2 genes are sensitive to longer wavelengths than other members of their respective arrays; therefore, endogenous TH acts upon each opsin array to shift overall spectral sensitivity toward longer wavelengths, underlying coordinated changes in visual system function during development and growth.