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1. Short-wavelength-sensitive 2 (Sws2) visual photopigment models combined with atomistic molecular simulations to predict spectral peaks of absorbance

   https://doi.org/https://doi.org/10.1371/journal.pcbi.1008212  

   Patel, Dharmeshkumar; Barnes, Jonathan E.; Davies, Wayne I.; Stenkamp, Deborah L.; Patel, Jagdish S. (October 2020, PLoS computational biology)

   null (Ed.)

   For many species, vision is one of the most important sensory modalities for mediating essential tasks that include navigation, predation and foraging, predator avoidance, and numerous social behaviors. The vertebrate visual process begins when photons of the light interact with rod and cone photoreceptors that are present in the neural retina. Vertebrate visual photopigments are housed within these photoreceptor cells and are sensitive to a wide range of wavelengths that peak within the light spectrum, the latter of which is a function of the type of chromophore used and how it interacts with specific amino acid residues found within the opsin protein sequence. Minor differences in the amino acid sequences of the opsins are known to lead to large differences in the spectral peak of absorbance (i.e. the λmax value). In our prior studies, we developed a new approach that combined homology modeling and molecular dynamics simulations to gather structural information associated with chromophore conformation, then used it to generate statistical models for the accurate prediction of λmax values for photopigments derived from Rh1 and Rh2 amino acid sequences. In the present study, we test our novel approach to predict the λmax of phylogenetically distant Sws2 cone opsins. To build a model that can predict the λmax using our approach presented in our prior studies, we selected a spectrally-diverse set of 11 teleost Sws2 photopigments for which both amino acid sequence information and experimentally measured λmax values are known. The final first-order regression model, consisting of three terms associated with chromophore conformation, was sufficient to predict the λmax of Sws2 photopigments with high accuracy. This study further highlights the breadth of our approach in reliably predicting λmax values of Sws2 cone photopigments, evolutionary-more distant from template bovine RH1, and provided mechanistic insights into the role of known spectral tuning sites 

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2. Secondary not subordinate: Opsin localization suggests possibility for color sensitivity in salticid secondary eyes

   https://doi.org/10.1016/j.visres.2024.108367  

   Steck, Mireille; Hanscom, Sophia J; Iwanicki, Tom; Sung, Jenny Y; Outomuro, David; Morehouse, Nathan I; Porter, Megan L (April 2024, Vision Research)

   The principal eyes of jumping spiders (Salticidae) integrate a dual-lens system, a tiered retinal matrix with multiple photoreceptor classes and muscular control of retinal movements to form high resolution images, extract color information, and dynamically evaluate visual scenes. While much work has been done to characterize these more complex principal anterior eyes, little work has investigated the three other pairs of simpler secondary eyes: the anterior lateral eye pair and two posterior (lateral and median) pairs of eyes. We investigated the opsin protein component of visual pigments in the eyes of three species of salticid using transcriptomics and immunohistochemistry. Based on characterization and localization of a set of three conserved opsins (Rh1 - green sensitive, Rh2 - blue sensitive, and Rh3 - ultraviolet sensitive) we have identified potential photoreceptors for blue light detection in the eyes of two out of three species: Menemerus bivittatus (Chrysillini) and Habrocestum africanum (Hasarinii). Additionally, the photoreceptor diversity of the secondary eyes exhibits more variation than previous estimates, particularly for the small, posterior median eyes previously considered vestigial in some species. In all three species investigated the lateral eyes were dominated by green-sensitive visual pigments (RH1 opsins), while the posterior median retinas were dominated by opsins forming short-wavelength sensitive visual pigments (e.g. RH2 and/or RH3/RH4). There was also variation among secondary eye types and among species in the distribution of opsins in retinal photoreceptors, particularly for the putatively blue-sensitive visual pigment formed from RH2. Our findings suggest secondary eyes have the potential for color vision, with observed differences between species likely associated with different ecologies and visual tasks. 

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3. Vision using multiple distinct rod opsins in deep-sea fishes

   https://doi.org/10.1126/science.aav4632  

   Musilova, Zuzana; Cortesi, Fabio; Matschiner, Michael; Davies, Wayne I.; Patel, Jagdish S.; Stieb, Sara M.; Busserolles, Fanny; Malmstrom, Martin; Torresen, Ole K.; Brown, Celeste J.; et al (May 2019, Science magazine)

   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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4. Additive and epistatic effects influence spectral tuning in molluscan retinochrome opsin

   https://doi.org/10.1242/jeb.242929  

   Smedley, G. Dalton; McElroy, Kyle E.; Feller, Kathryn D.; Serb, Jeanne M. (May 2022, Journal of Experimental Biology)

   ABSTRACT The relationship between genotype and phenotype is non-trivial because of the often complex molecular pathways that make it difficult to unambiguously relate phenotypes to specific genotypes. Photopigments, comprising an opsin apoprotein bound to a light-absorbing chromophore, present an opportunity to directly relate the amino acid sequence to an absorbance peak phenotype (λmax). We examined this relationship by conducting a series of site-directed mutagenesis experiments of retinochrome, a non-visual opsin, from two closely related species: the common bay scallop, Argopecten irradians, and the king scallop, Pecten maximus. Using protein folding models, we identified three amino acid sites of likely functional importance and expressed mutated retinochrome proteins in vitro. Our results show that the mutation of amino acids lining the opsin binding pocket is responsible for fine spectral tuning, or small changes in the λmax of these light-sensitive proteins. Mutations resulted in a blue or red shift as predicted, but with dissimilar magnitudes. Shifts ranged from a 16 nm blue shift to a 12 nm red shift from the wild-type λmax. These mutations do not show an additive effect, but rather suggest the presence of epistatic interactions. This work highlights the importance of binding pocket shape in the evolution of spectral tuning and builds on our ability to relate genotypic changes to phenotypes in an emerging model for opsin functional analysis. 

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5. Multiple Mechanisms of Photoreceptor Spectral Tuning in Heliconius Butterflies

   https://doi.org/10.1093/molbev/msac067  

   McCulloch, Kyle J.; Macias-Muñoz, Aide; Mortazavi, Ali; Briscoe, Adriana D. (April 2022, Molecular Biology and Evolution)

   Chang, Belinda (Ed.)

   Abstract The evolution of color vision is often studied through the lens of receptor gain relative to an ancestor with fewer spectral classes of photoreceptor. For instance, in Heliconius butterflies, a genus-specific UVRh opsin duplication led to the evolution of UV color discrimination in Heliconius erato females, a rare trait among butterflies. However, color vision evolution is not well understood in the context of loss. In Heliconius melpomene and Heliconius ismenius lineages, the UV2 receptor subtype has been lost, which limits female color vision in shorter wavelengths. Here, we compare the visual systems of butterflies that have either retained or lost the UV2 photoreceptor using intracellular recordings, ATAC-seq, and antibody staining. We identify several ways these butterflies modulate their color vision. In H. melpomene, chromatin reorganization has downregulated an otherwise intact UVRh2 gene, whereas in H. ismenius, pseudogenization has led to the truncation of UVRh2. In species that lack the UV2 receptor, the peak sensitivity of the remaining UV1 photoreceptor cell is shifted to longer wavelengths. Across Heliconius, we identify the widespread use of filtering pigments and co-expression of two opsins in the same photoreceptor cells. Multiple mechanisms of spectral tuning, including the molecular evolution of blue opsins, have led to the divergence of receptor sensitivities between species. The diversity of photoreceptor and ommatidial subtypes between species suggests that Heliconius visual systems are under varying selection pressures for color discrimination. Modulating the wavelengths of peak sensitivities of both the blue- and remaining UV-sensitive photoreceptor cells suggests that Heliconius species may have compensated for UV receptor loss. 

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