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  • 1. Collin, Shaun P.
    et al.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Biological Sciences, The University of Western Australia, Perth, WA, Australia;The Oceans Graduate School, The University of Western Australia, Perth, WA, Australia;The Oceans Institute, The University of Western Australia, Perth, WA, Australia;Centre for Ophthalmology and Visual Science, Lions Eye Institute, The University of Western Australia, Perth, WA, Australia.
    Editorial: Biodiversity of Sensory Systems in Aquatic Vertebrates2020In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 8, article id 192Article in journal (Refereed)
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  • 2.
    Dakhel, Soran
    et al.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Joseph, Justin V.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Tomar, Tushar
    PamGene International B.V, 's-Hertogenbosch, Wolvenhoek 10, Netherlands.
    Remeseiro, Silvia
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).
    Gunhaga, Lena
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Chick fetal organ spheroids as a model to study development and disease2021In: BMC Molecular and Cell Biology, E-ISSN 2661-8850, Vol. 22, no 1, article id 37Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: Organ culture models have been used over the past few decades to study development and disease. The in vitro three-dimensional (3D) culture system of organoids is well known, however, these 3D systems are both costly and difficult to culture and maintain. As such, less expensive, faster and less complex methods to maintain 3D cell culture models would complement the use of organoids. Chick embryos have been used as a model to study human biology for centuries, with many fundamental discoveries as a result. These include cell type induction, cell competence, plasticity and contact inhibition, which indicates the relevance of using chick embryos when studying developmental biology and disease mechanisms.

    RESULTS: Here, we present an updated protocol that enables time efficient, cost effective and long-term expansion of fetal organ spheroids (FOSs) from chick embryos. Utilizing this protocol, we generated FOSs in an anchorage-independent growth pattern from seven different organs, including brain, lung, heart, liver, stomach, intestine and epidermis. These three-dimensional (3D) structures recapitulate many cellular and structural aspects of their in vivo counterpart organs and serve as a useful developmental model. In addition, we show a functional application of FOSs to analyze cell-cell interaction and cell invasion patterns as observed in cancer.

    CONCLUSION: The establishment of a broad ranging and highly effective method to generate FOSs from different organs was successful in terms of the formation of healthy, proliferating 3D organ spheroids that exhibited organ-like characteristics. Potential applications of chick FOSs are their use in studies of cell-to-cell contact, cell fusion and tumor invasion under defined conditions. Future studies will reveal whether chick FOSs also can be applicable in scientific areas such as viral infections, drug screening, cancer diagnostics and/or tissue engineering.

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  • 3.
    Davies, Wayne I. L.
    et al.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Sghari, Soufien
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Upton, Brian A.
    Nord, Christoffer
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Hahn, Max
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Ahlgren, Ulf
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Lang, Richard A.
    Gunhaga, Lena
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Distinct opsin 3 (Opn3) expression in the developing nervous system during mammalian embryogenesis2021In: eNeuro, E-ISSN 2373-2822, Vol. 8, no 5, article id ENEURO.0141-21.2021Article in journal (Refereed)
    Abstract [en]

    Opsin 3 (Opn3) is highly expressed in the adult brain, however, information for spatial and temporal expression patterns during embryogenesis is significantly lacking. Here, an Opn3-eGFP reporter mouse line was used to monitor cell body expression and axonal projections during embryonic and early postnatal to adult stages. By applying 2D and 3D fluorescence imaging techniques, we have identified the onset of Opn3 expression, which predominantly occurred during embryonic stages, in various structures during brain/head development. In ad-dition, this study defines over twenty Opn3-eGFP-positive neural structures never reported before. Opn3-eGFP was first observed at E9.5 in neural regions, including the ganglia that will ultimately form the trigeminal, facial and vestibulocochlear cranial nerves (CNs). As development proceeds, expanded Opn3-eGFP expression coincided with the formation and maturation of critical components of the central and peripheral nervous systems (CNS, PNS), including various motor-sensory tracts, such as the dorsal column-medial lemniscus (DCML) sensory tract, and olfactory, acoustic, and optic tracts. The widespread, yet distinct, detection of Opn3-eGFP already at early embryonic stages suggests that Opn3 might play important functional roles in the developing brain and spinal cord to regulate multiple motor and sensory circuitry systems, including proprio-ception, nociception, ocular movement, and olfaction, as well as memory, mood, and emotion. This study presents a crucial blueprint from which to investigate autonomic and cognitive opsin-dependent neural development and resultant behaviors under physiological and pathophysiological conditions.

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  • 4.
    Eilertsen, Mariann
    et al.
    Department of Biological Sciences, University of Bergen, Bergen, Norway.
    Davies, Wayne Iwan Lee
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Life Sciences, College of Science, Health and Engineering, La Trobe University, VIC, Melbourne, Australia.
    Patel, Dharmeshkumar
    Institute for Modeling Collaboration and Innovation (IMCI), University of Idaho, ID, Moscow, United States.
    Barnes, Jonathan E.
    Institute for Modeling Collaboration and Innovation (IMCI), University of Idaho, ID, Moscow, United States.
    Karlsen, Rita
    Department of Biological Sciences, University of Bergen, Bergen, Norway.
    Mountford, Jessica Kate
    School of Life Sciences, College of Science, Health and Engineering, La Trobe University, VIC, Melbourne, Australia; Lions Eye Institute, University of Western Australia, WA, Perth, Australia.
    Stenkamp, Deborah L.
    Department of Biological Sciences, University of Idaho, ID, Moscow, United States; Institute for Bioinformatics and Evolutionary Studies, University of Idaho, ID, Moscow, United States.
    Patel, Jagdish Suresh
    Institute for Modeling Collaboration and Innovation (IMCI), University of Idaho, ID, Moscow, United States; Department of Biological Sciences, University of Idaho, ID, Moscow, United States.
    Helvik, Jon Vidar
    Department of Biological Sciences, University of Bergen, Bergen, Norway.
    An EvoDevo Study of Salmonid Visual Opsin Dynamics and Photopigment Spectral Sensitivity2022In: Frontiers in Neuroanatomy, E-ISSN 1662-5129, Vol. 16, article id 945344Article in journal (Refereed)
    Abstract [en]

    Salmonids are ideal models as many species follow a distinct developmental program from demersal eggs and a large yolk sac to hatching at an advanced developmental stage. Further, these economically important teleosts inhabit both marine- and freshwaters and experience diverse light environments during their life histories. At a genome level, salmonids have undergone a salmonid-specific fourth whole genome duplication event (Ss4R) compared to other teleosts that are already more genetically diverse compared to many non-teleost vertebrates. Thus, salmonids display phenotypically plastic visual systems that appear to be closely related to their anadromous migration patterns. This is most likely due to a complex interplay between their larger, more gene-rich genomes and broad spectrally enriched habitats; however, the molecular basis and functional consequences for such diversity is not fully understood. This study used advances in genome sequencing to identify the repertoire and genome organization of visual opsin genes (those primarily expressed in retinal photoreceptors) from six different salmonids [Atlantic salmon (Salmo salar), brown trout (Salmo trutta), Chinook salmon (Oncorhynchus tshawytcha), coho salmon (Oncorhynchus kisutch), rainbow trout (Oncorhynchus mykiss), and sockeye salmon (Oncorhynchus nerka)] compared to the northern pike (Esox lucius), a closely related non-salmonid species. Results identified multiple orthologues for all five visual opsin classes, except for presence of a single short-wavelength-sensitive-2 opsin gene. Several visual opsin genes were not retained after the Ss4R duplication event, which is consistent with the concept of salmonid rediploidization. Developmentally, transcriptomic analyzes of Atlantic salmon revealed differential expression within each opsin class, with two of the long-wavelength-sensitive opsins not being expressed before first feeding. Also, early opsin expression in the retina was located centrally, expanding dorsally and ventrally as eye development progressed, with rod opsin being the dominant visual opsin post-hatching. Modeling by spectral tuning analysis and atomistic molecular simulation, predicted the greatest variation in the spectral peak of absorbance to be within the Rh2 class, with a ∼40 nm difference in λmax values between the four medium-wavelength-sensitive photopigments. Overall, it appears that opsin duplication and expression, and their respective spectral tuning profiles, evolved to maximize specialist color vision throughout an anadromous lifecycle, with some visual opsin genes being lost to tailor marine-based vision.

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  • 5.
    Eilertsen, Mariann
    et al.
    Department of Biological Sciences, University of Bergen, Bergen, Norway.
    Dolan, David W.P.
    Department of Informatics, University of Bergen, Bergen, Norway.
    Bolton, Charlotte M.
    Institute of Aquaculture, University of Stirling, Stirling, United Kingdom.
    Karlsen, Rita
    Department of Biological Sciences, University of Bergen, Bergen, Norway.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Life Sciences, College of Science, Health and Engineering, La Trobe University, Melbourne, Australia.
    Edvardsen, Rolf B.
    Institute of Marine Research, Bergen, Norway.
    Furmanek, Tomasz
    Institute of Marine Research, Bergen, Norway.
    Sveier, Harald
    Lerøy Seafood Group ASA, Bergen, Norway.
    Migaud, Herve
    Institute of Aquaculture, University of Stirling, Stirling, United Kingdom.
    Helvik, Jon Vidar
    Department of Biological Sciences, University of Bergen, Bergen, Norway.
    Photoreception and transcriptomic response to light during early development of a teleost with a life cycle tightly controlled by seasonal changes in photoperiod2022In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 18, no 12, article id e1010529Article in journal (Refereed)
    Abstract [en]

    Light cues vary along the axis of periodicity, intensity and spectrum and perception of light is dependent on the photoreceptive capacity encoded within the genome and the opsins expressed. A global approach was taken to analyze the photoreceptive capacity and the effect of differing light conditions on a developing teleost prior to first feeding. The transcriptomes of embryos and alevins of Atlantic salmon (Salmo salar) exposed to different light conditions were analyzed, including a developmental series and a circadian profile. The results showed that genes mediating nonvisual photoreception are present prior to hatching when the retina is poorly differentiated. The clock genes were expressed early, but the circadian profile showed that only two clock genes were significantly cycling before first feeding. Few genes were differentially expressed between day and night within a light condition; however, many genes were significantly different between light conditions, indicating that light environment has an impact on the transcriptome during early development. Comparing the transcriptome data from constant conditions to periodicity of white light or different colors revealed overrepresentation of genes related to photoreception, eye development, muscle contraction, degradation of metabolites and cell cycle among others, and in constant light, several clock genes were upregulated. In constant white light and periodicity of green light, genes associated with DNA replication, chromatin remodeling, cell division and DNA repair were downregulated. The study implies a direct influence of light conditions on the transcriptome profile at early developmental stages, by a complex photoreceptive system where few clock genes are cycling.

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  • 6. Hart, Nathan S.
    et al.
    Lamb, Trevor D.
    Patel, Hardip R.
    Chuah, Aaron
    Natoli, Riccardo C.
    Hudson, Nicholas J.
    Cutmore, Scott C.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Collin, Shaun P.
    Hunt, David M.
    Visual Opsin Diversity in Sharks and Rays2020In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 37, no 3, p. 811-827Article in journal (Refereed)
    Abstract [en]

    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.

  • 7. Hickey, Doron G.
    et al.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Nuffield Laboratory of Ophthalmology, University of Oxford, UK; 4 School of Life Sciences, College of Science, Health and Engineering, La Trobe University, Melbourne, Australia.
    Hughes, Steven
    Rodgers, Jessica
    Thavanesan, Navamayooran
    MacLaren, Robert E.
    Hankins, Mark W.
    Chimeric human opsins as optogenetic light sensitisers2021In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 224, no 14, article id jeb240580Article in journal (Refereed)
    Abstract [en]

    Human opsin-based photopigments have great potential as light-sensitisers, but their requirement for phototransduction cascade-specific second messenger proteins may restrict their functionality in non-native cell types. In this study, eight chimeric human opsins were generated consisting of a backbone of either a rhodopsin (RHO) or long-wavelength-sensitive (LWS) opsin and intracellular domains from G(q/11)-coupled human melanopsin. Rhodopsin/melanopsin chimeric opsins coupled to both Gi and G(q/11) pathways. Greater substitution of the intracellular surface with corresponding melanopsin domains generally showed greater G(q/11) activity with a decrease in Gi activation. Unlike melanopsin, rhodopsin and rhodopsin/melanopsin chimeras were dependent upon exogenous chromophore to function. By contrast, wild-type LWS opsin and LWS opsin/melanopsin chimeras showed only weak Gi activation in response to light, whilst G(q/11) pathway activation was not detected. Immunocytochemistry (ICC) demonstrated that chimeric opsins with more intracellular domains of melanopsin were less likely to be trafficked to the plasma membrane. This study demonstrates the importance of Ga coupling efficiency to the speed of cellular responses and created human opsins with a unique combination of properties to expand the range of customised optogenetic biotools for basic research and translational therapies.

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  • 8.
    Karthikeyan, Ramanujam
    et al.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Life Sciences, College of Science, Health and Engineering, La Trobe University, Melbourne Campus, VIC, Melbourne, Australia.
    Gunhaga, Lena
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Non-image-forming functional roles of OPN3, OPN4 and OPN5 photopigments2023In: Journal of Photochemistry and Photobiology, E-ISSN 2666-4690, Vol. 15, article id 100177Article in journal (Refereed)
    Abstract [en]

    Detecting different wavelengths and intensities of environmental light is crucial for the survival of many animals. In response, a multiplicity of opsins (a special group of photosensitive G protein-coupled receptors), when combined with a retinal chromophore, is able to directly detect light and initiate different downstream phototransduction signaling cascades. Although avian studies from the 1930s suggested the presence of deep brain photoreceptors that could respond to seasonal changes in the light/dark cycle, it was only a few decades ago that photopigments other than those found in the visual system (i.e. rods and cones) were identified as functional photoreceptors. It is now established that several classes of non-visual photoreceptors and the photopigments they express, in lower vertebrates to higher mammals alike, can regulate a plethora of mechanisms that function outside of vision. These include the synchronization of light/dark cycles with biological/cellular rhythms of the body (i.e. photoentrainment); melanogenesis in dermal tissues; thermoregulation in adipose tissue; embryonic eye development; smooth muscle relaxation; and the development of certain cancers. These and other mechanisms have been shown, in part at least, to be controlled by the expression of three important non-visual opsin genes, namely OPN3, OPN4 and OPN5, although other vertebrate opsin classes exist, many with unknown or unclear functional roles assigned to them presently. Specifically, these three opsins have been shown to be expressed during early embryogenesis and throughout adulthood, which will be discussed here. Moreover, this review highlights recent studies that focus on several key non-image-forming functional roles of OPN3, OPN4 and OPN5, and in particular those that impact photoreception in developing structures and pathways, as well as in adulthood.

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  • 9. Katti, Christiana
    et al.
    Stacey-Solis, Micaela
    Anahí Coronel-Rojas, Nicole
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Oceans Graduate School, University of Western Australia, Crawley, Australia; Oceans Institute, University of Western Australia, Crawley, Australia; School of Biological Sciences, University of Western Australia, Perth, Australia; Center for Ophthalmology and Visual Science, Lions Eye Institute, University of Western Australia, Perth, Australia.
    The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles2019In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 7, article id 352Article in journal (Refereed)
    Abstract [en]

    Reptiles are a highly diverse class that consists of snakes, geckos, iguanid lizards, and chameleons among others. Given their unique phylogenetic position in relation to both birds and mammals, reptiles are interesting animal models with which to decipher the evolution of vertebrate photopigments (opsin protein plus a light-sensitive retinal chromophore) and their contribution to vision. Reptiles possess different types of retinae that are defined primarily by variations in photoreceptor morphology, which range from pure-cone to rod-dominated retinae with many species possessing duplex (rods and cones) retinae. In most cases, the type of retina is thought to reflect both the lifestyle and the behavior of the animal, which can vary between diurnal, nocturnal, or crepuscular behavioral activities. Reptiles, and in particular geckos and snakes, have been used as prime examples for the “transmutation” hypothesis proposed by Walls in the 1930s-1940s, which postulates that some reptilian species have migrated from diurnality to nocturnality, before subsequently returning to diurnal activities once again. This theory further states that these behavioral changes are reflected in subsequent changes in photoreceptor morphology and function from cones to rods, with a return to cone-like photoreceptors once again. Modern sequencing techniques have further investigated the “transmutation” hypothesis by using molecular biology to study the phototransduction cascades of rod- and cone-like photoreceptors in the reptilian retina. This review will discuss what is currently known about the evolution of opsin-based photopigments in reptiles, relating habitat to photoreceptor morphology, as well as opsin and phototransduction cascade gene expression.

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  • 10.
    Lehrstrand, Joakim
    et al.
    Umeå University, Faculty of Medicine, Department of Medical and Translational Biology.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Department of Medical and Translational Biology.
    Hahn, Max
    Umeå University, Faculty of Medicine, Department of Medical and Translational Biology.
    Korsgren, Olle
    Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.
    Alanentalo, Tomas
    Umeå University, Faculty of Medicine, Department of Medical and Translational Biology.
    Ahlgren, Ulf
    Umeå University, Faculty of Medicine, Department of Medical and Translational Biology.
    Illuminating the complete ß-cell mass of the human pancreas - signifying a new view on the islets of Langerhans2024In: Nature Communications, E-ISSN 2041-1723, Vol. 15, no 1, article id 3318Article in journal (Refereed)
    Abstract [en]

    Pancreatic islets of Langerhans play a pivotal role in regulating blood glucose homeostasis, but critical information regarding their mass, distribution and composition is lacking within a whole organ context. Here, we apply a 3D imaging pipeline to generate a complete account of the insulin-producing islets throughout the human pancreas at a microscopic resolution and within a maintained spatial 3D context. These data show that human islets are far more heterogenous than previously accounted for with regards to their size distribution and cellular make up. By deep tissue 3D imaging, this in-depth study demonstrates that 50% of the human insulin-expressing islets are virtually devoid of glucagon-producing α-cells, an observation with significant implications for both experimental and clinical research.

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  • 11. Mohun, Samantha Mila
    et al.
    Davies, Wayne Iwan Lee
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Oceans Graduate School, University of Western Australia, Crawley, WA, Australia; Oceans Institute, University of Western Australia, Crawley, WA, Australia; School of Biological Sciences, University of Western Australia, Crawley, WA, Australia; Center for Ophthalmology and Visual Science, Lions Eye Institute, University of Western Australia, Crawley, WA, Australia.
    The Evolution of Amphibian Photoreception2019In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 7, article id 321Article, review/survey (Refereed)
    Abstract [en]

    There have been a growing number of studies into the visual evolution of vertebrates. However, there remain few detailed integrative studies on the visual system of amphibians using morphological, molecular and physiological methods outside of a few model species. There are many examples of amphibian species that are closely related phylogenetically, but occupy vastly different ecological niches and so provide a substantial resource for the study of adaptive evolution. This review will examine the published literature on the three living orders of amphibians, the Anurans, Caudata, and Gymnophiona.

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  • 12. Musilova, Zuzana
    et al.
    Cortesi, Fabio
    Matschiner, Michael
    Davies, Wayne I. L.
    UWA Oceans Institute; School of Biological Sciences; Lions Eye Institute; Oceans Graduate School, The University of Western Australia, Perth, WA, Australia.
    Patel, Jagdish Suresh
    Stieb, Sara M.
    de Busserolles, Fanny
    Malmstrom, Martin
    Torresen, Ole K.
    Brown, Celeste J.
    Mountford, Jessica K.
    Hanel, Reinhold
    Stenkamp, Deborah L.
    Jakobsen, Kjetill S.
    Carleton, Karen L.
    Jentoft, Sissel
    Marshall, Justin
    Salzburger, Walter
    Vision using multiple distinct rod opsins in deep-sea fishes2019In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 364, no 6440, p. 588-+Article in journal (Refereed)
    Abstract [en]

    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.

  • 13.
    Nagloo, Nicolas
    et al.
    School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia; Department of Biology, Lund University, Lund, Sweden; The UWA Oceans Institute, The University of Western Australia, WA, Nedlands, Australia.
    Mountford, Jessica K.
    School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia; The UWA Oceans Institute, The University of Western Australia, WA, Nedlands, Australia; Oceans Graduate School, The University of Western Australia, WA, Crawley, Australia; Clinical Genetics and Epidemiology, Centre for Ophthalmology and Visual Science incorporating the Lions Eye Institute, The University of Western Australia, WA, Nedlands, Australia.
    Gundry, Ben J.
    School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia.
    Hart, Nathan S.
    School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia; School of Natural Sciences, Macquarie University, NSW, Sydney, Australia.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia; The UWA Oceans Institute, The University of Western Australia, WA, Nedlands, Australia; Oceans Graduate School, The University of Western Australia, WA, Crawley, Australia; Clinical Genetics and Epidemiology, Centre for Ophthalmology and Visual Science incorporating the Lions Eye Institute, The University of Western Australia, WA, Nedlands, Australia; School of Agriculture, Biomedicine and Environment, La Trobe University, VIC, Bundoora, Australia.
    Collin, Shaun P.
    School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia; The UWA Oceans Institute, The University of Western Australia, WA, Nedlands, Australia; Oceans Graduate School, The University of Western Australia, WA, Crawley, Australia; Clinical Genetics and Epidemiology, Centre for Ophthalmology and Visual Science incorporating the Lions Eye Institute, The University of Western Australia, WA, Nedlands, Australia; School of Agriculture, Biomedicine and Environment, La Trobe University, VIC, Bundoora, Australia.
    Hemmi, Jan M.
    School of Biological Sciences, The University of Western Australia, WA, Crawley, Australia; The UWA Oceans Institute, The University of Western Australia, WA, Nedlands, Australia.
    Enhanced short-wavelength sensitivity in the blue-tongued skink Tiliqua rugosa2022In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 225, no 11, article id jeb244317Article in journal (Refereed)
    Abstract [en]

    Despite lizards using a wide range of colour signals, the limited variation in photoreceptor spectral sensitivities across lizards suggests only weak selection for species-specific, spectral tuning of photoreceptors. Some species, however, have enhanced short-wavelength sensitivity, which probably helps with the detection of signals rich in ultraviolet and short wavelengths. In this study, we examined the visual system of Tiliqua rugosa, which has an ultraviolet/blue tongue, to gain insight into this species' visual ecology. We used electroretinograms, opsin sequencing and immunohistochemical labelling to characterize whole-eye spectral sensitivity and the elements that shape it. Our findings reveal that T. rugosa expresses all five opsins typically found in lizards (SWS1, SWS2, RH1, RH2 and LWS) but possesses greatly enhanced short-wavelength sensitivity compared with other diurnal lizards. This enhanced short-wavelength sensitivity is characterized by a broadening of the spectral sensitivity curve of the eye towards shorter wavelengths while the peak sensitivity of the eye at longer wavelengths (560 nm) remains similar to that of other diurnal lizards. While an increased abundance of SWS1 photoreceptors is thought to mediate elevated ultraviolet sensitivity in a couple of other lizard species, SWS1 photoreceptor abundance remains low in this species. Instead, our findings suggest that short-wavelength sensitivity is driven by multiple factors which include a potentially red-shifted SWS1 photoreceptor and the absence of short-wavelength-absorbing oil droplets. Examining the coincidence of enhanced short-wavelength sensitivity with blue tongues among lizards of this genus will provide further insight into the co-evolution of conspecific signals and whole-eye spectral sensitivity.

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  • 14. Patel, Dharmeshkumar
    et al.
    Barnes, Jonathan E.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Biological Sciences, University of Western Australia, Perth, WA, Australia; The Oceans Graduate School, University of Western Australia, Perth, WA, Australia; The Oceans Institute, University of Western Australia, Perth, WA, Australia; Lions Eye Institute, University of Western Australia, Perth, WA, Australia.
    Stenkamp, Deborah L.
    Patel, Jagdish Suresh
    Short-wavelength-sensitive 2 (Sws2) visual photopigment models combined with atomistic molecular simulations to predict spectral peaks of absorbance2020In: PloS Computational Biology, ISSN 1553-734X, E-ISSN 1553-7358, Vol. 16, no 10, article id e1008212Article in journal (Refereed)
    Abstract [en]

    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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  • 15.
    Schluessel, Vera
    et al.
    Institute of Zoology, Rheinische Friedrich-Wilhelms-Universitat Bonn, Poppelsdorfer Schloss, Meckenheimer Allee 169, Bonn, Germany.
    Rick, Ingolf P.
    Institute of Zoology, Rheinische Friedrich-Wilhelms-Universitat Bonn, Poppelsdorfer Schloss, Meckenheimer Allee 169, Bonn, Germany.
    Seifert, Friederike Donata
    Institute of Zoology, Rheinische Friedrich-Wilhelms-Universitat Bonn, Poppelsdorfer Schloss, Meckenheimer Allee 169, Bonn, Germany.
    Baumann, Christina
    Institute of Zoology, Rheinische Friedrich-Wilhelms-Universitat Bonn, Poppelsdorfer Schloss, Meckenheimer Allee 169, Bonn, Germany.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Institute of Zoology, Rheinische Friedrich-Wilhelms-Universitat Bonn, Poppelsdorfer Schloss, Meckenheimer Allee 169, Bonn, Germany; School of Life Sciences, College of Science, Health and Engineering, La Trobe University, Melbourne Campus, VIC, Melbourne, Australia.
    Not just shades of grey: Life is full of colour for the ocellate river stingray (Potamotrygon motoro)2021In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 224, no 9, article id jeb226142Article in journal (Refereed)
    Abstract [en]

    Previous studies have shown that marine stingrays have the anatomical and physiological basis for colour vision, with cone spectral sensitivity in the blue to green range of the visible spectrum. Behavioural studies on Glaucostegus typus also showed that blue and grey can be perceived and discriminated. The present study is the first to assess visual opsin genetics in the ocellate river stingray (Potamotrygon motoro) and test whether individuals perceive colour in two alternative forced choice experiments. Retinal transcriptome profiling using RNA-Seq and quantification demonstrated the presence of lws and rh2 cone opsin genes and a highly expressed single rod (rh1) opsin gene. Spectral tuning analysis predicted these vitamin A1-based visual photopigments to exhibit spectral absorbance maxima at 461 nm (rh2), 496 nm (rh1) and 555 nm (lws); suggesting the presence of dichromacy in this species. Indeed, P. motoro demonstrates the potential to be equally sensitive to wavelengths from 380 to 600 nm of the visible spectrum. Behavioural results showed that red and green plates, as well as blue and yellow plates, were readily discriminated based on colour; however, brightness differences also played a part in the discrimination of blue and yellow. Red hues of different brightness were distinguished significantly above chance level from one another. In conclusion, the genetic and behavioural results support prior data on marine stingrays. However, this study suggests that freshwater stingrays of the family Potamotrygonidae may have a visual colour system that has ecologically adapted to a riverine habitat.

  • 16.
    Sghari, Soufien
    et al.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Gunhaga, Lena
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM).
    Elucidation of Cellular Mechanisms That Regulate the Sustained Contraction and Relaxation of the Mammalian Iris2020In: Investigative Ophthalmology and Visual Science, ISSN 0146-0404, E-ISSN 1552-5783, Vol. 61, no 11, article id 5Article in journal (Refereed)
    Abstract [en]

    PURPOSE. In mammals, pupil constriction and dilation form the pupillary light reflex (PLR), which is mediated by both brain-regulated (parasympathetic) and local iris-driven reflexes. To better understand the cellular mechanisms that regulate pupil physiological dynamics via central and local photoreception, we have examined the regulation of the PLR via parasympathetic and local activation, respectively.

    METHODS. In this study, the PLR was examined in mouse enucleated eyes ex vivo in real-time under different ionic conditions in response to acetylcholine and/or blue light (480 nm). The use of pupillometry recordings captured the relaxation, contraction, and pupil escape (redilation) processes for 10 minutes up to 1 hour.

    RESULTS. Among others, our results show that ryanodine receptor channels are the main driver for iridal stimulation-contraction coupling, in which extracellular influx of Ca2+ is required for amplification of pupil constriction. Both local and parasympathetic iridal activations are necessary, but not sufficient for sustained pupil constriction. Moreover, the degree of membrane potential repolarization in the dark is correlated with the latency and velocity of iridal constriction. Furthermore, pupil escape is driven by membrane potential hyperpolarization where voltage-gated potassium channels play a crucial role.

    CONCLUSIONS. Together, this study presents new mechanisms regulating synchronized pupil dilation and contraction, sustained pupil constriction, iridal stimulation-contraction coupling, and pupil escape.

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  • 17. Warrington, Rachael E.
    et al.
    Davies, Wayne I. L.
    Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). School of Biological Sciences, The University of Western Australia, Perth, Western Australia, Australia; Oceans Institute, The University of Western Australia, Perth, Western Australia, Australia; Centre for Ophthalmology and Visual Science, Lions Eye Institute, University of Western Australia, Perth, Western Australia, Australia; School of Life Sciences, La Trobe University, Melbourne, Victoria, Australia.
    Hemmi, Jan M.
    Hart, Nathan S.
    Potter, Ian C.
    Collin, Shaun P.
    Hunt, David M.
    Visual opsin expression and morphological characterization of retinal photoreceptors in the pouched lamprey (Geotria australis, Gray)2021In: Journal of Comparative Neurology, ISSN 0021-9967, E-ISSN 1096-9861, Vol. 529, no 9, p. 2265-2282Article in journal (Refereed)
    Abstract [en]

    Lampreys are extant members of the agnathan (jawless) vertebrates that diverged ~500 million years ago, during a critical stage of vertebrate evolution when image‐forming eyes first emerged. Among lamprey species assessed thus far, the retina of the southern hemisphere pouched lamprey, Geotria australis, is unique, in that it possesses morphologically distinct photoreceptors and expresses five visual photopigments. This study focused on determining the number of different photoreceptors present in the retina of G. australis and whether each cell type expresses a single opsin class. Five photoreceptor subtypes were identified based on ultrastructure and differential expression of one of each of the five different visual opsin classes (lws, sws1, sws2, rh1, and rh2) known to be expressed in the retina. This suggests, therefore, that the retina of G. australis possesses five spectrally and morphologically distinct photoreceptors, with the potential for complex color vision. Each photoreceptor subtype was shown to have a specific spatial distribution in the retina, which is potentially associated with changes in spectral radiance across different lines of sight. These results suggest that there have been strong selection pressures for G. australis to maintain broad spectral sensitivity for the brightly lit surface waters that this species inhabits during its marine phase. These findings provide important insights into the functional anatomy of the early vertebrate retina and the selection pressures that may have led to the evolution of complex color vision.

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