Metazoan opsin evolution reveals a simple route to animal vision

Feuda, Roberto; Hamilton, Sinead C.; McInerney, James O.; Pisani, Davide

doi:10.1073/pnas.1204609109

Cited by 170 publications

(241 citation statements)

References 35 publications

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“…7 in Leys and Meech (Leys and Meech, 2006)]. So far, no true opsin has been found in either the Amphimedon queenslandica or Oscarella carmela genomes nor in any transcriptome from sponges (Feuda et al, 2012).…”

Section: Sensory Cells In the Larvamentioning

confidence: 99%

Elements of a ‘nervous system’ in sponges

Leys

2015

Journal of Experimental Biology

123

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Genomic and transcriptomic analyses show that sponges possess a large repertoire of genes associated with neuronal processes in other animals, but what is the evidence these are used in a coordination or sensory context in sponges? The very different phylogenetic hypotheses under discussion today suggest very different scenarios for the evolution of tissues and coordination systems in early animals. The sponge genomic 'toolkit' either reflects a simple, pre-neural system used to protect the sponge filter or represents the remnants of a more complex signalling system and sponges have lost cell types, tissues and regionalization to suit their current suspensionfeeding habit. Comparative transcriptome data can be informative but need to be assessed in the context of knowledge of sponge tissue structure and physiology. Here, I examine the elements of the sponge neural toolkit including sensory cells, conduction pathways, signalling molecules and the ionic basis of signalling. The elements described do not fit the scheme of a loss of sophistication, but seem rather to reflect an early specialization for suspension feeding, which fits with the presumed ecological framework in which the first animals evolved.

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Section: Sensory Cells In the Larvamentioning

confidence: 99%

Elements of a ‘nervous system’ in sponges

Leys

2015

Journal of Experimental Biology

123

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“…Ramirez and colleagues have proposed that a repertoire of at least nine opsin paralogs was present in the bilaterian ancestor (Ramirez et al, 2016). In regard to the cnidarian opsins, there are conflicting results regarding their position in the phylogenetic tree (Feuda et al, 2012;Liegertova et al, 2015;Plachetzki et al, 2007;Porter et al, 2012;Suga et al, 2008). The function of most opsins consists of two steps: light absorption and G-protein activation in both visual and non-visual systems.…”

Section: Introductionmentioning

confidence: 99%

The opsin repertoire of the European lancelet: a window into light detection in a basal chordate

Pantzartzi

Pergner²,

Kozmiková³

et al. 2017

Int. J. Dev. Biol.

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Light detection in animals is predominantly based on the photopigment composed of a protein moiety, the opsin, and the chromophore retinal. Animal opsins originated very early in metazoan evolution from within the G-Protein Coupled Receptor (GPCR) gene superfamily and diversified into several distinct branches prior to the cnidarian-bilaterian split. The origin of opsin diversity, opsin classification and interfamily relationships have been the matter of long-standing debate. Comparative studies of opsins from various Metazoa provide key insight into the evolutionary history of opsins and the visual perception in animals. Here, we have analyzed the genome assembly of the cephalochordate Branchiostoma lanceolatum, applying BLAST, gene prediction tools and manual curation in order to predict de novo its complete opsin repertoire. We investigated the structure of predicted opsin genes, encoded proteins, their phylogenetic placement, and expression. We identified a total of 22 opsin genes in B. lanceolatum, of which 21 are expressed and the remaining one appears to be a pseudogene. According to our phylogenetic analysis, representatives from the three major opsin groups, namely C-type, the R-type and the Group 4, can be identified in B. lanceolatum. Most of the B. lanceolatum opsins exhibit a stage-specific, but not a tissue-specific, expression pattern. The large number of opsins detected in B. lanceolatum, the observed similarities and differences in terms of sequence characteristics and expression patterns lead us to conclude that there may be a fine tuning in opsin utilization in order to facilitate visually-guided behavior of European amphioxus under various environmental settings.

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“…There are at least three major groups of opsins: the r-opsins, c-opsins and Go/RGR (retinal G-protein-coupled receptor) opsins (Porter et al, 2012;Feuda et al, 2012). While c-opsins are typically thought to detect light in vertebrate eyes and r-opsins in invertebrate eyes, various opsins are expressed in the skin of many animals (Ramirez et al, 2011), and opsins have been localized to receptors dispersed across the body of animals from multiple phyla, including cnidarians, echinoderms, annelids and vertebrates (Plachetzki et al, 2012;Raible et al, 2006;Backfisch et al, 2013;Bellono et al, 2013;Fulgione et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

Ramirez

Oakley

2015

Journal of Experimental Biology

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Cephalopods are renowned for changing the color and pattern of their skin for both camouflage and communication. Yet, we do not fully understand how cephalopods control the pigmented chromatophore organs in their skin and change their body pattern. Although these changes primarily rely on eyesight, we found that light causes chromatophores to expand in excised pieces of Octopus bimaculoides skin. We call this behavior light-activated chromatophore expansion (or LACE). To uncover how octopus skin senses light, we used antibodies against r-opsin phototransduction proteins to identify sensory neurons that express r-opsin in the skin. We hypothesized that octopus LACE relies on the same r-opsin phototransduction cascade found in octopus eyes. By creating an action spectrum for the latency to LACE, we found that LACE occurred most quickly in response to blue light. We fit our action spectrum data to a standard opsin curve template and estimated the λ max of LACE to be 480 nm. Consistent with our hypothesis, the maximum sensitivity of the light sensors underlying LACE closely matches the known spectral sensitivity of opsin from octopus eyes. LACE in isolated preparations suggests that octopus skin is intrinsically light sensitive and that this dispersed light sense might contribute to their unique and novel patterning abilities. Finally, our data suggest that a common molecular mechanism for light detection in eyes may have been co-opted for light sensing in octopus skin and then used for LACE.

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Metazoan opsin evolution reveals a simple route to animal vision

Cited by 170 publications

References 35 publications

Elements of a ‘nervous system’ in sponges

Elements of a ‘nervous system’ in sponges

The opsin repertoire of the European lancelet: a window into light detection in a basal chordate

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

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