The last common ancestor of most bilaterian animals possessed at least 9 opsins

Ramirez, M. Desmond; Pairett, Autum N.; Pankey, M. Sabrina; Serb, Jeanne M.; Speiser, Daniel I.; Swafford, Austin D.; Oakley, Todd H.

doi:10.1101/052902

Cited by 22 publications

(41 citation statements)

References 73 publications

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“…To phylogenetically place each transcript within known opsin evolutionary diversity, the resulting alignment of 565 in-group opsin amino acid sequences, 12 out-group sequences from Trichoplax adhaerens Schultze, 1883 and closely related nonopsin G protein-coupled receptors (e.g., mouse melatonin receptor and human thyroid-stimulating hormone receptor) were used to estimate phylogenetic relationships and node confidence as bootstrap values using RAxML (Stamatakis 2006(Stamatakis , 2014Stamatakis et al 2008;Pattengale et al 2010;Liu et al 2012). Our phylogeny confirms earlier studies that the Araneae spiders contain opsins from three of the nine major opsin lineages present in the bilaterian ancestor (Ramirez et al, 2016): canonical r-opsins, canonical c-opsins, and peropsins ( Fig. 5; Koyanagi et al 2008;Nagata et al 2010 Schomburg et al 2015).…”

Section: Spider Phototransduction: Preliminary Clues Into Variationsupporting

confidence: 72%

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

Morehouse

Buschbeck

Zurek

et al. 2017

The Biological Bulletin

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Spiders are among the world's most species-rich animal lineages, and their visual systems are likewise highly diverse. These modular visual systems, composed of four pairs of image-forming "camera" eyes, have taken on a huge variety of forms, exhibiting variation in eye size, eye placement, image resolution, and field of view, as well as sensitivity to color, polarization, light levels, and motion cues. However, despite this conspicuous diversity, our understanding of the genetic underpinnings of these visual systems remains shallow. Here, we review the current literature, analyze publicly available transcriptomic data, and discuss hypotheses about the origins and development of spider eyes. Our efforts highlight that there are many new things to discover from spider eyes, and yet these opportunities are set against a backdrop of deep homology with other arthropod lineages. For example, many (but not all) of the genes that appear important for early eye development in spiders are familiar players known from the developmental networks of other model systems (e.g., Drosophila). Similarly, our analyses of opsins and related phototransduction genes suggest that spider photoreceptors employ many of the same genes and molecular mechanisms known from other arthropods, with a hypothesized ancestral spider set of four visual and four nonvisual opsins. This deep homology provides a number of useful footholds into new work on spider vision and the molecular basis of its extant variety. We therefore discuss what some of these first steps might be in the hopes of convincing others to join us in studying the vision of these fascinating creatures.

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Section: Spider Phototransduction: Preliminary Clues Into Variationsupporting

confidence: 72%

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

Morehouse

Buschbeck

Zurek

et al. 2017

The Biological Bulletin

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“…Phylogenetic analyses indicate the presence of at least seven opsins in the last common ancestor of Bilateria (Ramirez et al, 2016), thus suggesting that light reception had many roles very early in animal evolution. These opsins, together with present-day animal opsins, have been classified into four groups: (i) tetraopsins (Go-opsins, RGR/retinochrome opsins and neuropsins), (ii) xenopsins, (iii) Gq-opsins (including canonical and non-canonical r-opsins as well as "chaopsins"), and (iv) c-opsins, i.e., canonical c-opsins and bathyopsins (Ramirez et al, 2016). While the canonical c-and r-opsin groups have been extensively studied, little is known about the Go opsin group included in the tetraopsin clade (Gühmann et al, 2015).…”

Section: Ancientness Of Go-opsinsmentioning

confidence: 99%

“…The fact that the two bilateral photoreceptors connected to the apical organ of the pluteus larva use a Go-opsin, while ropsins are present in similar structures of nearly all other larvae, results remarkable. One possible explanation to why putative homologous paired photoreceptors express distinct opsins in different Bilateria clades could be that Urbilateria had bilaterally paired photoreceptors with r-opsin, c-opsins and Go-opsins serving different functions (Feuda et al, 2012;Ramirez et al, 2016). This variety of functions can be ascribed to the need of different spectral or temporal properties, as well as to different roles in the transducing the light signal.…”

Section: Bilateral Disposition and Lack Of Shading Pigmentsmentioning

confidence: 99%

“…Opsins are G-protein coupled receptors involved in lightperception. Based on their amino acid sequence, they can be divided into four groups: tetraopsin, xenopsin, Gq-opsin, and c-opsin (Ramirez et al, 2016; for other classifications see: Plachetzki et al, 2007;Arendt, 2008;Koyanagi et al, 2008;Porter et al, 2011;Feuda et al, 2012). The presence of opsins provides a clear landmark for localizing putative photoreceptor cells even in the absence of shading pigments and, as a consequence, the localization of opsin-expressing cells is important for finding directional and non-directional photoreceptors.…”

Section: Introductionmentioning

confidence: 99%

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Non-directional Photoreceptors in the Pluteus of Strongylocentrotus purpuratus

et al. 2016

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In comparison to complex visual systems, non-directional photoreception-the most primitive form of biological photodetection-has been poorly investigated, although it is essential to many biological processes such as circadian and seasonal rhythms. Here we describe the spatiotemporal expression pattern of the major molecular actors mediating light reception-opsins-localized in the Strongylocentrotus purpuratus larva. In contrast to other zooplanktonic larvae, the echinopluteus lacks photoreceptor cells with observable shading pigments involved in directional visual tasks. Nonetheless, the echinopluteus expresses two distinct classes of opsins: a Go-opsin and a rhabdomeric opsin. The Go-opsin, Sp-opsin3.2, is detectable at early (3 days post fertilization) and four armed pluteus stages (4 days post fertilization) in two cells that flank the apical organ. To rule out the presence of shading pigments involved in directional photoreception, we used electron microscopy to explore the expression domain of Go-opsin Sp-opsin3.2 positive cells. The rhabdomeric opsin Sp-Opsin4 expression is detectable in clusters of cells located around the primary podia at the five-fold ectoderm pentagonal disc stage (day 18-21) and thereafter, thus indicating that Sp-Opsin4 may not be involved in the photoreception mechanism of the larva, but only of the juvenile. We discuss the putative function of the relevant cells in their neural context, and propose a model for understanding simple photodetection in marine larvae.

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“…The evolution of opsin genes has been the subject of many studies because opsins play an essential role in vision and light detection. Much research has focused on deciphering the opsin phylogenetic tree in an effort to better understand the evolution of eyes and vision [1][2][3][4]. Visual opsin genes often encode G-protein coupled receptors that initiate the phototransduction cascade, a mechanism by which light information is converted into an electrical signal to be interpreted by the brain.…”

Section: Introductionmentioning

confidence: 99%

Molecular evolution and expression of opsin genes in Hydra vulgaris

Macias-Muñoz

Murad

Mortazavi

2019

Preprint

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Background: The evolution of opsin genes is of great interest because it can provide insight into the evolution of light detection and vision. An interesting group in which to study opsins is Cnidaria because it is a basal phylum sister to Bilateria with much visual diversity within the phylum. Hydra vulgaris (H. vulgaris) is a cnidarian with a plethora of genomic resources to characterize the opsin gene family. This eyeless cnidarian has a behavioral reaction to light, but it remains unknown which of its many opsins functions in light detection. Here, we used phylogenetics and RNA-seq to investigate the molecular evolution of opsin genes and their expression in H. vulgaris. We explored where opsin genes are located relative to each other in an improved genome assembly and where they belong in a cnidarian opsin phylogenetic tree. In addition, we used RNA-seq data from different tissues of the H. vulgaris adult body and different time points during regeneration and budding stages to gain insight into their potential functions. Results: We identified 45 opsin genes in H. vulgaris, many of which were located near each other suggesting evolution by tandem duplications. Our phylogenetic tree of cnidarian opsin genes supported previous claims that they are evolving by lineage-specific duplications. We identified two H. vulgaris genes (HvOpA1 and HvOpB1) that fall outside of the two commonly determined Hydra groups; these genes possibly have a function in nematocytes and mucous gland cells respectively. We also found opsin genes that have similar expression patterns to phototransduction genes in H. vulgaris. We propose a H. vulgaris phototransduction cascade that has components of both ciliary and rhabdomeric cascades. Conclusions: This extensive study provides an in-depth look at the molecular evolution and expression of H. vulgarisopsin genes. The expression data that we have quantified can be used as a springboard for additional studies looking into the specific function of opsin genes in this species. Our phylogeny and expression data are valuable to investigations of opsin gene evolution and cnidarian biology.

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The last common ancestor of most bilaterian animals possessed at least 9 opsins

Cited by 22 publications

References 73 publications

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

Non-directional Photoreceptors in the Pluteus of Strongylocentrotus purpuratus

Molecular evolution and expression of opsin genes in Hydra vulgaris

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