Lowe EK et al. (2018), The crowns have eyes: multiple opsins found in ...

ECB-ART-46746

BMC Evol Biol 2018 Nov 12;181:168. doi: 10.1186/s12862-018-1276-0.

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The crowns have eyes: multiple opsins found in the eyes of the crown-of-thorns starfish Acanthaster planci.

Lowe EK , Garm AL , Ullrich-Lüter E , Cuomo C , Arnone MI .

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BACKGROUND: Opsins are G protein-coupled receptors used for both visual and non-visual photoreception, and these proteins evolutionarily date back to the base of the bilaterians. In the current sequencing age, phylogenomic analysis has proven to be a powerful tool, facilitating the increase in knowledge about diversity within the opsin subclasses and, so far, at least nine types of opsins have been identified. Within echinoderms, opsins have been studied in Echinoidea and Ophiuroidea, which do not possess proper image forming eyes, but rather widely dispersed dermal photoreceptors. However, most species of Asteroidea, the starfish, possess true eyes and studying them will shed light on the diversity of opsin usage within echinoderms and help resolve the evolutionary history of opsins. RESULTS: Using high-throughput RNA sequencing, we have sequenced and analyzed the transcriptomes of different Acanthaster planci tissue samples: eyes, radial nerve, tube feet and a mixture of tissues from other organs. At least ten opsins were identified, and eight of them were found significantly differentially expressed in both eyes and radial nerve, with R-opsin being the most highly expressed in the eye. CONCLUSION: This study provides new important insight into the involvement of opsins in visual and nonvisual photoreception. Of relevance, we found the first indication of an r-opsin photopigment expressed in a well-developed visual eye in a deuterostome animal. Additionally, we provided tissue specific A. planci transcriptomes that will aid in future Evo Devo studies.

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Genes referenced: rhol1

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	Fig. 1. The compound eye of A. planci. The eyes are found on the distalmost tube foot on each arm tip and the fully grown eye has about 300 ommatidia here seen as red rings formed by the screening pigment (arrow). The eyes are image forming and each ommatidium is thought to constitute a separate pixel in the image. Scale bar = 100 Î¼m
	Fig. 2. Phylogenomic bayesian tree of 169 opsin sequences with melatonin receptors as the outgroup. There are 10 A. planci opsins (bold and checkered background) which classify into 7 different groups: 4 c-opsins, 1 chaopsin, 1 r-opsin, 1 peropsin, 1 RGR opsin, 1 go-opsin, and 1 neuropsin. No bathyopsin was found in A. planci, and has yet to be identified in any starfish species. The tree was generated by using Mr. Bayes (v3.2.5) [33] 50 million generations, with the GTR + G amino acid substitution model
	Fig. 3. Differential expression of the eye tissue samples versus the mixed tissue samples. The y-axis shows log2 fold change of gene expression, with points greater than 0 being more highly expressed in the eye tissue samples compared to the mixed tissue samples and the x-axis are mean normalized counts of the 3 replicates for each transcript. Points in pale blue have an adjusted p-value greater than 0.05, while points in grey are said to be significantly differentially expressed, having an adjusted p-value less than 0.05. Points of different shapes and colors represent the various opsins. R-opsin is the most differentially expressed, followed by chaopsin. With the exception of c-opsin 1.1b and neuropsin, all opsins are significantly differentially expressed in the eyes of A. planci compared to the mixed tissue samples
	Fig. 4. Summary of differential opsin expression data from the four different A. planci tissue samples. Counts were normalized for transcripts length and library size using transcripts per kilobase million (TPM) in order to compare opsins for each tissue type. For eyes (red) the highest expressed opsins are r-opsin, peropsin, chaopsin, RGR opsin, and go-opsin, with c-opsin 1.2, c-opsin 1.3, and neuropsin being expressed at low amounts, while no expression is observed in c-opsin 1.1b. RGR opsin and peropsin were the highest expressed amongst the other tissues. The mixed tissue (green) and tube feet (purple) have little to no expression (TPM < 0.5) of c-opsin 1.2, c-opsin 1.3, go-opsin, and chaopsin
	Fig. 5. Three of four c-opsins found on same scaffold in decreasing order of expression. The boxes below the two panels represent â€œgbr_scaffold65â€ from the Great Barrier Reef assembly of the A. planci genome. Each box represents a gene and the size of the box correlates to the size of the gene. Three of the four Ap-c-opsins are located on the same scaffold all being transcripted 3â€² to 5â€²; Ap-c-opsin 1.1a (red), Ap-c-opsin 1.2 (orange) and Ap-c-opsin 1.3 (purple). Bottom panel: The log2 fold change of significantly differentially expressed genes (FDR < 0.05) comparing A. planci eyes the mixed tissue samples, with the three Ap-c-opsins highlighted. Top panel: Expression of the three Ap-c-opsins clustered on â€œgbr_scaffold65â€, the expression level correlates with the spatial ordering within the cluster (in the direction 3â€² to 5â€²), the most 3â€² having the highest expression and the most 5â€² having the lowest expression

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