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Sci Rep
2020 Feb 25;101:3348. doi: 10.1038/s41598-020-60167-3.
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Holothurians have a reduced GPCR and odorant receptor-like repertoire compared to other echinoderms.
Marquet N, Cardoso JCR, Louro B, Fernandes SA, Silva SC, Canário AVM.
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Sea cucumbers lack vision and rely on chemical sensing to reproduce and survive. However, how they recognize and respond to environmental cues remains unknown. Possible candidates are the odorant receptors (ORs), a diverse family of G protein-coupled receptors (GPCRs) involved in olfaction. The present study aimed at characterizing the chemosensory GPCRs in sea cucumbers. At least 246 distinct GPCRs, of which ca. 20% putative ORs, were found in a transcriptome assembly of putative chemosensory (tentacles, oral cavity, calcareous ring, and papillae/tegument) and reproductive (ovary and testis) tissues from Holothuria arguinensis (57 ORs) and in the Apostichopus japonicus genome (79 ORs). The sea cucumber ORs clustered with those of sea urchin and starfish into four main clades of gene expansions sharing a common ancestor and evolving under purifying selection. However, the sea cucumber ORs repertoire was the smallest among the echinoderms and the olfactory receptor signature motif LxxPxYxxxxxLxxxDxxxxxxxxP was better conserved in cluster OR-l1 which also had more members. ORs were expressed in tentacles, oral cavity, calcareous ring, and papillae/tegument, supporting their potential role in chemosensing. This study is the first comprehensive survey of chemosensory GPCRs in sea cucumbers, and provides the molecular basis to understand how they communicate.
Figure 1. Phylogeny of the sea cucumber OR-like candidates (H. arguinensis, 78 sequences and A. japonicus, 112 sequences) selected by the HMM analysis with OR-like/olfactory and non-olfactory rhodopsins from other echinoderms (A. planci, starfish and S. purpuratus, sea urchin), cnidaria (N. vectensis, sea anemone) and ORs from cephalochordates (B. floridae, amphioxus) and aquatic vertebrates (O. latipes, teleost fish). The ML tree was rooted with the chordates (amphioxus and teleost fish) cluster. The different OR-like/olfactory clusters are highlighted by a coloured line, corresponding to the respective group, around the tree. The four echinoderm OR-like clades are shaded in grey and numbered according to the cluster name: 1 is OR-l1, 2 is OR-l2, 3 is OR-l3 and 4 is OR-l4. The sea cucumber specific gene expansions are designated as SC-1, SC-2, SC-3 and SC-4. Branch support was represented only when at least one of the three methods used (aLRT-Chi2, aBayes and SH-LRT) had statistically significant supporting values. Tree branch symbol: full circle: three methods were significant; circle with a dot: two methods were significant and empty circle: one method was significant. SC: sea cucumber.
Figure 2. Number and percentage of GPCRs, including the percentage of OR-like within the Rhodopsin family, in different species: N. vectensis28,47, A. japonicus and H. arguinensis (present manuscript), S. purpuratus33,47 (ORs: surreal-GPCRs; groups A-F), A. planci34 (ORs: groups A-K), H. sapiens47,48, D. rerio30,48, T. rubripes30,48 and B. floridae29,86. The cladogram corresponds to a species tree that was built using the ML method with concatenated sequence of four ORs per species. The values of the bootstrap are seen at the nodes of the trees. This species tree is in agreement with the generic tree defined in the Tree of Life93 (http://tolweb.org). The percentage of OR-like Rhodopsin found within the Rhodopsin family is represented in light blue.
Figure 3. Mapping of the OR-like gene candidates in A. japonicus genome. Only scaffolds containing at least two OR-like genes are represented. Horizontal lines represent the genome fragments and each vertical coloured line represents an exon. There are putative sea cucumber OR-like genes with two exons. Gene orientation is denoted by colour: genes in the sense strand are represented in green and genes in the antisense strand are represented in red. The bar on top indicates the absolute distance in kilo base pairs (kbp).
Figure 4. Weblogo obtained from the alignment of the motif LxxPxYxxxxxLxxxDxxxxxxxxP. A consensus echinoderm weblogo resulting from the alignment of all sequences identified per echinoderm cluster is represented with the yellow background. The height of each symbol indicates the relative frequency of each amino acid at that position.
Figure 5. Venn diagrams showing the distribution of the OR-like candidates from each cluster (a: OR-l1, b: OR-l2, c: OR-l3, d: OR-l4) among tissues. OC: oral cavity, P + T: papillae/tegument, CR: calcareous ring, Tt: tentacles, O: ovary). N = number of OR-like receptors found in each clade.
Figure 6. Expression of 20 H. arguinensis OR-like gene candidates from the four echinoderm OR-like groups analysed by qPCR in (a) tentacles, (b) papillae/tegument, (c) oral cavity. Data are presented as the mean ± SEM (n = 3 biological replicates). Notice the difference in scale in the ordinates.
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