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. 2019 Feb 27;286(1897):20182929.
doi: 10.1098/rspb.2018.2929.

Genomic Signatures of G-protein-coupled Receptor Expansions Reveal Functional Transitions in the Evolution of Cephalopod Signal Transduction

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Free PMC article

Genomic Signatures of G-protein-coupled Receptor Expansions Reveal Functional Transitions in the Evolution of Cephalopod Signal Transduction

Elena A Ritschard et al. Proc Biol Sci. .
Free PMC article

Abstract

Coleoid cephalopods show unique morphological and neural novelties, such as arms with tactile and chemosensory suckers and a large complex nervous system. The evolution of such cephalopod novelties has been attributed at a genomic level to independent gene family expansions, yet the exact association and the evolutionary timing remain unclear. In the octopus genome, one such expansion occurred in the G-protein-coupled receptors (GPCRs) repertoire, a superfamily of proteins that mediate signal transduction. Here, we assessed the evolutionary history of this expansion and its relationship with cephalopod novelties. Using phylogenetic analyses, at least two cephalopod- and two octopus-specific GPCR expansions were identified. Signatures of positive selection were analysed within the four groups, and the locations of these sequences in the Octopus bimaculoides genome were inspected. Additionally, the expression profiles of cephalopod GPCRs across various tissues were extracted from available transcriptomic data. Our results reveal the evolutionary history of cephalopod GPCRs. Unexpanded cephalopod GPCRs shared with other bilaterians were found to be mainly nervous tissue specific. By contrast, duplications that are shared between octopus and the bobtail squid or specific to the octopus' lineage generated copies with divergent expression patterns devoted to tissues outside of the brain. The acquisition of novel expression domains was accompanied by gene order rearrangement through either translocation or duplication and gene loss. Lastly, expansions showed signs of positive selection and some were found to form tandem clusters with shared conserved expression profiles in cephalopod innovations such as the axial nerve cord. Altogether, our results contribute to the understanding of the molecular and evolutionary history of signal transduction and provide insights into the role of this expansion during the emergence of cephalopod novelties and/or adaptations.

Keywords: G-protein-coupled receptors; cephalopod evolution; gene duplication; gene family expansion; signal transduction.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Phylogenetic trees for class A and B. Each colour corresponds to a species; abbreviations as follow. ANOGA: Anopheles gambiae, BRAFL: Branchiostoma floridae, CAEEL: Caenorhabditis elegans, CAPTE: Capitella teleta, CRAGI: Crassostrea gigas, DROME: Drosophila melanogaster, ESCOL: Euprymna scolopes, HELRO: Helobdella robusta, HUMAN, LOTGI: Lottia gigantea, MIZYE: Mizuhopecten yessoensis, OCMIN: Callistoctopus minor, OCTBM: Octopus bimaculoides, SACKO: Saccoglossus kowalevskii, SCHMA: Schistosoma mansoni, STRPU: Strongylocentrotus purpuratus. Zoom-ins show the expanded groups identified (1–4). Thicker branches represent significant S–H support (greater than 0.7). Bar length indicates 0.5 substitutions per site corresponding to approximately 250 Myr. Tree visualization was performed with the ggtree package [51] using R v3.4.2 [52]. (Online version in colour.)
Figure 2.
Figure 2.
Heatmap of all E. scolopes, O. bimaculoides, and C. minor GPCRs. Genes (rows) are clustered following the trees resulting from the phylogenetic analyses performed for each class (af) independently. Clades highlighted in grey represent the four groups depicted in figure 1, group number is given to the right of the C. minor heatmap. Dotted lines connect corresponding expanded groups in both species. Tissues (columns) with transcriptomic data for E. scolopes: haemocytes, accessory nidamental gland, light organ (LO), gills, eyes, brain, and skin. Tissues (columns) with transcriptomic data for O. bimaculoides: sucker, testes, stage 15 (St15) embryo, ova, skin, posterior salivary gland (Psg), viscera (heart, kidney, and hepatopancreas), subesophageal brain (sub), supraesophageal brain (supra), optic lobe (OL), axial nerve cord (Anc), and retina. Tissues (columns) with transcriptomic data for C. minor: liver, kidney, stomach, caecum intestine (Cec_int), posterior salivary gland (Psg), buccal mass (Bucc_mass), bronchial heart (BH), systemic heart (heart), suckers, arms, skin, gills, siphon, brain, eye, spermatophore sac (Sp_sac), testes, and ovary. Heatmap generated with the heatmap.2 function (gplots v3.0.1 package [53]) using R v3.4.2 [52]. (Online version in colour.)
Figure 3.
Figure 3.
Expression profiles, positive selection results, and gene localization of cephalopod-specific expansions (groups 1 and 2) and octopus-specific expansions (groups 3 and 4) for O. bimaculoides. Genes (rows) in heatmaps are clustered following the trees resulting from the phylogenetic analyses. Spaces between rows indicate the presence of other sequences of cephalopod species as determined in the phylogenetic analyses. Black stars represent positive selection (ω > 1). The scaffold with the most co-localized genes per group is represented below the heatmaps (see detailed information in the electronic supplementary material, table S2). Exon–intron composition of the genes is depicted as thick bars (exons) and grey lines connecting them (introns). Direction of transcription is shown with an arrow. Asterisks (*) represent other genes (no GPCRs) found in the surrounding space of the co-localized GPCRs.
Figure 4.
Figure 4.
Expression proportions of E. scolopes, O. bimaculoides, and C. minor genes in each tissue in non-expanded GPCRs, cephalopod-specific expansions, and octopus-specific expansions. Tissue colouration gradient follows the mean values of gene expression proportion as shown in electronic supplementary material, figures S5–S7. Warmer colours represent the highest proportion of gene expression. E. scolopes (illustration designed by Hannah Schmidbaur) tissues: accessory nidamental gland (ANG), light organ (LO), gills, eyes, brain, and skin. O. bimaculoides tissues: sucker, testes, stage 15 (St15) embryo, ovary, skin, posterior salivary gland (Psg), viscera (heart, kidney, and hepatopancreas), subesophageal brain (sub), supraesophageal brain (supra), optic lobe (OL), axial nerve cord (Anc), and retina. C. minor tissues: liver, kidney, stomach, caecum intestine (CI), posterior salivary gland (Psg), buccal mass (BM), bronchial heart (BH), systemic heart (heart), suckers, arms, skin, gills, siphon, brain, eye, spermatophore sac (Sp sac), testes, and ovary. (Online version in colour.)

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