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BMC Genomics
2017 May 23;181:400. doi: 10.1186/s12864-017-3793-4.
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Identification of putative olfactory G-protein coupled receptors in Crown-of-Thorns starfish, Acanthaster planci.
Roberts RE
,
Motti CA
,
Baughman KW
,
Satoh N
,
Hall MR
,
Cummins SF
.
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BACKGROUND: In marine organisms, and in particular for benthic invertebrates including echinoderms, olfaction is a dominant sense with chemosensation being a critical signalling process. Until recently natural product chemistry was the primary investigative approach to elucidate the nature of chemical signals but advances in genomics and transcriptomics over the last decade have facilitated breakthroughs in understanding not only the chemistry but also the molecular mechanisms underpinning chemosensation in aquatic environments. Integration of these approaches has the potential to reveal the fundamental elements influencing community structure of benthic ecosystems as chemical signalling modulates intra- and inter-species interactions. Such knowledge also offers avenues for potential development of novel biological control methods for pest species such as the predatory Crown-of-Thorns starfish (COTS), Acanthaster planci which are the primary biological cause of coral cover loss in the Indo-Pacific.
RESULTS: In this study, we have analysed the COTS sensory organs through histological and electron microscopy. We then investigated key elements of the COTS molecular olfactory toolkit, the putative olfactory rhodopsin-like G protein-protein receptors (GPCRs) within its genome and olfactory organ transcriptomes. Many of the identified Acanthaster planci olfactory receptors (ApORs) genes were found to cluster within the COTS genome, indicating rapid evolution and replication from an ancestral olfactory GPCR sequence. Tube feet and terminal sensory tentacles contain the highest proportion of ApORs. In situ hybridisation confirmed the presence of four ApORs, ApOR15, 18, 25 and 43 within COTS sensory organs, however expression of these genes was not specific to the adhesive epidermis, but also within the nerve plexus of tube feet stems and within the myomesothelium. G alpha subunit proteins were also identified in the sensory organs, and we report the spatial localisation of Gαi within the tube foot and sensory tentacle.
CONCLUSIONS: We have identified putative COTS olfactory receptors that localise to sensory organs. These results provide a basis for future studies that may enable the development of a biological control not only for COTS, but also other native pest or invasive starfish.
Fig. 1. Heat map showing relative tissue distribution of candidate olfactory GPCRs. Candidate olfactory GPCRs used for subsequent in situ hybridisation are indicated
Fig. 2. Characterisation of candidate olfactory GPCRs within COTS genome scaffold 10. a 12 genes (A-L, including ApOR2, 3 and 4) encoding 7TM proteins are clustered and found in both transcriptional orientations. b Comparative multiple sequence alignment of scaffold 10 olfactory GPCRs. Green bars indicate extracellular loops (OUT), blue bars indicate intracellular loops (IN) and red bars indicated TM domain regions
Fig. 3. Phylogenetic analysis of putative ApOR sequences, sea urchin surreal-GPCRs, and ORs and CRs from several other vertebrate and invertebrate species. ApORs are indicated by dark blue lines, surreal-GPCRs are indicated by light blue, C. elegans CRs are indicated by purple, A. californica CRs are indicated by green, and H. sapiens and M. musculus ORs are indicated by red. ApORs which cluster in the COTS genome are indicated by coloured asterisks, with each different colour representing a different genomic cluster. ApORs used for in situ hybridisation are indicated by black arrows. Scale bar represents number of amino acid substitutions per site
Fig. 5. In situ hybridisation of COTS tube feet and sensory tentacles using digoxigenin-labelled antisense RNA probes to show spatial expression of candidate olfactory receptors, ApOR 15, 18, 25, 43, and positive control actin. AE, adhesive epidermis; NE, Non-adhesive epidermis; CL, connective tissue radial laminae; CT, connective tissue layer; D, disc; S, stem; L, water-vascular lumen; M, myomesothelium; NP, nerve plexus; C, cuticle; E, epidermis. Scale bars = 200 μm
Fig. 6. Phylogenetic tree of G alpha subunit proteins from COTS and various species. Main families of G alpha proteins are indicated by coloured lines: Gα12/13 indicated by purple lines, Gαi/o/t/z by green, Gαs/olf by red and Gαq/11/14/15 by light blue. Grey lines indicate sequences which do not cluster into these main families. Scale bar represents number of amino acid substitutions per site
Fig. 7.
a Western blot showing staining of a protein band at approximately 40 kDa (arrow) in tube feet extracts using anti-Gαi. b Immunofluoresence (green) staining of Gαi protein in COTS tube foot tissue section. Blue represents DAPI nuclear fluorescence. c A higher-resolution micrograph of the area boxed in (b). d Negative control showing only nuclear staining. e Immunofluoresence (green) staining of Gαi protein in COTS sensory tentacles. f A higher-resolution micrograph of the area boxed in (e). g Negative control showing only nuclear staining. AE, adhesive epidermis; NE, Non-adhesive epidermis; CT, connective tissue layer; M, myomesothelium; NP, nerve plexus; C, cuticle. Scale bars = 200 μm
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