TY - JOUR

T1 - Transcriptomic analysis of crustacean neuropeptide signaling during the moult cycle of the green shore crab, Carcinus maenas.

AU - Oliphant, Andrew

AU - Alexander, Jodi L

AU - Swain, Martin T

AU - Webster, Simon G

AU - Wilcockson, David C

PY - 2018/9/26

Y1 - 2018/9/26

N2 - AbstractBackground: Ecdysis is an innate behaviour programme by which all arthropods moult their exoskeletons. Thecomplex suite of interacting neuropeptides that orchestrate ecdysis is well studied in insects, but details of thecrustacean ecdysis cassette are fragmented and our understanding of this process is comparatively crude,preventing a meaningful evolutionary comparison. To begin to address this issue we identified transcripts codingfor neuropeptides and their putative receptors in the central nervous system (CNS) and Y-organs (YO) within thecrab, Carcinus maenas, and mapped their expression profiles across accurately defined stages of the moult cycleusing RNA-sequencing. We also studied gene expression within the epidermally-derived YO, the only defined rolefor which is the synthesis of ecdysteroid moulting hormones, to elucidate peptides and G protein-coupledreceptors (GPCRs) that might have a function in ecdysis.Results: Transcriptome mining of the CNS transcriptome yielded neuropeptide transcripts representing 47neuropeptide families and 66 putative GPCRs. Neuropeptide transcripts that were differentially expressed across themoult cycle included carcikinin, crustacean hyperglycemic hormone-2, and crustacean cardioactive peptide, whilst asingle putative neuropeptide receptor, proctolin R1, was differentially expressed. Carcikinin mRNA in particularexhibited dramatic increases in expression pre-moult, suggesting a role in ecdysis regulation. Crustaceanhyperglycemic hormone-2 mRNA expression was elevated post- and pre-moult whilst that for crustaceancardioactive peptide, which regulates insect ecdysis and plays a role in stereotyped motor activity duringcrustacean ecdysis, was elevated in pre-moult.In the YO, several putative neuropeptide receptor transcripts were differentially expressed across the moult cycle, aswas the mRNA for the neuropeptide, neuroparsin-1. Whilst differential gene expression of putative neuropeptidereceptors was expected, the discovery and differential expression of neuropeptide transcripts was surprising.Analysis of GPCR transcript expression between YO and epidermis revealed 11 to be upregulated in the YO andthus are now candidates for peptide control of ecdysis.Conclusions: The data presented represent a comprehensive survey of the deduced C. maenas neuropeptidomeand putative GPCRs. Importantly, we have described the differential expression profiles of these transcripts acrossaccurately staged moult cycles in tissues key to the ecdysis programme. This study provides important avenues forthe future exploration of functionality of receptor-ligand pairs in crustaceans.Keywords: Ecdysis, G protein-coupled receptor, Central nervous system, Y-organ

AB - AbstractBackground: Ecdysis is an innate behaviour programme by which all arthropods moult their exoskeletons. Thecomplex suite of interacting neuropeptides that orchestrate ecdysis is well studied in insects, but details of thecrustacean ecdysis cassette are fragmented and our understanding of this process is comparatively crude,preventing a meaningful evolutionary comparison. To begin to address this issue we identified transcripts codingfor neuropeptides and their putative receptors in the central nervous system (CNS) and Y-organs (YO) within thecrab, Carcinus maenas, and mapped their expression profiles across accurately defined stages of the moult cycleusing RNA-sequencing. We also studied gene expression within the epidermally-derived YO, the only defined rolefor which is the synthesis of ecdysteroid moulting hormones, to elucidate peptides and G protein-coupledreceptors (GPCRs) that might have a function in ecdysis.Results: Transcriptome mining of the CNS transcriptome yielded neuropeptide transcripts representing 47neuropeptide families and 66 putative GPCRs. Neuropeptide transcripts that were differentially expressed across themoult cycle included carcikinin, crustacean hyperglycemic hormone-2, and crustacean cardioactive peptide, whilst asingle putative neuropeptide receptor, proctolin R1, was differentially expressed. Carcikinin mRNA in particularexhibited dramatic increases in expression pre-moult, suggesting a role in ecdysis regulation. Crustaceanhyperglycemic hormone-2 mRNA expression was elevated post- and pre-moult whilst that for crustaceancardioactive peptide, which regulates insect ecdysis and plays a role in stereotyped motor activity duringcrustacean ecdysis, was elevated in pre-moult.In the YO, several putative neuropeptide receptor transcripts were differentially expressed across the moult cycle, aswas the mRNA for the neuropeptide, neuroparsin-1. Whilst differential gene expression of putative neuropeptidereceptors was expected, the discovery and differential expression of neuropeptide transcripts was surprising.Analysis of GPCR transcript expression between YO and epidermis revealed 11 to be upregulated in the YO andthus are now candidates for peptide control of ecdysis.Conclusions: The data presented represent a comprehensive survey of the deduced C. maenas neuropeptidomeand putative GPCRs. Importantly, we have described the differential expression profiles of these transcripts acrossaccurately staged moult cycles in tissues key to the ecdysis programme. This study provides important avenues forthe future exploration of functionality of receptor-ligand pairs in crustaceans.Keywords: Ecdysis, G protein-coupled receptor, Central nervous system, Y-organ

KW - Ecdysis, G protein-coupled receptor, Central nervous system, Y-organ

UR - https://static-content.springer.com/esm/art%3A10.1186%2Fs12864-018-5057-3/MediaObjects/12864_2018_5057_MOESM1_ESM.docx

U2 - 10.1186/s12864-018-5057-3

DO - 10.1186/s12864-018-5057-3

M3 - Article

C2 - 30257651

VL - 19

SP - 711

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 711

M1 - 19:711

ER -