Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling

Yáñez-Guerra, Luis Alfonso; Zhong, Xingxing; Moghul, Ismail; Butts, Thomas; Zampronio, Cleidiane G.; Jones, Alexandra M. E.; Mirabeau, Olivier; Elphick, Maurice R.

doi:10.7554/elife.57640

Cited by 32 publications

(39 citation statements)

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“…The classification of U. unicinctus neuropeptides is mainly based on the researches of Jékely [ 28 ] and Conzelmann [ 30 ], and we have also updated the classification status of LFRYamide [ 72 , 73 ], Cerebrin [ 28 , 63 , 74 , 75 ] and RGWamide [ 30 , 44 , 45 , 62 – 64 , 76 , 77 ] according to recent studies.…”

Section: Methodsmentioning

confidence: 99%

Identification of the neuropeptide precursor genes potentially involved in the larval settlement in the Echiuran worm Urechis unicinctus

et al. 2020

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Background In marine invertebrate life cycles, which often consist of planktonic larval and benthonic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory–neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not fully understood yet. Results In this study, a total of 54 neuropeptide precursors (pNPs) were identified in the Urechis unicinctus larva and adult transcriptome databases using local BLAST and NpSearch prediction, of which 10 pNPs belonging to the ancient eumetazoa, 24 pNPs belonging to the ancient bilaterian, 3 pNPs belonging to the ancient protostome, 9 pNPs exclusive in lophotrochozoa, 3 pNPs exclusive in annelid, and 5 pNPs only found in U. unicinctus. Furthermore, four pNPs (MIP, FRWamide, FxFamide and FILamide) which may be associated with the settlement and metamorphosis of U. unicinctus larvae were analysed by qRT-PCR. Whole-mount in situ hybridization results showed that all the four pNPs were expressed in the region of the apical organ of the larva, and the positive signals were also detected in the ciliary band and abdomen chaetae. We speculated that these pNPs may regulate the movement of larval cilia and chaeta by sensing external attachment signals. Conclusions This study represents the first comprehensive identification of neuropeptides in Echiura, and would contribute to a complete understanding on the roles of various neuropeptides in larval settlement of most marine benthonic invertebrates.

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Section: Methodsmentioning

confidence: 99%

Identification of the neuropeptide precursor genes potentially involved in the larval settlement in the Echiuran worm Urechis unicinctus

et al. 2020

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show abstract

“…The classi cation of U. unicinctus neuropeptides is mainly based on the researches of Jékely [28] and Conzelmann [29], and we have also updated the classi cation status of LFRYamide [72,73], Cerebrin [28,63,74,75] and RGWamide [29, 43, 44, 62-64, 76, 77] according to recent studies.…”

Section: Identification Classi Cation and Sequence Alignment Of Neurmentioning

confidence: 99%

Identification of the Neuropeptide Precursor Genes Potentially Involved in the Larval Settlement in the Echiuran Worm Urechis unicinctus

Hou

Qin

Wei

et al. 2020

Preprint

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Background: In marine invertebrate life cycles, which often consist of planktonic larval and benthonic adult stages, settlement of the free-swimming larva to the sea ﬂoor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory–neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not fully understood yet.Results: In this study, a total of 54 neuropeptide precursors (pNPs) were identified in the Urechis unicinctus larva and adult transcriptome databases using local BLAST and NpSearch prediction, of which 10 pNPs belonging to the ancient eumetazoa, 24 pNPs belonging to the ancient bilaterian, 3 pNPs belonging to the ancient protostome, 9 pNPs exclusive in lophotrochozoa, 3 pNPs exclusive in annelid, and 5 pNPs only found in U. unicinctus. Furthermore, four pNPs (MIP, FRWamide, FxFamide and FILamide) which may be associated with the settlement and metamorphosis of U. unicinctus larvae were analysed by qRT-PCR. Whole-mount in situ hybridization results showed that all the four pNPs were expressed in the region of the apical organ of the larva, and the positive signals were also detected in the ciliary band and abdomen chaetae. We speculated that these pNPs may regulate the movement of larval cilia and chaeta by sensing external attachment signals.Conclusions: This study represents the ﬁrst comprehensive identiﬁcation of neuropeptides in Echiura, and would contribute to a complete understanding on the roles of various neuropeptides in larval settlement of most marine benthonic invertebrates.

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“…The longer (several hundred amino acids) and more conserved sequence of GPCRs make phylogenetic analyses feasible when reconstructing the evolution of peptidergic systems (Jekely, 2013; Mirabeau and Joly, 2013). Another useful approach is to compare the exon-intron structure of pNPs (Mair et al , 2000; Yañez-Guerra et al , 2020; Zhang et al , 2020). In several cases, the overall organisation of orthologous pNP genes can be conserved (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…a region coding for the signal peptide followed by a single peptide and a C-terminal Cys-containing domain) (Semmens et al , 2015; Liutkeviciute et al , 2016). Furthermore, an increased sampling across taxa has often helped to clarify relationships, revealing hidden orthologs or lineage specific losses, gains and divergences (Jekely, 2013; Mirabeau and Joly, 2013; Semmens et al , 2016; Martín-Durán et al., 2017; Thiel et al , 2018; Yañez-Guerra et al , 2020). Some lineages can retain signalling systems that had been lost in related species.…”

Section: Introductionmentioning

confidence: 99%

“…For example, corazonin, luqin and short neuropeptide F are widespread neuropeptides in protostomes but not detectable in vertebrates. These pNPs and their receptors are, however, present in ambulacrarians like the hemichordate Saccoglossus kovalevski or the starfish Asterias rubens , indicating that they represent ancestral bilaterian signaling systems (Tian et al , 2016; Yañez-Guerra et al , 2018, 2020; Yañez-Guerra and Elphick, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Nemertean, brachiopod and phoronid neuropeptidomics reveals ancestral spiralian signalling systems

Thiel

Yáñez-Guerra

Franz‐Wachtel

et al. 2021

Preprint

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Neuropeptides are diverse signalling molecules in animals commonly acting through G-protein coupled receptors (GPCRs). Neuropeptides and their receptors underwent extensive diversification in bilaterians and the relationships of many peptide-receptor systems have been clarified. However, we lack a detailed picture of neuropeptide evolution in lophotrochozoans as in-depth studies only exist for molluscs and annelids. Here we analyse peptidergic systems in Nemertea, Brachiopoda and Phoronida. We screened transcriptomes from thirteen nemertean, six brachiopod and four phoronid species for proneuropeptides and neuropeptide GPCRs. With mass spectrometry from the nemertean Lineus longissimus, we validated several predicted peptides and identified novel ones. Molecular phylogeny combined with peptide-sequence and gene-structure comparisons allowed us to comprehensively map spiralian neuropeptide evolution. We found most mollusc and annelid peptidergic systems also in nemerteans, brachiopods and phoronids. We uncovered previously hidden relationships including the orthologies of spiralian CCWamides to arthropod agatoxin-like peptides and of mollusc APGWamides to RGWamides from annelids, with orthologues systems in nemerteans, brachiopods and phoronids. We found that pleurin neuropeptides previously only found in molluscs are also present in nemerteans and brachiopods. We also identified cases of gene family duplications and losses. These include a protostome-specific expansion of RFamide/Wamide signalling, a spiralian expansion of GnRH-related peptides, and duplications of vasopressin/oxytocin before the divergence of brachiopods, phoronids and nemerteans. This analysis expands our knowledge of peptidergic signalling in spiralians and protostomes. Our annotated dataset of nearly 1,300 proneuropeptide sequences and 600 GPCRs presents a useful resource for further studies of neuropeptide signalling in protostomes.

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Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling

Cited by 32 publications

References 80 publications

Identification of the neuropeptide precursor genes potentially involved in the larval settlement in the Echiuran worm Urechis unicinctus

Identification of the neuropeptide precursor genes potentially involved in the larval settlement in the Echiuran worm Urechis unicinctus

Identification of the Neuropeptide Precursor Genes Potentially Involved in the Larval Settlement in the Echiuran Worm Urechis unicinctus

Nemertean, brachiopod and phoronid neuropeptidomics reveals ancestral spiralian signalling systems

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