[en] Neuropeptides are one of the largest and most diverse families of signaling molecules in animals and, accordingly, they regulate many physiological processes and behaviors. Genome and transcriptome sequencing has enabled the identification of genes encoding neuropeptide precursor proteins in species from a growing variety of taxa, including bilaterian and non-bilaterian animals. Of particular interest are deuterostome invertebrates such as the phylum Echinodermata, which occupies a phylogenetic position that has facilitated reconstruction of the evolution of neuropeptide signaling systems in Bilateria. However, our knowledge of neuropeptide signaling in echinoderms is largely based on bioinformatic and experimental analysis of eleutherozoans-Asterozoa (starfish and brittle stars) and Echinozoa (sea urchins and sea cucumbers). Little is known about neuropeptide signaling in crinoids (feather stars and sea lilies), which are a sister clade to the Eleutherozoa. Therefore, we have analyzed transcriptome/genome sequence data from three feather star species, Anneissia japonica, Antedon mediterranea, and Florometra serratissima, to produce the first comprehensive identification of neuropeptide precursors in crinoids. These include representatives of bilaterian neuropeptide precursor families and several predicted crinoid neuropeptide precursors. Using A. mediterranea as an experimental model, we have investigated the expression of selected neuropeptides in larvae (doliolaria), post-metamorphic pentacrinoids and adults, providing new insights into the cellular architecture of crinoid nervous systems. Thus, using mRNA in situ hybridization F-type SALMFamide precursor transcripts were revealed in a previously undescribed population of peptidergic cells located dorso-laterally in doliolaria. Furthermore, using immunohistochemistry a calcitonin-type neuropeptide was revealed in the aboral nerve center, circumoral nerve ring and oral tube feet in pentacrinoids and in the ectoneural and entoneural compartments of the nervous system in adults. Moreover, functional analysis of a vasopressin/oxytocin-type neuropeptide (crinotocin), which is expressed in the brachial nerve of the arms in A. mediterranea, revealed that this peptide causes a dose-dependent change in the mechanical behavior of arm preparations in vitro-the first reported biological action of a neuropeptide in a crinoid. In conclusion, our findings provide new perspectives on neuropeptide signaling in echinoderms and the foundations for further exploration of neuropeptide expression/function in crinoids as a sister clade to eleutherozoan echinoderms.
Disciplines :
Zoology
Author, co-author :
Aleotti, Alessandra ; Department of Environmental Science and Policy, University of Milan, Milan, Italy ; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Wilkie, Iain C; Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom
Yañez-Guerra, Luis A; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Gattoni, Giacomo; Department of Environmental Science and Policy, University of Milan, Milan, Italy ; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Rahman, Tahshin A; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Wademan, Richard F; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Ahmad, Zakaryya; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Ivanova, Deyana A; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Semmens, Dean C; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Delroisse, Jérôme ; Université de Mons - UMONS > Faculté des Science > Service de Biologie des Organismes Marins et Biomimétism
Cai, Weigang; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Odekunle, Esther; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Egertová, Michaela; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
Ferrario, Cinzia; Department of Environmental Science and Policy, University of Milan, Milan, Italy
Sugni, Michela; Department of Environmental Science and Policy, University of Milan, Milan, Italy
Bonasoro, Francesco; Department of Environmental Science and Policy, University of Milan, Milan, Italy
Elphick, Maurice R; School of Biological & Behavioural Sciences, Queen Mary University of London, London, United Kingdom
S864 - Biologie des Organismes Marins et Biomimétisme
Research institute :
Research Institute for Biosciences
Funders :
Biotechnology and Biological Sciences Research Council Leverhulme Trust
Funding text :
This research was supported by a Leverhulme Trust Emeritus Fellowship (EM-2016-018) awarded to IW, a BBSRC grant (BB/M001644/1) awarded to MRE, and Erasmus Scholarships awarded to AA (Erasmus+ 2015/16 and Erasmus+ 2016/17).
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