Molecular analysis of two FMRFamide‐encoding transcripts expressed during the development of the tropical abalone <i>haliotis asinina</i>

Cummins, Scott F.; Tollenaere, Alina; Degnan, Bernard M.; Croll, Roger P.

doi:10.1002/cne.22621

Cited by 22 publications

(30 citation statements)

References 66 publications

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“…As for other H. asinina neuropeptides, namely Has-SLP, Has-MIP, Has-HGAP [44] and Has-FMRFamide [45], we demonstrate here that prohormones encoded by Has-Myomodulin, Has-APGWamide and Has-Whitnin are processed to yield a repertoire of small neuropeptides. The Has-Myomodulin gene encodes 7 copies of the highly conserved PMNMLRLamide, compared to 9 to 10 copies of the corresponding myomodulin in other characterised gastropods [34,38,39].…”

Section: Discussionsupporting

confidence: 70%

Marked changes in neuropeptide expression accompany broadcast spawnings in the gastropod Haliotis asinina

et al. 2012

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IntroductionA huge diversity of marine species reproduce by synchronously spawning their gametes into the water column. Although this species-specific event typically occurs in a particular season, the precise time and day of spawning often can not be predicted. There is little understanding of how the environment (e.g. water temperature, day length, tidal and lunar cycle) regulates a population’s reproductive physiology to synchronise a spawning event. The Indo-Pacific tropical abalone, Haliotis asinina, has a highly predictable spawning cycle, where individuals release gametes on the evenings of spring high tides on new and full moons during the warmer half of the year. These calculable spawning events uniquely allow for the analysis of the molecular and cellular processes underlying reproduction. Here we characterise neuropeptides produced in H. asinina ganglia that are known in egg-laying molluscs to control vital aspects of reproduction.ResultsWe demonstrate that genes encoding APGWamide, myomodulin, the putative proctolin homologue whitnin, FMRFamide, a schistosomin-like peptide (SLP), a molluscan insulin-related peptide (MIP) and a haliotid growth-associated peptide (HGAP) all are differentially expressed in the anterior ganglia during the two week spawning cycle in both male and female abalone. Each gene has a unique and sex-specific expression profile. Despite these differences, expression levels in most of the genes peak at or within 12 h of the spawning event. In contrast, lowest levels of transcript abundance typically occurs 36 h before and 24 h after spawning, with differences in peak and low expression levels being most pronounced in genes orthologous to known molluscan reproduction neuromodulators.ConclusionsExploiting the predictable semi-lunar spawning cycle of the gastropod H. asinina, we have identified a suite of evolutionarily-conserved, mollusc-specific and rapidly-evolving neuropeptides that appear to contribute to the regulation of spawning. Dramatic increases and decreases in ganglionic neuropeptide expression levels from 36 h before to 24 h after the broadcast spawning event are consistent with these peptides having a regulatory role in translating environmental signals experienced by a population into a synchronous physiological output, in this case, the release of gametes.

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Section: Discussionsupporting

confidence: 70%

Marked changes in neuropeptide expression accompany broadcast spawnings in the gastropod Haliotis asinina

et al. 2012

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“…Sense and antisense digoxigenin (DIG)-labelled riboprobes were prepared using a DIG RNA labelling mix kit (Roche) as per protocol [39], using SP6 and T7 polymerase (SP6 5’-TAATACGACTCACTATAGGG -3', T7 5'-ATTTAGGTGACACTATAG3'). COTS tube foot and sensory tentacles were fixed in 4% paraformaldehyde overnight at 4°C, then placed in 30% sucrose in PBS overnight before being embedded in OCT compound and frozen at -80°C.…”

Section: Methodsmentioning

confidence: 99%

“…Hybridisation was performed using the same solution with 200 ng/ml DIG-labelled riboprobe added and incubated overnight at 42°C. Washing, detection and mounting for viewing was performed as described by Cummins et al [39]. Sections were viewed under a confocal laser-scanning microscope (Nikon).…”

Section: Methodsmentioning

confidence: 99%

Identification of putative olfactory G-protein coupled receptors in Crown-of-Thorns starfish, Acanthaster planci

et al. 2017

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BackgroundIn 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.ResultsIn 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.ConclusionsWe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3793-4) contains supplementary material, which is available to authorized users.

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“…In T. diomedea , a role for SCP in regulation of larval feeding behavior was proposed (Kempf et al, 1987), whilst in H. rufescens a correlation between expression of SCP and initiation of metamorphosis suggested that SCP-immunoreactive neurons may participate in perception of external metamorphic cues (Barlow and Truman, 1992). Analysis of neuropeptide precursor transcript sequence data has revealed that in H. rufescens FMRFamide-related peptides are encoded by two transcripts that appear to be splice variants of a single gene and the two transcript types are expressed in partially overlapping populations of neurons in the larval nervous system (Cummins et al, 2011). The apical organ of many mollusc trochophores is characterized by strong FMRFamide immunoreactivity (ir) (Croll and Voronezhskaya, 1996; Dickinson et al, 1999, 2000; Voronezhskaya et al, 2008) and in larvae of the gastropod Ilyanassa obsolete FMRFamide causes muscular contractions and arrest of ciliary beating (Dickinson and Croll, 2003; Braubach et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens

et al. 2016

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Neuropeptides are an ancient class of neuronal signaling molecules that regulate a variety of physiological and behavioral processes in animals. The life cycle of many animals includes a larval stage(s) that precedes metamorphic transition to a reproductively active adult stage but, with the exception of Drosophila melanogaster and other insects, research on neuropeptide signaling has hitherto largely focused on adult animals. However, recent advances in genome/transcriptome sequencing have facilitated investigation of neuropeptide expression/function in the larvae of protostomian (e.g., the annelid Platynereis dumerilii) and deuterostomian (e.g., the urochordate Ciona intestinalis) invertebrates. Accordingly, here we report the first multi-gene investigation of larval neuropeptide precursor expression in a species belonging to the phylum Echinodermata—the starfish Asterias rubens. Whole-mount mRNA in situ hybridization was used to visualize in bipinnaria and brachiolaria stage larvae the expression of eight neuropeptide precursors: L-type SALMFamide (S1), F-type SALMFamide (S2), vasopressin/oxytocin-type, NGFFYamide, thyrotropin-releasing hormone-type, gonadotropin-releasing hormone-type, calcitonin-type and corticotropin-releasing hormone-type. Expression of only three of the precursors (S1, S2, NGFFYamide) was observed in bipinnaria larvae but by the brachiolaria stage expression of all eight precursors was detected. An evolutionarily conserved feature of larval nervous systems is the apical organ and in starfish larvae this comprises the bilaterally symmetrical lateral ganglia, but only the S1 and S2 precursors were found to be expressed in these ganglia. A prominent feature of brachiolaria larvae is the attachment complex, comprising the brachia and adhesive disk, which mediates larval attachment to a substratum prior to metamorphosis. Interestingly, all of the neuropeptide precursors examined here are expressed in the attachment complex, with distinctive patterns of expression suggesting potential roles for neuropeptides in the attachment process. Lastly, expression of several neuropeptide precursors is associated with ciliary bands, suggesting potential roles for the neuropeptides derived from these precursors in control of larval locomotion and/or feeding. In conclusion, our findings provide novel perspectives on the evolution and development of neuropeptide signaling systems and neuroanatomical insights into neuropeptide function in echinoderm larvae.

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Molecular analysis of two FMRFamide‐encoding transcripts expressed during the development of the tropical abalone haliotis asinina

Cited by 22 publications

References 66 publications

Marked changes in neuropeptide expression accompany broadcast spawnings in the gastropod Haliotis asinina

Marked changes in neuropeptide expression accompany broadcast spawnings in the gastropod Haliotis asinina

Identification of putative olfactory G-protein coupled receptors in Crown-of-Thorns starfish, Acanthaster planci

Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens

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