Dataset Information

Whole-head recording of chemosensory activity in the marine annelid Platynereis dumerilii.

ABSTRACT: Chemical detection is key to various behaviours in both marine and terrestrial animals. Marine species, though highly diverse, have been underrepresented so far in studies on chemosensory systems, and our knowledge mostly concerns the detection of airborne cues. A broader comparative approach is therefore desirable. Marine annelid worms with their rich behavioural repertoire represent attractive models for chemosensation. Here, we study the marine worm Platynereis dumerilii to provide the first comprehensive investigation of head chemosensory organ physiology in an annelid. By combining microfluidics and calcium imaging, we record neuronal activity in the entire head of early juveniles upon chemical stimulation. We find that Platynereis uses four types of organs to detect stimuli such as alcohols, esters, amino acids and sugars. Antennae are the main chemosensory organs, compared to the more differentially responding nuchal organs or palps. We report chemically evoked activity in possible downstream brain regions including the mushroom bodies (MBs), which are anatomically and molecularly similar to insect MBs. We conclude that chemosensation is a major sensory modality for marine annelids and propose early Platynereis juveniles as a model to study annelid chemosensory systems.

SUBMITTER: Chartier TF

PROVIDER: S-EPMC6223215 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Whole-head recording of chemosensory activity in the marine annelid <i>Platynereis dumerilii</i>.

Chartier Thomas F TF Deschamps Joran J Dürichen Wiebke W Jékely Gáspár G Arendt Detlev D

Open biology 20181031 10

Chemical detection is key to various behaviours in both marine and terrestrial animals. Marine species, though highly diverse, have been underrepresented so far in studies on chemosensory systems, and our knowledge mostly concerns the detection of airborne cues. A broader comparative approach is therefore desirable. Marine annelid worms with their rich behavioural repertoire represent attractive models for chemosensation. Here, we study the marine worm <i>Platynereis dumerilii</i> to provide the ...[more]

PMID: 30381362

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Project description:Background:Wnt/β-catenin (or canonical) signalling pathway activity is necessary and used independently several times for specification of vegetal fate and endoderm, gut differentiation, maintenance of epithelium in adult intestine and the development of gut-derived organs in various vertebrate and non-vertebrate organisms. However, its conservation in later stages of digestive tract development still remains questionable due to the lack of detailed data, mainly from Spiralia. Results:Here we characterize the Pdu-Tcf gene, a Tcf/LEF orthologue and a component of Wnt/β-catenin pathway from Platynereis dumerilii, a spiralian, marine annelid worm. Pdu-Tcf undergoes extensive alternative splicing in the C-terminal region of the gene generating as many as eight mRNA isoforms some of which differ in the presence or absence of a C-clamp domain which suggests a distinct DNA binding activity of individual protein variants. Pdu-Tcf is broadly expressed throughout development which is indicative of many functions. One of the most prominent domains that exhibits rather strong Pdu-Tcf expression is in the putative precursors of endodermal gut cells which are detected after 72 h post-fertilization (hpf). At day 5 post-fertilization (dpf), Pdu-Tcf is expressed in the hindgut and pharynx (foregut), whereas at 7 dpf stage, it is strongly transcribed in the now-cellularized midgut for the first time. In order to gain insight into the role of Wnt/β-catenin signalling, we disrupted its activity using pharmacological inhibitors between day 5 and 7 of development. The inhibition of Wnt/β-catenin signalling led to the loss of midgut marker genes Subtilisin-1, Subtilisin-2, α-Amylase and Otx along with a drop in β-catenin protein levels, Axin expression in the gut and nearly the complete loss of proliferative activity throughout the body of larva. At the same time, a hindgut marker gene Legumain was expanded to the midgut compartment under the same conditions. Conclusions:Our findings suggest that high Wnt/β-catenin signalling in the midgut might be necessary for proper differentiation of the endoderm to an epithelium capable of secreting digestive enzymes. Together, our data provide evidence for the role of Wnt/β-catenin signalling in gut differentiation in Platynereis.

Project description:BackgroundRestorative regeneration, the capacity to reform a lost body part following amputation or injury, is an important and still poorly understood process in animals. Annelids, or segmented worms, show amazing regenerative capabilities, and as such are a crucial group to investigate. Elucidating the molecular mechanisms that underpin regeneration in this major group remains a key goal. Among annelids, the nereididae Platynereis dumerilii (re)emerged recently as a front-line regeneration model. Following amputation of its posterior part, Platynereis worms can regenerate both differentiated tissues of their terminal part as well as a growth zone that contains putative stem cells. While this regeneration process follows specific and reproducible stages that have been well characterized, the transcriptomic landscape of these stages remains to be uncovered.ResultsWe generated a high-quality de novo Reference transcriptome for the annelid Platynereis dumerilii. We produced and analyzed three RNA-sequencing datasets, encompassing five stages of posterior regeneration, along with blastema stages and non-amputated tissues as controls. We included two of these regeneration RNA-seq datasets, as well as embryonic and tissue-specific datasets from the literature to produce a Reference transcriptome. We used this Reference transcriptome to perform in depth analyzes of RNA-seq data during the course of regeneration to reveal the important dynamics of the gene expression, process with thousands of genes differentially expressed between stages, as well as unique and specific gene expression at each regeneration stage. The study of these genes highlighted the importance of the nervous system at both early and late stages of regeneration, as well as the enrichment of RNA-binding proteins (RBPs) during almost the entire regeneration process.ConclusionsIn this study, we provided a high-quality de novo Reference transcriptome for the annelid Platynereis that is useful for investigating various developmental processes, including regeneration. Our extensive stage-specific transcriptional analysis during the course of posterior regeneration sheds light upon major molecular mechanisms and pathways, and will foster many specific studies in the future.

Dataset Information

Whole-head recording of chemosensory activity in the marine annelid Platynereis dumerilii.

Publications

Whole-head recording of chemosensory activity in the marine annelid <i>Platynereis dumerilii</i>.

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