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The development of early pioneer neurons in the annelid Malacoceros fuliginosus

BACKGROUND: Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is in...

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Autores principales: Kumar, Suman, Tumu, Sharat Chandra, Helm, Conrad, Hausen, Harald
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7489019/
https://www.ncbi.nlm.nih.gov/pubmed/32928118
http://dx.doi.org/10.1186/s12862-020-01680-x
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author Kumar, Suman
Tumu, Sharat Chandra
Helm, Conrad
Hausen, Harald
author_facet Kumar, Suman
Tumu, Sharat Chandra
Helm, Conrad
Hausen, Harald
author_sort Kumar, Suman
collection PubMed
description BACKGROUND: Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus. RESULTS: We performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 h postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d(221)), which after 7 cleavages starts expressing Neurogenin, Acheate-Scute and NeuroD. CONCLUSIONS: We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. We suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems.
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spelling pubmed-74890192020-09-16 The development of early pioneer neurons in the annelid Malacoceros fuliginosus Kumar, Suman Tumu, Sharat Chandra Helm, Conrad Hausen, Harald BMC Evol Biol Research Article BACKGROUND: Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus. RESULTS: We performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 h postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d(221)), which after 7 cleavages starts expressing Neurogenin, Acheate-Scute and NeuroD. CONCLUSIONS: We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. We suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems. BioMed Central 2020-09-14 /pmc/articles/PMC7489019/ /pubmed/32928118 http://dx.doi.org/10.1186/s12862-020-01680-x Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Kumar, Suman
Tumu, Sharat Chandra
Helm, Conrad
Hausen, Harald
The development of early pioneer neurons in the annelid Malacoceros fuliginosus
title The development of early pioneer neurons in the annelid Malacoceros fuliginosus
title_full The development of early pioneer neurons in the annelid Malacoceros fuliginosus
title_fullStr The development of early pioneer neurons in the annelid Malacoceros fuliginosus
title_full_unstemmed The development of early pioneer neurons in the annelid Malacoceros fuliginosus
title_short The development of early pioneer neurons in the annelid Malacoceros fuliginosus
title_sort development of early pioneer neurons in the annelid malacoceros fuliginosus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7489019/
https://www.ncbi.nlm.nih.gov/pubmed/32928118
http://dx.doi.org/10.1186/s12862-020-01680-x
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