Cargando…
Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus
BACKGROUND: The sea urchin is a basal deuterostome that is more closely related to vertebrates than many organisms traditionally used to study neurogenesis. This phylogenetic position means that the sea urchin can provide insights into the evolution of the nervous system by helping resolve which dev...
Autores principales: | , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2019
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6371548/ https://www.ncbi.nlm.nih.gov/pubmed/30792836 http://dx.doi.org/10.1186/s13227-019-0115-8 |
_version_ | 1783394574749663232 |
---|---|
author | Slota, Leslie A. Miranda, Esther M. McClay, David R. |
author_facet | Slota, Leslie A. Miranda, Esther M. McClay, David R. |
author_sort | Slota, Leslie A. |
collection | PubMed |
description | BACKGROUND: The sea urchin is a basal deuterostome that is more closely related to vertebrates than many organisms traditionally used to study neurogenesis. This phylogenetic position means that the sea urchin can provide insights into the evolution of the nervous system by helping resolve which developmental processes are deuterostome innovations, which are innovations in other clades, and which are ancestral. However, the nervous system of echinoderms is one of the least understood of all major metazoan phyla. To gain insights into echinoderm neurogenesis, spatial and temporal gene expression data are essential. Then, functional data will enable the building of a detailed gene regulatory network for neurogenesis in the sea urchin that can be compared across metazoans to resolve questions about how nervous systems evolved. RESULTS: Here, we analyze spatiotemporal gene expression during sea urchin neurogenesis for genes that have been shown to be neurogenic in one or more species. We report the expression of 21 genes expressed in areas of neurogenesis in the sea urchin embryo from blastula stage (just before neural progenitors begin their specification sequence) through pluteus larval stage (when much of the nervous system has been patterned). Among those 21 gene expression patterns, we report expression of 11 transcription factors and 2 axon guidance genes, each expressed in discrete domains in the neuroectoderm or in the endoderm. Most of these genes are expressed in and around the ciliary band. Some including the transcription factors Lv-mbx, Lv-dmrt, Lv-islet, and Lv-atbf1, the nuclear protein Lv-prohibitin, and the guidance molecule Lv-semaa are expressed in the endoderm where they are presumably involved in neurogenesis in the gut. CONCLUSIONS: This study builds a foundation to study how neurons are specified and evolved by analyzing spatial and temporal gene expression during neurogenesis in a basal deuterostome. With these expression patterns, we will be able to understand what genes are required for neural development in the sea urchin. These data can be used as a starting point to (1) build a spatial gene regulatory network for sea urchin neurogenesis, (2) identify how subtypes of neurons are specified, (3) perform comparative studies with the sea urchin, protostome, and vertebrate organisms. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0115-8) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6371548 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-63715482019-02-21 Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus Slota, Leslie A. Miranda, Esther M. McClay, David R. EvoDevo Research BACKGROUND: The sea urchin is a basal deuterostome that is more closely related to vertebrates than many organisms traditionally used to study neurogenesis. This phylogenetic position means that the sea urchin can provide insights into the evolution of the nervous system by helping resolve which developmental processes are deuterostome innovations, which are innovations in other clades, and which are ancestral. However, the nervous system of echinoderms is one of the least understood of all major metazoan phyla. To gain insights into echinoderm neurogenesis, spatial and temporal gene expression data are essential. Then, functional data will enable the building of a detailed gene regulatory network for neurogenesis in the sea urchin that can be compared across metazoans to resolve questions about how nervous systems evolved. RESULTS: Here, we analyze spatiotemporal gene expression during sea urchin neurogenesis for genes that have been shown to be neurogenic in one or more species. We report the expression of 21 genes expressed in areas of neurogenesis in the sea urchin embryo from blastula stage (just before neural progenitors begin their specification sequence) through pluteus larval stage (when much of the nervous system has been patterned). Among those 21 gene expression patterns, we report expression of 11 transcription factors and 2 axon guidance genes, each expressed in discrete domains in the neuroectoderm or in the endoderm. Most of these genes are expressed in and around the ciliary band. Some including the transcription factors Lv-mbx, Lv-dmrt, Lv-islet, and Lv-atbf1, the nuclear protein Lv-prohibitin, and the guidance molecule Lv-semaa are expressed in the endoderm where they are presumably involved in neurogenesis in the gut. CONCLUSIONS: This study builds a foundation to study how neurons are specified and evolved by analyzing spatial and temporal gene expression during neurogenesis in a basal deuterostome. With these expression patterns, we will be able to understand what genes are required for neural development in the sea urchin. These data can be used as a starting point to (1) build a spatial gene regulatory network for sea urchin neurogenesis, (2) identify how subtypes of neurons are specified, (3) perform comparative studies with the sea urchin, protostome, and vertebrate organisms. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0115-8) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-12 /pmc/articles/PMC6371548/ /pubmed/30792836 http://dx.doi.org/10.1186/s13227-019-0115-8 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. |
spellingShingle | Research Slota, Leslie A. Miranda, Esther M. McClay, David R. Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus |
title | Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus |
title_full | Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus |
title_fullStr | Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus |
title_full_unstemmed | Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus |
title_short | Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus |
title_sort | spatial and temporal patterns of gene expression during neurogenesis in the sea urchin lytechinus variegatus |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6371548/ https://www.ncbi.nlm.nih.gov/pubmed/30792836 http://dx.doi.org/10.1186/s13227-019-0115-8 |
work_keys_str_mv | AT slotalesliea spatialandtemporalpatternsofgeneexpressionduringneurogenesisintheseaurchinlytechinusvariegatus AT mirandaestherm spatialandtemporalpatternsofgeneexpressionduringneurogenesisintheseaurchinlytechinusvariegatus AT mcclaydavidr spatialandtemporalpatternsofgeneexpressionduringneurogenesisintheseaurchinlytechinusvariegatus |