Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus

Leslie A Slota,Esther M Miranda,David R Mcclay

doi:10.1186/s13227-019-0115-8

Abstract

BackgroundThe 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.ResultsHere, 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.ConclusionsThis 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.

Highlights

The sea urchin is a basal deuterostome that is more closely related to vertebrates than many organisms traditionally used to study neurogenesis
Identification of genes expressed in the embryonic sea urchin nervous system As part of an effort to identify components of the neurogenic gene regulatory network (GRN) in the sea urchin, a molecular cloning and an in situ hybridization screening were performed
To choose candidate genes for this screening, we queried the published Stronglyocentrotus purpuratus developmental transcriptome and focused on annotated sea urchin orthologs of genes expressed during embryonic development that belong to the functional classification of neurogenesis [16]

Summary

Introduction

The sea urchin is a basal deuterostome that is more closely related to vertebrates than many organisms traditionally used to study neurogenesis. Comparisons of genomic sequences across the animal kingdom indicate that metazoan nervous systems largely employ a conserved set of genes during embryonic development [1]. Studying those genes in a number of organisms, especially those with simplified nervous systems, has the promise of revealing how nervous systems develop, and how they evolved. Much remains to be learned about how complex nervous systems develop

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