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

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.Electronic supplementary materialThe online version of this article (10.1186/s13227-019-0115-8) contains supplementary material, which is available to authorized users.

Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, Hemicentrotus pulcherrimus

“…The present Netrin stripe along the ciliary band seems consistent with a previous in situ report on sea urchin larva by Slota et al [21] that showed the Netrin gene expression site on the circumoral ectoderm side of the ciliary band. The Netrin gene expression site by the ciliary band is reminiscent of the midline ectoderm in vertebrates and invertebrates [42][43][44].…”

“…A close spatial association of the Netrin stripe with the ciliary band on the larval surface occurred later, by the 2dpf 4aPL stage (Figure 6A,B). The spatial closeness between the Netrin stripe and the DRD1-expressing ciliary band may occur near the early 2aPL stage, and this appears to be in good agreement with Lv-Netrin in situ reports on the circumoral ectoderm along the ciliary band by Slota et al [21]; this will be further discussed later.…”

Phylogenetic analysis and embryonic expression of panarthropod Dmrt genes

“…[55] Dunn et al 2008). A very recent paper describes the expression of an uncharacterized Dmrt gene in a sea urchin which is exclusively expressed in the foregut ([74] Slota et al 2019). We assume that this Dmrt gene is a likely ortholog of Dmrt93B which could place the origin of its function in mouth/foregut development at the base of the Bilateria.…”

Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour

“…Apical organ cells express different ion channels that are associated with mechanosensation in vertebrates. For example, cells in the apical organ of sea urchin, Platynereis and cnidarian larvae express ASIC, and/or TRP channels such as NOMPC or TRPV [343][344][345][346]. Whether and how these cells contribute to substrate or flow sensation is yet to be explored.…”