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Spatial and Temporal Patterns of Gene Expression During Neurogenesis in the Sea Urchin Lytechinus variegatus

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Spatial and Temporal Patterns of Gene Expression During Neurogenesis in the Sea Urchin Lytechinus variegatus

Leslie A Slota et al. Evodevo.

Abstract

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.

Keywords: Gene regulatory state; Neural specification; Neurogenesis; Sea urchin.

Figures

Fig. 1
Fig. 1
Transcription factors expressed in the apical organ. al Lv-egr is expressed in the anterior two-thirds of the embryo from 10 to 12 hpf (hours post fertilization) (brackets in ab) and then comes on in cells in the apical organ starting at 24 hpf (h). mx Lv-hey is expressed in scattered cells of the vegetal plate from 10 to 12 hpf (arrowheads in n, o). Inset image of o shows posterior view of vegetal plate. One to two cells express Lv-hey in the elongating archenteron at 16 hpf (arrowhead in p). Then, at 24 hpf, Lv-hey is expressed in 2–4 cells in the apical organ (tx). Lv-hey is also expressed in scattered mesodermal cells at 30 hpf onward (arrowhead in W) and in 1–2 cells in the gut endoderm (arrowhead in x). a′l′ Lv-elk is expressed lightly in skeletogenic mesodermal cells from 10 to 18 hpf (a′e′) (arrows). From 20 to 22 hpf, Lv-elk is expressed in the non-skeletogenic mesoderm (brackets in f′, g′). At 24 hpf, Lv-elk turns off in the non-skeletogenic mesoderm and turns back on in a subset of skeletogenic mesoderm (arrow in H′). At 28 hpf, Lv-elk is expressed in 1–2 cells of the apical organ (arrowheads in j′l′). Scale bars = 50 μm
Fig. 2
Fig. 2
Expression of transcription factors in or near the ciliary band. al Lv-ap2 is expressed starting at 24 hpf in the oral ectoderm near the ciliary band (bracket in h) where it remains through 32 hpf. mx Lv-ese is expressed in the non-skeletogenic mesoderm from 10 to 22 hpf. At 22 hpf, Lv-ese is expressed in the lateral ciliary band (shown in bracket in t, inset image shows lateral perspective). It remains in cells of the lateral ciliary band and also turns on in the postoral neurons (shown in inset images in vx). a′l′ Lv-scratch is expressed beginning at 24 hpf in cells scattered in the ciliary band. Cells expressing Lv-scratch increase in number through 32 hpf. m′x′ Lv-prox is expressed in the non-skeletogenic mesoderm until 32 hpf when it is also expressed throughout the ciliary band (arrow heads in x′). Scale bars = 50 μm
Fig. 3
Fig. 3
Transcription factors expressed in the foregut. al Expression of Lv-mbx begins at 16 hpf in the elongating archenteron (arrowhead in d, e). Lv-mbx is expressed in the foregut from then through 32 hpf and is also expressed at pluteus stages in the ectoderm near the mouth. mx Lv-islet is expressed in the developing foregut from 16 to 32 hpf. Starting at 18 hpf, Lv-islet expression is not just in the foregut but in the stripe of ectoderm near the foregut (q). a′l′ Lv-dmrt is expressed in the foregut from 22 hpf (g′) through 32 hpf. m′x′ Lv-atbf1 is expressed in the ectoderm from 10 to 22 hpf. At 24 hpf, Lv-atbf1 also turns on in the foregut (arrowhead in t′), where it remains through 32 hpf. Scale bars = 50 μm
Fig. 4
Fig. 4
Expression of axon guidance molecules. al Lv-netrin is expressed from 12 to 16 hpf in a ring in the vegetal plate (brackets in bd). Lv-netrin turns on briefly in the apical organ (arrowhead in e). By 22 hpf, Lv-netrin is expressed in the edges of the oral ectoderm near the ciliary band. mx Lv-semaa is expressed in a ring in the vegetal plate at 14 hpf (bracket in o). At 16 hpf, it is also expressed in the ventral ectoderm (arrowhead in p) and the apical organ. Through 32 hpf, Lv-semaa is expressed in the apical organ and the hindgut. Scale bars = 50um
Fig. 5
Fig. 5
Expression of survival and proliferation genes in the nervous system. al Lv-app is expressed in the anterior two-thirds of the embryo from 10 to 14 hpf (brackets in ac). At 24 hpf, Lv-app is expressed in the tip of the archenteron, and by 26 hpf, it is expressed in the coelomic pouches (arrowhead in i) and in the postoral neurons (inset images in il). mx Lv-trk is not expressed until 24 hpf when it turns on in the postoral neurons (arrowhead in t) and remains there through 32 hpf. a′l′ Lv-prohibitin is expressed in the mid- and hindgut (bracket in h′) beginning at 24 hpf through 32 hpf. m′x′ Lv-rasO is expressed in the ectoderm and vegetal plate at 10 hpf. By 14 hpf, Lv-rasO remains in the ectoderm and is in a band of expression surrounding the vegetal plate (arrows in o′, p′). By 20 hpf, Lv-rasO is expressed in one or both lateral sides of ciliary band (arrowhead in r′). By 22 hpf, Lv-rasO expression is on a single side of the lateral ciliary band. Expression then diminishes by 28 hpf. a″l″ Lv-hells is expressed in the ciliary band (arrowhead in h″) as well as the apical organ and hindgut. Scale bars = 50 μm
Fig. 6
Fig. 6
Expression of neurotransmitter-related genes. al Lv-vacht is expressed beginning in some embryos at 22 hpf in the postoral neurons (arrowhead in g) where it remains through 32 hpf. mx Lv-drd1 is expressed starting at 24 hpf in the ectoderm near the stomodeum and near the postoral neurons (arrowheads in t), where it remains through 32 hpf. a′l′ Lv-asicl4 is expressed beginning at 24 hpf in the developing apical organ (arrowhead in h′) through 32 hpf. Scale bars = 50 μm
Fig. 7
Fig. 7
Schematic of genes expressed in different regions of the ectoderm and endoderm at late gastrula and pluteus larva stages. a, b Schematics show 3 ectodermal territories (apical organ, ciliary band, and postoral region) and the list of genes from this study expressed in those regions at two time points (22 hpf and 32 hpf). Expression within a region does not mean that the genes are necessarily co-expressed with one another. c, d Schematics show endodermal territories where genes from this study are expressed at late gastrula and pluteus stages. Expression within a region does not mean that the genes are necessarily co-expressed. A anterior, P posterior

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