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Spatial and Temporal Patterns of Gene Expression During Neurogenesis in the Sea Urchin Lytechinus Variegatus Leslie A

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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 (2019) 10:2 https://doi.org/10.1186/s13227-019-0115-8 EvoDevo RESEARCH Open Access Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus Leslie A. Slota , Esther M. Miranda and David R. McClay* 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 inno- vations, 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 regula- tory 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 specifca- tion 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 presum- ably involved in neurogenesis in the gut. Conclusions: This study builds a foundation to study how neurons are specifed 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 specifed, (3) perform comparative studies with the sea urchin, protostome, and vertebrate organisms. Keywords: Neurogenesis, Neural specifcation, Sea urchin, Gene regulatory state Background indirect (animals with larval stages) and direct devel- Te formation of a nervous system is a key innovation in oping organisms. Comparisons of genomic sequences evolution that allows for an organism to integrate sensory across the animal kingdom indicate that metazoan nerv- information and interact with its environment through ous systems largely employ a conserved set of genes dur- motor output. Neurogenesis is a tightly controlled pro- ing embryonic development [1]. Studying those genes in cess that occurs during embryonic development in both a number of organisms, especially those with simplifed nervous systems, has the promise of revealing not only *Correspondence: [email protected] how nervous systems develop, but also how they evolved. Department of Biology, Duke University, 124 Science Dr., Box 90338, Over the past decade, much has been learned about the Durham, NC 27708, USA © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/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://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Slota et al. EvoDevo (2019) 10:2 Page 2 of 16 origins of the vertebrate nervous system, and informa- protostome neurogenesis [2]. Tis suggests that deuter- tion has accumulated for neurogenesis of other deuter- ostome neurogenesis is quite conserved. An examination ostomes, including the sea urchin. Nevertheless, much of how sea urchin neurogenesis occurs can be extremely remains to be learned about how complex nervous sys- informative, particularly in instances where neurogenic tems develop. GRNs difer between deuterostomes and protostomes. Echinoderms are a basal deuterostome group charac- Another compelling reason for exploring sea urchin terized by pentaradial symmetry. Unlike the adults, echi- neurogenesis is from a developmental perspective; the noderm embryos are bilaterally symmetric. Te nervous simplicity and speed of neurogenesis in the sea urchin system of the bilaterally symmetric sea urchin embryo is embryo, along with an ability to identify and place GRN composed of 3 major regions. Te frst is the apical organ, components efciently, allow for a thorough dissection of which is a collection of 2–6 serotonergic neurons as well which genes are used and how they are used to build a as several other neural cell types found in the anterior deuterostome nervous system. end of the embryo [2–4]. Te apical organ is considered Te transcription factors shown to be necessary to be the embryonic central nervous system and the pro- for neurogenesis in the sea urchin include soxC and cessing center of the embryo [5]. Te second region is brn1/2/4, which are expressed broadly in the nervous the ciliary band, an ectodermal band of ciliated cells and system and are required for neurons throughout the neurons thought to aid in swimming and sensory behav- embryo [5, 13]. Furthermore, some transcription factors iors [6–8]. Associated with the ciliary band is a collection are expressed only by specifc types of neural progenitors of neurons known as the postoral neurons which lie just in the sea urchin and are required for the development outside the ciliary band and connect axons to the ciliary of subsets of neurons in the nervous system. Neurogenin band axonal tract [9]. Together, the ciliary band and pos- is required for specifcation of cholinergic neurons in toral neurons are considered to be part of the peripheral the ciliary band, orthopedia is required for specifca- nervous system of the embryo [5, 9]. Te third region of tion of postoral neurons, and achaete–scute and zfhx1 the embryonic nervous system is in the endoderm where have been shown to be required for specifcation or dif- several neurons within the gut, as well as in the develop- ferentiation of serotonergic neurons in the apical organ, ing mouth and anus, aid in swallowing and movement of respectively [2, 13, 15]. Additionally, soxb1, insm, and food through the digestive tract. Neurons in the gut have sip1 are expressed during the initial proneural specifca- been shown to be specifed directly within the endoderm tion period in the sea urchin [14]. Perturbations of these [10]. transcription factors led to the construction of prelimi- Over the last 20 years, much efort has been put into nary gene regulatory networks for neurogenesis. Inhi- creating a developmental gene regulatory network bition of signaling pathways such as Nodal, FGF, Delta/ (GRN) for sea urchin development. A big advance in that Notch and signaling molecules such as Wnt ligands has research occurred with publication of the frst sea urchin also contributed to the knowledge of inputs into nerv- genome in 2006, and the availability of the genomic ous system development in the sea urchin [2, 5, 14, 15]. information spurred deeper insights into many proper- Before GRNs can be assembled to reveal detailed neuro- ties of the embryo [11]. During the annotation phase of genic specifcation sequences, and allow for evolution- the genome project, a large number of dedicated neural ary comparisons, many additional neural transcription molecules were identifed [12], and over the last several factors and signaling molecules must be characterized. years, eforts have begun to build GRN states for the sea Tus, identifcation of additional genes involved in neu- urchin [2, 5, 13, 14]. However, only a limited number of rogenesis and their spatiotemporal expression profles these neural molecules have been spatiotemporally and is a necessary beginning point toward that goal. With a functionally characterized. Fewer than 20 specifers have vastly expanded group of involved genes, one will then be been localized to neural precursors and assembled into able to ask questions about patterning: Is neural develop- GRN models of the more than 70 transcription factors ment similar to vertebrates? Are the same genes used in identifed in the genome (based on sequence orthologs similar ways as fies and vertebrates? Which neural pro- of transcription factors identifed as neural in other sys- cesses and phenomena are vertebrate or deuterostome tems) [2, 5, 12–15]. innovations, and which evolved earlier? What are the Expanding the sea urchin neurogenic GRN can be innovations (if any) made within the echinoderm lineage benefcial for many reasons. Te frst is the evolution- to get their unique organization of the nervous system? ary insights that can be gained. Te phylogenetic posi- Here we report the spatial and temporal expression tion of sea urchins as a basal deuterostome has already patterns of 21 genes from blastula through pluteus stage shown, with a limited dataset, that sea urchin neuro- in the sea urchin Lytechinus variegatus that are expressed genesis resembles vertebrate neurogenesis, more than in areas of the nervous system and have been reported Slota et al. EvoDevo (2019) 10:2 Page 3 of 16 to be involved in neurogenesis in other model systems. been patterned and larvae have begun to use their sim- Tese patterns of gene expression provide a template ple nervous system.
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