Development of a larval nervous system in the sea urchin

McClay, David R.

doi:10.1016/bs.ctdb.2021.10.002

Cited by 6 publications

(9 citation statements)

References 85 publications

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“…At the same stages considered above, Dkk3 is also expressed in the anterior ectoderm, similar to sFRP1/2/5a (Supplementary Figure 5). This reveals a timing and position tentatively congruent with a role of sFRP1/2/5a and Dkk3 in blocking Wnt signalling anteriorly, as described in the sea urchin 31,58 . Moreover, at the gastrula stage Otx is expressed in the antero-dorsal portion of the embryo, corresponding to the anterior portion of the neural plate and including the entire neural expression of Six3/6 (Supplementary Figure 5).…”

Section: Resultssupporting

confidence: 76%

“…During the restriction, two secreted Wnt inhibitors, sFRP1/2/5a and Dkk3, are produced from the anterior-dorsal tip of the embryo. This suggest that Wnt signalling acts through mutually repressive interactions to restrict the size and position of the aGRN to the dorsal anterior (apical) side of the embryo, as described in ambulacrarians 31,36,58 . This territorial restriction happens exclusively in the ectoderm, since GSK3 inhibition does not block the mesodermal expression of any of the EAP genes.…”

Section: Discussionmentioning

confidence: 81%

“…This chimeric brain hypothesis 56 , very similar to the earlier "animal-axial" hypothesis 57 , proposes that the ANS corresponds to the AO of invertebrate larvae, while the BNS corresponds to the remaining nervous system (posterior to the AO). However, both hypotheses pose the same fundamental problem regarding the conflicting fate of anterior neuroectodermal precursors in ambulacrarians and chordates: in ambulacrarians the ANE forms the AO 58 , while in chordates the ANE gives rise to the forebrain 21,47,59 .…”

Section: Introductionmentioning

confidence: 99%

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An ancient gene regulatory network sets the position of the forebrain in chordates

Gattoni

Keitley

Sawle

et al. 2023

Preprint

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The evolutionary origin of the vertebrate brain is still a major subject of debate. Its distinctive dorsal position and development from a tubular neuroepithelium are unique to the chordate phylum. Conversely, apical organs (AO) are larval sensory/neurosecretory centers found in many invertebrate taxa, including in animals without a brain. Previous studies have shown that AOs are specified by a conserved set of genes under the influence of Wnt signalling. Although most of these genes are expressed in chordate nervous systems (including vertebrates), no AOs have ever been described in this group of animals. Here we have exploited single-cell genomic approaches to characterize cells showing AO profiles in sea urchin (ambulacrarian), amphioxus (invertebrate chordate) and zebrafish (vertebrate chordate). This, in combination with co-expression analysis in amphioxus embryos, has allowed us to identify an active and dynamic anterior Gene Regulatory Network (aGRN) in the three deuterostome species. We have further discovered that as well as controlling AO specification in sea urchin, this aGRN is involved in the formation of the hypothalamic region in amphioxus and zebrafish. Using a functional approach, we find that the aGRN is controlled by Wnt signalling in amphioxus, and that suppression of the aGRN by Wnt overactivation leads to a loss of forebrain cell types. The loss of the forebrain does not equate to a reduction of neuronal tissue, but to a loss of identity, suggesting a new role for Wnt in amphioxus in specifically positioning the forebrain. We thus propose that the aGRN is conserved throughout bilaterians and that in the chordate lineage was incorporated into the process of neurulation to position the brain, thereby linking the evolution of the AO to that of the chordate forebrain.

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Section: Resultssupporting

confidence: 76%

Section: Discussionmentioning

confidence: 81%

Section: Introductionmentioning

confidence: 99%

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An ancient gene regulatory network sets the position of the forebrain in chordates

Gattoni

Keitley

Sawle

et al. 2023

Preprint

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“…Group 6, with Brn1/2/4, Otp, Onecut, and Z166, has high expression in ciliary band and postoral neurons, aligning with studies that found a shared embryonic origin for these neural cell types (reviewed in McClay, 2022). This analysis also identified potential genes that may regulate the differentiation of the unidentified adult neural cell clusters, with the TFs in groups 9 and 10 showing high expression levels in these cells.…”

Section: Larval Cell Types Insupporting

confidence: 84%

Contrasting the development of larval and adult body plans during the evolution of biphasic lifecycles in sea urchins

McDonald,

Massri,

Escobar

et al. 2024

Preprint

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Biphasic lifecycles are widespread among animals, but little is known about how the developmental transition between larvae and adults is regulated. Sea urchins are a unique system for studying this phenomenon because of the stark differences between their bilateral larval and pentaradial adult body plans. Here, we use single cell RNA-sequencing to analyze the development of Heliocidaris erythrogramma (He), a sea urchin species with an accelerated, non-feeding mode of larval development. The sequencing time course extends from early embryogenesis to roughly a day before the onset of metamorphosis in He larvae, which is a period that has not been covered by previous datasets. We find that the non-feeding developmental strategy of He is associated with several changes in the specification of larval cell types compared to sea urchins with feeding larvae, such as the loss of a larva-specific skeletal cell population. Furthermore, the development of the larval and adult body plans in sea urchins may utilize largely different sets of regulatory genes. These findings lay the groundwork for extending existing developmental gene regulatory networks to cover additional stages of biphasic lifecycles.

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“…Examples include the discovery of cyclins (1), which ultimately led to currently approved drugs targeting metastatic cancers (2), and the first descriptions of gene regulatory networks (3,4), which have become a foundational framework for understanding development (5)(6)(7). Sea urchins remain favorites for study across diverse fields including gene regulation of development (8)(9)(10), innate immunity (11)(12)(13)(14)(15)(16), biomineralization (17)(18)(19)(20)(21), nervous system development (22)(23)(24), reproduction (25)(26)(27), and developmental physiology (28)(29)(30).…”

Section: Introductionmentioning

confidence: 99%

Stable germline transgenesis using theMinosTc1/marinerelement in the sea urchin,Lytechinus pictus

Jackson,

Romero,

Kling

et al. 2024

Preprint

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Stable transgenesis is a transformative tool in model organism biology. While the sea urchin is one of the oldest animal models in cell and developmental biology, it has relied on transient manipulations of wild animals, and has lacked a strategy for stable transgenesis. Here we build on recent progress to develop a more genetically tractable sea urchin species, Lytechinus pictus, to establish a robust transgene integration method. Three commonly used transposons (Minos, Tol2, piggyBac) were tested for non-autonomous transposition, using plasmids containing a polyubiquitin promoter upstream of a H2B-mCerulean nuclear marker. Minos was the only transposable element that resulted in significant expression past metamorphosis. F0 animals were raised to sexual maturity and spawned to determine germline integration, transgene inheritance frequency, and to characterize expression patterns of the transgene in F1 progeny. The results demonstrated transgene transmission through the germline, the first example of a germline transgenic sea urchin, and indeed of any echinoderm. This milestone paves the way for the generation of diverse transgenic resources that will dramatically enhance the utility, reproducibility, and efficiency of sea urchin research.

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Development of a larval nervous system in the sea urchin

Cited by 6 publications

References 85 publications

An ancient gene regulatory network sets the position of the forebrain in chordates

An ancient gene regulatory network sets the position of the forebrain in chordates

Contrasting the development of larval and adult body plans during the evolution of biphasic lifecycles in sea urchins

Stable germline transgenesis using theMinosTc1/marinerelement in the sea urchin,Lytechinus pictus

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