The gene regulatory control of sea urchin gastrulation

Ettensohn, Charles A.

doi:10.1016/j.mod.2020.103599

Cited by 17 publications

(9 citation statements)

References 129 publications

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“…Similarly, plotting genes involved in the aboral ectoderm gene regulatory network ( Ben-Tabou de-Leon et al, 2013 ), we found all genes in both the aboral ectoderm cluster as well as in the apical plate cells ( Figure 5B ). On the other hand, plotting members of the pre-gastrula skeletogenic mesoderm regulatory network ( Figure 5C ) revealed most were still active in the pluteus larva and specific to skeletal cells ( Oliveri et al, 2008 ; Shashikant and Ettensohn, 2019 ; Khor et al, 2019 ; Ettensohn, 2020 ). These findings illustrate the immediate benefit of our dataset to drastically expand our knowledge of larval regulatory networks.…”

Section: Resultsmentioning

confidence: 99%

Single-cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome

Paganos

Voronov

Musser

et al. 2021

eLife

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Identifying the molecular fingerprint of organismal cell types is key for understanding their function and evolution. Here, we use single cell RNA sequencing (scRNA-seq) to survey the cell types of the sea urchin early pluteus larva, representing an important developmental transition from non-feeding to feeding larva. We identify 21 distinct cell clusters, representing cells of the digestive, skeletal, immune, and nervous systems. Further subclustering of these reveal a highly detailed portrait of cell diversity across the larva, including the identification of neuronal cell types. We then validate important gene regulatory networks driving sea urchin development and reveal new domains of activity within the larval body. Focusing on neurons that co-express Pdx-1 and Brn1/2/4, we identify an unprecedented number of genes shared by this population of neurons in sea urchin and vertebrate endocrine pancreatic cells. Using differential expression results from Pdx-1 knockdown experiments, we show that Pdx1 is necessary for the acquisition of the neuronal identity of these cells. We hypothesize that a network similar to the one orchestrated by Pdx1 in the sea urchin neurons was active in an ancestral cell type and then inherited by neuronal and pancreatic developmental lineages in sea urchins and vertebrates.

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Section: Resultsmentioning

confidence: 99%

Single-cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome

Paganos

Voronov

Musser

et al. 2021

eLife

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“…At this stage, the embryos were characterized by the inward bending of the remaining vegetal plate, which created the first opening of the future digestive tract, the blastopore, which will subsequently develop into the anus. This morphogenetic movement has been proposed to be driven by various mechanisms, such as swelling, cell shape changes, pulling, and/or apical secretion, but the exact mechanism at play still remains enigmatic ( Ettensohn, 2020 ). Within the blastocoel, the SM cells concomitantly started migrating, extending filopodia, and attaching and detaching them from the blastocoel wall.…”

Section: Resultsmentioning

confidence: 99%

Developmental atlas of the indirect-developing sea urchin Paracentrotus lividus: From fertilization to juvenile stages

Formery

Wakefield²,

Gesson³

et al. 2022

Front. Cell Dev. Biol.

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The sea urchin Paracentrotus lividus has been used as a model system in biology for more than a century. Over the past decades, it has been at the center of a number of studies in cell, developmental, ecological, toxicological, evolutionary, and aquaculture research. Due to this previous work, a significant amount of information is already available on the development of this species. However, this information is fragmented and rather incomplete. Here, we propose a comprehensive developmental atlas for this sea urchin species, describing its ontogeny from fertilization to juvenile stages. Our staging scheme includes three periods divided into 33 stages, plus 15 independent stages focused on the development of the coeloms and the adult rudiment. For each stage, we provide a thorough description based on observations made on live specimens using light microscopy, and when needed on fixed specimens using confocal microscopy. Our descriptions include, for each stage, the main anatomical characteristics related, for instance, to cell division, tissue morphogenesis, and/or organogenesis. Altogether, this work is the first of its kind providing, in a single study, a comprehensive description of the development of P. lividus embryos, larvae, and juveniles, including details on skeletogenesis, ciliogenesis, myogenesis, coelomogenesis, and formation of the adult rudiment as well as on the process of metamorphosis in live specimens. Given the renewed interest for the use of sea urchins in ecotoxicological, developmental, and evolutionary studies as well as in using marine invertebrates as alternative model systems for biomedical investigations, this study will greatly benefit the scientific community and will serve as a reference for specialists and non-specialists interested in studying sea urchins.

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“…This morphogenesis is commonly called “tissue invagination”. Tissue invagination during gastrulation has been characterized at molecular-, cellular- and mechanical levels for several model invertebrates including sea urchins ( Davidson et al, 1995 ; Ettensohn, 2020 ), fruit flies ( Gheisari, Aakhte & Müller, 2020 ; Rauzi et al, 2013 ; Sweeton et al, 1991 ), ascidians ( Fiuza & Lemaire, 2021 ; Sherrard et al, 2010 ). It was shown that tissue invagination is based on a series of coordinated cell shape changes ( Hardin & Keller, 1988 ; Keller, Davidson & Shook, 2003 ; Leptin & Grunewald, 1990 ; Sawyer et al, 2010 ; Sherrard et al, 2010 ).…”

Section: Discussionmentioning

confidence: 99%

“…Involution of the blastopore lip was observed in the gastrulation of many model objects including amphibians ( Keller, Davidson & Shook, 2003 ) and sea urchins ( Ettensohn, 2020 ). However, the cellular mechanism of involution differs in different animals.…”

Section: Discussionmentioning

confidence: 99%

Embryonic development of the moon jellyfishAurelia aurita(Cnidaria, Scyphozoa): another variant on the theme of invagination

Kraus

Osadchenko

Kosevich

2022

PeerJ

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Background Aurelia aurita (Scyphozoa, Cnidaria) is an emblematic species of the jellyfish. Currently, it is an emerging model of Evo-Devo for studying evolution and molecular regulation of metazoans’ complex life cycle, early development, and cell differentiation. For Aurelia, the genome was sequenced, the molecular cascades involved in the life cycle transitions were characterized, and embryogenesis was studied on the level of gross morphology. As a reliable representative of the class Scyphozoa, Aurelia can be used for comparative analysis of embryonic development within Cnidaria and between Cnidaria and Bilateria. One of the intriguing questions that can be posed is whether the invagination occurring during gastrulation of different cnidarians relies on the same cellular mechanisms. To answer this question, a detailed study of the cellular mechanisms underlying the early development of Aurelia is required. Methods We studied the embryogenesis of A. aurita using the modern methods of light microscopy, immunocytochemistry, confocal laser microscopy, scanning and transmission electron microscopy. Results In this article, we report a comprehensive study of the early development of A. aurita from the White Sea population. We described in detail the embryonic development of A. aurita from early cleavage up to the planula larva. We focused mainly on the cell morphogenetic movements underlying gastrulation. The dynamics of cell shape changes and cell behavior during invagination of the archenteron (future endoderm) were characterized. That allowed comparing the gastrulation by invagination in two cnidarian species—scyphozoan A. aurita and anthozoan Nematostella vectensis. We described the successive stages of blastopore closure and found that segregation of the germ layers in A. aurita is linked to the ’healing’ of the blastopore lip. We followed the developmental origin of the planula body parts and characterized the planula cells’ ultrastructure. We also found that the planula endoderm consists of three morphologically distinct compartments along the oral-aboral axis. Conclusions Epithelial invagination is a fundamental morphogenetic movement that is believed as highly conserved across metazoans. Our data on the cell shaping and behaviours driving invagination in A. aurita contribute to understanding of morphologically similar morphogenesis in different animals. By comparative analysis, we clearly show that invagination may differ at the cellular level between cnidarian species belonging to different classes (Anthozoa and Scyphozoa). The number of cells involved in invagination, the dynamics of the shape of the archenteron cells, the stage of epithelial-mesenchymal transition that these cells can reach, and the fate of blastopore lip cells may vary greatly between species. These results help to gain insight into the evolution of morphogenesis within the Cnidaria and within Metazoa in general.

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The gene regulatory control of sea urchin gastrulation

Cited by 17 publications

References 129 publications

Single-cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome

Single-cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome

Developmental atlas of the indirect-developing sea urchin Paracentrotus lividus: From fertilization to juvenile stages

Embryonic development of the moon jellyfishAurelia aurita(Cnidaria, Scyphozoa): another variant on the theme of invagination

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