Spdeadringer, a sea urchin embryo gene required separately in skeletogenic and oral ectoderm gene regulatory networks

By gastrulation the ectodermal territories of the sea urchin embryo have developed an unexpectedly complex spatial pattern of sharply bounded regulatory states, organized orthogonally with respect to the animal/vegetal and oral/aboral axes of the embryo. Although much is known of the gene regulatory network (GRN) linkages that generate these regulatory states, the principles by which the boundaries between them are positioned and maintained have remained undiscovered. Here we determine the encoded genomic logic responsible for the boundaries of the oral aspect of the embryo that separate endoderm from ectoderm and ectoderm from neurogenic apical plate and that delineate the several further subdivisions into which the oral ectoderm per se is partitioned. Comprehensive regulatory state maps, including all spatially expressed oral ectoderm regulatory genes, were established. The circuitry at each boundary deploys specific repressors of regulatory states across the boundary, identified in this work, plus activation by broadly expressed positive regulators. These network linkages are integrated with previously established interactions on the oral/aboral axis to generate a GRN model encompassing the 2D organization of the regulatory state pattern in the pregastrular oral ectoderm of the embryo.

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Robustness and Accuracy in Sea Urchin Developmental Gene Regulatory Networks

Frontiers in Genetics ◽

10.3389/fgene.2016.00016 ◽

2016 ◽

Vol 7 ◽

Cited By ~ 1

Author(s):

Smadar Ben-Tabou de-Leon

Keyword(s):

Sea Urchin ◽

Gene Regulatory Networks ◽

Regulatory Networks ◽

Developmental Gene ◽

Gene Regulatory

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Developmental single-cell transcriptomics in the Lytechinus variegatus sea urchin embryo

Development ◽

10.1242/dev.198614 ◽

2021 ◽

Author(s):

Abdull J. Massri ◽

Laura Greenstreet ◽

Anton Afanassiev ◽

Alejandro Berrio ◽

Gregory A. Wray ◽

...

Keyword(s):

Sea Urchin ◽

Regulatory Networks ◽

Developmental Trajectories ◽

Primordial Germ Cell ◽

Equatorial Region ◽

Lytechinus Variegatus ◽

Sea Urchin Embryo ◽

Transcriptional Changes ◽

Gene Regulatory ◽

Cell Trajectories

Using scRNA-seq coupled with computational approaches, we studied transcriptional changes in cell states of sea urchin embryos during development to the larval stage. Eighteen closely spaced time points were taken during the first 24 hours of development of Lytechinus variegatus (Lv). Developmental trajectories were constructed using Waddington-OT, a computational approach to "stitch" together developmental timepoints. Skeletogenic and primordial germ cell trajectories diverged early in cleavage. Ectodermal progenitors were distinct from other lineages by sixth cleavage, though a small percentage of ectoderm cells briefly co-expressed endoderm markers indicating an early ecto-endoderm cell state, likely in cells originating from the equatorial region of the egg. Endomesoderm cells originated at 6th cleavage also and this state persisted for more than two cleavages, then diverged into distinct endoderm and mesoderm fates asynchronously, with some cells retaining an intermediate specification status until gastrulation. 79 of 80 genes (99%) examined, and included in published developmental gene regulatory networks (dGRNs), are present in the Lv-scRNA-seq dataset, and expressed in the correct lineages in which the dGRN circuits operate.

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The Developmental Transcriptome for Lytechinus variegatus Exhibits Temporally Punctuated Gene Expression Changes

10.1101/572388 ◽

2019 ◽

Author(s):

John D. Hogan ◽

Jessica L. Keenan ◽

Lingqi Luo ◽

Dakota Y. Hawkins ◽

Jonas Ibn-Salem ◽

...

Keyword(s):

Gene Expression ◽

Larval Development ◽

Sea Urchin ◽

Gene Regulatory Networks ◽

Regulatory Networks ◽

Lytechinus Variegatus ◽

Stable Gene ◽

Major Transitions ◽

Gene Regulatory ◽

Embryonic And Larval Development

AbstractEmbryonic development is arguably the most complex process an organism undergoes during its lifetime, and understanding this complexity is best approached with a systems-level perspective. The sea urchin has become a highly valuable model organism for understanding developmental specification, morphogenesis, and evolution. As a non-chordate deuterostome, the sea urchin occupies an important evolutionary niche between protostomes and vertebrates. Lytechinus variegatus (Lv) is an Atlantic species that has been well studied, and which has provided important insights into signal transduction, patterning, and morphogenetic changes during embryonic and larval development. The Pacific species, Strongylocentrotus purpuratus (Sp), is another well-studied sea urchin, particularly for gene regulatory networks (GRNs) and cis-regulatory analyses. A well-annotated genome and transcriptome for Sp are available, but similar resources have not been developed for Lv. Here, we provide an analysis of the Lv transcriptome at 11 timepoints during embryonic and larval development. The data indicate that the gene regulatory networks that underlie specification are well-conserved among sea urchin species. We show that the major transitions in variation of embryonic transcription divide the developmental time series into four distinct, temporally sequential phases. Our work shows that sea urchin development occurs via sequential intervals of relatively stable gene expression states that are punctuated by abrupt transitions.

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The surprising complexity of the transcriptional regulation of the spdri gene reveals the existence of new linkages inside sea urchin's PMC and Oral Ectoderm Gene Regulatory Networks

Developmental Biology ◽

10.1016/j.ydbio.2008.07.036 ◽

2008 ◽

Vol 322 (2) ◽

pp. 425-434 ◽

Cited By ~ 1

Author(s):

Abdullah Al Mahmud ◽

Gabriele Amore

Keyword(s):

Transcriptional Regulation ◽

Gene Regulatory Networks ◽

Regulatory Networks ◽

Oral Ectoderm ◽

Gene Regulatory

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Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development

Nature Communications ◽

10.1038/s41467-020-20023-4 ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Gregory A. Cary ◽

Brenna S. McCauley ◽

Olga Zueva ◽

Joseph Pattinato ◽

William Longabaugh ◽

...

Keyword(s):

Early Development ◽

Sea Urchin ◽

Gene Regulatory Networks ◽

Regulatory Networks ◽

Morphological Diversity ◽

Sea Star ◽

Animal Diversity ◽

Evolutionarily Conserved ◽

Overall Stability ◽

Gene Regulatory

AbstractThe extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordinated process of embryogenesis. A particular challenge in understanding the origins of animal diversity lies in determining how GRNs incorporate novelty while preserving the overall stability of the network, and hence, embryonic viability. Here we assemble a comprehensive GRN for endomesoderm specification in the sea star from zygote through gastrulation that corresponds to the GRN for sea urchin development of equivalent territories and stages. Comparison of the GRNs identifies how novelty is incorporated in early development. We show how the GRN is resilient to the introduction of a transcription factor, pmar1, the inclusion of which leads to a switch between two stable modes of Delta-Notch signaling. Signaling pathways can function in multiple modes and we propose that GRN changes that lead to switches between modes may be a common evolutionary mechanism for changes in embryogenesis. Our data additionally proposes a model in which evolutionarily conserved network motifs, or kernels, may function throughout development to stabilize these signaling transitions.

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