ECB-ART-48994
Development
2021 Oct 01;14819:. doi: 10.1242/dev.198614.
Show Gene links
Show Anatomy links
Developmental single-cell transcriptomics in the Lytechinus variegatus sea urchin embryo.
Massri AJ
,
Greenstreet L
,
Afanassiev A
,
Berrio A
,
Wray GA
,
Schiebinger G
,
McClay DR
.
???displayArticle.abstract???
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 h of development of Lytechinus variegatus (Lv). Developmental trajectories were constructed using Waddington-OT, a computational approach to 'stitch' together developmental time points. Skeletogenic and primordial germ cell trajectories diverged early in cleavage. Ectodermal progenitors were distinct from other lineages by the 6th cleavage, although a small percentage of ectoderm cells briefly co-expressed endoderm markers that indicated an early ecto-endoderm cell state, likely in cells originating from the equatorial region of the egg. Endomesoderm cells also originated at the 6th cleavage 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. Seventy-nine out of 80 genes (99%) examined, and included in published developmental gene regulatory networks (dGRNs), are present in the Lv-scRNA-seq dataset and are expressed in the correct lineages in which the dGRN circuits operate.
???displayArticle.pubmedLink??? 34463740
???displayArticle.pmcLink??? PMC8502253
???displayArticle.link??? Development
???displayArticle.grants??? [+]
RO1 HD14483 NIH HHS , DGE-1644868 National Science Foundation, RO1 HD 14483 NIH HHS , IOS-1457305 National Science Foundation, Burroughs Wellcome Fund, Klarman Cell Observatory, Natural Sciences and Engineering Research Council of Canada, New Frontiers in Research Fund, Natural Sciences and Engineering Research Council of Canada Universities Space Research Association, T32 HD040372 NICHD NIH HHS , P01 HD037105 NICHD NIH HHS , R01 HD014483 NICHD NIH HHS
References [+] :
Alles,
Cell fixation and preservation for droplet-based single-cell transcriptomics.
2017, Pubmed
Alles, Cell fixation and preservation for droplet-based single-cell transcriptomics. 2017, Pubmed
Andrikou, Logics and properties of a genetic regulatory program that drives embryonic muscle development in an echinoderm. 2015, Pubmed , Echinobase
Angerer, A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. 2000, Pubmed , Echinobase
Becht, Dimensionality reduction for visualizing single-cell data using UMAP. 2018, Pubmed
Ben-Tabou de-Leon, Gene regulatory control in the sea urchin aboral ectoderm: spatial initiation, signaling inputs, and cell fate lockdown. 2013, Pubmed , Echinobase
Bradham, Chordin is required for neural but not axial development in sea urchin embryos. 2009, Pubmed , Echinobase
Brandman, Feedback loops shape cellular signals in space and time. 2008, Pubmed
Cameron, Lineage and fate of each blastomere of the eight-cell sea urchin embryo. 1987, Pubmed , Echinobase
Campanale, Migration of sea urchin primordial germ cells. 2014, Pubmed , Echinobase
Cao, Comprehensive single-cell transcriptional profiling of a multicellular organism. 2017, Pubmed
Cary, Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development. 2020, Pubmed , Echinobase
Chen, PBMC fixation and processing for Chromium single-cell RNA sequencing. 2018, Pubmed
Cole, Two ParaHox genes, SpLox and SpCdx, interact to partition the posterior endoderm in the formation of a functional gut. 2009, Pubmed , Echinobase
Croce, Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo. 2010, Pubmed , Echinobase
Croce, Expression pattern of Brachyury in the embryo of the sea urchin Paracentrotus lividus. 2001, Pubmed , Echinobase
Davidson, A genomic regulatory network for development. 2002, Pubmed , Echinobase
Davidson, Chromosomal-Level Genome Assembly of the Sea Urchin Lytechinus variegatus Substantially Improves Functional Genomic Analyses. 2020, Pubmed , Echinobase
Driever, A gradient of bicoid protein in Drosophila embryos. 1988, Pubmed
Duboc, Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. 2004, Pubmed , Echinobase
Duboc, Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. 2005, Pubmed , Echinobase
Duboc, Lefty acts as an essential modulator of Nodal activity during sea urchin oral-aboral axis formation. 2008, Pubmed , Echinobase
Duboc, Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo. 2010, Pubmed , Echinobase
Erkenbrack, Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses. 2015, Pubmed , Echinobase
Erwin, The evolution of hierarchical gene regulatory networks. 2009, Pubmed
Ettensohn, Alx1, a member of the Cart1/Alx3/Alx4 subfamily of Paired-class homeodomain proteins, is an essential component of the gene network controlling skeletogenic fate specification in the sea urchin embryo. 2003, Pubmed , Echinobase
Farrell, Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis. 2018, Pubmed
Fincher, Cell type transcriptome atlas for the planarian Schmidtea mediterranea. 2018, Pubmed
Foster, Single cell RNA-seq in the sea urchin embryo show marked cell-type specificity in the Delta/Notch pathway. 2019, Pubmed , Echinobase
Foster, A single cell RNA sequencing resource for early sea urchin development. 2020, Pubmed , Echinobase
Gross, The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. 2001, Pubmed , Echinobase
Guo, par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. 1995, Pubmed
Hafemeister, Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. 2019, Pubmed
Han, Mapping the Mouse Cell Atlas by Microwell-Seq. 2018, Pubmed
Haque, A practical guide to single-cell RNA-sequencing for biomedical research and clinical applications. 2017, Pubmed
Henry, Early inductive interactions are involved in restricting cell fates of mesomeres in sea urchin embryos. 1989, Pubmed , Echinobase
Hinman, Evolutionary plasticity of developmental gene regulatory network architecture. 2007, Pubmed , Echinobase
Hinman, Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. 2003, Pubmed , Echinobase
Israel, Comparative Developmental Transcriptomics Reveals Rewiring of a Highly Conserved Gene Regulatory Network during a Major Life History Switch in the Sea Urchin Genus Heliocidaris. 2016, Pubmed , Echinobase
Juliano, Isolating specific embryonic cells of the sea urchin by FACS. 2014, Pubmed , Echinobase
Karaiskos, The Drosophila embryo at single-cell transcriptome resolution. 2017, Pubmed
Kemphues, Identification of genes required for cytoplasmic localization in early C. elegans embryos. 1988, Pubmed
Li, New regulatory circuit controlling spatial and temporal gene expression in the sea urchin embryo oral ectoderm GRN. 2013, Pubmed , Echinobase
Logan, The allocation of early blastomeres to the ectoderm and endoderm is variable in the sea urchin embryo. 1997, Pubmed , Echinobase
Logan, Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. 1999, Pubmed , Echinobase
Longabaugh, Visualization, documentation, analysis, and communication of large-scale gene regulatory networks. 2009, Pubmed
Luo, Opposing nodal and BMP signals regulate left-right asymmetry in the sea urchin larva. 2012, Pubmed , Echinobase
Malik, Parallel embryonic transcriptional programs evolve under distinct constraints and may enable morphological conservation amidst adaptation. 2017, Pubmed , Echinobase
Martik, Deployment of a retinal determination gene network drives directed cell migration in the sea urchin embryo. 2015, Pubmed , Echinobase
Martik, New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus. 2017, Pubmed , Echinobase
Massri, Methodologies for Following EMT In Vivo at Single Cell Resolution. 2021, Pubmed , Echinobase
Materna, A comprehensive analysis of Delta signaling in pre-gastrular sea urchin embryos. 2012, Pubmed , Echinobase
McClay, Embryo dissociation, cell isolation, and cell reassociation. 1986, Pubmed , Echinobase
McClay, Evolutionary crossroads in developmental biology: sea urchins. 2011, Pubmed , Echinobase
McClay, Gastrulation in the sea urchin. 2020, Pubmed , Echinobase
McIntyre, Short-range Wnt5 signaling initiates specification of sea urchin posterior ectoderm. 2013, Pubmed , Echinobase
Nishida, macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. 2001, Pubmed
Nüsslein-Volhard, Mutations affecting segment number and polarity in Drosophila. 1980, Pubmed
Oliveri, A regulatory gene network that directs micromere specification in the sea urchin embryo. 2002, Pubmed , Echinobase
Oliveri, Activation of pmar1 controls specification of micromeres in the sea urchin embryo. 2003, Pubmed , Echinobase
Oliveri, Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. 2006, Pubmed , Echinobase
Oliveri, Global regulatory logic for specification of an embryonic cell lineage. 2008, Pubmed , Echinobase
Perillo, Regulation of dynamic pigment cell states at single-cell resolution. 2020, Pubmed , Echinobase
Peter, The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. 2010, Pubmed , Echinobase
Peter, A gene regulatory network controlling the embryonic specification of endoderm. 2011, Pubmed , Echinobase
Plass, Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. 2018, Pubmed
Rafiq, Genome-wide analysis of the skeletogenic gene regulatory network of sea urchins. 2014, Pubmed , Echinobase
Range, Maternal Oct1/2 is required for Nodal and Vg1/Univin expression during dorsal-ventral axis specification in the sea urchin embryo. 2011, Pubmed , Echinobase
Range, Integration of canonical and noncanonical Wnt signaling pathways patterns the neuroectoderm along the anterior-posterior axis of sea urchin embryos. 2013, Pubmed , Echinobase
Ransick, New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. 2002, Pubmed , Echinobase
Revilla-i-Domingo, A missing link in the sea urchin embryo gene regulatory network: hesC and the double-negative specification of micromeres. 2007, Pubmed , Echinobase
Rizzo, Identification and developmental expression of the ets gene family in the sea urchin (Strongylocentrotus purpuratus). 2006, Pubmed , Echinobase
Röttinger, FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis [corrected] and regulate gastrulation during sea urchin development. 2008, Pubmed , Echinobase
Saudemont, Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. 2010, Pubmed , Echinobase
Saunders, Sub-circuits of a gene regulatory network control a developmental epithelial-mesenchymal transition. 2014, Pubmed , Echinobase
Schiebinger, Optimal-Transport Analysis of Single-Cell Gene Expression Identifies Developmental Trajectories in Reprogramming. 2019, Pubmed
Sethi, Sequential signaling crosstalk regulates endomesoderm segregation in sea urchin embryos. 2012, Pubmed , Echinobase
Sherwood, LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. 1999, Pubmed , Echinobase
Slota, Identification of neural transcription factors required for the differentiation of three neuronal subtypes in the sea urchin embryo. 2018, Pubmed , Echinobase
Stenzel, The univin gene encodes a member of the transforming growth factor-beta superfamily with restricted expression in the sea urchin embryo. 1994, Pubmed , Echinobase
Svensson, Power analysis of single-cell RNA-sequencing experiments. 2017, Pubmed
Tintori, A Transcriptional Lineage of the Early C. elegans Embryo. 2016, Pubmed
Voronina, Vasa protein expression is restricted to the small micromeres of the sea urchin, but is inducible in other lineages early in development. 2008, Pubmed , Echinobase
Wagner, Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo. 2018, Pubmed
Yeger-Lotem, Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction. 2004, Pubmed
Ziegenhain, Comparative Analysis of Single-Cell RNA Sequencing Methods. 2017, Pubmed