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Nat Ecol Evol
2022 Dec 01;612:1907-1920. doi: 10.1038/s41559-022-01906-9.
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Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins.
Davidson PL
,
Guo H
,
Swart JS
,
Massri AJ
,
Edgar A
,
Wang L
,
Berrio A
,
Devens HR
,
Koop D
,
Cisternas P
,
Zhang H
,
Zhang Y
,
Byrne M
,
Fan G
,
Wray GA
.
Abstract
Changes in developmental gene regulatory networks (dGRNs) underlie much of the diversity of life, but the evolutionary mechanisms that operate on regulatory interactions remain poorly understood. Closely related species with extreme phenotypic divergence provide a valuable window into the genetic and molecular basis for changes in dGRNs and their relationship to adaptive changes in organismal traits. Here we analyse genomes, epigenomes and transcriptomes during early development in two Heliocidaris sea urchin species that exhibit highly divergent life histories and in an outgroup species. Positive selection and chromatin accessibility modifications within putative regulatory elements are enriched on the branch leading to the derived life history, particularly near dGRN genes. Single-cell transcriptomes reveal a dramatic delay in cell fate specification in the derived state, which also has far fewer open chromatin regions, especially near conserved cell fate specification genes. Experimentally perturbing key transcription factors reveals profound evolutionary changes to early embryonic patterning events, disrupting regulatory interactions previously conserved for ~225 million years. These results demonstrate that natural selection can rapidly reshape developmental gene expression on a broad scale when selective regimes abruptly change. More broadly, even highly conserved dGRNs and patterning mechanisms in the early embryo remain evolvable under appropriate ecological circumstances.
Abrusán,
TEclass--a tool for automated classification of unknown eukaryotic transposable elements.
2009, Pubmed
Abrusán,
TEclass--a tool for automated classification of unknown eukaryotic transposable elements.
2009,
Pubmed
Becht,
Dimensionality reduction for visualizing single-cell data using UMAP.
2018,
Pubmed
Berrio,
Identifying branch-specific positive selection throughout the regulatory genome using an appropriate proxy neutral.
2020,
Pubmed
Blanchette,
Aligning multiple genomic sequences with the threaded blockset aligner.
2004,
Pubmed
Bolger,
Trimmomatic: a flexible trimmer for Illumina sequence data.
2014,
Pubmed
Brůna,
BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database.
2021,
Pubmed
Brůna,
GeneMark-EP+: eukaryotic gene prediction with self-training in the space of genes and proteins.
2020,
Pubmed
Buchfink,
Fast and sensitive protein alignment using DIAMOND.
2015,
Pubmed
Camacho,
BLAST+: architecture and applications.
2009,
Pubmed
Cameron,
Lineage and fate of each blastomere of the eight-cell sea urchin embryo.
1987,
Pubmed
,
Echinobase
Corces,
An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues.
2017,
Pubmed
Croce,
Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo.
2010,
Pubmed
,
Echinobase
Davidson,
Chromosomal-Level Genome Assembly of the Sea Urchin Lytechinus variegatus Substantially Improves Functional Genomic Analyses.
2020,
Pubmed
,
Echinobase
Davidson,
Evolutionary Changes in the Chromatin Landscape Contribute to Reorganization of a Developmental Gene Network During Rapid Life History Evolution in Sea Urchins.
2022,
Pubmed
,
Echinobase
Davidson,
Lineage-specific gene expression and the regulative capacities of the sea urchin embryo: a proposed mechanism.
1989,
Pubmed
,
Echinobase
Davidson,
Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms.
1998,
Pubmed
,
Echinobase
Dobin,
STAR: ultrafast universal RNA-seq aligner.
2013,
Pubmed
Dudchenko,
De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds.
2017,
Pubmed
Durand,
Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments.
2016,
Pubmed
Edgar,
Embryo microinjection of the lecithotrophic sea urchin Heliocidaris erythrogramma.
2019,
Pubmed
,
Echinobase
Emlet,
Larval spicules, cilia, and symmetry as remnants of indirect development in the direct developing sea urchin Heliocidaris erythrogramma.
1995,
Pubmed
,
Echinobase
Emms,
OrthoFinder: phylogenetic orthology inference for comparative genomics.
2019,
Pubmed
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
Flynn,
RepeatModeler2 for automated genomic discovery of transposable element families.
2020,
Pubmed
Gildor,
Comparative Study of Regulatory Circuits in Two Sea Urchin Species Reveals Tight Control of Timing and High Conservation of Expression Dynamics.
2015,
Pubmed
,
Echinobase
Haas,
Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments.
2008,
Pubmed
Hafemeister,
Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression.
2019,
Pubmed
Hinman,
Developmental gene regulatory network architecture across 500 million years of echinoderm evolution.
2003,
Pubmed
,
Echinobase
Hinrichs,
The UCSC Genome Browser Database: update 2006.
2006,
Pubmed
Huang,
HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly.
2017,
Pubmed
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
Koop,
Nodal and BMP expression during the transition to pentamery in the sea urchin Heliocidaris erythrogramma: insights into patterning the enigmatic echinoderm body plan.
2017,
Pubmed
,
Echinobase
Koren,
Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation.
2017,
Pubmed
Korsunsky,
Fast, sensitive and accurate integration of single-cell data with Harmony.
2019,
Pubmed
Li,
The Sequence Alignment/Map format and SAMtools.
2009,
Pubmed
Lomsadze,
Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm.
2014,
Pubmed
Love,
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
2014,
Pubmed
Lunter,
Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads.
2011,
Pubmed
Marçais,
A fast, lock-free approach for efficient parallel counting of occurrences of k-mers.
2011,
Pubmed
McClay,
Evolutionary crossroads in developmental biology: sea urchins.
2011,
Pubmed
,
Echinobase
Murrell,
Gene-wide identification of episodic selection.
2015,
Pubmed
O'Leary,
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation.
2016,
Pubmed
Oliveri,
Gene regulatory network controlling embryonic specification in the sea urchin.
2004,
Pubmed
,
Echinobase
Oliveri,
Global regulatory logic for specification of an embryonic cell lineage.
2008,
Pubmed
,
Echinobase
Oliveri,
Activation of pmar1 controls specification of micromeres in the sea urchin embryo.
2003,
Pubmed
,
Echinobase
Patro,
Salmon provides fast and bias-aware quantification of transcript expression.
2017,
Pubmed
Pond,
HyPhy: hypothesis testing using phylogenies.
2005,
Pubmed
Pryszcz,
Redundans: an assembly pipeline for highly heterozygous genomes.
2016,
Pubmed
Quinlan,
BEDTools: a flexible suite of utilities for comparing genomic features.
2010,
Pubmed
Raff,
Constraint, flexibility, and phylogenetic history in the evolution of direct development in sea urchins.
1987,
Pubmed
,
Echinobase
Raff,
Direct-developing sea urchins and the evolutionary reorganization of early development.
1992,
Pubmed
,
Echinobase
Raff,
The active evolutionary lives of echinoderm larvae.
2006,
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
Rho,
The control of foxN2/3 expression in sea urchin embryos and its function in the skeletogenic gene regulatory network.
2011,
Pubmed
,
Echinobase
Servant,
HiC-Pro: an optimized and flexible pipeline for Hi-C data processing.
2015,
Pubmed
Siepel,
Phylogenetic estimation of context-dependent substitution rates by maximum likelihood.
2004,
Pubmed
Stanke,
Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources.
2006,
Pubmed
Storer,
The Dfam community resource of transposable element families, sequence models, and genome annotations.
2021,
Pubmed
Vurture,
GenomeScope: fast reference-free genome profiling from short reads.
2017,
Pubmed
Walker,
Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement.
2014,
Pubmed
Wang,
Genetic basis for divergence in developmental gene expression in two closely related sea urchins.
2020,
Pubmed
,
Echinobase
Wilson,
Dissociation of expression patterns of homeodomain transcription factors in the evolution of developmental mode in the sea urchins Heliocidaris tuberculata and H. erythrogramma.
2005,
Pubmed
,
Echinobase
Wong,
RepeatCraft: a meta-pipeline for repetitive element de-fragmentation and annotation.
2019,
Pubmed
Wray,
Evolutionary modification of cell lineage in the direct-developing sea urchin Heliocidaris erythrogramma.
1989,
Pubmed
,
Echinobase
Wray,
Novel origins of lineage founder cells in the direct-developing sea urchin Heliocidaris erythrogramma.
1990,
Pubmed
,
Echinobase
Wu,
The Snail repressor is required for PMC ingression in the sea urchin embryo.
2007,
Pubmed
,
Echinobase
Yamazaki,
Expession patterns of mesenchyme specification genes in two distantly related echinoids, Glyptocidaris crenularis and Echinocardium cordatum.
2015,
Pubmed
,
Echinobase
Zhang,
Model-based analysis of ChIP-Seq (MACS).
2008,
Pubmed