The Establishment of Cell-Type Specific Gene Regulation in the Sea Urchin Embryo
Cell-fate commitment in metazoan development relies on precise gene regulatory programs. This study presents a comprehensive single-cell atlas of gene expression (scRNA-seq), nascent transcription (scSLAM-seq), and chromatin accessibility (scATAC-seq) in the purple sea urchin, Strongylocentrotus purpuratus, from early cleavage to pluteus larva stages. Our findings reveal a dynamic regulatory landscape with extensive usage of distal and intronic regulatory elements, which often exhibit cell-type-specific motifs and accessibility profiles that closely track gene expression. We identify a major wave of zygotic genome activation (ZGA) at the 128-cell stage, coinciding with the loss of developmental plasticity, alongside evidence of restricted, lineage-specific gene activation preceding widespread ZGA. Motif analysis highlights distinct regulatory grammars for these early accessible regions. Regulatory element usage largely clusters by germ layer, indicating shared accessibility among related cell types. We delve into the regulatory intricacies of neurons and skeletogenic cells. Sea urchin neurodevelopment proceeds through three distinct lineages, utilizing transcription factors with conserved roles in mammalian neurogenesis. Surprisingly, skeletogenic cells show significant transcriptional and regulatory diversity across their subpopulations, and we identify novel genes associated with calcification. This research offers unprecedented insights into the dynamic regulatory genome of a non-chordate deuterostome, highlighting both conserved principles of gene regulation and unique features that underscore the sea urchins importance as a model for understanding developmental and evolutionary genomics in ecologically critical marine species.