Abstract
The cranial neural crest generates a huge diversity of derivatives, including the bulk of connective and skeletal tissues of the vertebrate head. How neural crest cells acquire such extraordinary lineage potential remains unresolved. By integrating single-cell transcriptome and chromatin accessibility profiles of cranial neural crest-derived cells across the zebrafish lifetime, we observe progressive and region-specific establishment of enhancer accessibility for distinct fates. Neural crest-derived cells rapidly diversify into specialized progenitors, including multipotent skeletal progenitors, stromal cells with a regenerative signature, fibroblasts with a unique metabolic signature linked to skeletal integrity, and gill-specific progenitors generating cell types for respiration. By retrogradely mapping the emergence of lineage-specific chromatin accessibility, we identify a wealth of candidate lineage-priming factors, including a Gata3 regulatory circuit for respiratory cell fates. Rather than multilineage potential being established during cranial neural crest specification, our findings support progressive and region-specific chromatin remodeling underlying acquisition of diverse potential.
Highlights
The cranial neural crest generates a huge diversity of derivatives, including the bulk of connective and skeletal tissues of the vertebrate head
Posterior arch Cranial neural crest-derived cells (CNCCs) contribute to a distinct set of organs, including the thymus, parathyroid, and cardiac outflow tract, and in fishes cell types important for respiration, including specialized endothelial-like pillar cells that promote gas exchange[2]
We find that chromatin accessibility underlying multilineage potential is largely gained after CNCC migration, arguing against an epigenetic pre-pattern in premigratory CNCCs for diverse fate potential
Summary
The cranial neural crest generates a huge diversity of derivatives, including the bulk of connective and skeletal tissues of the vertebrate head. By integrating single-cell transcriptome and chromatin accessibility profiles of cranial neural crest-derived cells across the zebrafish lifetime, we observe progressive and region-specific establishment of enhancer accessibility for distinct fates. Individual avian CNCCs can generate multiple types of derivatives in vitro, including ectomesenchyme and neuroglial cells, suggesting multilineage potential is an intrinsic property[4]. Mesodermal cells can contribute to gill cartilage, a classically considered CNCC-derived structure, suggesting that, rather than cell potential being a unique intrinsic property of CNCCs, extrinsic cues from the local arch environment may induce similar cell fates in mesenchyme of diverse origins in certain contexts[9]. We find that chromatin accessibility underlying multilineage potential is largely gained after CNCC migration, arguing against an epigenetic pre-pattern in premigratory CNCCs for diverse fate potential
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