Shared evolutionary origin of vertebrate neural crest and cranial placodes.

TitleShared evolutionary origin of vertebrate neural crest and cranial placodes.
Publication TypeJournal Article
Year of Publication2018
AuthorsHorie, R, Hazbun, A, Chen, K, Cao, C, Levine, M, Horie, T
JournalNature
Volume560
Issue7717
Pagination228-232
Date Published2018 08
ISSN1476-4687
KeywordsAnimals, Base Sequence, Biological Evolution, Cell Lineage, Ciona, Ectoderm, Gonadotropin-Releasing Hormone, Larva, Neural Crest, Neural Plate, Single-Cell Analysis, Vertebrates, Xenopus
Abstract

<p>Placodes and neural crests represent defining features of vertebrates, yet their relationship remains unclear despite extensive investigation. Here we use a combination of lineage tracing, gene disruption and single-cell RNA-sequencing assays to explore the properties of the lateral plate ectoderm of the proto-vertebrate, Ciona intestinalis. There are notable parallels between the patterning of the lateral plate in Ciona and the compartmentalization of the neural plate ectoderm in vertebrates. Both systems exhibit sequential patterns of Six1/2, Pax3/7 and Msxb expression that depend on a network of interlocking regulatory interactions. In Ciona, this compartmentalization network produces distinct but related types of sensory cells that share similarities with derivatives of both cranial placodes and the neural crest in vertebrates. Simple genetic disruptions result in the conversion of one sensory cell type into another. We focused on bipolar tail neurons, because they arise from the tail regions of the lateral plate and possess properties of the dorsal root ganglia, a derivative of the neural crest in vertebrates. Notably, bipolar tail neurons were readily transformed into palp sensory cells, a proto-placodal sensory cell type that arises from the anterior-most regions of the lateral plate in the Ciona tadpole. Proof of transformation was confirmed by whole-embryo single-cell RNA-sequencing assays. These findings suggest that compartmentalization of the lateral plate ectoderm preceded the advent of vertebrates, and served as a common source for the evolution of both cranial placodes and neural crest.</p>

DOI10.1038/s41586-018-0385-7
Alternate JournalNature
PubMed ID30069052
PubMed Central IDPMC6390964
Grant ListR01 NS076542 / NS / NINDS NIH HHS / United States