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Evolution of the new head by gradual acquisition of neural crest regulatory circuits

Martik, Megan L. and Ghandi, Shashank and Uy, Benjamin R. and Gillis, J. Andrew and Green, Stephen A. and Simões-Costa, Marcos and Bronner, Marianne E. (2019) Evolution of the new head by gradual acquisition of neural crest regulatory circuits. Nature, 574 (7780). pp. 675-678. ISSN 0028-0836. https://resolver.caltech.edu/CaltechAUTHORS:20190916-095004029

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[img] MS Word (Supplementary Table 1 - Alignment percentage scores for lamprey/chicken alignments) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 1: Heterochronic shifts of cranial specific gene regulatory nodes from later neural crest derivatives to an early specification program throughout gnathostome evolution) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 2: P. marinus Dmbx is homologous to gnathostome Dmbx genes) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 3: Expression of cranial circuit genes in the neural crest of the little skate) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 4: Pharyngeal neural crest derivative expression of cranial circuit orthologues in stage 25 L. erinacea embryos) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 5: Expression of cranial circuit genes in the NC of the zebrafish) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 6: Expression of cranial circuit orthologues in pharyngeal NC derivatives of D. rerio embryos at 3 days post fertilization) - Supplemental Material
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Abstract

The neural crest, an embryonic stem-cell population, is a vertebrate innovation that has been proposed to be a key component of the ‘new head’, which imbued vertebrates with predatory behaviour. Here, to investigate how the evolution of neural crest cells affected the vertebrate body plan, we examined the molecular circuits that control neural crest development along the anteroposterior axis of a jawless vertebrate, the sea lamprey. Gene expression analysis showed that the cranial subpopulation of the neural crest of the lamprey lacks most components of a transcriptional circuit that is specific to the cranial neural crest in amniotes and confers the ability to form craniofacial cartilage onto non-cranial neural crest subpopulations3. Consistent with this, hierarchical clustering analysis revealed that the transcriptional profile of the lamprey cranial neural crest is more similar to the trunk neural crest of amniotes. Notably, analysis of the cranial neural crest in little skate and zebrafish embryos demonstrated that the transcriptional circuit that is specific to the cranial neural crest emerged via the gradual addition of network components to the neural crest of gnathostomes, which subsequently became restricted to the cephalic region. Our results indicate that the ancestral neural crest at the base of the vertebrate lineage possessed a trunk-like identity. We propose that the emergence of the cranial neural crest, by progressive assembly of an axial-specific regulatory circuit, allowed the elaboration of the new head during vertebrate evolution.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41586-019-1691-4DOIArticle
https://rdcu.be/bV7sKPublisherFree ReadCube access
ORCID:
AuthorORCID
Martik, Megan L.0000-0003-1186-4085
Uy, Benjamin R.0000-0003-0438-880X
Simões-Costa, Marcos0000-0003-1452-7068
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2019 Springer Nature Limited. Received 22 October 2018; Accepted 26 September 2019; Published 23 October 2019. Data availability: All raw sequencing data for all RNA-seq libraries (Fig. 3) and merged reference transcriptomes are available online (NCBI BioProject# PRJNA497902). Sequences of in situ probe templates for Figs. 1b, c, 2a, c are available through GenBank accession codes (see Methods). Code availability: Code used to analyse sequencing datasets are available from the corresponding author upon request. We thank J. Tan-Cabugao and E. Grossman for technical assistance; D. Mayorga and R. Fraser for help with fish husbandry; B. Martik for illustrating the adult animals for our expression matrices; the Caltech Millard and Muriel Jacobs Genetics and Genomics Laboratory and in particular I. Antoshechkin for sequencing of our RNA-seq libraries; and R. Diamond, J. Tijerina, D. Perez, and P. Cannon of the The Caltech Flow Cytometry Cell Sorting Facility for cell sorting assistance. This work is supported by NIH grants R01NS086907, R01DE024157, and R35NS111564 to M.E.B. M.L.M. is supported by a Helen Hay Whitney Foundation postdoctoral fellowship. S.G. is supported by a graduate fellowship from the American Heart Association (18PRE34050063). Author Contributions: Project and analysis conception were designed by M.L.M., M.S.-C., and M.E.B. Writing and interpretation were performed by M.L.M., S.G., B.R.U., J.A.G., S.A.G., M.S.-C., and M.E.B. Lamprey orthologue cloning and all in situ hybridization, imaging, and analysis were performed by M.L.M. Bioinformatics and chicken RNA-seq were performed by S.G. Phylogenetic analysis and lamprey embryo acquisition were performed by S.A.G. Cloning of skate orthologues and skate embryo acquisition were performed by J.A.G. Lamprey embryo dissections and library preparations were performed by B.R.U. and M.S.C. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
NIHR01NS086907
NIHR01DE024157
NIHR35NS111564
Helen Hay Whitney FoundationUNSPECIFIED
American Heart Association18PRE34050063
Subject Keywords:Embryology; Evolutionary developmental biology
Issue or Number:7780
Record Number:CaltechAUTHORS:20190916-095004029
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190916-095004029
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:98650
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:23 Oct 2019 17:26
Last Modified:04 Nov 2019 23:27

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