Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation

The epiblast of vertebrate embryos is comprised of neural and non-neural ectoderm, with the border territory at their intersection harboring neural crest and cranial placode progenitors. Here, we a generate single-cell atlas of the developing chick epiblast from late gastrulation through early neuru...

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Main Authors: Ruth M Williams, Martyna Lukoseviciute, Tatjana Sauka-Spengler, Marianne E Bronner
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/74464
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author Ruth M Williams
Martyna Lukoseviciute
Tatjana Sauka-Spengler
Marianne E Bronner
author_facet Ruth M Williams
Martyna Lukoseviciute
Tatjana Sauka-Spengler
Marianne E Bronner
author_sort Ruth M Williams
collection DOAJ
description The epiblast of vertebrate embryos is comprised of neural and non-neural ectoderm, with the border territory at their intersection harboring neural crest and cranial placode progenitors. Here, we a generate single-cell atlas of the developing chick epiblast from late gastrulation through early neurulation stages to define transcriptional changes in the emerging ‘neural plate border’ as well as other regions of the epiblast. Focusing on the border territory, the results reveal gradual establishment of heterogeneous neural plate border signatures, including novel genes that we validate by fluorescent in situ hybridization. Developmental trajectory analysis infers that segregation of neural plate border lineages only commences at early neurulation, rather than at gastrulation as previously predicted. We find that cells expressing the prospective neural crest marker Pax7 contribute to multiple lineages, and a subset of premigratory neural crest cells shares a transcriptional signature with their border precursors. Together, our results suggest that cells at the neural plate border remain heterogeneous until early neurulation, at which time progenitors become progressively allocated toward defined neural crest and placode lineages. The data also can be mined to reveal changes throughout the developing epiblast.
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spelling doaj.art-d85d940a3b544a908207c9b15c4b21702022-12-22T03:24:24ZengeLife Sciences Publications LtdeLife2050-084X2022-01-011110.7554/eLife.74464Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulationRuth M Williams0https://orcid.org/0000-0002-2628-7834Martyna Lukoseviciute1Tatjana Sauka-Spengler2https://orcid.org/0000-0001-9289-0263Marianne E Bronner3https://orcid.org/0000-0003-4274-1862California Institute of Technology, Division of Biology and Biological engineering, Pasadena, United States; University of Oxford, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, Oxford, United KingdomUniversity of Oxford, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, Oxford, United KingdomUniversity of Oxford, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, Oxford, United KingdomCalifornia Institute of Technology, Division of Biology and Biological engineering, Pasadena, United StatesThe epiblast of vertebrate embryos is comprised of neural and non-neural ectoderm, with the border territory at their intersection harboring neural crest and cranial placode progenitors. Here, we a generate single-cell atlas of the developing chick epiblast from late gastrulation through early neurulation stages to define transcriptional changes in the emerging ‘neural plate border’ as well as other regions of the epiblast. Focusing on the border territory, the results reveal gradual establishment of heterogeneous neural plate border signatures, including novel genes that we validate by fluorescent in situ hybridization. Developmental trajectory analysis infers that segregation of neural plate border lineages only commences at early neurulation, rather than at gastrulation as previously predicted. We find that cells expressing the prospective neural crest marker Pax7 contribute to multiple lineages, and a subset of premigratory neural crest cells shares a transcriptional signature with their border precursors. Together, our results suggest that cells at the neural plate border remain heterogeneous until early neurulation, at which time progenitors become progressively allocated toward defined neural crest and placode lineages. The data also can be mined to reveal changes throughout the developing epiblast.https://elifesciences.org/articles/74464neural plate borderneural crestsingle-cellplacodePax7chick
spellingShingle Ruth M Williams
Martyna Lukoseviciute
Tatjana Sauka-Spengler
Marianne E Bronner
Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
eLife
neural plate border
neural crest
single-cell
placode
Pax7
chick
title Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
title_full Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
title_fullStr Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
title_full_unstemmed Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
title_short Single-cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
title_sort single cell atlas of early chick development reveals gradual segregation of neural crest lineage from the neural plate border during neurulation
topic neural plate border
neural crest
single-cell
placode
Pax7
chick
url https://elifesciences.org/articles/74464
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AT tatjanasaukaspengler singlecellatlasofearlychickdevelopmentrevealsgradualsegregationofneuralcrestlineagefromtheneuralplateborderduringneurulation
AT marianneebronner singlecellatlasofearlychickdevelopmentrevealsgradualsegregationofneuralcrestlineagefromtheneuralplateborderduringneurulation