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Single-cell morphometrics reveals ancestral principles of notochord development

Embryonic tissues are shaped by the dynamic behaviours of their constituent cells. To understand such cell behaviours and how they evolved, new approaches are needed to map out morphogenesis across different organisms. Here, we apply a quantitative approach to learn how the notochord forms during th...

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Autores principales: Andrews, Toby G. R., Pönisch, Wolfram, Paluch, Ewa K., Steventon, Benjamin J., Benito-Gutierrez, Elia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8406538/
https://www.ncbi.nlm.nih.gov/pubmed/34343262
http://dx.doi.org/10.1242/dev.199430
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author Andrews, Toby G. R.
Pönisch, Wolfram
Paluch, Ewa K.
Steventon, Benjamin J.
Benito-Gutierrez, Elia
author_facet Andrews, Toby G. R.
Pönisch, Wolfram
Paluch, Ewa K.
Steventon, Benjamin J.
Benito-Gutierrez, Elia
author_sort Andrews, Toby G. R.
collection PubMed
description Embryonic tissues are shaped by the dynamic behaviours of their constituent cells. To understand such cell behaviours and how they evolved, new approaches are needed to map out morphogenesis across different organisms. Here, we apply a quantitative approach to learn how the notochord forms during the development of amphioxus: a basally branching chordate. Using a single-cell morphometrics pipeline, we quantify the geometries of thousands of amphioxus notochord cells, and project them into a common mathematical space, termed morphospace. In morphospace, notochord cells disperse into branching trajectories of cell shape change, revealing a dynamic interplay between cell shape change and growth that collectively contributes to tissue elongation. By spatially mapping these trajectories, we identify conspicuous regional variation, both in developmental timing and trajectory topology. Finally, we show experimentally that, unlike ascidians but like vertebrates, posterior cell division is required in amphioxus to generate full notochord length, thereby suggesting this might be an ancestral chordate trait that is secondarily lost in ascidians. Altogether, our novel approach reveals that an unexpectedly complex scheme of notochord morphogenesis might have been present in the first chordates. This article has an associated ‘The people behind the papers’ interview.
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spelling pubmed-84065382021-09-09 Single-cell morphometrics reveals ancestral principles of notochord development Andrews, Toby G. R. Pönisch, Wolfram Paluch, Ewa K. Steventon, Benjamin J. Benito-Gutierrez, Elia Development Research Article Embryonic tissues are shaped by the dynamic behaviours of their constituent cells. To understand such cell behaviours and how they evolved, new approaches are needed to map out morphogenesis across different organisms. Here, we apply a quantitative approach to learn how the notochord forms during the development of amphioxus: a basally branching chordate. Using a single-cell morphometrics pipeline, we quantify the geometries of thousands of amphioxus notochord cells, and project them into a common mathematical space, termed morphospace. In morphospace, notochord cells disperse into branching trajectories of cell shape change, revealing a dynamic interplay between cell shape change and growth that collectively contributes to tissue elongation. By spatially mapping these trajectories, we identify conspicuous regional variation, both in developmental timing and trajectory topology. Finally, we show experimentally that, unlike ascidians but like vertebrates, posterior cell division is required in amphioxus to generate full notochord length, thereby suggesting this might be an ancestral chordate trait that is secondarily lost in ascidians. Altogether, our novel approach reveals that an unexpectedly complex scheme of notochord morphogenesis might have been present in the first chordates. This article has an associated ‘The people behind the papers’ interview. The Company of Biologists Ltd 2021-08-19 /pmc/articles/PMC8406538/ /pubmed/34343262 http://dx.doi.org/10.1242/dev.199430 Text en © 2021. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Andrews, Toby G. R.
Pönisch, Wolfram
Paluch, Ewa K.
Steventon, Benjamin J.
Benito-Gutierrez, Elia
Single-cell morphometrics reveals ancestral principles of notochord development
title Single-cell morphometrics reveals ancestral principles of notochord development
title_full Single-cell morphometrics reveals ancestral principles of notochord development
title_fullStr Single-cell morphometrics reveals ancestral principles of notochord development
title_full_unstemmed Single-cell morphometrics reveals ancestral principles of notochord development
title_short Single-cell morphometrics reveals ancestral principles of notochord development
title_sort single-cell morphometrics reveals ancestral principles of notochord development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8406538/
https://www.ncbi.nlm.nih.gov/pubmed/34343262
http://dx.doi.org/10.1242/dev.199430
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