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Single-cell morphometrics reveals ancestral principles of notochord development

View ORCID ProfileToby G R Andrews, Wolfram Pönisch, Ewa Paluch, Benjamin J Steventon, View ORCID ProfileElia Benito-Gutierrez
doi: https://doi.org/10.1101/2020.07.08.193813
Toby G R Andrews
1Department of Zoology, University of Cambridge, United Kingdom
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Wolfram Pönisch
2Department of Physiology, Development and Neuroscience, University of Cambridge, United Kingdom
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Ewa Paluch
2Department of Physiology, Development and Neuroscience, University of Cambridge, United Kingdom
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Benjamin J Steventon
3Department of Genetics, University of Cambridge, United Kingdom
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Elia Benito-Gutierrez
1Department of Zoology, University of Cambridge, United Kingdom
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  • For correspondence: eb647@cam.ac.uk
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ABSTRACT

During development, embryonic tissues are formed by the dynamic behaviours of their constituent cells, whose collective actions are tightly regulated in space and time. To understand such cell behaviours and how they have evolved, it is necessary to develop quantitative approaches to map out morphogenesis, so comparisons can be made across different tissues and organisms. With this idea in mind, here we sought to investigate ancestral principles of notochord development, by building a quantitative portrait of notochord morphogenesis in the amphioxus embryo – a basally-branching member of the chordate phylum. To this end, we developed a single-cell morphometrics pipeline to comprehensively catalogue the morphologies of thousands of notochord cells, and to project them simultaneously into a common mathematical space termed morphospace. This approach revealed complex patterns of cell-type specific shape trajectories, akin to those obtained using single-cell genomic approaches. By spatially mapping single-cell shape trajectories in whole segmented notochords, we found evidence of spatial and temporal variation in developmental dynamics. Such variations included temporal gradients of morphogenesis spread across the anterior-posterior axis, divergence of trajectories to different morphologies, and the convergence of different trajectories onto common morphologies. Through geometric modelling, we also identified an antagonistic relationship between cell shape regulation and growth that enables convergent extension to occur in two steps. First, by allowing growth to counterbalance loss of anterior-posterior cell length during cell intercalation. Secondly, by allowing growth to further increase cell length once cells have intercalated and aligned to the axial midline, thereby facilitating a second phase of tissue elongation. Finally, we show that apart from a complex coordination of individual cellular behaviours, posterior addition from proliferating progenitors is essential for full notochord elongation in amphioxus, a mechanism previously described only in vertebrates. This novel approach to quantifying morphogenesis paves the way towards comparative studies, and mechanistic explanations for the emergence of form over developmental and evolutionary time scales.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted July 30, 2020.
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Single-cell morphometrics reveals ancestral principles of notochord development
Toby G R Andrews, Wolfram Pönisch, Ewa Paluch, Benjamin J Steventon, Elia Benito-Gutierrez
bioRxiv 2020.07.08.193813; doi: https://doi.org/10.1101/2020.07.08.193813
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Single-cell morphometrics reveals ancestral principles of notochord development
Toby G R Andrews, Wolfram Pönisch, Ewa Paluch, Benjamin J Steventon, Elia Benito-Gutierrez
bioRxiv 2020.07.08.193813; doi: https://doi.org/10.1101/2020.07.08.193813

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