Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock

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Abstract

In vertebrate development, the sequential and rhythmic segmentation of the body axis is regulated by a 'segmentation clock.' This clock is comprised of a population of coordinated oscillating cells that together produce rhythmic gene expression patterns in the embryo. Whether individual cells autonomously maintain oscillations, or whether oscillations depend on signals from neighboring cells is unknown. Using a transgenic zebrafish reporter line for the cyclic transcription factor Her1, we recorded single tailbud cells in vitro. We demonstrate that individual cells can behave as autonomous cellular oscillators. We described the observed variability in cell behavior using a theory of generic oscillators with correlated noise. Single cells have longer periods and lower precision than the tissue, highlighting the role of collective processes in the segmentation clock. Our work reveals a population of cells from the zebrafish segmentation clock that behave as self-sustained, autonomous oscillators with distinctive noisy dynamics.

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Alexis B Webb

The Francis Crick Institute, London, United Kingdom

Competing interests
No competing interests declared.
Iván M Lengyel

Departamento de Física, FCEyN UBA and IFIBA, CONICET, Buenos Aires, Argentina

Competing interests
No competing interests declared.
David J Jörg

Max Planck Institute for the Physics of Complex Systems, Dresden, Germany

Competing interests
No competing interests declared.
Guillaume Valentin

Genoway, Lyon, France

Competing interests
No competing interests declared.
Frank Jülicher

Max Planck Institute for the Physics of Complex Systems, Dresden, Germany

Competing interests
Frank Jülicher, Reviewing editor, eLife.
Luis G Morelli

Departamento de Física, FCEyN UBA and IFIBA, CONICET, Buenos Aires, Argentina

Competing interests
No competing interests declared.
Andrew C Oates

Mill Hill Laboratory, The Francis Crick Institute, London, United Kingdom

For correspondence
andrew.oates@crick.ac.uk

Competing interests
No competing interests declared.

Ethics

Animal experimentation: Zebrafish experimentation was carried out in strict accordance with the ethics and regulations of the Saxonian Ministry of the Environment and Agriculture in Germany under licence Az. 74-9165.40-9-2001, and the Home Office in the United Kingdom under project licence PPL No. 70/7675.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.