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Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans

Animals increase by orders of magnitude in volume during development. Therefore, small variations in growth rates among individuals could amplify to a large heterogeneity in size. By live imaging of C. elegans, we show that amplification of size heterogeneity is prevented by an inverse coupling of t...

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Autores principales: Stojanovski, Klement, Großhans, Helge, Towbin, Benjamin D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9170734/
https://www.ncbi.nlm.nih.gov/pubmed/35668054
http://dx.doi.org/10.1038/s41467-022-29720-8
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author Stojanovski, Klement
Großhans, Helge
Towbin, Benjamin D.
author_facet Stojanovski, Klement
Großhans, Helge
Towbin, Benjamin D.
author_sort Stojanovski, Klement
collection PubMed
description Animals increase by orders of magnitude in volume during development. Therefore, small variations in growth rates among individuals could amplify to a large heterogeneity in size. By live imaging of C. elegans, we show that amplification of size heterogeneity is prevented by an inverse coupling of the volume growth rate to the duration of larval stages and does not involve strict size thresholds for larval moulting. We perturb this coupling by changing the developmental tempo through manipulation of a transcriptional oscillator that controls the duration of larval development. As predicted by a mathematical model, this perturbation alters the body volume. Model analysis shows that an inverse relation between the period length and the growth rate is an intrinsic property of genetic oscillators and can occur independently of additional complex regulation. This property of genetic oscillators suggests a parsimonious mechanism that counteracts the amplification of size differences among individuals during development.
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spelling pubmed-91707342022-06-08 Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans Stojanovski, Klement Großhans, Helge Towbin, Benjamin D. Nat Commun Article Animals increase by orders of magnitude in volume during development. Therefore, small variations in growth rates among individuals could amplify to a large heterogeneity in size. By live imaging of C. elegans, we show that amplification of size heterogeneity is prevented by an inverse coupling of the volume growth rate to the duration of larval stages and does not involve strict size thresholds for larval moulting. We perturb this coupling by changing the developmental tempo through manipulation of a transcriptional oscillator that controls the duration of larval development. As predicted by a mathematical model, this perturbation alters the body volume. Model analysis shows that an inverse relation between the period length and the growth rate is an intrinsic property of genetic oscillators and can occur independently of additional complex regulation. This property of genetic oscillators suggests a parsimonious mechanism that counteracts the amplification of size differences among individuals during development. Nature Publishing Group UK 2022-06-06 /pmc/articles/PMC9170734/ /pubmed/35668054 http://dx.doi.org/10.1038/s41467-022-29720-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Stojanovski, Klement
Großhans, Helge
Towbin, Benjamin D.
Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans
title Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans
title_full Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans
title_fullStr Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans
title_full_unstemmed Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans
title_short Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans
title_sort coupling of growth rate and developmental tempo reduces body size heterogeneity in c. elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9170734/
https://www.ncbi.nlm.nih.gov/pubmed/35668054
http://dx.doi.org/10.1038/s41467-022-29720-8
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