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Physical constraints on growth dynamics guide C. elegans developmental trajectories and animal shape

View ORCID ProfileJoy Nyaanga, View ORCID ProfileChristina Goss, View ORCID ProfileGaotian Zhang, Hannah N. Ahmed, Elliot J. Andersen, Isabella R. Miller, Justine K. Rozenich, Iris L. Swarthout, Jordan A. Vaughn, View ORCID ProfileErik C. Andersen, View ORCID ProfileNiall M. Mangan, View ORCID ProfileSasha Shirman
doi: https://doi.org/10.1101/2021.04.01.438121
Joy Nyaanga
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
2Interdisciplinary Biological Sciences Program, Northwestern University, Evanston, IL 60208, USA
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  • ORCID record for Joy Nyaanga
Christina Goss
3Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL 60208, USA
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  • ORCID record for Christina Goss
Gaotian Zhang
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Hannah N. Ahmed
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Elliot J. Andersen
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Isabella R. Miller
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Justine K. Rozenich
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Iris L. Swarthout
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Jordan A. Vaughn
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Erik C. Andersen
1Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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  • ORCID record for Erik C. Andersen
Niall M. Mangan
3Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL 60208, USA
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Sasha Shirman
3Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL 60208, USA
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  • ORCID record for Sasha Shirman
  • For correspondence: shirman.sasha@gmail.com
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Abstract

Growth control is essential to establish organism size, so organisms must have mechanisms to both sense and adjust growth. Studies of single cells have revealed that size homeostasis can be achieved using distinct control methods: Sizer, Timer, and Adder. In multicellular organisms, mechanisms that regulate body size must not only control single cell growth but also integrate it across organs and tissues during development to generate adult size and shape. To investigate body size and growth control in metazoans, we can leverage the roundworm Caenorhabditis elegans as a scalable and tractable model. We collected precise growth measurements of thousands of individuals throughout larval development, measured feeding behavior to pinpoint larval transitions, and quantified highly accurate changes in animal size and shape during development. We find differences in the growth of animal length and width during larval transitions. Using a combination of quantitative measurements and mathematical modeling, we present two physical mechanisms by which C. elegans can control growth. First, constraints on cuticle stretch generate mechanical signals through which animals sense body size and initiate larval-stage transitions. Second, mechanical control of food intake drives growth rate within larval stages, but between stages, regulatory mechanisms influence growth. These results suggest how physical constraints control developmental timing and growth rate in C. elegans.

Author summary Precise growth control is essential to the development of proper adult body size and shape. Although a larger body size can increase an organism’s competitive advantage, an increased body size also requires added time and nutrients to develop. As such, organisms must have mechanisms to both sense and adjust growth during development. Studies of single cells have revealed that proper body size can be achieved using size or time control mechanisms. In multicellular organisms, additional levels of control are required as growth must be differentially regulated across cells, tissues, and organs. We leveraged the roundworm Caenorhabditis elegans as a scalable model to investigate growth control in metazoans. As animals transitioned from one developmental stage to the next, we observed changes in body shape while body size remained constant, suggesting that animals might sense shape to set developmental timing. Two mechanisms likely control growth rate, physical control of feeding rate and metabolic regulation, and we are able to identify developmental periods where each govern growth. Our results demonstrate how physical constraints in tandem with other regulation can be used to broadly control developmental timing and growth rate across diverse organisms.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Funding: For this work, J.N., C.G., G.Z., E.C.A., N.M.M, and S.S. received support from the NSF-Simons Center for Quantitative Biology at Northwestern University (awards Simons Foundation/SFARI 597491-RWC and the National Science Foundation 1764421). C.G., S.S., and N.M.M. received support from the National Science Foundation RTG: Interdisciplinary Training in Quantitative Biological Modeling, award 1547394). C.G. was supported in part by the Murphy Scholars Program of the Robert R. McCormick School of Engineering and Applied Science at Northwestern University.

  • Competing interests: The authors have no competing interests.

  • Emails and ORCIDs:

    JN: JoyNyaanga2024{at}u.northwestern.edu

    CG: christinagoss2021{at}u.northwestern.edu

    GZ: gaotian.zhang{at}northwestern.edu

    HNA: hannahahmed02{at}gmail.com

    EJA: elliotjandersen{at}gmail.com

    IRM: miller.ir18{at}gmail.com

    JKR: justine.rozenich{at}icloud.com

    ILS: IrisSwarthout2023{at}u.northwestern.edu

    JAV: JordanVaughn2023{at}u.northwestern.edu

    ECA: erik.andersen{at}gmail.com

    NMM: niallmm{at}gmail.com

    SS: shirman.sasha{at}gmail.com

  • https://github.com/AndersenLab/C.elegans-growth-manuscript

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 4.0 International license.
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Posted April 02, 2021.
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Physical constraints on growth dynamics guide C. elegans developmental trajectories and animal shape
Joy Nyaanga, Christina Goss, Gaotian Zhang, Hannah N. Ahmed, Elliot J. Andersen, Isabella R. Miller, Justine K. Rozenich, Iris L. Swarthout, Jordan A. Vaughn, Erik C. Andersen, Niall M. Mangan, Sasha Shirman
bioRxiv 2021.04.01.438121; doi: https://doi.org/10.1101/2021.04.01.438121
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Physical constraints on growth dynamics guide C. elegans developmental trajectories and animal shape
Joy Nyaanga, Christina Goss, Gaotian Zhang, Hannah N. Ahmed, Elliot J. Andersen, Isabella R. Miller, Justine K. Rozenich, Iris L. Swarthout, Jordan A. Vaughn, Erik C. Andersen, Niall M. Mangan, Sasha Shirman
bioRxiv 2021.04.01.438121; doi: https://doi.org/10.1101/2021.04.01.438121

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