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Maintenance of appropriate size scaling of the C. elegans pharynx by YAP-1

Author

Listed:
  • Klement Stojanovski

    (University of Bern)

  • Ioana Gheorghe

    (University of Bern
    University of Bern)

  • Peter Lenart

    (University of Bern)

  • Anne Lanjuin

    (Harvard TH Chan School of Public Health)

  • William B. Mair

    (Harvard TH Chan School of Public Health)

  • Benjamin D. Towbin

    (University of Bern)

Abstract

Even slight imbalance between the growth rate of different organs can accumulate to a large deviation from their appropriate size during development. Here, we use live imaging of the pharynx of C. elegans to ask if and how organ size scaling nevertheless remains uniform among individuals. Growth trajectories of hundreds of individuals reveal that pharynxes grow by a near constant volume per larval stage that is independent of their initial size, such that undersized pharynxes catch-up in size during development. Tissue-specific depletion of RAGA-1, an activator of mTOR and growth, shows that maintaining correct pharynx-to-body size proportions involves a bi-directional coupling between pharynx size and body growth. In simulations, this coupling cannot be explained by limitation of food uptake alone, and genetic experiments reveal an involvement of the mechanotransducing transcriptional co-regulator yap-1. Our data suggests that mechanotransduction coordinates pharynx growth with other tissues, ensuring body plan uniformity among individuals.

Suggested Citation

  • Klement Stojanovski & Ioana Gheorghe & Peter Lenart & Anne Lanjuin & William B. Mair & Benjamin D. Towbin, 2023. "Maintenance of appropriate size scaling of the C. elegans pharynx by YAP-1," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43230-1
    DOI: 10.1038/s41467-023-43230-1
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    1. Clotilde Cadart & Sylvain Monnier & Jacopo Grilli & Pablo J. Sáez & Nishit Srivastava & Rafaele Attia & Emmanuel Terriac & Buzz Baum & Marco Cosentino-Lagomarsino & Matthieu Piel, 2018. "Size control in mammalian cells involves modulation of both growth rate and cell cycle duration," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    2. Geoffrey B. West & James H. Brown & Brian J. Enquist, 1997. "A General Model for the Origin of Allometric Scaling Laws in Biology," Working Papers 97-03-019, Santa Fe Institute.
    3. Nicola Gritti & Simone Kienle & Olga Filina & Jeroen Sebastiaan van Zon, 2016. "Long-term time-lapse microscopy of C. elegans post-embryonic development," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
    4. Ravi S. Kamath & Andrew G. Fraser & Yan Dong & Gino Poulin & Richard Durbin & Monica Gotta & Alexander Kanapin & Nathalie Le Bot & Sergio Moreno & Marc Sohrmann & David P. Welchman & Peder Zipperlen &, 2003. "Systematic functional analysis of the Caenorhabditis elegans genome using RNAi," Nature, Nature, vol. 421(6920), pages 231-237, January.
    5. Fisun Hamaratoglu & Aitana Morton de Lachapelle & George Pyrowolakis & Sven Bergmann & Markus Affolter, 2011. "Dpp Signaling Activity Requires Pentagone to Scale with Tissue Size in the Growing Drosophila Wing Imaginal Disc," PLOS Biology, Public Library of Science, vol. 9(10), pages 1-17, October.
    6. Klement Stojanovski & Helge Großhans & Benjamin D. Towbin, 2022. "Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Brad T Moore & James M Jordan & L Ryan Baugh, 2013. "WormSizer: High-throughput Analysis of Nematode Size and Shape," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-13, February.
    8. Emilie Boone & Julien Colombani & Ditte S. Andersen & Pierre Léopold, 2016. "The Hippo signalling pathway coordinates organ growth and limits developmental variability by controlling dilp8 expression," Nature Communications, Nature, vol. 7(1), pages 1-8, December.
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