Multiscale analysis reveals that diet-dependent midgut plasticity emerges from alterations in both stem cell niche coupling and enterocyte size

  1. Alessandro Bonfini
  2. Adam J Dobson
  3. David Duneau
  4. Jonathan Revah
  5. Xi Liu
  6. Philip Houtz
  7. Nicolas Buchon  Is a corresponding author
  1. Cornell University, United States
  2. University of Glasgow, United Kingdom
  3. CNRS, UMR5174 EDB (Laboratoire Évolution and Diversité Biologique, France

Abstract

The gut is the primary interface between an animal and food, but how it adapts to qualitative dietary variation is poorly defined. We find that the Drosophila midgut plastically resizes following changes in dietary composition. A panel of nutrients collectively promote gut growth, which sugar opposes. Diet influences absolute and relative levels of enterocyte loss and stem cell proliferation, which together determine cell numbers. Diet also influences enterocyte size. A high sugar diet inhibits translation and uncouples ISC proliferation from expression of niche-derived signals but, surprisingly, rescuing these effects genetically was not sufficient to modify diet's impact on midgut size. However, when stem cell proliferation was deficient, diet's impact on enterocyte size was enhanced, and reducing enterocyte-autonomous TOR signaling was sufficient to attenuate diet-dependent midgut resizing. These data clarify the complex relationships between nutrition, epithelial dynamics, and cell size, and reveal a new mode of plastic, diet-dependent organ resizing.

Data availability

Data have been submitted with an ArrayExpress accession E-MTAB-10812.

Article and author information

Author details

  1. Alessandro Bonfini

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6642-8665
  2. Adam J Dobson

    Molecular Cell & Systems Biology, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1541-927X
  3. David Duneau

    CNRS, UMR5174 EDB (Laboratoire Évolution and Diversité Biologique, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8323-1511
  4. Jonathan Revah

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Xi Liu

    Cornell Institute of Host-Microbe Interactions and Disease, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Philip Houtz

    Cornell Institute of Host-Microbe Interactions and Disease, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Nicolas Buchon

    Department of Entomology, Cornell University, Ithaca, United States
    For correspondence
    nicolas.buchon@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3636-8387

Funding

National Institutes of Health (1R21AG065733-01,1R01AI148541-01A1)

  • Alessandro Bonfini
  • Jonathan Revah
  • Xi Liu
  • Philip Houtz
  • Nicolas Buchon

National Science Foundation (IOS-1656118,IOS-1653021)

  • Alessandro Bonfini
  • Jonathan Revah
  • Xi Liu
  • Philip Houtz
  • Nicolas Buchon

UK Research and Innovation (MR/S033939/1)

  • Adam J Dobson

Agence Nationale de la Recherche (ANR-10-LABX-41; ANR-11-IDEX-0002-02)

  • David Duneau

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Lucy Erin O'Brien, Stanford University School of Medicine, United States

Version history

  1. Received: December 16, 2020
  2. Accepted: September 22, 2021
  3. Accepted Manuscript published: September 23, 2021 (version 1)
  4. Version of Record published: October 19, 2021 (version 2)

Copyright

© 2021, Bonfini et al.

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.

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  1. Alessandro Bonfini
  2. Adam J Dobson
  3. David Duneau
  4. Jonathan Revah
  5. Xi Liu
  6. Philip Houtz
  7. Nicolas Buchon
(2021)
Multiscale analysis reveals that diet-dependent midgut plasticity emerges from alterations in both stem cell niche coupling and enterocyte size
eLife 10:e64125.
https://doi.org/10.7554/eLife.64125

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https://doi.org/10.7554/eLife.64125

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