1. Computational and Systems Biology
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Distributing tasks via multiple input pathways increase cellular survival in stress

  1. Alejandro A Granados
  2. Matthew M Crane
  3. Luis F Montano-Gutierrez
  4. Reiko J Tanaka
  5. Margaritis Voliotis
  6. Peter Swain  Is a corresponding author
  1. University of Edinburgh, United Kingdom
  2. Imperial College London, United Kingdom
  3. University of Exeter, United Kingdom
Research Article
  • Cited 21
  • Views 1,951
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Cite this article as: eLife 2017;6:e21415 doi: 10.7554/eLife.21415

Abstract

Improving in one aspect of a task can undermine performance in another, but how such opposing demands play out in single cells and impact on fitness is mostly unknown. Here we study budding yeast in dynamic environments of hyperosmotic stress and show how the corresponding signalling network increases cellular survival both by assigning the requirements of high response speed and high response accuracy to two separate input pathways and by having these pathways interact to converge on Hog1, a p38 MAP kinase. Cells with only the less accurate, reflex-like pathway are fitter in sudden stress, whereas cells with only the slow, more accurate pathway are fitter in fluctuating but increasing stress. Our results demonstrate that cellular signalling is vulnerable to trade-offs in performance, but that these trade-offs can be mitigated by assigning the opposing tasks to different signalling subnetworks. Such division of labour could function broadly within cellular signal transduction.

Article and author information

Author details

  1. Alejandro A Granados

    SynthSys - Synthetic and Systems Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Matthew M Crane

    SynthSys - Synthetic and Systems Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Luis F Montano-Gutierrez

    SynthSys - Synthetic and Systems Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Reiko J Tanaka

    Department of Bioengineering, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0769-9382
  5. Margaritis Voliotis

    Department of Mathematics, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Peter Swain

    SynthSys - Synthetic and Systems Biology, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    peter.swain@ed.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7489-8587

Funding

Human Frontier Science Program (Research grant)

  • Matthew M Crane
  • Peter Swain

Biotechnology and Biological Sciences Research Council (Responsive mode grant)

  • Matthew M Crane
  • Peter Swain

Engineering and Physical Sciences Research Council (EP/N014391/1)

  • Alejandro A Granados
  • Reiko J Tanaka
  • Margaritis Voliotis

Wellcome Trust (PhD studentship)

  • Luis F Montano-Gutierrez

Consejo Nacional de Ciencia y Tecnología (PhD studentship)

  • Alejandro A Granados
  • Luis F Montano-Gutierrez

SULSA

  • Matthew M Crane
  • Peter Swain

Medical Research Council (Fellowship)

  • Margaritis Voliotis

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

Reviewing Editor

  1. Naama Barkai, Weizmann Institute of Science, Israel

Publication history

  1. Received: September 10, 2016
  2. Accepted: May 12, 2017
  3. Accepted Manuscript published: May 17, 2017 (version 1)
  4. Version of Record published: June 8, 2017 (version 2)

Copyright

© 2017, Granados 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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