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Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast

Author

Listed:
  • Fridtjof Brauns

    (Ludwig-Maximilians-Universität München
    University of California Santa Barbara)

  • Leila Iñigo de la Cruz

    (Delft University of Technology)

  • Werner K.-G. Daalman

    (Delft University of Technology)

  • Ilse Bruin

    (Delft University of Technology)

  • Jacob Halatek

    (Ludwig-Maximilians-Universität München)

  • Liedewij Laan

    (Delft University of Technology)

  • Erwin Frey

    (Ludwig-Maximilians-Universität München
    Max Planck School Matter to Life)

Abstract

How can a self-organized cellular function evolve, adapt to perturbations, and acquire new sub-functions? To make progress in answering these basic questions of evolutionary cell biology, we analyze, as a concrete example, the cell polarity machinery of Saccharomyces cerevisiae. This cellular module exhibits an intriguing resilience: it remains operational under genetic perturbations and recovers quickly and reproducibly from the deletion of one of its key components. Using a combination of modeling, conceptual theory, and experiments, we propose that multiple, redundant self-organization mechanisms coexist within the protein network underlying cell polarization and are responsible for the module’s resilience and adaptability. Based on our mechanistic understanding of polarity establishment, we hypothesize that scaffold proteins, by introducing new connections in the existing network, can increase the redundancy of mechanisms and thus increase the evolvability of other network components. Moreover, our work gives a perspective on how a complex, redundant cellular module might have evolved from a more rudimental ancestral form.

Suggested Citation

  • Fridtjof Brauns & Leila Iñigo de la Cruz & Werner K.-G. Daalman & Ilse Bruin & Jacob Halatek & Liedewij Laan & Erwin Frey, 2023. "Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42100-0
    DOI: 10.1038/s41467-023-42100-0
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    References listed on IDEAS

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    1. Balázs Papp & Csaba Pál & Laurence D. Hurst, 2003. "Dosage sensitivity and the evolution of gene families in yeast," Nature, Nature, vol. 424(6945), pages 194-197, July.
    2. Ryan N Gutenkunst & Joshua J Waterfall & Fergal P Casey & Kevin S Brown & Christopher R Myers & James P Sethna, 2007. "Universally Sloppy Parameter Sensitivities in Systems Biology Models," PLOS Computational Biology, Public Library of Science, vol. 3(10), pages 1-8, October.
    3. Tina Freisinger & Ben Klünder & Jared Johnson & Nikola Müller & Garwin Pichler & Gisela Beck & Michael Costanzo & Charles Boone & Richard A. Cerione & Erwin Frey & Roland Wedlich-Söldner, 2013. "Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops," Nature Communications, Nature, vol. 4(1), pages 1-11, June.
    4. Steven J. Altschuler & Sigurd B. Angenent & Yanqin Wang & Lani F. Wu, 2008. "On the spontaneous emergence of cell polarity," Nature, Nature, vol. 454(7206), pages 886-889, August.
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