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

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...

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Autores principales: Brauns, Fridtjof, Iñigo de la Cruz, Leila, Daalman, Werner K.-G., de Bruin, Ilse, Halatek, Jacob, Laan, Liedewij, Frey, Erwin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10579396/
https://www.ncbi.nlm.nih.gov/pubmed/37845215
http://dx.doi.org/10.1038/s41467-023-42100-0
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author Brauns, Fridtjof
Iñigo de la Cruz, Leila
Daalman, Werner K.-G.
de Bruin, Ilse
Halatek, Jacob
Laan, Liedewij
Frey, Erwin
author_facet Brauns, Fridtjof
Iñigo de la Cruz, Leila
Daalman, Werner K.-G.
de Bruin, Ilse
Halatek, Jacob
Laan, Liedewij
Frey, Erwin
author_sort Brauns, Fridtjof
collection PubMed
description 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.
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spelling pubmed-105793962023-10-18 Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast Brauns, Fridtjof Iñigo de la Cruz, Leila Daalman, Werner K.-G. de Bruin, Ilse Halatek, Jacob Laan, Liedewij Frey, Erwin Nat Commun Article 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. Nature Publishing Group UK 2023-10-16 /pmc/articles/PMC10579396/ /pubmed/37845215 http://dx.doi.org/10.1038/s41467-023-42100-0 Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Brauns, Fridtjof
Iñigo de la Cruz, Leila
Daalman, Werner K.-G.
de Bruin, Ilse
Halatek, Jacob
Laan, Liedewij
Frey, Erwin
Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
title Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
title_full Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
title_fullStr Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
title_full_unstemmed Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
title_short Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
title_sort redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10579396/
https://www.ncbi.nlm.nih.gov/pubmed/37845215
http://dx.doi.org/10.1038/s41467-023-42100-0
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