Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast

BACKGROUND: The impact of genetic interaction networks on evolution is a fundamental issue. Previous studies have demonstrated that the topology of the network is determined by the properties of the cellular machinery. Functionally related genes frequently interact with one another, and they establi...

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Autores principales: Klim, Joanna, Zielenkiewicz, Urszula, Skoneczny, Marek, Skoneczna, Adrianna, Kurlandzka, Anna, Kaczanowski, Szymon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8157726/
https://www.ncbi.nlm.nih.gov/pubmed/34039270
http://dx.doi.org/10.1186/s12862-021-01830-9
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author Klim, Joanna
Zielenkiewicz, Urszula
Skoneczny, Marek
Skoneczna, Adrianna
Kurlandzka, Anna
Kaczanowski, Szymon
author_facet Klim, Joanna
Zielenkiewicz, Urszula
Skoneczny, Marek
Skoneczna, Adrianna
Kurlandzka, Anna
Kaczanowski, Szymon
author_sort Klim, Joanna
collection PubMed
description BACKGROUND: The impact of genetic interaction networks on evolution is a fundamental issue. Previous studies have demonstrated that the topology of the network is determined by the properties of the cellular machinery. Functionally related genes frequently interact with one another, and they establish modules, e.g., modules of protein complexes and biochemical pathways. In this study, we experimentally tested the hypothesis that compensatory evolutionary modifications, such as mutations and transcriptional changes, occur frequently in genes from perturbed modules of interacting genes. RESULTS: Using Saccharomyces cerevisiae haploid deletion mutants as a model, we investigated two modules lacking COG7 or NUP133, which are evolutionarily conserved genes with many interactions. We performed laboratory evolution experiments with these strains in two genetic backgrounds (with or without additional deletion of MSH2), subjecting them to continuous culture in a non-limiting minimal medium. Next, the evolved yeast populations were characterized through whole-genome sequencing and transcriptome analyses. No obvious compensatory changes resulting from inactivation of genes already included in modules were identified. The supposedly compensatory inactivation of genes in the evolved strains was only rarely observed to be in accordance with the established fitness effect of the genetic interaction network. In fact, a substantial majority of the gene inactivations were predicted to be neutral in the experimental conditions used to determine the interaction network. Similarly, transcriptome changes during continuous culture mostly signified adaptation to growth conditions rather than compensation of the absence of the COG7, NUP133 or MSH2 genes. However, we noticed that for genes whose inactivation was deleterious an upregulation of transcription was more common than downregulation. CONCLUSIONS: Our findings demonstrate that the genetic interactions and the modular structure of the network described by others have very limited effects on the evolutionary trajectory following gene deletion of module elements in our experimental conditions and has no significant impact on short-term compensatory evolution. However, we observed likely compensatory evolution in functionally related (albeit non-interacting) genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-021-01830-9.
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spelling pubmed-81577262021-05-28 Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast Klim, Joanna Zielenkiewicz, Urszula Skoneczny, Marek Skoneczna, Adrianna Kurlandzka, Anna Kaczanowski, Szymon BMC Ecol Evol Research Article BACKGROUND: The impact of genetic interaction networks on evolution is a fundamental issue. Previous studies have demonstrated that the topology of the network is determined by the properties of the cellular machinery. Functionally related genes frequently interact with one another, and they establish modules, e.g., modules of protein complexes and biochemical pathways. In this study, we experimentally tested the hypothesis that compensatory evolutionary modifications, such as mutations and transcriptional changes, occur frequently in genes from perturbed modules of interacting genes. RESULTS: Using Saccharomyces cerevisiae haploid deletion mutants as a model, we investigated two modules lacking COG7 or NUP133, which are evolutionarily conserved genes with many interactions. We performed laboratory evolution experiments with these strains in two genetic backgrounds (with or without additional deletion of MSH2), subjecting them to continuous culture in a non-limiting minimal medium. Next, the evolved yeast populations were characterized through whole-genome sequencing and transcriptome analyses. No obvious compensatory changes resulting from inactivation of genes already included in modules were identified. The supposedly compensatory inactivation of genes in the evolved strains was only rarely observed to be in accordance with the established fitness effect of the genetic interaction network. In fact, a substantial majority of the gene inactivations were predicted to be neutral in the experimental conditions used to determine the interaction network. Similarly, transcriptome changes during continuous culture mostly signified adaptation to growth conditions rather than compensation of the absence of the COG7, NUP133 or MSH2 genes. However, we noticed that for genes whose inactivation was deleterious an upregulation of transcription was more common than downregulation. CONCLUSIONS: Our findings demonstrate that the genetic interactions and the modular structure of the network described by others have very limited effects on the evolutionary trajectory following gene deletion of module elements in our experimental conditions and has no significant impact on short-term compensatory evolution. However, we observed likely compensatory evolution in functionally related (albeit non-interacting) genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-021-01830-9. BioMed Central 2021-05-26 /pmc/articles/PMC8157726/ /pubmed/34039270 http://dx.doi.org/10.1186/s12862-021-01830-9 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Klim, Joanna
Zielenkiewicz, Urszula
Skoneczny, Marek
Skoneczna, Adrianna
Kurlandzka, Anna
Kaczanowski, Szymon
Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
title Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
title_full Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
title_fullStr Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
title_full_unstemmed Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
title_short Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
title_sort genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8157726/
https://www.ncbi.nlm.nih.gov/pubmed/34039270
http://dx.doi.org/10.1186/s12862-021-01830-9
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