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The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons

We analyzed 80 different genomic experiments, and found a positive correlation between both RNA polymerase II transcription and mRNA degradation with growth rates in yeast. Thus, in spite of the marked variation in mRNA turnover, the total mRNA concentration remained approximately constant. Some gen...

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Autores principales: García-Martínez, José, Delgado-Ramos, Lidia, Ayala, Guillermo, Pelechano, Vicent, Medina, Daniel A., Carrasco, Fany, González, Ramón, Andrés-León, Eduardo, Steinmetz, Lars, Warringer, Jonas, Chávez, Sebastián, Pérez-Ortín, José E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4856968/
https://www.ncbi.nlm.nih.gov/pubmed/26717982
http://dx.doi.org/10.1093/nar/gkv1512
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author García-Martínez, José
Delgado-Ramos, Lidia
Ayala, Guillermo
Pelechano, Vicent
Medina, Daniel A.
Carrasco, Fany
González, Ramón
Andrés-León, Eduardo
Steinmetz, Lars
Warringer, Jonas
Chávez, Sebastián
Pérez-Ortín, José E.
author_facet García-Martínez, José
Delgado-Ramos, Lidia
Ayala, Guillermo
Pelechano, Vicent
Medina, Daniel A.
Carrasco, Fany
González, Ramón
Andrés-León, Eduardo
Steinmetz, Lars
Warringer, Jonas
Chávez, Sebastián
Pérez-Ortín, José E.
author_sort García-Martínez, José
collection PubMed
description We analyzed 80 different genomic experiments, and found a positive correlation between both RNA polymerase II transcription and mRNA degradation with growth rates in yeast. Thus, in spite of the marked variation in mRNA turnover, the total mRNA concentration remained approximately constant. Some genes, however, regulated their mRNA concentration by uncoupling mRNA stability from the transcription rate. Ribosome-related genes modulated their transcription rates to increase mRNA levels under fast growth. In contrast, mitochondria-related and stress-induced genes lowered mRNA levels by reducing mRNA stability or the transcription rate, respectively. We also detected these regulations within the heterogeneity of a wild-type cell population growing in optimal conditions. The transcriptomic analysis of sorted microcolonies confirmed that the growth rate dictates alternative expression programs by modulating transcription and mRNA decay. The regulation of overall mRNA turnover keeps a constant ratio between mRNA decay and the dilution of [mRNA] caused by cellular growth. This regulation minimizes the indiscriminate transmission of mRNAs from mother to daughter cells, and favors the response capacity of the latter to physiological signals and environmental changes. We also conclude that, by uncoupling mRNA synthesis from decay, cells control the mRNA abundance of those gene regulons that characterize fast and slow growth.
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spelling pubmed-48569682016-05-09 The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons García-Martínez, José Delgado-Ramos, Lidia Ayala, Guillermo Pelechano, Vicent Medina, Daniel A. Carrasco, Fany González, Ramón Andrés-León, Eduardo Steinmetz, Lars Warringer, Jonas Chávez, Sebastián Pérez-Ortín, José E. Nucleic Acids Res Gene regulation, Chromatin and Epigenetics We analyzed 80 different genomic experiments, and found a positive correlation between both RNA polymerase II transcription and mRNA degradation with growth rates in yeast. Thus, in spite of the marked variation in mRNA turnover, the total mRNA concentration remained approximately constant. Some genes, however, regulated their mRNA concentration by uncoupling mRNA stability from the transcription rate. Ribosome-related genes modulated their transcription rates to increase mRNA levels under fast growth. In contrast, mitochondria-related and stress-induced genes lowered mRNA levels by reducing mRNA stability or the transcription rate, respectively. We also detected these regulations within the heterogeneity of a wild-type cell population growing in optimal conditions. The transcriptomic analysis of sorted microcolonies confirmed that the growth rate dictates alternative expression programs by modulating transcription and mRNA decay. The regulation of overall mRNA turnover keeps a constant ratio between mRNA decay and the dilution of [mRNA] caused by cellular growth. This regulation minimizes the indiscriminate transmission of mRNAs from mother to daughter cells, and favors the response capacity of the latter to physiological signals and environmental changes. We also conclude that, by uncoupling mRNA synthesis from decay, cells control the mRNA abundance of those gene regulons that characterize fast and slow growth. Oxford University Press 2016-05-05 2015-12-29 /pmc/articles/PMC4856968/ /pubmed/26717982 http://dx.doi.org/10.1093/nar/gkv1512 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Gene regulation, Chromatin and Epigenetics
García-Martínez, José
Delgado-Ramos, Lidia
Ayala, Guillermo
Pelechano, Vicent
Medina, Daniel A.
Carrasco, Fany
González, Ramón
Andrés-León, Eduardo
Steinmetz, Lars
Warringer, Jonas
Chávez, Sebastián
Pérez-Ortín, José E.
The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons
title The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons
title_full The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons
title_fullStr The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons
title_full_unstemmed The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons
title_short The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons
title_sort cellular growth rate controls overall mrna turnover, and modulates either transcription or degradation rates of particular gene regulons
topic Gene regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4856968/
https://www.ncbi.nlm.nih.gov/pubmed/26717982
http://dx.doi.org/10.1093/nar/gkv1512
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