Regulation of transcription elongation anticipates alternative gene expression strategies across the cell cycle

A growing body of evidence supports the idea that RNA polymerase II (RNAP II) activity during transcription elongation can be regulated to control transcription rates. Using genomic run-on and RNAP II chromatin immunoprecipitation, we measured both active and total RNAP II across the bodies of genes at three different stages of the mitotic cell cycle in Saccharomyces cerevisiae: G1, S, and G2/M. Comparison of active and total RNAP II levels at these stages revealed distinct patterns of transcription elongation control throughout the cell cycle. Previously characterized cycling genes were associated with some of these elongation patterns. A cluster of genes with highly divergent genomic run-on and RNAP II chromatin immunoprecipitation patterns was notably enriched in genes related to ribosome biogenesis and the structural components of the ribosome. We confirmed that the expression of ribosome biogenesis mRNAs increases after G1 but decreases following mitosis. Finally, we analyzed the contribution of mRNA stability to each cluster and found that a coordinated regulation of RNAP II activity and mRNA decay is necessary to fully understand the alternative strategies of gene expression across the cell cycle.

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Publication Details

Journal
PLoS ONE
Published
2025-05-07
DOI
https://doi.org/10.1371/journal.pone.0317650
Primary Topic
Genomics and Chromatin Dynamics
Type
article
Field-Weighted Citation Impact
0.00

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article

Regulation of transcription elongation anticipates alternative gene expression strategies across the cell cycle

Jesús de la Cruz, Ildefonso Cases, José E. Pérez‐Ortín, Sebastián Chávez et al.
PLoS ONE
Genomics and Chromatin Dynamics
article

Regulation of transcription elongation anticipates alternative gene expression strategies across the cell cycle

Jesús de la Cruz, Ildefonso Cases, José E. Pérez‐Ortín, Sebastián Chávez, Romela Pasion, Mari Cruz Muñoz-Centeno, Douglas Maya‐Miles, José García‐Martínez
article en

Abstract

A growing body of evidence supports the idea that RNA polymerase II (RNAP II) activity during transcription elongation can be regulated to control transcription rates. Using genomic run-on and RNAP II chromatin immunoprecipitation, we measured both active and total RNAP II across the bodies of genes at three different stages of the mitotic cell cycle in Saccharomyces cerevisiae: G1, S, and G2/M. Comparison of active and total RNAP II levels at these stages revealed distinct patterns of transcription elongation control throughout the cell cycle. Previously characterized cycling genes were associated with some of these elongation patterns. A cluster of genes with highly divergent genomic run-on and RNAP II chromatin immunoprecipitation patterns was notably enriched in genes related to ribosome biogenesis and the structural components of the ribosome. We confirmed that the expression of ribosome biogenesis mRNAs increases after G1 but decreases following mitosis. Finally, we analyzed the contribution of mRNA stability to each cluster and found that a coordinated regulation of RNAP II activity and mRNA decay is necessary to fully understand the alternative strategies of gene expression across the cell cycle.

PLoS ONEVol. 20(5)
Universitat de València (ES), Centro Andaluz de Biología del Desarrollo (ES), Centro de Investigación Biomédica en Red (ES), Hospital Universitario Virgen del Rocío (ES), Universidad de Sevilla (ES)
Generalitat Valenciana, Ministerio de Ciencia e Innovación, European Regional Development Fund, Agencia Estatal de Investigación
Openalex Percentile: Top 91%
Genomics and Chromatin Dynamics
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