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Heterogeneous recruitment abilities to RNA polymerases generate nonlinear scaling of gene expression with cell volume

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  • Qirun Wang

    (Peking University)

  • Jie Lin

    (Peking University
    Peking University)

Abstract

While most genes’ expression levels are proportional to cell volumes, some genes exhibit nonlinear scaling between their expression levels and cell volume. Therefore, their mRNA and protein concentrations change as the cell volume increases, which often have crucial biological functions such as cell-cycle regulation. However, the biophysical mechanism underlying the nonlinear scaling between gene expression and cell volume is still unclear. In this work, we show that the nonlinear scaling is a direct consequence of the heterogeneous recruitment abilities of promoters to RNA polymerases based on a gene expression model at the whole-cell level. Those genes with weaker (stronger) recruitment abilities than the average ability spontaneously exhibit superlinear (sublinear) scaling with cell volume. Analysis of the promoter sequences and the nonlinear scaling of Saccharomyces cerevisiae’s mRNA levels shows that motifs associated with transcription regulation are indeed enriched in genes exhibiting nonlinear scaling, in concert with our model.

Suggested Citation

  • Qirun Wang & Jie Lin, 2021. "Heterogeneous recruitment abilities to RNA polymerases generate nonlinear scaling of gene expression with cell volume," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26952-y
    DOI: 10.1038/s41467-021-26952-y
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    1. Kora-Lee Claude & Daniela Bureik & Dimitra Chatzitheodoridou & Petia Adarska & Abhyudai Singh & Kurt M. Schmoller, 2021. "Transcription coordinates histone amounts and genome content," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Kurt M. Schmoller & J. J. Turner & M. Kõivomägi & Jan M. Skotheim, 2015. "Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size," Nature, Nature, vol. 526(7572), pages 268-272, October.
    3. Jie Lin & Ariel Amir, 2018. "Homeostasis of protein and mRNA concentrations in growing cells," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    4. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
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