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Differential regulation of mRNA stability modulates transcriptional memory and facilitates environmental adaptation

Author

Listed:
  • Bingnan Li

    (Shandong University
    Karolinska Institutet)

  • Patrice Zeis

    (Genome Biology Unit
    Institute of Molecular and Clinical Ophthalmology Basel)

  • Yujie Zhang

    (Karolinska Institutet)

  • Alisa Alekseenko

    (Karolinska Institutet)

  • Eliska Fürst

    (Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC Berlin))

  • Yerma Pareja Sanchez

    (Karolinska Institutet)

  • Gen Lin

    (Genome Biology Unit
    AbbVie Pte Ltd)

  • Manu M. Tekkedil

    (Genome Biology Unit)

  • Ilaria Piazza

    (Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC Berlin))

  • Lars M. Steinmetz

    (Genome Biology Unit
    Stanford University
    Stanford University)

  • Vicent Pelechano

    (Karolinska Institutet)

Abstract

Transcriptional memory, by which cells respond faster to repeated stimuli, is key for cellular adaptation and organism survival. Chromatin organization has been shown to play a role in the faster response of primed cells. However, the contribution of post-transcriptional regulation is not yet explored. Here we perform a genome-wide screen to identify novel factors modulating transcriptional memory in S. cerevisiae in response to galactose. We find that depletion of the nuclear RNA exosome increases GAL1 expression in primed cells. Our work shows that gene-specific differences in intrinsic nuclear surveillance factor association can enhance both gene induction and repression in primed cells. Finally, we show that primed cells present altered levels of RNA degradation machinery and that both nuclear and cytoplasmic mRNA decay modulate transcriptional memory. Our results demonstrate that mRNA post-transcriptional regulation, and not only transcription regulation, should be considered when investigating gene expression memory.

Suggested Citation

  • Bingnan Li & Patrice Zeis & Yujie Zhang & Alisa Alekseenko & Eliska Fürst & Yerma Pareja Sanchez & Gen Lin & Manu M. Tekkedil & Ilaria Piazza & Lars M. Steinmetz & Vicent Pelechano, 2023. "Differential regulation of mRNA stability modulates transcriptional memory and facilitates environmental adaptation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36586-x
    DOI: 10.1038/s41467-023-36586-x
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    References listed on IDEAS

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    1. Zhenyu Xu & Wu Wei & Julien Gagneur & Fabiana Perocchi & Sandra Clauder-Münster & Jurgi Camblong & Elisa Guffanti & Françoise Stutz & Wolfgang Huber & Lars M. Steinmetz, 2009. "Bidirectional promoters generate pervasive transcription in yeast," Nature, Nature, vol. 457(7232), pages 1033-1037, February.
    2. Robin Andersson & Claudia Gebhard & Irene Miguel-Escalada & Ilka Hoof & Jette Bornholdt & Mette Boyd & Yun Chen & Xiaobei Zhao & Christian Schmidl & Takahiro Suzuki & Evgenia Ntini & Erik Arner & Eivi, 2014. "An atlas of active enhancers across human cell types and tissues," Nature, Nature, vol. 507(7493), pages 455-461, March.
    3. Helen Neil & Christophe Malabat & Yves d’Aubenton-Carafa & Zhenyu Xu & Lars M. Steinmetz & Alain Jacquier, 2009. "Widespread bidirectional promoters are the major source of cryptic transcripts in yeast," Nature, Nature, vol. 457(7232), pages 1038-1042, February.
    4. Murat Acar & Attila Becskei & Alexander van Oudenaarden, 2005. "Enhancement of cellular memory by reducing stochastic transitions," Nature, Nature, vol. 435(7039), pages 228-232, May.
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