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Chance promoter activities illuminate the origins of eukaryotic intergenic transcriptions

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  • Haiqing Xu

    (University of Michigan
    Stanford University)

  • Chuan Li

    (University of Michigan
    Microsoft)

  • Chuan Xu

    (University of Michigan
    Shanghai Jiao Tong University)

  • Jianzhi Zhang

    (University of Michigan)

Abstract

It is debated whether the pervasive intergenic transcription from eukaryotic genomes has functional significance or simply reflects the promiscuity of RNA polymerases. We approach this question by comparing chance promoter activities with the expression levels of intergenic regions in the model eukaryote Saccharomyces cerevisiae. We build a library of over 105 strains, each carrying a 120-nucleotide, chromosomally integrated, completely random sequence driving the potential transcription of a barcode. Quantifying the RNA concentration of each barcode in two environments reveals that 41–63% of random sequences have significant, albeit usually low, promoter activities. Therefore, even in eukaryotes, where the presence of chromatin is thought to repress transcription, chance transcription is prevalent. We find that only 1–5% of yeast intergenic transcriptions are unattributable to chance promoter activities or neighboring gene expressions, and these transcriptions exhibit higher-than-expected environment-specificity. These findings suggest that only a minute fraction of intergenic transcription is functional in yeast.

Suggested Citation

  • Haiqing Xu & Chuan Li & Chuan Xu & Jianzhi Zhang, 2023. "Chance promoter activities illuminate the origins of eukaryotic intergenic transcriptions," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37610-w
    DOI: 10.1038/s41467-023-37610-w
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    References listed on IDEAS

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    1. 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.
    2. Joseph A. Martens & Lisa Laprade & Fred Winston, 2004. "Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene," Nature, Nature, vol. 429(6991), pages 571-574, June.
    3. 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.
    4. Avihu H. Yona & Eric J. Alm & Jeff Gore, 2018. "Random sequences rapidly evolve into de novo promoters," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    5. Jason Gertz & Eric D. Siggia & Barak A. Cohen, 2009. "Analysis of combinatorial cis-regulation in synthetic and genomic promoters," Nature, Nature, vol. 457(7226), pages 215-218, January.
    6. Matthew J Hangauer & Ian W Vaughn & Michael T McManus, 2013. "Pervasive Transcription of the Human Genome Produces Thousands of Previously Unidentified Long Intergenic Noncoding RNAs," PLOS Genetics, Public Library of Science, vol. 9(6), pages 1-13, June.
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