Abstract

Intron splicing increases proteome complexity, promotes RNA stability, and enhances transcription. However, introns and the concomitant need for splicing extend the time required for gene expression and can cause an undesirable delay in the activation of genes. Here, we show that the plant microRNA processing factor SERRATE (SE) plays an unexpected and pivotal role in the regulation of intronless genes. Arabidopsis SE associated with more than 1000, mainly intronless, genes in a transcription-dependent manner. Chromatin-bound SE liaised with paused and elongating polymerase II complexes and promoted their association with intronless target genes. Our results indicate that stress-responsive genes contain no or few introns, which negatively affects their expression strength, but that some genes circumvent this limitation via a novel SE-dependent transcriptional activation mechanism. Transcriptome analysis of a Drosophila mutant defective in ARS2, the metazoan homologue of SE, suggests that SE/ARS2 function in regulating intronless genes might be conserved across kingdoms.

Data availability

Raw data have been deposited under accession codes accession number ERP016859 (ENA), PXD006004 (Pride) and GSE99367 (Geo Omnibus).

The following data sets were generated
    1. Martinho C
    2. Speth C
    3. Szabo EX
    4. Laubinger S
    (2018) RNA-seq of se mutants
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE99367).
The following previously published data sets were used

Article and author information

Author details

  1. Corinna Speth

    Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Emese Xochitl Szabo

    Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Claudia Martinho

    Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Silvio Collani

    Department of Plant Physiology, Umeå University, Umeå, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9603-0882
  5. Sven zur Oven-Krockhaus

    Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Sandra Richter

    Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Irina Droste-Borel

    Proteome Centre, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Boris Macek

    Proteome Centre, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. York-Dieter Stierhof

    Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Markus Schmid

    Department of Plant Physiology, Umeå University, Umeå, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  11. Chang Liu

    Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2859-4288
  12. Sascha Laubinger

    Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    For correspondence
    sascha.laubinger@uol.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6682-0728

Funding

Deutsche Forschungsgemeinschaft

  • Sascha Laubinger

Max-Planck-Gesellschaft (Open-access funding)

  • Sven zur Oven-Krockhaus
  • York-Dieter Stierhof
  • Sascha Laubinger

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Yijun Qi, School of Life Sciences, Tsinghua University, China

Version history

  1. Received: March 28, 2018
  2. Accepted: August 22, 2018
  3. Accepted Manuscript published: August 28, 2018 (version 1)
  4. Version of Record published: September 12, 2018 (version 2)

Copyright

© 2018, Speth et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Corinna Speth
  2. Emese Xochitl Szabo
  3. Claudia Martinho
  4. Silvio Collani
  5. Sven zur Oven-Krockhaus
  6. Sandra Richter
  7. Irina Droste-Borel
  8. Boris Macek
  9. York-Dieter Stierhof
  10. Markus Schmid
  11. Chang Liu
  12. Sascha Laubinger
(2018)
Arabidopsis RNA processing factor SERRATE regulates the transcription of intronless genes
eLife 7:e37078.
https://doi.org/10.7554/eLife.37078

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https://doi.org/10.7554/eLife.37078