Widespread premature transcription termination of Arabidopsis thaliana NLR genes by the spen protein FPA

  1. Matthew T Parker
  2. Katarzyna Knop
  3. Vasiliki Zacharaki
  4. Anna V Sherwood
  5. Daniel Tome
  6. Xuhong Yu
  7. Pascal GP Martin
  8. Jim Beynon
  9. Scott Michaels
  10. Geoffrey John Barton
  11. Gordon Grant Simpson  Is a corresponding author
  1. University of Dundee, United Kingdom
  2. University of Warwick, United Kingdom
  3. Indiana University, United States

Abstract

Genes involved in disease resistance are some of the fastest evolving and most diverse components of genomes. Large numbers of nucleotide-binding, leucine-rich repeat (NLR) genes are found in plant genomes and are required for disease resistance. However, NLRs can trigger autoimmunity, disrupt beneficial microbiota or reduce fitness. It is therefore crucial to understand how NLRs are controlled. Here we show that the RNA-binding protein FPA mediates widespread premature cleavage and polyadenylation of NLR transcripts, thereby controlling their functional expression and impacting immunity. Using long-read Nanopore direct RNA sequencing, we resolved the complexity of NLR transcript processing and gene annotation. Our results uncover a co-transcriptional layer of NLR control with implications for understanding the regulatory and evolutionary dynamics of NLRs in the immune responses of plants.

Data availability

IVI-MS data is available from the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD022684. FPA and Pol II ChIP-Seq data is available from ENA accession PRJNA449914. Col-0 nanopore DRS data is available from ENA accession PRJEB32782. fpa-8 and 35S::FPA:YFP nanopore DRS data is available from ENA accession PRJEB41451. hen2-2 nanopore DRS data is available from ENA accession PRJEB41381. Col-0, fpa-8 and 35S::FPA:YFP Helicos DRS data is available from Zenodo DOI 10.5281/zenodo.4309752 ahead of submission to ENA. Col-0, fpa-8 and 35S::FPA:YFP Illumina RNA-Seq data is available from ENA accession PRJEB41455.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Matthew T Parker

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0891-8495
  2. Katarzyna Knop

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2636-9450
  3. Vasiliki Zacharaki

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5543-2332
  4. Anna V Sherwood

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Daniel Tome

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Xuhong Yu

    Department of Biology, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Pascal GP Martin

    Department of Biology, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4271-658X
  8. Jim Beynon

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Scott Michaels

    Department of Biology, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Geoffrey John Barton

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9014-5355
  11. Gordon Grant Simpson

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    g.g.simpson@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6744-5889

Funding

Biotechnology and Biological Sciences Research Council (BB/M010066/1)

  • Geoffrey John Barton
  • Gordon Grant Simpson

Biotechnology and Biological Sciences Research Council (BB/J00247X/1)

  • Geoffrey John Barton
  • Gordon Grant Simpson

Biotechnology and Biological Sciences Research Council (BB/M004155/1)

  • Geoffrey John Barton
  • Gordon Grant Simpson

H2020 Marie Skłodowska-Curie Actions (799300)

  • Katarzyna Knop

Wellcome (097945/B/11/Z)

  • Geoffrey John Barton
  • Gordon Grant Simpson

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

Reviewing Editor

  1. Hao Yu, National University of Singapore & Temasek Life Sciences Laboratory, Singapore

Publication history

  1. Received: December 7, 2020
  2. Accepted: April 26, 2021
  3. Accepted Manuscript published: April 27, 2021 (version 1)
  4. Version of Record published: May 12, 2021 (version 2)
  5. Version of Record updated: June 4, 2021 (version 3)

Copyright

© 2021, Parker 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. Matthew T Parker
  2. Katarzyna Knop
  3. Vasiliki Zacharaki
  4. Anna V Sherwood
  5. Daniel Tome
  6. Xuhong Yu
  7. Pascal GP Martin
  8. Jim Beynon
  9. Scott Michaels
  10. Geoffrey John Barton
  11. Gordon Grant Simpson
(2021)
Widespread premature transcription termination of Arabidopsis thaliana NLR genes by the spen protein FPA
eLife 10:e65537.
https://doi.org/10.7554/eLife.65537
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