Regulation of rice root development by a retrotransposon acting as a microRNA sponge

  1. Jungnam Cho
  2. Jerzy Paszkowski  Is a corresponding author
  1. Sainsbury Laboratory, United Kingdom
  2. The Sainsbury Laboratory, United Kingdom

Abstract

It is well documented that transposable elements (TEs) can regulate the expression of neighbouring genes. However, their ability to act in trans and influence ectopic loci has been reported rarely. We searched in rice transcriptomes for tissue-specific expression of TEs and found them to be regulated developmentally. They often shared sequence homology with co-expressed genes and contained potential microRNA-binding sites, which suggested possible contributions to gene regulation. In fact, we have identified a retrotransposon that is highly transcribed in roots and whose spliced transcript constitutes a target mimic for miR171. miR171 destabilizes mRNAs encoding the root-specific family of SCARECROW-Like transcription factors. We demonstrate that retrotransposon-derived transcripts act as decoys for miR171, triggering its degradation and thus results in the root-specific accumulation of SCARECROW-Like mRNAs. Such transposon-mediated post-transcriptional control of miR171 levels is conserved in diverse rice species.

Data availability

The following previously published data sets were used
    1. Wei L
    2. Gu L
    3. Cao X
    (2014) Control of agricultural traits by hc-siRNA associated MITEs in rice
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE50778).
    1. Zhai R
    2. Cheng S
    (2013) Transcriptome Analysis of Rice Root Heterosis by RNA-Seq
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE41797).

Article and author information

Author details

  1. Jungnam Cho

    University of Cambridge, Sainsbury Laboratory, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4078-7763
  2. Jerzy Paszkowski

    University of Cambridge, The Sainsbury Laboratory, Cambridge, United Kingdom
    For correspondence
    jerzy.paszkowski@slcu.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1378-5666

Funding

European Research Council (322621)

  • Jungnam Cho
  • Jerzy Paszkowski

Gatsby Charitable Foundation (AT3273/GLE)

  • Jerzy Paszkowski

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

Reviewing Editor

  1. Christian S. Hardtke, University of Lausanne, Switzerland

Version history

  1. Received: June 29, 2017
  2. Accepted: August 21, 2017
  3. Accepted Manuscript published: August 26, 2017 (version 1)
  4. Version of Record published: September 14, 2017 (version 2)

Copyright

© 2017, Cho & Paszkowski

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.

Metrics

  • 3,752
    Page views
  • 772
    Downloads
  • 57
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jungnam Cho
  2. Jerzy Paszkowski
(2017)
Regulation of rice root development by a retrotransposon acting as a microRNA sponge
eLife 6:e30038.
https://doi.org/10.7554/eLife.30038

Share this article

https://doi.org/10.7554/eLife.30038

Further reading

    1. Plant Biology
    Daniel S Yu, Megan A Outram ... Simon J Williams
    Research Article

    Plant pathogens secrete proteins, known as effectors, that function in the apoplast or inside plant cells to promote virulence. Effector recognition by cell-surface or cytosolic receptors results in the activation of defence pathways and plant immunity. Despite their importance, our general understanding of fungal effector function and recognition by immunity receptors remains poor. One complication often associated with effectors is their high sequence diversity and lack of identifiable sequence motifs precluding prediction of structure or function. In recent years, several studies have demonstrated that fungal effectors can be grouped into structural classes, despite significant sequence variation and existence across taxonomic groups. Using protein X-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors Avr1 (SIX4) and Avr3 (SIX1) represent the founding members of the Fol dual-domain (FOLD) effector class, with members containing two distinct domains. Using AlphaFold2, we predicted the full SIX effector repertoire of Fol and show that SIX6 and SIX13 are also FOLD effectors, which we validated experimentally for SIX6. Based on structural prediction and comparisons, we show that FOLD effectors are present within three divisions of fungi and are expanded in pathogens and symbionts. Further structural comparisons demonstrate that Fol secretes effectors that adopt a limited number of structural folds during infection of tomato. This analysis also revealed a structural relationship between transcriptionally co-regulated effector pairs. We make use of the Avr1 structure to understand its recognition by the I receptor, which leads to disease resistance in tomato. This study represents an important advance in our understanding of Fol-tomato, and by extension plant–fungal interactions, which will assist in the development of novel control and engineering strategies to combat plant pathogens.

    1. Ecology
    2. Plant Biology
    Jamie Mitchel Waterman, Tristan Michael Cofer ... Matthias Erb
    Research Article

    Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.