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Site-specific analysis reveals candidate cross-kingdom small RNAs, tRNA and rRNA fragments, and signs of fungal RNA phasing in the barley-powdery mildew interaction

View ORCID ProfileStefan Kusch, Mansi Singh, Hannah Thieron, View ORCID ProfilePietro D. Spanu, View ORCID ProfileRalph Panstruga
doi: https://doi.org/10.1101/2022.07.26.501657
Stefan Kusch
1Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany
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  • ORCID record for Stefan Kusch
Mansi Singh
1Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany
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Hannah Thieron
1Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany
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Pietro D. Spanu
1Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany
2Imperial College, London, United Kingdom
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  • For correspondence: p.spanu@imperial.ac.uk
Ralph Panstruga
1Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Worringerweg 1, D-52056 Aachen, Germany
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Abstract

The establishment of host-microbe interactions requires molecular communication between both partners, which involves the mutual transfer of noncoding small RNAs. Previous evidence suggests that this is also true for the barley powdery mildew disease, which is caused by the fungal pathogen Blumeria hordei. However, previous studies lacked spatial resolution regarding the accumulation of small RNAs upon host infection by B. hordei. Here, we analysed site-specific small RNA repertoires in the context of the barley-B. hordei interaction. To this end, we dissected infected leaves into separate fractions representing different sites that are key to the pathogenic process: epiphytic fungal mycelium, infected plant epidermis, isolated haustoria, a vesicle-enriched fraction from infected epidermis, and extracellular vesicles. Unexpectedly, we discovered enrichment of specific 31- to 33-base long 5’-terminal fragments of barley 5.8S ribosomal RNA (rRNA) in extracellular vesicles and infected epidermis, as well as particular B. hordei tRNA fragments in haustoria. We describe canonical small RNAs from both the plant host and the fungal pathogen that may confer cross-kingdom RNA interference activity. Interestingly, we found first evidence of phased small RNAs (phasiRNAs) in B. hordei, a feature usually attributed to plants, which may be associated with the post-transcriptional control of fungal coding genes, pseudogenes, and transposable elements. Our data suggests a key and possibly site-specific role for cross-kingdom RNA interference and noncoding RNA fragments in the host-pathogen communication between B. hordei and its host barley.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Error in the title (typographical insertion lead to spurious title)

  • Abbreviations

    Ago
    Argonaute
    Dcl
    Dicer-like
    EPI
    epidermis (colonized by B. hordei but epiphytic fungal mycelium removed)
    dsRNA
    double-stranded RNA
    EV
    extracellular vesicle
    FDR
    false discovery rate
    GO
    gene ontology
    HAU
    haustoria of B. hordei
    milRNA
    micro RNA-like
    miRNA
    micro RNA
    MYC
    mycelium of B. hordei
    phasiRNA
    phased siRNA
    P40
    microsomes from B. hordei-infected epidermis
    RNAi
    RNA interference
    rDNA
    ribosomal DNA
    rRF
    ribosomal RNA-derived small RNA fragment
    rRNA
    ribosomal RNA
    sRNA
    small RNA
    siRNA
    small interfering RNA
    tasiRNA
    trans-acting short interfering RNA
    TPM
    transcripts per million
    tRF
    transfer RNA-derived small RNA fragment
    tRNA
    transfer RNA
  • Copyright 
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    Posted August 11, 2022.
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    Site-specific analysis reveals candidate cross-kingdom small RNAs, tRNA and rRNA fragments, and signs of fungal RNA phasing in the barley-powdery mildew interaction
    Stefan Kusch, Mansi Singh, Hannah Thieron, Pietro D. Spanu, Ralph Panstruga
    bioRxiv 2022.07.26.501657; doi: https://doi.org/10.1101/2022.07.26.501657
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    Site-specific analysis reveals candidate cross-kingdom small RNAs, tRNA and rRNA fragments, and signs of fungal RNA phasing in the barley-powdery mildew interaction
    Stefan Kusch, Mansi Singh, Hannah Thieron, Pietro D. Spanu, Ralph Panstruga
    bioRxiv 2022.07.26.501657; doi: https://doi.org/10.1101/2022.07.26.501657

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