CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication

  1. Zhen-Jia Zhang  Is a corresponding author
  2. Qiang Gao
  3. Xiao-Dong Fang
  4. Zhi-Hang Ding
  5. Dong-Min Gao
  6. Wen-Ya Xu
  7. Qing Cao
  8. Ji-Hui Qiao
  9. Yi-Zhou Yang
  10. Chenggui Han
  11. Ying Wang
  12. Xuefeng Yuan
  13. Dawei Li
  14. Xian-Bing Wang  Is a corresponding author
  1. China Agricultural University, China
  2. College of Plant Protection, Shandong Agricultural University, China

Abstract

Carbon catabolite repression 4 (CCR4) is a conserved mRNA deadenylase regulating posttranscriptional gene expression. However, regulation of CCR4 in virus infections is less understood. Here, we characterized a pro-viral role of CCR4 in replication of a plant cytorhabdovirus, Barley yellow striate mosaic virus (BYSMV). The barley (Hordeum vulgare) CCR4 protein (HvCCR4) was identified to interact with the BYSMV phosphoprotein (P). The BYSMV P protein recruited HvCCR4 from processing bodies (PBs) into viroplasm-like bodies. Overexpression of HvCCR4 promoted BYSMV replication in plants. Conversely, knockdown of the small brown planthopper CCR4 inhibited viral accumulation in the insect vector. Biochemistry experiments revealed that HvCCR4 was recruited into N–RNA complexes by the BYSMV P protein and triggered turnover of N-bound cellular mRNAs, thereby releasing RNA-free N protein to bind viral genomic RNA for optimal viral replication. Our results demonstrate that the co-opted the CCR4-mediated RNA decay facilitates cytorhabdovirus replication in plants and insects.

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All data generated or analysed during this study are included in the manuscript and supporting files.

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Author details

  1. Zhen-Jia Zhang

    College of Biological Sciences, China Agricultural University, Beijing, China
    For correspondence
    zjzhang@cau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  2. Qiang Gao

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Xiao-Dong Fang

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Zhi-Hang Ding

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Dong-Min Gao

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Wen-Ya Xu

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Qing Cao

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Ji-Hui Qiao

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Yi-Zhou Yang

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Chenggui Han

    State Key Laboratory of Agro-Biotechnology, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Ying Wang

    College of Plant Protection, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Xuefeng Yuan

    Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai'an, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Dawei Li

    College of Biological Sciences, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Xian-Bing Wang

    College of Biological Sciences, China Agricultural University, Beijing, China
    For correspondence
    wangxianbing@cau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3082-2462

Funding

National Natural Science Foundation of China (31872920 and 31571978)

  • Xian-Bing Wang

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

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: November 19, 2019
  2. Accepted: March 21, 2020
  3. Accepted Manuscript published: March 24, 2020 (version 1)
  4. Version of Record published: March 30, 2020 (version 2)

Copyright

© 2020, Zhang 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. Zhen-Jia Zhang
  2. Qiang Gao
  3. Xiao-Dong Fang
  4. Zhi-Hang Ding
  5. Dong-Min Gao
  6. Wen-Ya Xu
  7. Qing Cao
  8. Ji-Hui Qiao
  9. Yi-Zhou Yang
  10. Chenggui Han
  11. Ying Wang
  12. Xuefeng Yuan
  13. Dawei Li
  14. Xian-Bing Wang
(2020)
CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
eLife 9:e53753.
https://doi.org/10.7554/eLife.53753

Share this article

https://doi.org/10.7554/eLife.53753

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