Viral-inducible Argonaute18 confers broad-spectrum virus resistance in rice by sequestering a host microRNA

  1. Jianguo Wu
  2. Zhirui Yang
  3. Yu Wang
  4. Lijia Zheng
  5. Ruiqiang Ye
  6. Yinghua Ji
  7. Shanshan Zhao
  8. Shaoyi Ji
  9. Ruofei Liu
  10. Le Xu
  11. Hong Zheng
  12. Yijun Zhou
  13. Xin Zhang
  14. Xiaofeng Cao
  15. Lianhui Xie
  16. Zujian Wu
  17. Yijun Qi
  18. Yi Li  Is a corresponding author
  1. Peking University, China
  2. Tsinghua University, China
  3. Jiangsu Academy of Agricultural Sciences, China
  4. Chinese Academy of Agricultural Sciences, China
  5. Institute of Genetics and Developmental Biology, China
  6. Fujian Agriculture and Forestry University, China

Abstract

Viral pathogens are a major threat to rice production worldwide. Although RNA interference (RNAi) is known to mediate antiviral immunity in plant and animal models, the mechanism of antiviral RNAi in rice and other economically important crops is poorly understood. Here, we report that rice resistance to evolutionarily diverse viruses requires Argonaute18 (AGO18). Genetic studies reveal that the antiviral function of AGO18 depends on its activity to sequester microRNA168 (miR168) to alleviate repression of rice AGO1 essential for antiviral RNAi. Expression of miR168-resistant AGO1a in ago18 background rescues or increases rice antiviral activity. Notably, stable transgenic expression of AGO18 confers broad-spectrum virus resistance in rice. Our findings uncover a novel cooperative antiviral activity of two distinct AGO proteins and suggest a new strategy for the control of viral diseases in rice.

Article and author information

Author details

  1. Jianguo Wu

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Zhirui Yang

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Yu Wang

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Lijia Zheng

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ruiqiang Ye

    Center for Plant Biology, Tsinghua-Peking Center for Life Sciences, College of Life Sciences, Tsinghua University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yinghua Ji

    Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Shanshan Zhao

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Shaoyi Ji

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Ruofei Liu

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Le Xu

    Center for Plant Biology, Tsinghua-Peking Center for Life Sciences, College of Life Sciences, Tsinghua University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Hong Zheng

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Yijun Zhou

    Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Xin Zhang

    Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Xiaofeng Cao

    State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Lianhui Xie

    Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  16. Zujian Wu

    Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  17. Yijun Qi

    Center for Plant Biology, Tsinghua-Peking Center for Life Sciences, College of Life Sciences, Tsinghua University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  18. Yi Li

    State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China
    For correspondence
    liyi@pku.edu.cn
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. David Baulcombe, University of Cambridge, United Kingdom

Version history

  1. Received: November 22, 2014
  2. Accepted: February 13, 2015
  3. Accepted Manuscript published: February 17, 2015 (version 1)
  4. Version of Record published: March 13, 2015 (version 2)

Copyright

© 2015, Wu 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. Jianguo Wu
  2. Zhirui Yang
  3. Yu Wang
  4. Lijia Zheng
  5. Ruiqiang Ye
  6. Yinghua Ji
  7. Shanshan Zhao
  8. Shaoyi Ji
  9. Ruofei Liu
  10. Le Xu
  11. Hong Zheng
  12. Yijun Zhou
  13. Xin Zhang
  14. Xiaofeng Cao
  15. Lianhui Xie
  16. Zujian Wu
  17. Yijun Qi
  18. Yi Li
(2015)
Viral-inducible Argonaute18 confers broad-spectrum virus resistance in rice by sequestering a host microRNA
eLife 4:e05733.
https://doi.org/10.7554/eLife.05733

Share this article

https://doi.org/10.7554/eLife.05733

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