Letter

ROS accumulation and antiviral defence control by microRNA528 in rice

  • Nature Plants 3, Article number: 16203 (2017)
  • doi:10.1038/nplants.2016.203
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Abstract

MicroRNAs (miRNAs) are key regulators of plant–pathogen interactions. Modulating miRNA function has emerged as a new strategy to produce virus resistance traits1,​2,​3,​4,​5. However, the miRNAs involved in antiviral defence and the underlying mechanisms remain largely elusive. We previously demonstrated that sequestration by Argonaute (AGO) proteins plays an important role in regulating miRNA function in antiviral defence pathways6. Here we reveal that cleavage-defective AGO18 complexes sequester microRNA528 (miR528) upon viral infection. We show that miR528 negatively regulates viral resistance in rice by cleaving L-ascorbate oxidase (AO) messenger RNA, thereby reducing AO-mediated accumulation of reactive oxygen species. Upon viral infection, miR528 becomes preferentially associated with AGO18, leading to elevated AO activity, higher basal reactive oxygen species accumulation and enhanced antiviral defence. Our findings reveal a mechanism in which antiviral defence is boosted through suppression of an miRNA that negatively regulates viral resistance. This mechanism could be manipulated to engineer virus-resistant crop plants.

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Acknowledgements

We thank F. Qu (Ohio State University) and Y. Li (Tsinghua-Peking Center for Life Sciences) for critical reading of the manuscript, L. Li (Peking University) for technical assistance, G. Liu (Tsinghua University) for assistance with the AO and AsA assay and the Integrated R & D Services – WuXi AppTec for generating the antisera used in this study. This work was supported by grants from the National Basic Research Program 973 (2014CB138400), Natural Science Foundation of China (91540203, 31530062, 31420103904, 31123007 and 31272018), the National Key Research and Development Program of China (2016YFD0100904), the Transgenic Research Program (2016ZX08010-001 and 2016ZX08009001-005) and state key laboratories of protein and plant gene research, plant genomics. J.W. was supported in part by the Postdoctoral Fellowship of Peking-Tsinghua Center for Life Sciences.

Author information

Author notes

    • Jianguo Wu
    • , Rongxin Yang
    •  & Zhirui Yang

    These authors contributed equally to this work.

Affiliations

  1. The State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing 100871, China

    • Jianguo Wu
    • , Zhirui Yang
    • , Shengze Yao
    • , Shanshan Zhao
    • , Yu Wang
    • , Lian Jin
    •  & Yi Li
  2. State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou 350002, China

    • Jianguo Wu
    •  & Lianhui Xie
  3. State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

    • Rongxin Yang
    • , Xianwei Song
    • , Chengcai Chu
    •  & Xiaofeng Cao
  4. Agriculture and Agri-Food Canada, Morden, Manitoba R6M 1Y5, Canada

    • Pingchuan Li
  5. Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China

    • Tong Zhou
    •  & Ying Lan
  6. State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou 310029, China

    • Xueping Zhou
  7. Center for Plant Biology, Tsinghua-Peking Center for Life Sciences, College of Life Sciences, Tsinghua University, Beijing 100084, China

    • Yijun Qi
  8. CAS Center for Excellence in Molecular Plant Sciences, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

    • Xiaofeng Cao

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Contributions

J.W., Z.Y., X.C. and Y. Li designed the experiments; J.W., Z.Y., R.Y., Z.Y., S.Z., Y.W., L.J., P.L., X.S., T.Z. and Y. Lan performed the experiments; J.W., Z.Y., R.Y., L.X., X.Z., C.C., Y.Q., X.C. and Y. Li analysed the data; J.W., Z.Y. and Y. Li wrote the paper. All the authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Xiaofeng Cao or Yi Li.

Supplementary information

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    Supplementary Information

    Supplementary Figures 1–10, Supplementary Tables 1–3.