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Coat proteins of necroviruses target 14-3-3a to subvert MAPKKKα-mediated antiviral immunity in plants

Author

Listed:
  • Zongyu Gao

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Dingliang Zhang

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Xiaoling Wang

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Xin Zhang

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Zhiyan Wen

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Qianshen Zhang

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Dawei Li

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

  • Savithramma P. Dinesh-Kumar

    (College of Biological Sciences, University of California, Davis)

  • Yongliang Zhang

    (State Key Laboratory of Agro-Biotechnology and Ministry of Agriculture Key Laboratory of Soil Microbiology, College of Biological Sciences, China Agricultural University)

Abstract

Mitogen-activated protein kinase (MAPK) cascades play an important role in innate immunity against various pathogens in plants and animals. However, we know very little about the importance of MAPK cascades in plant defense against viral pathogens. Here, we used a positive-strand RNA necrovirus, beet black scorch virus (BBSV), as a model to investigate the relationship between MAPK signaling and virus infection. Our findings showed that BBSV infection activates MAPK signaling, whereas viral coat protein (CP) counteracts MAPKKKα-mediated antiviral defense. CP does not directly target MAPKKKα, instead it competitively interferes with the binding of 14-3-3a to MAPKKKα in a dose-dependent manner. This results in the instability of MAPKKKα and subversion of MAPKKKα-mediated antiviral defense. Considering the conservation of 14-3-3-binding sites in the CPs of diverse plant viruses, we provide evidence that 14-3-3-MAPKKKα defense signaling module is a target of viral effectors in the ongoing arms race of defense and viral counter-defense.

Suggested Citation

  • Zongyu Gao & Dingliang Zhang & Xiaoling Wang & Xin Zhang & Zhiyan Wen & Qianshen Zhang & Dawei Li & Savithramma P. Dinesh-Kumar & Yongliang Zhang, 2022. "Coat proteins of necroviruses target 14-3-3a to subvert MAPKKKα-mediated antiviral immunity in plants," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28395-5
    DOI: 10.1038/s41467-022-28395-5
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    References listed on IDEAS

    as
    1. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    2. Cristiane Zorzatto & João Paulo B. Machado & Kênia V. G. Lopes & Kelly J. T. Nascimento & Welison A. Pereira & Otávio J. B. Brustolini & Pedro A. B. Reis & Iara P. Calil & Michihito Deguchi & Gilberto, 2015. "NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism," Nature, Nature, vol. 520(7549), pages 679-682, April.
    3. Yongliang Zhang & Gaoyuan Song & Neeraj K. Lal & Ugrappa Nagalakshmi & Yuanyuan Li & Wenjie Zheng & Pin-jui Huang & Tess C. Branon & Alice Y. Ting & Justin W. Walley & Savithramma P. Dinesh-Kumar, 2019. "TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
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