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Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway

Author

Listed:
  • Jing-Ru Zhang

    (Zhejiang University)

  • Yi-Ming Liu

    (Zhejiang University)

  • Di Li

    (Zhejiang University)

  • Yi-Jie Wu

    (Zhejiang University)

  • Shi-Xing Zhao

    (Zhejiang University)

  • Xiao-Wei Wang

    (Zhejiang University)

  • Shu-Sheng Liu

    (Zhejiang University)

  • Linda L. Walling

    (University of California)

  • Li-Long Pan

    (Zhejiang University
    Zhejiang University)

Abstract

Hemipteran insects transmit viruses when infesting plants, during which vectors activate salicylic acid (SA)-regulated antiviral defenses. How vector-borne plant viruses circumvent these antiviral defenses is largely unexplored. During co-infections of begomoviruses and betasatellites in plants, betasatellite-encoded βC1 proteins interfere with SA signaling and reduce the activation of antiviral resistance. βC1 inhibits SA-induced degradation of NbNPR3 (Nicotiana benthamiana nonexpressor of pathogenesis-related genes 3), a negative regulator of SA signaling. βC1 does not bind directly to NbNPR3, but regulates NbNPR3 degradation via heat shock protein 90s (NbHSP90s). NbHSP90s bind to both NbNPR3 and βC1 and suppress SA signaling. This viral success strategy appears to be conserved as it is also documented for viral proteins encoded by two aphid-borne viruses. Our findings reveal an exquisite mechanism that facilitates the persistence of vector-borne plant viruses and provide important insights into the intricacies of the virus life cycle.

Suggested Citation

  • Jing-Ru Zhang & Yi-Ming Liu & Di Li & Yi-Jie Wu & Shi-Xing Zhao & Xiao-Wei Wang & Shu-Sheng Liu & Linda L. Walling & Li-Long Pan, 2024. "Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53894-y
    DOI: 10.1038/s41467-024-53894-y
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    References listed on IDEAS

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    1. Qian Gong & Yunjing Wang & Linfang He & Fan Huang & Danfeng Zhang & Yan Wang & Xiang Wei & Meng Han & Haiteng Deng & Lan Luo & Feng Cui & Yiguo Hong & Yule Liu, 2023. "Molecular basis of methyl-salicylate-mediated plant airborne defence," Nature, Nature, vol. 622(7981), pages 139-148, October.
    2. Hehong Zhang & Fengmin Wang & Weiqi Song & Zihang Yang & Lulu Li & Qiang Ma & Xiaoxiang Tan & Zhongyan Wei & Yanjun Li & Junmin Li & Fei Yan & Jianping Chen & Zongtao Sun, 2023. "Different viral effectors suppress hormone-mediated antiviral immunity of rice coordinated by OsNPR1," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Renhou Wang & Yi Zhang & Martin Kieffer & Hong Yu & Stefan Kepinski & Mark Estelle, 2016. "HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
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