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The pathogen effector BcSSP2 suppresses the NPC phase separation to facilitate Botrytis cinerea infection

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  • Jiaojiao Wang

    (Beijing Forestry University
    Tsinghua University)

  • Dewei Wu

    (Tsinghua University
    Chinese Academy of Agricultural Sciences)

  • Gaofeng Pei

    (Tsinghua University; Tsinghua University-Peking University Joint Center for Life Sciences)

  • Yupei Wang

    (Tsinghua University)

  • Xiaokang Liu

    (Tsinghua University)

  • Shiping Tian

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Zhanquan Zhang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xiaolin Zhang

    (Tsinghua University)

  • Pilong Li

    (Tsinghua University; Tsinghua University-Peking University Joint Center for Life Sciences)

  • Daoxin Xie

    (Tsinghua University)

  • Xiaoyi Shan

    (Tsinghua University)

Abstract

Biomolecular phase separation-mediated immunity was recently uncovered as an important strategy of plants and animals for their survival in the challenging environment. Effectors are powerful weapons evolved by pathogens to overcome host defense response for effective infection. However, plant pathogen effectors were rarely identified to suppress the phase separation-mediated host defense response. Here, we report a pathogen effector that disrupts phase separation process in host cells to suppress host defense response and facilitate pathogen infection. We identify a host-internalized effector protein BcSSP2 from a disastrous pathogen Botrytis cinerea targets the central barrier of plant nuclear pore complex (NPC). BcSSP2 disrupts the phase separation of NUP62 and attenuates phase separation-dependent nuclear transport of immune regulator MPK3 to suppress plant defense response for effective pathogen infection. Intriguingly, BcSSP2 homologs are widely distributed among necrotrophic ascomycetes and also interfere with NUP62 phase separation, suggesting that disrupting plant NPC phase separation might be an evolutionarily conserved strategy evolved by these necrotrophic pathogens to facilitate their infection.

Suggested Citation

  • Jiaojiao Wang & Dewei Wu & Gaofeng Pei & Yupei Wang & Xiaokang Liu & Shiping Tian & Zhanquan Zhang & Xiaolin Zhang & Pilong Li & Daoxin Xie & Xiaoyi Shan, 2025. "The pathogen effector BcSSP2 suppresses the NPC phase separation to facilitate Botrytis cinerea infection," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-63632-7
    DOI: 10.1038/s41467-025-63632-7
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    1. Kailey M. Slavik & Benjamin R. Morehouse & Adelyn E. Ragucci & Wen Zhou & Xianlong Ai & Yuqiang Chen & Lihua Li & Ziming Wei & Heike Bähre & Martin König & Roland Seifert & Amy S. Y. Lee & Hua Cai & J, 2021. "cGAS-like receptors sense RNA and control 3′2′-cGAMP signalling in Drosophila," Nature, Nature, vol. 597(7874), pages 109-113, September.
    2. Wen Song & Li Liu & Dongli Yu & Hanna Bernardy & Jan Jirschitzka & Shijia Huang & Aolin Jia & Wictoria Jemielniak & Julia Acker & Henriette Laessle & Junli Wang & Qiaochu Shen & Weijie Chen & Pilong L, 2024. "Substrate-induced condensation activates plant TIR domain proteins," Nature, Nature, vol. 627(8005), pages 847-853, March.
    3. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    4. Shuai Huang & Shiwei Zhu & Pradeep Kumar & John D. MacMicking, 2021. "A phase-separated nuclear GBPL circuit controls immunity in plants," Nature, Nature, vol. 594(7863), pages 424-429, June.
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