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XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis

Author

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  • Ying-Lan Chen

    (Academia Sinica
    National Cheng Kung University)

  • Fan-Wei Lin

    (Academia Sinica)

  • Kai-Tan Cheng

    (Academia Sinica)

  • Chi-Hsin Chang

    (Academia Sinica
    Taiwan International Graduate Program, Academia Sinica
    National Chung-Hsing University)

  • Sheng-Chi Hung

    (Academia Sinica
    National Taiwan University)

  • Thomas Efferth

    (Johannes Gutenberg University)

  • Yet-Ran Chen

    (Academia Sinica
    Taiwan International Graduate Program, Academia Sinica
    National Chung-Hsing University
    National Taiwan University)

Abstract

Proteolytic activation of cytokines regulates immunity in diverse organisms. In animals, cysteine-dependent aspartate-specific proteases (caspases) play central roles in cytokine maturation. Although the proteolytic production of peptide cytokines is also essential for plant immunity, evidence for cysteine-dependent aspartate-specific proteases in regulating plant immunity is still limited. In this study, we found that the C-terminal proteolytic processing of a caspase-like substrate motif “CNYD” within Pathogenesis-related protein 1 (PR1) generates an immunomodulatory cytokine (CAPE9) in Arabidopsis. Salicylic acid enhances CNYD-targeted protease activity and the proteolytic release of CAPE9 from PR1 in Arabidopsis. This process involves a protease exhibiting caspase-like enzyme activity, identified as Xylem cysteine peptidase 1 (XCP1). XCP1 exhibits a calcium-modulated pH-activity profile and a comparable activity to human caspases. XCP1 is required to induce systemic immunity triggered by pathogen-associated molecular patterns. This work reveals XCP1 as a key protease for plant immunity, which produces the cytokine CAPE9 from the canonical salicylic acid signaling marker PR1 to activate systemic immunity.

Suggested Citation

  • Ying-Lan Chen & Fan-Wei Lin & Kai-Tan Cheng & Chi-Hsin Chang & Sheng-Chi Hung & Thomas Efferth & Yet-Ran Chen, 2023. "XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40406-7
    DOI: 10.1038/s41467-023-40406-7
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    1. Bethany Huot & Christian Danve M. Castroverde & André C. Velásquez & Emily Hubbard & Jane A. Pulman & Jian Yao & Kevin L. Childs & Kenichi Tsuda & Beronda L. Montgomery & Sheng Yang He, 2017. "Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
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    1. Yu-Han Lin & Meng-Yun Xu & Chuan-Chih Hsu & Florensia Ariani Damei & Hui-Chun Lee & Wei-Lun Tsai & Cuong V. Hoang & Yin-Ru Chiang & Lay-Sun Ma, 2023. "Ustilago maydis PR-1-like protein has evolved two distinct domains for dual virulence activities," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Peng Liu & Chaonan Shi & Shuang Liu & Jiajia Lei & Qisen Lu & Haichao Hu & Yan Ren & Ning Zhang & Congwei Sun & Lu Chen & Yaoyao Jiang & Lixiao Feng & Tianye Zhang & Kaili Zhong & Jiaqian Liu & Juan Z, 2023. "A papain-like cysteine protease-released small signal peptide confers wheat resistance to wheat yellow mosaic virus," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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