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Endocytosis-mediated entry of a caterpillar effector into plants is countered by Jasmonate

Author

Listed:
  • Zi-Wei Yan

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

  • Fang-Yan Chen

    (Chinese Academy of Sciences (CAS)
    University of CAS
    CEMPS/SIPPE, CAS)

  • Xian Zhang

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

  • Wen-Juan Cai

    (Core Facility Center of CEMPS/SIPPE, CAS)

  • Chun-Yu Chen

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

  • Jie Liu

    (Chinese Academy of Sciences (CAS)
    Shanghai Normal University)

  • Man-Ni Wu

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

  • Ning-Jing Liu

    (CEMPS/SIPPE, CAS)

  • Bin Ma

    (CEMPS/SIPPE, CAS)

  • Mu-Yang Wang

    (Chinese Academy of Sciences (CAS))

  • Dai-Yin Chao

    (CEMPS/SIPPE, CAS)

  • Cai-Ji Gao

    (South China Normal University (SCNU))

  • Ying-Bo Mao

    (Chinese Academy of Sciences (CAS))

Abstract

Insects and pathogens release effectors into plant cells to weaken the host defense or immune response. While the imports of some bacterial and fungal effectors into plants have been previously characterized, the mechanisms of how caterpillar effectors enter plant cells remain a mystery. Using live cell imaging and real-time protein tracking, we show that HARP1, an effector from the oral secretions of cotton bollworm (Helicoverpa armigera), enters plant cells via protein-mediated endocytosis. The entry of HARP1 into a plant cell depends on its interaction with vesicle trafficking components including CTL1, PATL2, and TET8. The plant defense hormone jasmonate (JA) restricts HARP1 import by inhibiting endocytosis and HARP1 loading into endosomes. Combined with the previous report that HARP1 inhibits JA signaling output in host plants, it unveils that the effector and JA establish a defense and counter-defense loop reflecting the robust arms race between plants and insects.

Suggested Citation

  • Zi-Wei Yan & Fang-Yan Chen & Xian Zhang & Wen-Juan Cai & Chun-Yu Chen & Jie Liu & Man-Ni Wu & Ning-Jing Liu & Bin Ma & Mu-Yang Wang & Dai-Yin Chao & Cai-Ji Gao & Ying-Bo Mao, 2023. "Endocytosis-mediated entry of a caterpillar effector into plants is countered by Jasmonate," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42226-1
    DOI: 10.1038/s41467-023-42226-1
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    References listed on IDEAS

    as
    1. Ying-Bo Mao & Yao-Qian Liu & Dian-Yang Chen & Fang-Yan Chen & Xin Fang & Gao-Jie Hong & Ling-Jian Wang & Jia-Wei Wang & Xiao-Ya Chen, 2017. "Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    2. Marcelo L. Campos & Yuki Yoshida & Ian T. Major & Dalton de Oliveira Ferreira & Sarathi M. Weraduwage & John E. Froehlich & Brendan F. Johnson & David M. Kramer & Georg Jander & Thomas D. Sharkey & Gr, 2016. "Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs," Nature Communications, Nature, vol. 7(1), pages 1-10, November.
    3. Bryan Thines & Leron Katsir & Maeli Melotto & Yajie Niu & Ajin Mandaokar & Guanghui Liu & Kinya Nomura & Sheng Yang He & Gregg A. Howe & John Browse, 2007. "JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling," Nature, Nature, vol. 448(7154), pages 661-665, August.
    4. Nicolás M. Cecchini & Kevin Steffes & Michael R. Schläppi & Andrew N. Gifford & Jean T. Greenberg, 2015. "Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    5. Laura B. Sheard & Xu Tan & Haibin Mao & John Withers & Gili Ben-Nissan & Thomas R. Hinds & Yuichi Kobayashi & Fong-Fu Hsu & Michal Sharon & John Browse & Sheng Yang He & Josep Rizo & Gregg A. Howe & N, 2010. "Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor," Nature, Nature, vol. 468(7322), pages 400-405, November.
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    1. Lihui Jiang & Xiaoyan Zhang & Yiting Zhao & Haiyan Zhu & Qijing Fu & Xinqi Lu & Wuying Huang & Xinyue Yang & Xuan Zhou & Lixia Wu & Ao Yang & Xie He & Man Dong & Ziai Peng & Jing Yang & Liwei Guo & Ji, 2024. "Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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