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Autophagy promotes jasmonate-mediated defense against nematodes

Author

Listed:
  • Jinping Zou

    (Zhejiang University)

  • Xinlin Chen

    (Zhejiang University)

  • Chenxu Liu

    (Zhejiang University)

  • Mingyue Guo

    (Zhejiang University)

  • Mukesh Kumar Kanwar

    (Zhejiang University)

  • Zhenyu Qi

    (Zhejiang University
    Zhejiang University
    Ministry of Agriculture and Rural Affairs of China)

  • Ping Yang

    (Zhejiang University)

  • Guanghui Wang

    (Zhejiang University)

  • Yan Bao

    (Shanghai Jiao Tong University)

  • Diane C. Bassham

    (Iowa State University)

  • Jingquan Yu

    (Zhejiang University
    Zhejiang University
    Ministry of Agriculture and Rural Affairs of China)

  • Jie Zhou

    (Zhejiang University
    Zhejiang University
    Ministry of Agriculture and Rural Affairs of China
    Zhejiang University)

Abstract

Autophagy, as an intracellular degradation system, plays a critical role in plant immunity. However, the involvement of autophagy in the plant immune system and its function in plant nematode resistance are largely unknown. Here, we show that root-knot nematode (RKN; Meloidogyne incognita) infection induces autophagy in tomato (Solanum lycopersicum) and different atg mutants exhibit high sensitivity to RKNs. The jasmonate (JA) signaling negative regulators JASMONATE-ASSOCIATED MYC2-LIKE 1 (JAM1), JAM2 and JAM3 interact with ATG8s via an ATG8-interacting motif (AIM), and JAM1 is degraded by autophagy during RKN infection. JAM1 impairs the formation of a transcriptional activation complex between ETHYLENE RESPONSE FACTOR 1 (ERF1) and MEDIATOR 25 (MED25) and interferes with transcriptional regulation of JA-mediated defense-related genes by ERF1. Furthermore, ERF1 acts in a positive feedback loop and regulates autophagy activity by transcriptionally activating ATG expression in response to RKN infection. Therefore, autophagy promotes JA-mediated defense against RKNs via forming a positive feedback circuit in the degradation of JAMs and transcriptional activation by ERF1.

Suggested Citation

  • Jinping Zou & Xinlin Chen & Chenxu Liu & Mingyue Guo & Mukesh Kumar Kanwar & Zhenyu Qi & Ping Yang & Guanghui Wang & Yan Bao & Diane C. Bassham & Jingquan Yu & Jie Zhou, 2023. "Autophagy promotes jasmonate-mediated defense against nematodes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40472-x
    DOI: 10.1038/s41467-023-40472-x
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    References listed on IDEAS

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    1. Lijing Liu & Fathi-Mohamed Sonbol & Bethany Huot & Yangnan Gu & John Withers & Musoki Mwimba & Jian Yao & Sheng Yang He & Xinnian Dong, 2016. "Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity," Nature Communications, Nature, vol. 7(1), pages 1-10, December.
    2. 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.
    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.
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    Cited by:

    1. Mingyue Guo & Fengjun Yang & Lijuan Zhu & Leilei Wang & Zhichao Li & Zhenyu Qi & Vasileios Fotopoulos & Jingquan Yu & Jie Zhou, 2024. "Loss of cold tolerance is conferred by absence of the WRKY34 promoter fragment during tomato evolution," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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