IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40472-x.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40472-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40472-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    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. Yao Xia & Rongfeng Zou & Maxime Escouboué & Liang Zhong & Chengjun Zhu & Cécile Pouzet & Xueqiang Wu & Yongjin Wang & Guohua Lv & Haibo Zhou & Pinghua Sun & Ke Ding & Laurent Deslandes & Shuguang Yuan, 2021. "Secondary-structure switch regulates the substrate binding of a YopJ family acetyltransferase," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Qingsong Liu & Xiaoyun Hu & Shuangli Su & Yuese Ning & Yufa Peng & Gongyin Ye & Yonggen Lou & Ted C. J. Turlings & Yunhe Li, 2021. "Cooperative herbivory between two important pests of rice," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    5. Xiaoyue Chen & Graham A. Hudson & Charlotte Mineo & Bashar Amer & Edward E. K. Baidoo & Samantha A. Crowe & Yuzhong Liu & Jay D. Keasling & Henrik V. Scheller, 2023. "Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Ameneh Asadi-Sardari & Esmat Mahdikhani-Moghadam & Mohammad Zaki-Aghl & Ramesh Raju Vetukuri, 2022. "Constitutive and Inducible Expression of Genes Related to Salicylic Acid and Ethylene Pathways in a Moderately Resistant Tomato Cultivar Leads to Delayed Development of Meloidogyne javanica," Agriculture, MDPI, vol. 12(12), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40472-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.