IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42226-1.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42226-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42226-1?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. 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.
    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.
    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.
    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. 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.

    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. 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.
    2. Lingmin Yuan & Fei Gao & Zongyang Lv & Digant Nayak & Anindita Nayak & Priscila dos Santos Bury & Kristin E. Cano & Lijia Jia & Natalia Oleinik & Firdevs Cansu Atilgan & Besim Ogretmen & Katelyn M. Wi, 2022. "Crystal structures reveal catalytic and regulatory mechanisms of the dual-specificity ubiquitin/FAT10 E1 enzyme Uba6," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Shiyun Cao & Shoukai Kang & Haibin Mao & Jiayu Yao & Liangcai Gu & Ning Zheng, 2022. "Defining molecular glues with a dual-nanobody cannabidiol sensor," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. 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.
    5. 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.
    6. 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.
    7. 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_s41467-023-42226-1. 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.