IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40093-4.html
   My bibliography  Save this article

Fungal small RNAs ride in extracellular vesicles to enter plant cells through clathrin-mediated endocytosis

Author

Listed:
  • Baoye He

    (University of California)

  • Huan Wang

    (University of California)

  • Guosheng Liu

    (Wuhan University)

  • Angela Chen

    (University of California)

  • Alejandra Calvo

    (University of California)

  • Qiang Cai

    (Wuhan University)

  • Hailing Jin

    (University of California)

Abstract

Small RNAs (sRNAs) of the fungal pathogen Botrytis cinerea can enter plant cells and hijack host Argonaute protein 1 (AGO1) to silence host immunity genes. However, the mechanism by which these fungal sRNAs are secreted and enter host cells remains unclear. Here, we demonstrate that B. cinerea utilizes extracellular vesicles (EVs) to secrete Bc-sRNAs, which are then internalized by plant cells through clathrin-mediated endocytosis (CME). The B. cinerea tetraspanin protein, Punchless 1 (BcPLS1), serves as an EV biomarker and plays an essential role in fungal pathogenicity. We observe numerous Arabidopsis clathrin-coated vesicles (CCVs) around B. cinerea infection sites and the colocalization of B. cinerea EV marker BcPLS1 and Arabidopsis CLATHRIN LIGHT CHAIN 1, one of the core components of CCV. Meanwhile, BcPLS1 and the B. cinerea-secreted sRNAs are detected in purified CCVs after infection. Arabidopsis knockout mutants and inducible dominant-negative mutants of key components of the CME pathway exhibit increased resistance to B. cinerea infection. Furthermore, Bc-sRNA loading into Arabidopsis AGO1 and host target gene suppression are attenuated in those CME mutants. Together, our results demonstrate that fungi secrete sRNAs via EVs, which then enter host plant cells mainly through CME.

Suggested Citation

  • Baoye He & Huan Wang & Guosheng Liu & Angela Chen & Alejandra Calvo & Qiang Cai & Hailing Jin, 2023. "Fungal small RNAs ride in extracellular vesicles to enter plant cells through clathrin-mediated endocytosis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40093-4
    DOI: 10.1038/s41467-023-40093-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40093-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40093-4?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. Wim Dejonghe & Sabine Kuenen & Evelien Mylle & Mina Vasileva & Olivier Keech & Corrado Viotti & Jef Swerts & Matyáš Fendrych & Fausto Andres Ortiz-Morea & Kiril Mishev & Simon Delang & Stefan Scholl &, 2016. "Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
    2. Amy H. Buck & Gillian Coakley & Fabio Simbari & Henry J. McSorley & Juan F. Quintana & Thierry Le Bihan & Sujai Kumar & Cei Abreu-Goodger & Marissa Lear & Yvonne Harcus & Alessandro Ceroni & Simon A. , 2014. "Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    3. Saima Shahid & Gunjune Kim & Nathan R. Johnson & Eric Wafula & Feng Wang & Ceyda Coruh & Vivian Bernal-Galeano & Tamia Phifer & Claude W. dePamphilis & James H. Westwood & Michael J. Axtell, 2018. "MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs," Nature, Nature, vol. 553(7686), pages 82-85, January.
    4. Chunlai Cui & Yan Wang & Jingnan Liu & Jing Zhao & Peilu Sun & Sibao Wang, 2019. "A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    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. Nicholas C. Gervais & Rebecca S. Shapiro, 2024. "Discovering the hidden function in fungal genomes," Nature Communications, Nature, vol. 15(1), pages 1-12, 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. 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.
    2. Ziwei Zhu & Jun Xiong & Hao Shi & Yuchen Liu & Junjie Yin & Kaiwei He & Tianyu Zhou & Liting Xu & Xiaobo Zhu & Xiang Lu & Yongyan Tang & Li Song & Qingqing Hou & Qing Xiong & Long Wang & Daihua Ye & T, 2023. "Magnaporthe oryzae effector MoSPAB1 directly activates rice Bsr-d1 expression to facilitate pathogenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Anna Kokla & Martina Leso & Xiang Zhang & Jan Simura & Phanu T. Serivichyaswat & Songkui Cui & Karin Ljung & Satoko Yoshida & Charles W. Melnyk, 2022. "Nitrogen represses haustoria formation through abscisic acid in the parasitic plant Phtheirospermum japonicum," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Maxim V. Zagoskin & Jianbin Wang & Ashley T. Neff & Giovana M. B. Veronezi & Richard E. Davis, 2022. "Small RNA pathways in the nematode Ascaris in the absence of piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-19, 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_s41467-023-40093-4. 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.