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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
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    References listed on IDEAS

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    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. 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.
    4. 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.
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