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

Baoye He, Huan Wang, Guosheng Liu, Angela Chen, Alejandra Calvo, Qiang Cai and Hailing Jin ()
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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

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-40093-4

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