TY - JOUR
T1 - Plant mRNAs move into a fungal pathogen via extracellular vesicles to reduce infection
AU - Wang, Shumei
AU - He, Baoye
AU - Wu, Huaitong
AU - Cai, Qiang
AU - Ramírez-Sánchez, Obed
AU - Abreu-Goodger, Cei
AU - Birch, Paul R.J.
AU - Jin, Hailing
N1 - We thank Prof. Julia Bailey-Serres for helpful advice on TRAP and polysome analysis, as well as for sharing ultracentrifuge to isolate B. cinerea polysome fractions. We thank Dr. Angela Chen for assisting with the nanoparticle assay and Yifan Huang for TEM of EVs. This work was supported by grants from the National Institute of Health ( R35GM136379 ), the National Science Foundation ( IOS 2020731 ), and United State Department of Agriculture ( 2021-67013-34258 ) to H.J.; National Natural Science Foundation of China ( 32272029 , 32070288 ) and Hubei Provincial Natural Science Foundation of China ( 2022CFA079 ) to Q.C.; ERC Advanced grant PathEVome ( 787764 ) to P.B.
Publisher Copyright:
© 2023 The Authors
PY - 2024/1/10
Y1 - 2024/1/10
N2 - Cross-kingdom small RNA trafficking between hosts and microbes modulates gene expression in the interacting partners during infection. However, whether other RNAs are also transferred is unclear. Here, we discover that host plant Arabidopsis thaliana delivers mRNAs via extracellular vesicles (EVs) into the fungal pathogen Botrytis cinerea. A fluorescent RNA aptamer reporter Broccoli system reveals host mRNAs in EVs and recipient fungal cells. Using translating ribosome affinity purification profiling and polysome analysis, we observe that delivered host mRNAs are translated in fungal cells. Ectopic expression of two transferred host mRNAs in B. cinerea shows that their proteins are detrimental to infection. Arabidopsis knockout mutants of the genes corresponding to these transferred mRNAs are more susceptible. Thus, plants have a strategy to reduce infection by transporting mRNAs into fungal cells. mRNAs transferred from plants to pathogenic fungi are translated to compromise infection, providing knowledge that helps combat crop diseases.
AB - Cross-kingdom small RNA trafficking between hosts and microbes modulates gene expression in the interacting partners during infection. However, whether other RNAs are also transferred is unclear. Here, we discover that host plant Arabidopsis thaliana delivers mRNAs via extracellular vesicles (EVs) into the fungal pathogen Botrytis cinerea. A fluorescent RNA aptamer reporter Broccoli system reveals host mRNAs in EVs and recipient fungal cells. Using translating ribosome affinity purification profiling and polysome analysis, we observe that delivered host mRNAs are translated in fungal cells. Ectopic expression of two transferred host mRNAs in B. cinerea shows that their proteins are detrimental to infection. Arabidopsis knockout mutants of the genes corresponding to these transferred mRNAs are more susceptible. Thus, plants have a strategy to reduce infection by transporting mRNAs into fungal cells. mRNAs transferred from plants to pathogenic fungi are translated to compromise infection, providing knowledge that helps combat crop diseases.
UR - https://www.scopus.com/pages/publications/85180469056
U2 - 10.1016/j.chom.2023.11.020
DO - 10.1016/j.chom.2023.11.020
M3 - Article
C2 - 38103543
AN - SCOPUS:85180469056
SN - 1931-3128
VL - 32
SP - 93-105.e6
JO - Cell Host and Microbe
JF - Cell Host and Microbe
IS - 1
ER -