Plant mRNAs move into a fungal pathogen via extracellular vesicles to reduce infection.

cross-kingdom RNA trafficking extracellular vesicles mitochondria plant immunity plant-fungal interaction translating ribosome affinity purification profiling

Journal

Cell host & microbe
ISSN: 1934-6069
Titre abrégé: Cell Host Microbe
Pays: United States
ID NLM: 101302316

Informations de publication

Date de publication:
13 Dec 2023
Historique:
received: 27 07 2023
revised: 17 10 2023
accepted: 20 11 2023
medline: 17 12 2023
pubmed: 17 12 2023
entrez: 16 12 2023
Statut: aheadofprint

Résumé

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.

Identifiants

pubmed: 38103543
pii: S1931-3128(23)00470-5
doi: 10.1016/j.chom.2023.11.020
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Shumei Wang (S)

Department of Microbiology and Plant Pathology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, USA.

Baoye He (B)

Department of Microbiology and Plant Pathology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, USA.

Huaitong Wu (H)

Department of Microbiology and Plant Pathology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, USA.

Qiang Cai (Q)

State Key Laboratory of Hybrid Rice, College of Life Science, Wuhan University, Wuhan, China.

Obed Ramírez-Sánchez (O)

National Laboratory of Genomics for Biodiversity (Langebio), Cinvestav, Irapuato 36821 Guanajuato, Mexico.

Cei Abreu-Goodger (C)

Institute of Ecology and Evolution, School of Biological Sciences, the University of Edinburgh, Edinburgh EH9 3FL, UK.

Paul R J Birch (PRJ)

Division of Plant Sciences, School of Life Science, University of Dundee at James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK; Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK.

Hailing Jin (H)

Department of Microbiology and Plant Pathology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, USA. Electronic address: hailingj@ucr.edu.

Classifications MeSH