Plant YTHDF proteins are direct effectors of antiviral immunity against an N6-methyladenosine-containing RNA virus

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In virus–host interactions, nucleic acid-directed first lines of defense that allow viral clearance without compromising growth are of paramount importance. Plants use the RNA interference pathway as a basal antiviral immune system, but additional RNA-based mechanisms of defense also exist. The infectivity of a plant positive-strand RNA virus, alfalfa mosaic virus (AMV), relies on the demethylation of viral RNA by the recruitment of the cellular N6-methyladenosine (m6A) demethylase ALKBH9B, but how demethylation of viral RNA promotes AMV infection remains unknown. Here, we show that inactivation of the Arabidopsis cytoplasmic YT521-B homology domain (YTH)-containing m6A-binding proteins ECT2, ECT3, and ECT5 is sufficient to restore AMV infectivity in partially resistant alkbh9b mutants. We further show that the antiviral function of ECT2 is distinct from its previously demonstrated function in the promotion of primordial cell proliferation: an ect2 mutant carrying a small deletion in its intrinsically disordered region is partially compromised for antiviral defense but not for developmental functions. These results indicate that the m6A-YTHDF axis constitutes a novel branch of basal antiviral immunity in plants.
OriginalsprogEngelsk
Artikelnummere113378
TidsskriftEMBO Journal
Vol/bind42
Udgave nummer18
Antal sider17
ISSN0261-4189
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
We thank Lorena Corachán, Freja Asmussen, and Lena Bjørn Johansson for their excellent technical assistance, and Joao Rato, Daniel Torrent‐Silla, and the Bioinformatics Core Service at the Instituto de Biología Molecular y Celular de Plantas (IBMCP) for the support provided in the differential expression analysis of mRNA‐seq data. Emilie Oksbjerg is thanked for performing NextSeq runs of HyperTRIBE. Kamil Růžička is thanked for seeds of . We acknowledge the use of computational resources from The Danish National Life Science Supercomputing Center Computerome, the core facility for biocomputing at the Department of Biology, and the funding from the PRISM (Protein Interactions and Stability in Medicine and Genomics) center funded by the Novo Nordisk Foundation (to KL‐L; NNF18OC0033950). SB is a recipient of an EMBO postdoctoral fellowship (ALTF 810‐2022). MM‐P was the recipient of a Predoctoral Contract FPI‐2015‐072406 from the Subprograma FPI‐MINECO (Formación de Personal Investigador–Ministerio de Economía y Competitividad). This work was supported by grant PID2020‐115571RB‐I00 to VP and FA from the Spanish MCIN/AEI/ 10.13039/501100011033 granting agency and Fondo Europeo de Desarrollo Regional (FEDER), by a project grant from Villum Fonden (Project #13397) and by an infrastructure grant from Carlsberg Fondet (CF18‐1075) to PB. Part of this work was carried out in Prof. Brodersen's lab at the University of Copenhagen (Denmark) thanks to a FEBS (Federation of European Biochemical Societies) Short‐Term Fellowship from April to June 2019 to MM‐P. vir‐1

Publisher Copyright:
© 2023 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

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