Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana.

26S proteasome AGO5 Autophagy Plant antiviral defense RNA silencing Viral suppressors of RNA silencing (VSR)

Journal

Virus research
ISSN: 1872-7492
Titre abrégé: Virus Res
Pays: Netherlands
ID NLM: 8410979

Informations de publication

Date de publication:
09 2023
Historique:
received: 08 06 2023
revised: 18 07 2023
accepted: 19 07 2023
medline: 7 8 2023
pubmed: 23 7 2023
entrez: 22 7 2023
Statut: ppublish

Résumé

The argonaute (AGO) family proteins play a crucial role in preventing viral invasions through the plant antiviral RNA silencing pathway, with distinct AGO proteins recruited for specific antiviral mechanisms. Our previous study revealed that Nicotiana benthamiana AGO5 (NbAGO5) expression was significantly upregulated in response to bamboo mosaic virus (BaMV) infection. However, the roles of NbAGO5 in antiviral mechanisms remained to be explored. In this research, we examined the antiviral functions of NbAGO5 in the infections of different viruses. It was found that the accumulation of NbAGO5 was induced not only at the RNA but also at the protein level following the infections of BaMV, potato virus X (PVX), tobacco mosaic virus (TMV), and cucumber mosaic virus (CMV) in N. benthamiana. To explore the antiviral mechanism and regulatory function of NbAGO5, we generated NbAGO5 overexpression (OE-NbAGO5) and knockout (nbago5) transgenic N. benthamiana lines. Our findings reveal that NbAGO5 provides defense against BaMV, PVX, TMV, and a mutant CMV deficient in 2b gene, but not against the wild-type CMV and turnip mosaic virus (TuMV). Through affinity purification and small RNA northern blotting, we demonstrated that NbAGO5 exerts its antiviral function by binding to viral small interfering RNAs (vsiRNAs). Moreover, we observed that CMV 2b and TuMV HC-Pro interact with NbAGO5, triggering its degradation via the 26S proteasome and autophagy pathways, thereby allowing these viruses to overcome NbAGO5-mediated defense. In addition, TuMV HC-Pro provides another line of counter-defense by interfering with vsiRNA binding by NbAGO5. Our study provides further insights into the antiviral RNA interference mechanism and the complex interplay between NbAGO5 and plant viruses.

Identifiants

pubmed: 37481165
pii: S0168-1702(23)00141-7
doi: 10.1016/j.virusres.2023.199179
pmc: PMC10405324
pii:
doi:

Substances chimiques

Antiviral Agents 0
RNA 63231-63-0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

199179

Informations de copyright

Copyright © 2023. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Auteurs

Chin-Wei Tu (CW)

PhD Program in Microbial Genomics, National Chung Hsing University and Academia Sinica, Taichung 40227, Taiwan.

Ying-Wen Huang (YW)

Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, Taiwan.

Chin-Wei Lee (CW)

Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan.

Song-Yi Kuo (SY)

Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604, Singapore.

Na-Sheng Lin (NS)

Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan.

Yau-Heiu Hsu (YH)

Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, Taiwan.

Chung-Chi Hu (CC)

Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, Taiwan. Electronic address: cchu@dragon.nchu.edu.tw.

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Classifications MeSH