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

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 signifi...

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Autores principales: Tu, Chin-Wei, Huang, Ying-Wen, Lee, Chin-Wei, Kuo, Song-Yi, Lin, Na-Sheng, Hsu, Yau-Heiu, Hu, Chung-Chi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405324/
https://www.ncbi.nlm.nih.gov/pubmed/37481165
http://dx.doi.org/10.1016/j.virusres.2023.199179
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author Tu, Chin-Wei
Huang, Ying-Wen
Lee, Chin-Wei
Kuo, Song-Yi
Lin, Na-Sheng
Hsu, Yau-Heiu
Hu, Chung-Chi
author_facet Tu, Chin-Wei
Huang, Ying-Wen
Lee, Chin-Wei
Kuo, Song-Yi
Lin, Na-Sheng
Hsu, Yau-Heiu
Hu, Chung-Chi
author_sort Tu, Chin-Wei
collection PubMed
description 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.
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spelling pubmed-104053242023-08-08 Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana Tu, Chin-Wei Huang, Ying-Wen Lee, Chin-Wei Kuo, Song-Yi Lin, Na-Sheng Hsu, Yau-Heiu Hu, Chung-Chi Virus Res Article 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. Elsevier 2023-07-26 /pmc/articles/PMC10405324/ /pubmed/37481165 http://dx.doi.org/10.1016/j.virusres.2023.199179 Text en © 2023 The Authors. Published by Elsevier B.V. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Tu, Chin-Wei
Huang, Ying-Wen
Lee, Chin-Wei
Kuo, Song-Yi
Lin, Na-Sheng
Hsu, Yau-Heiu
Hu, Chung-Chi
Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
title Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
title_full Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
title_fullStr Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
title_full_unstemmed Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
title_short Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
title_sort argonaute 5-mediated antiviral defense and viral counter-defense in nicotiana benthamiana
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405324/
https://www.ncbi.nlm.nih.gov/pubmed/37481165
http://dx.doi.org/10.1016/j.virusres.2023.199179
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