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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-09-01
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| Series: | Virus Research |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0168170223001417 |
| _version_ | 1797755846020562944 |
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| author | Chin-Wei Tu Ying-Wen Huang Chin-Wei Lee Song-Yi Kuo Na-Sheng Lin Yau-Heiu Hsu Chung-Chi Hu |
| author_facet | Chin-Wei Tu Ying-Wen Huang Chin-Wei Lee Song-Yi Kuo Na-Sheng Lin Yau-Heiu Hsu Chung-Chi Hu |
| author_sort | Chin-Wei Tu |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-12T17:51:58Z |
| format | Article |
| id | doaj.art-d187b6a36e9746e7832939a6b0362af7 |
| institution | Directory Open Access Journal |
| issn | 1872-7492 |
| language | English |
| last_indexed | 2024-03-12T17:51:58Z |
| publishDate | 2023-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Virus Research |
| spelling | doaj.art-d187b6a36e9746e7832939a6b0362af72023-08-03T04:22:36ZengElsevierVirus Research1872-74922023-09-01334199179Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamianaChin-Wei Tu0Ying-Wen Huang1Chin-Wei Lee2Song-Yi Kuo3Na-Sheng Lin4Yau-Heiu Hsu5Chung-Chi Hu6PhD Program in Microbial Genomics, National Chung Hsing University and Academia Sinica, Taichung 40227, TaiwanGraduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, TaiwanGraduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, TaiwanTemasek Life Sciences Laboratory, National University of Singapore, Singapore 117604, SingaporeInstitute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, TaiwanGraduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, TaiwanGraduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, Taiwan; Corresponding author.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.http://www.sciencedirect.com/science/article/pii/S0168170223001417AGO5RNA silencingPlant antiviral defenseViral suppressors of RNA silencing (VSR)26S proteasomeAutophagy |
| spellingShingle | Chin-Wei Tu Ying-Wen Huang Chin-Wei Lee Song-Yi Kuo Na-Sheng Lin Yau-Heiu Hsu Chung-Chi Hu Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana Virus Research AGO5 RNA silencing Plant antiviral defense Viral suppressors of RNA silencing (VSR) 26S proteasome Autophagy |
| 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 | AGO5 RNA silencing Plant antiviral defense Viral suppressors of RNA silencing (VSR) 26S proteasome Autophagy |
| url | http://www.sciencedirect.com/science/article/pii/S0168170223001417 |
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