OpenLB
Open Library of Bioscience
Advanced Search
Virus research
09, 2023;334 199179.

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

Chin-Wei Tu, Ying-Wen Huang, Chin-Wei Lee, Song-Yi Kuo, Na-Sheng Lin, Yau-Heiu Hsu, Chung-Chi Hu
Author Information
  1. Chin-Wei Tu: PhD Program in Microbial Genomics, National Chung Hsing University and Academia Sinica, Taichung 40227, Taiwan.
  2. Ying-Wen Huang: Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, Taiwan.
  3. Chin-Wei Lee: Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan.
  4. Song-Yi Kuo: Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604, Singapore.
  5. Na-Sheng Lin: Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan.
  6. Yau-Heiu Hsu: Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 40227, Taiwan; Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung 40227, Taiwan.
  7. Chung-Chi Hu: 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.
PMID: 37481165 DOI: 10.1016/j.virusres.2023.199179

Abstract

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.

Keywords

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

References

J Exp Bot. 2023 Apr 9;74(7):2374-2388 [PMID: 36722331]
Plant Cell. 2015 Jun;27(6):1742-54 [PMID: 26023161]
Plant Physiol. 2018 Jan;176(1):649-662 [PMID: 29133371]
Virus Res. 2023 Jan 2;323:198964 [PMID: 36223861]
Mol Plant Microbe Interact. 2015 Jan;2015(1):28-39 [PMID: 27839076]
New Phytol. 2019 Oct;224(2):804-817 [PMID: 31283838]
Plant J. 2014 May;78(3):385-97 [PMID: 24635777]
Phytopathology. 2023 Apr;113(4):616-625 [PMID: 36441873]
PLoS One. 2013;8(3):e59534 [PMID: 23555698]
Sci Rep. 2017 Apr 21;7(1):1010 [PMID: 28432338]
J Exp Bot. 2015 Feb;66(3):919-32 [PMID: 25385769]
Mol Plant Microbe Interact. 2012 Jan;25(1):97-106 [PMID: 21936664]
Trends Plant Sci. 2017 Aug;22(8):646-648 [PMID: 28633985]
J Exp Bot. 2011 Mar;62(5):1611-20 [PMID: 21357774]
Proc Natl Acad Sci U S A. 2021 Aug 24;118(34): [PMID: 34408020]
Mol Plant Microbe Interact. 2023 Jul;36(7):425-433 [PMID: 36853196]
Viruses. 2022 Feb 20;14(2): [PMID: 35216025]
Microbiol Mol Biol Rev. 2023 Jun 28;87(2):e0003522 [PMID: 37052496]
Mol Plant Microbe Interact. 2021 Sep;34(9):1010-1023 [PMID: 33983824]
Science. 1985 Mar 8;227(4691):1229-31 [PMID: 17757866]
Bioinformatics. 2015 Apr 1;31(7):1120-3 [PMID: 25414360]
Front Plant Sci. 2022 Jun 23;13:924482 [PMID: 35812928]
Trends Microbiol. 2019 Sep;27(9):792-805 [PMID: 31213342]
Viruses. 2021 Sep 15;13(9): [PMID: 34578418]
Front Microbiol. 2015 Nov 09;6:1237 [PMID: 26617580]
J Exp Bot. 2020 Oct 22;71(20):6197-6210 [PMID: 32835379]
New Phytol. 2021 Feb;229(3):1289-1297 [PMID: 33037631]
J Gen Virol. 2021 Oct;102(10): [PMID: 34623234]
Sci Rep. 2019 Mar 14;9(1):4437 [PMID: 30872606]
Virology. 2012 May 10;426(2):178-87 [PMID: 22361475]
Development. 2012 Apr;139(8):1399-404 [PMID: 22399683]
Genes (Basel). 2017 Nov 28;8(12): [PMID: 29182547]
Plant Cell Physiol. 2020 May 1;61(5):957-966 [PMID: 32105323]
Plants (Basel). 2022 Sep 22;11(19): [PMID: 36235343]
Genome Biol. 2021 Dec 15;22(1):340 [PMID: 34911561]
Nat Plants. 2018 Mar;4(3):157-164 [PMID: 29497161]
Curr Opin Virol. 2018 Oct;32:88-99 [PMID: 30388659]
Front Plant Sci. 2020 Nov 12;11:594758 [PMID: 33281853]
Nat Commun. 2023 Jun 7;14(1):3333 [PMID: 37286636]
New Phytol. 2020 May;226(3):866-878 [PMID: 31880814]
Plant Cell. 2007 Jun;19(6):2053-63 [PMID: 17586651]
Nat Plants. 2017 Jan 06;3:16203 [PMID: 28059073]
Annu Rev Virol. 2020 Sep 29;7(1):403-419 [PMID: 32530794]
Curr Opin Plant Biol. 2015 Oct;27:111-7 [PMID: 26190744]
Plant Biotechnol J. 2014 Apr;12(3):330-43 [PMID: 24283212]
Curr Opin Plant Biol. 2018 Oct;45(Pt A):59-67 [PMID: 29857309]
Nat Rev Immunol. 2019 Jan;19(1):31-44 [PMID: 30301972]
Nat Commun. 2022 May 30;13(1):2994 [PMID: 35637208]
Proc Natl Acad Sci U S A. 2012 Sep 25;109(39):15942-6 [PMID: 23019378]
Curr Opin Virol. 2016 Apr;17:39-44 [PMID: 26802204]
Curr Opin Virol. 2021 Feb;46:65-72 [PMID: 33360834]
Plant Physiol. 2015 Jul;168(3):938-52 [PMID: 26015446]
Mol Plant Pathol. 2023 Aug;24(8):961-972 [PMID: 37118922]
Virology. 2018 Nov;524:127-139 [PMID: 30195250]
Mol Plant Pathol. 2010 Sep;11(5):641-9 [PMID: 20696002]
Mol Plant Pathol. 2021 Jun;22(6):627-643 [PMID: 33749125]
Plant Cell. 2021 Aug 31;33(8):2685-2700 [PMID: 34003932]
Virology. 2014 May;456-457:188-97 [PMID: 24889238]
PLoS One. 2011 Jan 31;6(1):e14639 [PMID: 21305057]
PLoS Pathog. 2010 Jul 15;6(7):e1000996 [PMID: 20657820]
Mol Plant Pathol. 2013 Aug;14(6):567-75 [PMID: 23578299]
Plant Physiol. 2023 Feb 12;191(2):904-924 [PMID: 36459587]
Viruses. 2016 Nov 19;8(11): [PMID: 27869775]
Nat Rev Microbiol. 2013 Nov;11(11):745-60 [PMID: 24129510]
Elife. 2015 Feb 17;4: [PMID: 25688565]
New Phytol. 2020 Oct;228(2):622-639 [PMID: 32479643]
Int J Mol Sci. 2022 Jan 08;23(2): [PMID: 35054880]
Plant Sci. 2019 Feb;279:87-95 [PMID: 30709497]
Plant Physiol. 2011 Jul;156(3):1548-55 [PMID: 21606315]
Plant J. 2022 Mar;109(5):1086-1097 [PMID: 34845788]
Virol J. 2023 Jan 17;20(1):10 [PMID: 36650505]
FEBS Lett. 2022 Sep;596(17):2152-2162 [PMID: 35404481]
J Virol. 2016 Dec 16;91(1): [PMID: 27795417]
Autophagy. 2022 Jun;18(6):1450-1462 [PMID: 34740306]
Nat Rev Mol Cell Biol. 2022 Oct;23(10):645-662 [PMID: 35710830]
Plant Cell. 2016 Feb;28(2):272-85 [PMID: 26869699]
J Virol. 2011 Sep;85(17):8829-40 [PMID: 21715476]
Front Plant Sci. 2022 Nov 17;13:1034419 [PMID: 36466235]
PLoS Pathog. 2015 Mar 25;11(3):e1004755 [PMID: 25806948]
Nat Commun. 2020 Nov 27;11(1):6031 [PMID: 33247135]
Plant Cell. 2017 Apr;29(4):708-725 [PMID: 28351993]
Int J Mol Sci. 2023 May 08;24(9): [PMID: 37176135]
Curr Top Microbiol Immunol. 2013;371:153-81 [PMID: 23686235]
Proc Natl Acad Sci U S A. 2019 Nov 5;116(45):22872-22883 [PMID: 31628252]
J Cell Sci. 2016 Oct 1;129(19):3553-3561 [PMID: 27521428]
Plant Physiol. 2019 Jul;180(3):1418-1435 [PMID: 31043494]
Virology. 2015 Dec;486:209-18 [PMID: 26454664]
Genes (Basel). 2019 Jul 12;10(7): [PMID: 31336929]
Virology. 2015 May;479-480:85-103 [PMID: 25766638]
Plant Cell. 2012 Sep;24(9):3613-29 [PMID: 23023169]
BMC Plant Biol. 2014 Nov 29;14:327 [PMID: 25432517]
Plant Cell. 2007 Aug;19(8):2583-94 [PMID: 17675402]
Plant Cell. 2011 Apr;23(4):1625-38 [PMID: 21467580]
Stress Biol. 2022 Aug 19;2(1):33 [PMID: 37676459]
Trends Plant Sci. 2019 Jun;24(6):519-529 [PMID: 31003895]
Bot Stud. 2020 Aug 3;61(1):22 [PMID: 32748085]
PLoS Pathog. 2023 Jan 25;19(1):e1010482 [PMID: 36696453]
EMBO J. 2021 Aug 2;40(15):e108050 [PMID: 34155657]
Proc Natl Acad Sci U S A. 2008 Sep 23;105(38):14732-7 [PMID: 18799732]
Int J Mol Sci. 2022 Aug 29;23(17): [PMID: 36077222]
Plants (Basel). 2021 Apr 26;10(5): [PMID: 33925878]
Plant Physiol. 2017 May;174(1):339-355 [PMID: 28270624]

MeSH Term

Antiviral Agents
RNA
Potyvirus
Cytomegalovirus Infections
Cucumovirus
RNA Interference
Plant Diseases
Nicotiana
Tymovirus

Chemicals

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

Word Cloud

Similar Articles

Cited By