Viral-inducible Argonaute18 Confers Broad-spectrum Virus Resistance in Rice by Sequestering a Host MicroRNA

Overview

Journal Elife

Specialty Biology

Date 2015 Feb 18

PMID 25688565

Citations 104

Authors

Jianguo Wu

Zhirui Yang

Yu Wang

Lijia Zheng

Ruiqiang Ye

Yinghua Ji

Shanshan Zhao

Shaoyi Ji

Ruofei Liu

Le Xu

Hong Zheng

Yijun Zhou

Xin Zhang

Xiaofeng Cao

Lianhui Xie

Zujian Wu

Yijun Qi

Yi Li

Affiliations

Soon will be listed here.

Abstract

Viral pathogens are a major threat to rice production worldwide. Although RNA interference (RNAi) is known to mediate antiviral immunity in plant and animal models, the mechanism of antiviral RNAi in rice and other economically important crops is poorly understood. Here, we report that rice resistance to evolutionarily diverse viruses requires Argonaute18 (AGO18). Genetic studies reveal that the antiviral function of AGO18 depends on its activity to sequester microRNA168 (miR168) to alleviate repression of rice AGO1 essential for antiviral RNAi. Expression of miR168-resistant AGO1a in ago18 background rescues or increases rice antiviral activity. Notably, stable transgenic expression of AGO18 confers broad-spectrum virus resistance in rice. Our findings uncover a novel cooperative antiviral activity of two distinct AGO proteins and suggest a new strategy for the control of viral diseases in rice.

Citing Articles

Perception of viral infections and initiation of antiviral defence in rice.

Huang Y, Yang J, Sun X, Li J, Cao X, Yao S Nature. 2025; .

PMID: 40074903 DOI: 10.1038/s41586-025-08706-8.

The Roles of MicroRNAs in the Regulation of Rice-Pathogen Interactions.

Jia Y, Wei K, Qin J, Zhai W, Li Q, Li Y Plants (Basel). 2025; 14(1.

PMID: 39795396 PMC: 11722856. DOI: 10.3390/plants14010136.

Resistance Induced by Viral Sense, Anti-sense, and Hairpin Constructs Against Beet Curly Top Virus and Beet Curly Top Iran Virus.

Montazeri R, Malboobi M, Shams-Bakhsh M Iran J Biotechnol. 2024; 22(3):e3831.

PMID: 39737209 PMC: 11682523. DOI: 10.30498/ijb.2024.425159.3831.

Identification of the Brassinazole-Resistant () Gene Family in Wheat ( L.) and the Molecular Cloning and Functional Characterization of .

Zhang Y, Qin J, Hou J, Liu C, Geng S, Qin M Int J Mol Sci. 2024; 25(23).

PMID: 39684257 PMC: 11641346. DOI: 10.3390/ijms252312545.

Major components of RNAi gene families in cultivar : discovery and characterization.

Naim M, Alamin M, Mosharof M, Imtiaj A, Haque Mollah M Heliyon. 2024; 10(22):e40395.

PMID: 39624287 PMC: 11609679. DOI: 10.1016/j.heliyon.2024.e40395.

References

Manavella P, Weigel D, Wu L . Argonaute10 as a miRNA locker. Cell. 2011; 145(2):173-4. DOI: 10.1016/j.cell.2011.03.045. View

Pfaff J, Hennig J, Herzog F, Aebersold R, Sattler M, Niessing D . Structural features of Argonaute-GW182 protein interactions. Proc Natl Acad Sci U S A. 2013; 110(40):E3770-9. PMC: 3791723. DOI: 10.1073/pnas.1308510110. View

Maunoury N, Vaucheret H . AGO1 and AGO2 act redundantly in miR408-mediated Plantacyanin regulation. PLoS One. 2011; 6(12):e28729. PMC: 3236769. DOI: 10.1371/journal.pone.0028729. View

Mallory A, Hinze A, Tucker M, Bouche N, Gasciolli V, Elmayan T . Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet. 2009; 5(9):e1000646. PMC: 2730571. DOI: 10.1371/journal.pgen.1000646. View

Frank F, Sonenberg N, Nagar B . Structural basis for 5'-nucleotide base-specific recognition of guide RNA by human AGO2. Nature. 2010; 465(7299):818-22. DOI: 10.1038/nature09039. View

Mallory A, Vaucheret H . Form, function, and regulation of ARGONAUTE proteins. Plant Cell. 2010; 22(12):3879-89. PMC: 3027166. DOI: 10.1105/tpc.110.080671. View

Harvey J, Lewsey M, Patel K, Westwood J, Heimstadt S, Carr J . An antiviral defense role of AGO2 in plants. PLoS One. 2011; 6(1):e14639. PMC: 3031535. DOI: 10.1371/journal.pone.0014639. View

Xiong R, Wu J, Zhou Y, Zhou X . Identification of a movement protein of the tenuivirus rice stripe virus. J Virol. 2008; 82(24):12304-11. PMC: 2593352. DOI: 10.1128/JVI.01696-08. View

Hauptmann J, Meister G . Argonaute regulation: two roads to the same destination. Dev Cell. 2013; 25(6):553-4. DOI: 10.1016/j.devcel.2013.06.009. View

10.

Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert K, Montgomery T, Nguyen T . Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell. 2012; 24(9):3613-29. PMC: 3480291. DOI: 10.1105/tpc.112.099945. View

11.

Guang S, Bochner A, Pavelec D, Burkhart K, Harding S, Lachowiec J . An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science. 2008; 321(5888):537-41. PMC: 2771369. DOI: 10.1126/science.1157647. View

12.

Qu F, Ye X, Morris T . Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci U S A. 2008; 105(38):14732-7. PMC: 2567185. DOI: 10.1073/pnas.0805760105. View

13.

Ji L, Liu X, Yan J, Wang W, Yumul R, Kim Y . ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet. 2011; 7(3):e1001358. PMC: 3069122. DOI: 10.1371/journal.pgen.1001358. View

14.

Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X . MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell. 2013; 153(3):562-74. PMC: 3694718. DOI: 10.1016/j.cell.2013.04.005. View

15.

Qi Y, Mi S . Purification of Arabidopsis argonaute complexes and associated small RNAs. Methods Mol Biol. 2009; 592:243-54. DOI: 10.1007/978-1-60327-005-2_16. View

16.

Vazquez F, Legrand S, Windels D . The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci. 2010; 15(6):337-45. DOI: 10.1016/j.tplants.2010.04.001. View

17.

Voinnet O, Rivas S, Mestre P, Baulcombe D . An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 2003; 33(5):949-56. DOI: 10.1046/j.1365-313x.2003.01676.x. View

18.

Burgyan J, Havelda Z . Viral suppressors of RNA silencing. Trends Plant Sci. 2011; 16(5):265-72. DOI: 10.1016/j.tplants.2011.02.010. View

19.

Wang X, Jovel J, Udomporn P, Wang Y, Wu Q, Li W . The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell. 2011; 23(4):1625-38. PMC: 3101545. DOI: 10.1105/tpc.110.082305. View

20.

Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C . DNA methylation mediated by a microRNA pathway. Mol Cell. 2010; 38(3):465-75. DOI: 10.1016/j.molcel.2010.03.008. View