Viral-inducible Argonaute18 confers broad-spectrum virus resistance in rice by sequestering a host microRNA

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.DOI: http://dx.doi.org/10.7554/eLife.05733.001

Functional and Genetic Analysis Identify a Role for Arabidopsis ARGONAUTE5 in Antiviral RNA Silencing

“…In vitro catalytic assays have shown that AGO2 and AGO5 possess a strong slicer activity against Tomato bushy stunt virus transcripts (Schuck et al, 2013). This is in contrast with AGO18, which does not appear to directly target viral RNA but rather functions by sequestering an endogenous microRNA targeting AGO1 (Wu et al, 2015). However, our results are in agreement with a previous study showing that the catalytic activity of AGO2 is required for defense against TuMV (Carbonell et al, 2012).…”

“…This induction is not dependant on the latter mutations as PlAMV, which infects Arabidopsis (Yamaji et al, 2012), induced AGO5 expression in wild-type Col-0 plants. Interestingly, it has recently been reported that AGO18, a member of a monocot-specific AGO protein clade, mediates virus resistance and is induced in virus-infected tissues (Wu et al, 2015). Whether systemic induction of AGO5 expression is induced by the presence of viral RNA itself, secondary vsiRNAs, or some other endogenous signal, and whether it shares similarities with AGO18 induction, remain to be elucidated.…”

RNAi in Plants: An Argonaute-Centered View

“…More recent studies have revealed that some AGOs have additional functions. These include Arabidopsis AGO10 and rice AGO18 that act as decoys of specific miRNAs Wu et al, 2015) and AGO2 that mediates DSB repair (Wei et al, 2012;Ba and Qi, 2013). Below we discuss the actions and mechanisms of AGOs in association with different classes of sRNAs.…”

“…Two plant AGO proteins, AGO10 in Arabidopsis and AGO18 in rice, have been demonstrated to compete with AGO1 for specific miRNAs and abrogate their activities through sequestration Wu et al, 2015). Arabidopsis AGO10 predominantly binds miR165/166, thereby preventing their loading into AGO1 and the subsequent repression of HD-ZIP III, targets of miR165/ 166 .…”

A Violaxanthin Deepoxidase Interacts with a Viral Suppressor of RNA Silencing to Inhibit Virus Amplification

“…Most antiviral responses are investigated using dicotyledonous plants, but recently, AGO18 and miRNA528 were reported to be involved in antiviral responses in rice (Wu et al, 2015. In addition, two quantitative resistance genes against SCMV in maize have been identified (Leng et al, 2017;Liu et al, 2017).…”