Nonsense-Mediated Decay Serves as a General Viral Restriction Mechanism in Plants

Summary

(+)strand RNA viruses have to overcome various points of restriction in the host to establish successful infection. In plants, this includes RNA silencing. To uncover additional bottlenecks to RNA virus infection, we genetically attenuated the impact of RNA silencing on transgenically expressed Potato virus X (PVX), a (+)strand RNA virus that replicates in Arabidopsis. A genetic screen in this sensitized background uncovered how nonsense-mediated decay (NMD), a host RNA quality control mechanism, recognizes and eliminates PVX RNAs with internal termination codons and long 3′ UTRs. NMD also operates in natural infection contexts, and while some viruses have evolved genome expression strategies to overcome this process altogether, the virulence of NMD-activating viruses entails their ability to directly suppress NMD or to promote an NMD-unfavorable cellular state. These principles of induction, evasion, and suppression define NMD as a general viral restriction mechanism in plants that also likely operates in animals.

Graphical Abstract

Highlights

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  A sensitized genetic screen for modifiers of (+)strand RNA virus accumulation in Arabidopsis

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  The host nonsense-mediated decay (NMD) pathway restricts PVX during natural infection

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  NMD targets viral RNAs containing internal termination codons and long 3′ UTRs

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  Some viruses have evolved to evade NMD altogether, while others may suppress NMD actively

Abstract

Garcia et al. identify the nonsense-mediated decay (NMD) pathway, an endogenous RNA quality control mechanism, as a general bottleneck to RNA virus infection in plants. They elucidate intrinsic features of RNA virus biology that trigger NMD during authentic infection and show that viruses have evolved to evade or suppress this process in order to thrive in their hosts.