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Satellite RNA pathogens of plants: impacts and origins—an RNA silencing perspective

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Viral satellite RNAs (satRNAs) are among the smallest RNA pathogens in plants. They have little or no protein‐coding capacity but can have a major impact on the host plants through trilateral interactions with helper viruses and host plants. Studies around the 1980s revealed much of what we know about satRNAs: they can affect helper virus accumulation, modulate helper virus‐induced disease symptoms, and induce their own symptoms with the assistance of helper viruses which depend on specific nucleotide sequences of their genome and host species. The molecular basis of these satRNA‐caused impacts and the origin of satRNAs have yet to be fully understood and revealed, but recent understanding of the antiviral RNA silencing pathways and advancement in RNA and DNA sequencing technologies have provided new avenues and opportunities to examine these unanswered questions. These RNA silencing‐based studies have revealed the existence of cross silencing between some satRNAs and helper viruses, the downregulation of helper virus‐encoded suppressor (VSR) of RNA silencing or inhibition/enhancement of VSR activity by satRNAs, the silencing of host‐encoded genes by satRNA‐derived small interfering RNA (siRNAs), and the presence of satRNA‐like small RNAs in uninfected host plants. These findings have provided alternative RNA silencing‐based models to explain the pathogenicity and origin of satRNAs. WIREs RNA 2016, 7:5–16. doi: 10.1002/wrna.1311 This article is categorized under: Regulatory RNAs/RNAi/Riboswitches > RNAi: Mechanisms of Action RNA in Disease and Development > RNA in Disease
Simplified schematic of the three basic RNA silencing pathways in Arabidopsis thaliana. Both the small interfering RNA (siRNA) pathway and the RNA‐directed DNA methylation (RdDM) pathway are involved in antiviral defense, where RNAs from RNA and DNA viruses and subviral agents are converted to dsRNA by host‐ or virus‐encoded RDR, which is then processed by DCL4 and DCL2 into 21–22 nt siRNAs to direct silencing against viral RNAs. Viral dsRNA, particularly that from DNA viruses, can also be processed by DCL3 into 24 nt siRNAs to direct DNA methylation at the viral genomic DNA, resulting in transcriptional silencing of viral genes. Asterisks indicate DNA methylation. TAS RNA—precursor transcript of trans‐acting siRNAs. ssRNA—single‐stranded RNA. hpRNA—short, mismatched hairpin RNA.
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A summary on the potential role of RNA silencing in helper virus‐satRNA‐host interaction and in viral disease development discussed in the text. Small interfering RNAs (siRNAs) and Viral Suppressor of RNA silencing (VSR) are the central components. The siRNAs from helper virus (vsiRNA) and satRNA (sat‐siRNA) can direct silencing against the helper virus and satRNA genome, respectively, to reduce their accumulation (Ia and Ib). In rare cases, these siRNAs can cause cross silencing between the helper virus and satRNA, which can also reduce their accumulation (dashed lines, IIa and IIb). To overcome the antiviral silencing, the helper virus encodes a VSR, which inhibits vsiRNA or sat‐siRNA‐directed self or cross silencing (IIIa, IIIb, IIIc, IIId). The VSR can also interfere with host miRNA and siRNA‐mediated gene regulation, resulting in developmental defects or disease symptoms (IVa, IVb, IVc). Beside this VSR mechanism, the helper virus can also induce disease symptoms through an unknown mechanism due to high‐level accumulation (V). The sat‐siRNAs can saturate the VSR due to high abundance, minimizing its silencing suppressor activity (VI). Consequently, the effect of VSR on host miRNA and siRNA function, and on antiviral silencing, is reduced, allowing for more normal plant development and lower level of helper virus accumulation, both of which lead to reduced disease symptoms. Some sat‐siRNAs can have sequence homology with a host gene, resulting in silencing of the host gene leading to satRNA‐specific symptoms (VIIa and VIIb). This host gene silencing can be inhibited by the VSR (VIII), which may explain why satRNA‐induced symptoms can vary with helper viruses.
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