RNA Silencing and its Suppressors in the Plant‐virus Interplay


Viruses are obligate intracellular parasites that need to evade the host defences targeted against them. In plants, activation of ribonucleic acid (RNA) silencing is among the most powerful responses against viruses. To overcome this defence, both deoxyribonucleic acid (DNA) and RNA plant viruses make use of viral products able to interfere with silencing mechanisms, and known collectively as RNA silencing suppressors (RSSs). RSSs present an extraordinary diversity in modes of action, and therefore, their study is providing valuable information about the different silencing pathways in plants. This article reviews our knowledge on RSSs, including the experimental systems used to identify them, and the mechanisms by which they act. Finally, the additional effects that they cause in the network of silencing pathways, and hence the need of a tight control of their activity, are also considered.

Key concepts:

  • Argonaute: Family of proteins that contain certain conserved domains, such as PIWI domain (found in Piwi, or P‐element‐induced wimpy testis in Drosophila, and related proteins) and PAZ domain (found in Piwi, Argonaute and Zwille proteins). Proteins of this family are the main components of RNA silencing effector complexes.

  • Dicer: Ribonuclease belonging to the RNase III family. Dicer‐like enzymes cleave hairpin or double‐strand RNA molecules into short RNA duplexes of 20–24 nucleotides with a 2‐nucleotides overhang at the 3′ ends, which are key components of the RNA silencing pathways.

  • microRNA (miRNA): Endogenous single‐strand RNA of 20–21 nucleotides, which derives from a hairpin precursor. miRNAs are incorporated into RISC, guiding it, by base complementary, to silence endogenous mRNAs.

  • RNA‐dependent RNA polymerase (RdRP, RDR): Enzyme able to synthesize RNA using RNA as template. These enzymes are involved in amplification steps of RNA silencing.

  • RNA‐induced silencing complex (RISC): Multicomponent complex including an Argonaute protein and a short RNA. RISC can silence mRNAs by endonucleolytic cleavage, decay acceleration and translation inhibition.

  • RNA‐induced transcriptional silencing complex (RITS): Multicomponent complex including an Argonaute protein and a short RNA that silence gene expression by inhibiting or downregulating the transcription activity.

  • RNA silencing: General term used to describe different events triggered by small RNAs to induce transcriptional or posttranscriptional gene downregulation in a sequence‐homology manner.

  • RNA silencing suppressor (RSS): Factor (usually a protein) with the capacity to interfere with the onset of RNA silencing or with its maintenance. The expression of viral RSSs is the most common strategy that plant viruses use to escape from RNA silencing.

  • Short interfering RNA (siRNA): Small RNA of 20–24 nucleotides derived from Dicer‐mediated cleavage of a double‐stranded RNA precursor. One of the strands of the siRNA is incorporated in RISC or RITS to guide their RNA silencing effector activities.

Keywords: RNA silencing; silencing suppression; antiviral resistance; plant defence

Figure 1.

Schematic representation of key steps of plant virus‐related RNA silencing. The silencing components that are targeted by some RSSs (depicted as red ovals with their abbreviations inside) are also indicated. See text for details.

Figure 2.

Agro‐infiltration assay for assessing the RNA silencing suppression activity of the P1b protein of the ipomovirus CVYV (Valli et al., ). (a) Co‐infiltration with A. tumefaciens strains expressing GFP and CVYV P1b allows to maintain high levels of GFP at late time post‐infiltration in N. benthamiana leaves. (b) Infiltration of A. tumefaciens expressing GFP in GFP‐transformed N. benthamiana line 16c induces the silencing of both exogenous and endogenous GFP transgenes. RNA silencing spread from cell to cell is manifested by a narrow red ring around the infiltrated spot (Voinnet and Baulcombe, ) (vector, black arrows), and can be disturbed by RSSs, for instance CVYV P1b (P1b, white arrows). (c) RNA silencing also spreads to upper nonagroinfiltrated leaves, and some silencing suppressors are able to block this systemic spread. The picture shows that, in spite of the strong local silencing suppression activity of CVYV P1b, this RSS is not able to prevent systemic silencing (red veins reveal silencing of the endogenous GFP transgene in the upper leaves). GFP fluorescence pictures were taken under UV irradiation.

Figure 3.

Schematic representations of some RNA silencing suppression assays. (a) RNA silencing suppression in grafted transgenic plants. RNA silencing spreads from a transgene‐silenced rootstock to scions obtained from plants actively expressing a homologous transgene (I; the minus signs indicate RSS absence, or co‐expression of an RSS candidate lacking detectable RNA silencing suppression activities). Transgenic coexpression of some RSSs in the rootstock (RSSl+s+) prevents local silencing in the rootstock and spreading of a systemic silencing signal to the scion (II). Some other RSSs (RSSl+s) prevent local silencing but do not interfere with silencing spread (III). It is also possible that an RSS (RSSls+) that does not affect local silencing is able to block the systemic spread of the silencing signal (IV). (b) Complementation of a defective mutant virus. RNA silencing suppression activity of an RSS candidate can be inferred from its ability to complement the movement defect of a mutant virus lacking its own RSS. The use of a recombinant virus expressing a reporter gene, for instance GFP, makes easier the assay. (c) Enhancement of PVX pathogenicity. Whereas PVX infection provokes mild symptoms in Nicotiana plants, recombinant PVX viruses expressing RSSs usually cause much more severe symptoms. (d) Genetic approaches to identify and to analyse RSSs. Transgenic plants expressing an RSS (transgenic RSS+) could show ‘symptoms’ resembling those displayed by infected plants (Wt+Wt virus), and those of a mutant plant defective in the silencing factor targeted by the RSS (silencing factor). Infection of wild‐type plants with a mutant virus defective in the silencing suppressor (Wt+ΔRSS virus) does not produce typical symptoms and gives rise to low viral accumulation levels (represented by small number of red wavy lines). The RSS‐defective virus infects the plant defective in the RSS target (silencing factor+ΔRSS virus) with similar efficiency than the wild‐type virus infects the wild‐type plant.

Figure 4.

Schematic representation of diverse antisilencing mechanisms used by viral RSSs. (a) RSSs able to bind long RNA duplexes can protect these molecules against DCL processing. (b) Sequestering of double‐stranded small RNA by RSS complexes interferes with effector activities. (c) Begomoviral AC4 is the unique RSS described to date showing high affinity by single‐stranded small RNA. (d) Direct interaction between cucumoviral 2b and AGO1 prevents RISC effector action. (e) Poleroviral P0 is an F‐box protein able to form an SCF active complex that mediates AGO1 degradation.

Figure 5.

RSS expression can disturb plant development. Developmental defects induced in transgenic A. thaliana plants expressing the RSSs P1b from the ipomovirus CVYV and P1‐HCPro from the potyvirus PPV (Valli and García, unpublished results). Bars, 5 mm.



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Further Reading

Baulcombe D (2004) RNA silencing in plants. Nature 431: 356–363.

Eamens A, Wang MB, Smith NA and Waterhouse PM (2008) RNA silencing in plants: Yesterday, today, and tomorrow. Plant Physiology 147: 456–468.

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Roth BM, Pruss GJ and Vance VB (2004) Plant viral suppressors of RNA silencing. Virus Research 102: 97–108.

Voinnet O (2008) Post‐transcriptional RNA silencing in plant‐microbe interactions: a touch of robustness and versatility. Current Opinion in Plant Biology 11: 464–470.

Xie Q and Guo HS (2006) Systemic antiviral silencing in plants. Virus Research 118: 1–6.

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Valli, Adrián, López‐Moya, Juan José, and García, Juan Antonio(Sep 2009) RNA Silencing and its Suppressors in the Plant‐virus Interplay. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021261]