Viral induction and suppression of RNA silencing in plants

https://doi.org/10.1016/j.bbagrm.2011.04.005Get rights and content

Abstract

RNA silencing in plants and insects can function as a defence mechanism against invading viruses. RNA silencing-based antiviral defence entails the production of virus-derived small interfering RNAs which guide specific antiviral effector complexes to inactivate viral genomes. As a response to this defence system, viruses have evolved viral suppressors of RNA silencing (VSRs) to overcome the host defence. VSRs can act on various steps of the different silencing pathways. Viral infection can have a profound impact on the host endogenous RNA silencing regulatory pathways; alterations of endogenous short RNA expression profile and gene expression are often associated with viral infections and their symptoms. Here we discuss our current understanding of the main steps of RNA-silencing responses to viral invasion in plants and the effects of VSRs on endogenous pathways. This article is part of a Special Issue entitled: MicroRNAs in viral gene regulation.

Research highlights

► Viral siRNAs contribute to plant antiviral response upon their incorporation into RISC. ► To counteract this effect, viruses encode viral silencing suppressor of RNA silencing. ► Viral siRNAs and viral silencing suppressors may alter endogenous RNA silencing pathways.

Introduction

Eucaryotic organisms depend on networks of gene regulatory pathways. Small RNAs (sRNAs), are key components of these networks. sRNAs are short (21–24 nt in length), endogenously expressed, and are processed from double stranded (ds)RNAs or dsRNA-like precursors. In both plants and animals, sRNAs exert their functions upon incorporation into ribonucleoprotein silencing complexes and through their base-paring capacity. They are implicated in a variety of processes, including post-transcriptional regulation of mRNA, mRNA stability and availability for translation, establishment of heterochromatin and silencing of transposons [1]. Different classes of sRNAs differ in the proteins required in their biogenesis, the constitution of ribonucleoprotein complexes that mediate their regulatory functions, their type of gene regulation, and the biological functions in which they are implicated. Plants display a remarkable diversity of sRNA types and sRNA pathways, likely needed for managing multiple environmental stimuli, including biotic and abiotic stresses. Several lines of evidence suggest that plant sRNAs play critical roles in plant–pathogen interactions. Indeed, upon infection, most plant pathogens can interfere with the expression of endogenous sRNAs, thus altering the expression of specific host factors implicated in the suppression or in the activation of plant defences. Evidence for these phenomena has been reported for bacterial and fungal pathogens (reviewed by [2]). Viruses are obligate infectious agents, whose life cycle (expression of viral proteins, viral genome replication and virion assembly) is integrated with host cell functions. Plant viruses can both modify the profiles of endogenous sRNAs (in common with bacteria and fungi) and induce the production of additional sRNAs derived from their own genomes (viral sRNAs; vsiRNAs). The latter gives a clear indication of the activation of RNA silencing-based responses of the plant. In some cases, this results in reduction of the titre of the invading virus and, in recovery of upper, non-inoculated leaves [3], [4]. To counteract RNA silencing, many plant viruses have evolved proteins (viral suppressors of RNA silencing: VSR) that target various components of the plant silencing machinery. Viruses can induce specific symptoms resembling developmental anomalies and affecting organs and tissues such as leaves, flowers and fruits. These anomalies are often reconcilable with virus-induced alterations of RNA silencing-based endogenous pathways, due to: i) the direct activity of VSRs on endogenous sRNAs or on silencing related effectors; ii) the abundance of vsiRNAs in competition with endogenous sRNAs; iii) the action of specific vsiRNAs entering into RNA silencing complexes and targeting specific host genes.

Here we provide an overview of the major cellular RNA silencing pathways in plants with particular reference to those involved in antiviral functions. Finally we highlight examples of the complex interactions between viral molecular processes and host RNA processes.

Section snippets

Fundamental RNA-silencing pathways in plants

Besides small non-coding RNAs that are not involved in RNA silencing (e.g. transfer (t)RNAs, small nuclear (sn)RNAs and small nucleolar (sno)RNAs), several classes of endogenous sRNAs with regulatory functions have been described in plants. Most of our knowledge on sRNA pathways in plants comes from studies carried out in Arabidopsis thaliana. In this section we recapitulate the major cellular pathways that are involved in biogenesis and functions of microRNAs (miRNAs) and other endogenous

sRNAs derived from viruses

In plants, sRNA generation (either of endogenous or exogenous sRNAs) requires at least two common biochemical steps: i) induction by dsRNAs and ii) processing of dsRNAs into sRNAs.

In the case of viruses, there are several types of RNAs that may account for dsRNA production. Positive (+) strand RNA viruses, the majority of plant viruses, accumulate several copies of (+) genomic RNA through negative-stranded RNA intermediates via the viral RNA-dependent RNA polymerase (RdRp). These replication

Alteration of miRNA profiles

miRNAs regulate many biological processes ranging from basal maintenance of cellular functions to responses to environmental stresses. On the other hand, developmental anomalies are often associated with plant virus infection. This opens the questions of whether viral infections interfere with cellular miRNA functions and/or whether miRNAs are involved in responses to viral infection. Inhibition of miRNA pathways may be a strategy for viruses to influence host gene expression and create a

Concluding remarks

Plant viruses alter endogenous RNA silencing pathways by at least two mechanisms: i) by producing their own sRNAs and ii) by altering endogenous sRNAs. Upon incorporation into AGOs these sRNAs contribute to virus-specific or non-specific plant defences by promoting mRNA regulation at transcriptional and post-transcriptional levels. VSRs are viral molecular tools, which possess the innate capacity to counteract the effect of sRNAs at various steps, and in turn they have been used as molecular

Acknowledgements

We are grateful to David Horner for critically reading the manuscript and for his valuable comments.

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