Biogenesis, Function, and Applications of Virus-Derived Small RNAs in Plants

Abstract

RNA silencing, an evolutionarily conserved and sequence-specific gene-inactivation system, has a pivotal role in antiviral defense in most eukaryotic organisms. In plants, a class of exogenous small RNAs (sRNAs) originating from the infecting virus called virus-derived small interfering RNAs (vsiRNAs) are predominantly responsible for RNA silencing-mediated antiviral immunity. Nowadays, the process of vsiRNA formation and the role of vsiRNAs in plant viral defense have been revealed through deep sequencing of sRNAs and diverse genetic analysis. The biogenesis of vsiRNAs is analogous to that of endogenous sRNAs, which require diverse essential components including dicer-like (DCL), argonaute (AGO), and RNA-dependent RNA polymerase (RDR) proteins. vsiRNAs trigger antiviral defense through post-transcriptional gene silencing (PTGS) or transcriptional gene silencing (TGS) of viral RNA, and they hijack the host RNA silencing system to target complementary host transcripts. Additionally, several applications that take advantage of the current knowledge of vsiRNAs research are being used, such as breeding antiviral plants through genetic engineering technology, reconstructing of viral genomes, and surveying viral ecology and populations. Here, we will provide an overview of vsiRNA pathways, with a primary focus on the advances in vsiRNA biogenesis and function, and discuss their potential applications as well as the future challenges in vsiRNAs research.

Keywords: AGOs; DCLs; RDRs; RNA silencing; plant antiviral defense; small RNAs; virus-derived small RNAs.

FIGURE 1

Antiviral RNA Silencing in Arabidopsis and Oryza stativa. RNA silencing is initiated by the recognition of viral dsRNAs or partially double-stranded hairpin RNAs, which are processed into viral siRNAs (vsiRNAs) by Dicer-like proteins (DCL2/3/4) in Arabidopsis (A) and Oryza stativa (B). Next, HSP90-activated AGO1/2/4/5/7/10 is loaded with a vsiRNA, thereby forming a large RNA-induced silencing complex (RISC), which has likely incorporated other proteins such as the GW motif-containing AGO interactors in Arabidopsis (A). In rice, AGO18 positively regulates AGO1 binding to vsiRNAs by sequestering miR168 (B). Afterward, the vsiRNA-loaded RISC targets viral RNAs by slicing or translational inhibition. Secondary vsiRNAs are produced in an amplification loop through the actions of RNA-dependent RNA polymerases (RDRs) and cofactors (SGS3 and SDE5). Diverse viral silencing suppressors (VSRs) target various steps of antiviral silencing in plants (A) and (B).