RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors
Citation
Li, F., Wang, A. (2018). RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors. PLoS Pathogens, [online] 14(8), http://dx.doi.org/10.1371/journal.ppat.1007228
Plain language summary
RNA silencing and RNA decay are two essential pathways that determine the fate of cellular RNA molecules. RNA decay has been suggested to compete with RNA silencing for the RNA substrates and thus to suppress RNA silencing in plants. In this report, we show that the deficiency of key cytoplasmic RNA decay pathway gene-encoded proteins (RDGs) rather than overexpression of them attenuates RNA silencing and facilitates viral RNA accumulation in turnip mosaic virus (TuMV)-infected Nicotiana benthamiana plants. RDGs can inhibit the accumulation of exogenous gene transcripts or viral RNA via the RNA decay pathway when RNA silencing is compromised. Therefore, RNA silencing and RNA decay are important defense mechanisms that coordinate to function against exogenous gene transcripts or viral RNA. It is well known that viruses have evolved to encode viral suppressors of RNA silencing (VSRs) that counteract RNA silencing for an invading virus to establish infection. We discover that two known VSRs of TuMV interact with RDGs and the interactions subvert RNA decay. Taken together, this study provides new insights into the concerted function of RNA silencing and RNA decay in plant immunity against exogenous gene transcripts and viral RNA, and reveals a novel function of VSRs. This work advances our understanding of co-evolutionary arms race between viruses and plants and assists in the development of novel antiviral strategies.
Abstract
Exonuclease-mediated RNA decay in plants is known to be involved primarily in endogenous RNA degradation, and several RNA decay components have been suggested to attenuate RNA silencing possibly through competing for RNA substrates. In this paper, we report that overexpression of key cytoplasmic 5’–3’ RNA decay pathway gene-encoded proteins (5’RDGs) such as decapping protein 2 (DCP2) and exoribonuclease 4 (XRN4) in Nicotiana benthamiana fails to suppress sense transgene-induced post-transcriptional gene silencing (S-PTGS). On the contrary, knock-down of these 5’RDGs attenuates S-PTGS and supresses the generation of small interfering RNAs (siRNAs). We show that 5’RDGs degrade transgene transcripts via the RNA decay pathway when the S-PTGS pathway is disabled. Thus, RNA silencing and RNA decay degrade exogenous gene transcripts in a hierarchical and coordinated manner. Moreover, we present evidence that infection by turnip mosaic virus (TuMV) activates RNA decay and 5’RDGs also negatively regulate TuMV RNA accumulation. We reveal that RNA silencing and RNA decay can mediate degradation of TuMV RNA in the same way that they target transgene transcripts. Furthermore, we demonstrate that VPg and HC-Pro, the two known viral suppressors of RNA silencing (VSRs) of potyviruses, bind to DCP2 and XRN4, respectively, and the interactions compromise their antiviral function. Taken together, our data highlight the overlapping function of the RNA silencing and RNA decay pathways in plants, as evidenced by their hierarchical and concerted actions against exogenous and viral RNA, and VSRs not only counteract RNA silencing but also subvert RNA decay to promote viral infection.