Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation

Abstract

Virus infections induce the expression of ARGONAUTE1 (AGO1) mRNA and in parallel enhance the accumulation of miR168 (regulator of AGO1 mRNA). Here, we show that in virus-infected plants the enhanced expression of AGO1 mRNA is not accompanied by increased AGO1 protein accumulation. We also show that the induction of AGO1 mRNA level is a part of the host defence reaction, whereas the induction of miR168, which overlaps spatially with virus-occupied sectors, is mediated mainly by the Tombusvirus p19 RNA-silencing suppressor. The absence of p19 results in the elimination of miR168 induction and accompanied with the enhanced accumulation of AGO1 protein. In transient expression study, p19 mediates the induction of miR168 and the down-regulation of endogenous AGO1 level. P19 is not able to efficiently bind miR168 in virus-infected plants, indicating that this activity is uncoupled from the small RNA-binding capacity of p19. Our results imply that plant viruses can inhibit the translational capacity of AGO1 mRNA by modulating the endogenous miR168 level to alleviate the anti-viral function of AGO1 protein.

Specific Argonautes Selectively Bind Small RNAs Derived from Potato Spindle Tuber Viroid and Attenuate Viroid Accumulation In Vivo

“…1A and B). Altogether, our data showed that, in contrast with the situation observed for representative RNA viruses (42,60), the effect of viroid infection on AGO1, if any, is not mediated by miR168 targeting of AGO1 mRNA.…”

“…As indicated above, AGO1 is a key player in the antiviral defense mediated by RNA silencing. Infection by plant RNA viruses induces and reduces the accumulation of AGO1 mRNA and AGO1 protein, respectively (42,60). The explanation for this apparent paradox is that expression of AGO1 mRNA is translationally repressed by miR168 (61), the accumulation of which is elicited by virus infection (42,60).…”

“…AGO4, AGO6, and AGO9 associate with 24-nt siRNAs to mediate transcriptional silencing through RNAdirected DNA methylation (38,39), and at least AGO4 binds to diverse classes of sRNAs, including siRNAs originating from transposable and repetitive elements, and cleaves target RNA transcripts (40). AGO10 acts in the translational control of several miRNA targets, like the mRNAs coding for AGO1 (41,42). Finally, the roles of AGO3 and AGO8 in sRNA-directed regulation remain unclear (29,30).…”

Comparative analysis of MIR168 promoters in three plant species

“…miR168 plays a pivotal role as it regulates the expression of AGO1, a mechanism through which all microRNAs can down-regulate their targets Gazzani et al, 2009). In addition, miR168 is reportedly involved in the regulation of plant growth, fruit development, and response to different stresses, such as UV-B and aluminum, and is also up-regulated during viral infection in plants, during which it is ubiquitous in plant-virus interactions (Várallyay et al, 2010;Lima et al, 2011;Wang et al, 2013;Xian et al, 2014).…”

Characterization of microRNAs and their target genes associated with transcriptomic changes in gamma-irradiated Arabidopsis

“…However, only limited information is available on the interaction of each miRNA with its target genes. For example, the translation of AGO1 mRNA is inhibited by miR168, which is induced by p19 RNA-silencing suppressor (Várallyay et al, 2010), while miR403 induces the post-transcriptional silencing (cleavage) of the AGO2 gene via interaction with AGO1 (Allen et al, 2005;Harvey et al, 2011). MEMB12 mRNA is targeted by miR393b* in association with AGO2, which is induced by DC3000 (Zhang et al, 2011b).…”