Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step

Abstract

RNA silencing suppressors from different plant viruses are structurally diverse. In addition to inhibiting the antiviral silencing response to condition susceptibility, many suppressors are pathogenicity factors that cause disease or developmental abnormalities. Here, unrelated suppressors from multiple viruses were shown to inhibit microRNA (miRNA) activities and trigger an overlapping series of severe developmental defects in transgenic Arabidopsis thaliana. This suggests that interference with miRNA-directed processes may be a general feature contributing to pathogenicity of many viruses. A normally labile intermediate in the miRNA biogenesis/RNA-induced silencing complex (RISC) assembly pathway, miRNA*, accumulated specifically in the presence of suppressors (P1/HC-Pro, p21, or p19) that inhibited miRNA-guided cleavage of target mRNAs. Both p21 and p19, but not P1/HC-Pro, interacted with miRNA/miRNA* complexes and hairpin RNA-derived short interfering RNAs (siRNAs) in vivo. In addition, p21 bound to synthetic miRNA/miRNA* and siRNA duplexes in vitro. We propose that several different suppressors act by distinct mechanisms to inhibit the incorporation of small RNAs into active RISCs.[Keywords: MicroRNA; RNA silencing; RNAi; virus-encoded suppressors; RISC] Supplemental material is available at http://www.genesdev.org.

A Structured Viroid RNA Serves as a Substrate for Dicer-Like Cleavage To Produce Biologically Active Small RNAs but Is Resistant to RNA-Induced Silencing Complex-Mediated Degradation

“…To test this possibility, we examined the effects of several well-characterized viral silencing suppressors, which can interfere with siRNA production from dsRNA precursor, on srPSTVd accumulation. The coat protein of turnip crinkle virus has been shown to selectively inhibit the production of siRNAs (16,18,24,70) but have little effect on the production of miRNAs in plants (16,24). P19 from tomato bushy stunt virus and P1/HC-Pro from tobacco etch virus were shown to affect siRNA accumulation in some systems (P19 [35,70,80] and HC-Pro [24,35,52,54]).…”

Fine tuning of auxin signaling by miRNAs

“…Recently, we have identified several miRNAs in rice that are up-regulated in response to Tungro virus infection (N. Sanan-Mishra unpublished results). Viral suppressors of gene silencing like HC-Pro, p19, p21, and p69 are important pathogenicity factors that help in disease symptom appearance and various developmental abnormalities in infected plants (Chapman et al, 2004). Several studies have shown that these suppressors are involved in the regulation of miRNA activities (Kasschau et al, 2003;Chen et al, 2004;Chapman et al, 2004).…”

“…Viral suppressors of gene silencing like HC-Pro, p19, p21, and p69 are important pathogenicity factors that help in disease symptom appearance and various developmental abnormalities in infected plants (Chapman et al, 2004). Several studies have shown that these suppressors are involved in the regulation of miRNA activities (Kasschau et al, 2003;Chen et al, 2004;Chapman et al, 2004). HC-Pro inhibited the expression level and activity of miR171, and caused developmental deficiency (Kasschau et al, 2003).…”

Modulation of host plant immunity by Tobamovirus proteins

“…Several studies demonstrated that transgenic expression of VSRs leads to the alteration of miRNA accumulation and, consequently, numerous developmental abnormalities are produced (Kasschau et al, 2003;Chapman et al, 2004). These alterations underlie many disease symptoms typically observed during plant viral infections (Siddiqui et al, 2008;Bazzini et al, 2011;Shimura and Pantaleo, 2011).…”