Direct and Indirect Roles of Viral Suppressors of RNA Silencing in Pathogenesis

Center for Plant Cell Biology, Department of Plant Pathology and Microbiology, University of California, Riverside, California 92521, USA.
Annual Review of Phytopathology (Impact Factor: 9.62). 10/2008; 46(1):303-26. DOI: 10.1146/annurev.phyto.46.081407.104746
Source: PubMed

ABSTRACT Plant and animal viruses overcome host antiviral silencing by encoding diverse viral suppressors of RNA silencing (VSRs). Prior to the identification and characterization of their silencing suppression activities mostly in transgene silencing assays, plant VSRs were known to enhance virus accumulation in the inoculated protoplasts, promote cell-to-cell virus movement in the inoculated leaves, facilitate the phloem-dependent long-distance virus spread, and/or intensify disease symptoms in systemically infected tissues. Here we discuss how the various silencing suppression activities of VSRs may facilitate these distinct steps during plant infection and why VSRs may not play a direct role in eliciting disease symptoms by general impairments of host endogenous small RNA pathways. We also highlight many of the key questions still to be addressed on the role of viral suppression of antiviral silencing in plant infection.

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    • "To counter this antiviral defense, most plant viruses identified to date encode viral suppressors of RNA silencing (VSRs), which inhibit or inactivate various components of the RNA-silencing pathways (3, 4). Additionally, many VSR molecules play important roles in viral symptom induction (5). "
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    ABSTRACT: Unlabelled: The Cucumber Mosaic Virus (CMV) 2b protein is an RNA-silencing suppressor that plays roles in CMV accumulation and virulence. The 2b proteins of subgroup IA CMV strains partition between the nucleus and cytoplasm, but the biological significance of this is uncertain. We fused an additional nuclear localization signal (NLS) to the 2b protein of subgroup IA strain Fny-CMV to create 2b-NLS and tested its effects on subcellular distribution, silencing, and virulence. The additional NLS enhanced 2b protein nuclear and nucleolar accumulation, but nuclear and nucleolar enrichment correlated with markedly diminished silencing suppressor activity in patch assays and abolished 2b protein-mediated disruption of microRNA activity in transgenic Arabidopsis. Nucleus/nucleolus-localized 2b protein possesses at least some ability to inhibit antiviral silencing, but this was not sufficient to prevent recovery from disease in younger, developing leaves in Arabidopsis. However, enhanced nuclear and nucleolar accumulation of 2b increased virulence and accelerated symptom appearance in older leaves. Experiments with Arabidopsis lines carrying mutant Dicer-like alleles demonstrated that compromised suppressor activity explained the diminished ability of 2b-NLS to enhance virus accumulation. Remarkably, the increased virulence that 2b-NLS engendered was unrelated to effects on microRNA- or short interfering RNA-regulated host functions. Thus, although nucleus- and nucleolus-localized 2b protein is less efficient at silencing suppression than cytoplasm-localized 2b, it enhances CMV virulence. We propose that partitioning of the 2b protein between the cytoplasmic and nuclear/nucleolar compartments allows CMV to regulate the balance between virus accumulation and damage to the host, presumably to maximize the benefit for the virus. Importance: In this work, the main finding is that nucleus/nucleolus-localized 2b protein is strongly associated with CMV virulence, which is independent of its effect on small RNA pathways. Moreover, this work supports the contention that the silencing suppressor activity of CMV 2b protein is predominantly exerted by that portion of the 2b protein residing in the cytoplasm. Thus, we propose that partitioning of the 2b protein between the cytoplasmic and nuclear/nucleolar compartments allows CMV to regulate the balance between virus accumulation and damage to the host, presumably to maximize the benefit for the virus.
    Journal of Virology 03/2014; 88(10). DOI:10.1128/JVI.00284-14 · 4.44 Impact Factor
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    • "From almost all virus genus that infect plants, over 50 individual VSRs have been identified, strongly suggesting that successful virus infection requires their expression [47] [55]. The data available in the literature suggest that almost all viruses encode at least one suppressor, but in many cases, viruses encode more than one [47]. "
    Current Issues in Molecular Virology - Viral Genetics and Biotechnological Applications, Edited by Victor Romanowski, 11/2013: chapter 11: pages 251-285; , ISBN: ISBN 978-953-51-1207-5
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    • "To cope with this mechanism, viruses have evolved to encode in their genomes RNA silencing suppressors (RSS) that perturb one or more steps thereof (Csorba et al., 2009; Ding, 2010). Since the defensive branch of RNA silencing overlaps to some extent with another branch regulating plant homeostasis via miRNAs and siRNAs, the developmental alterations caused by viruses are deemed lateral effects of their RSS acting on both branches (Kasschau et al., 2003; Jay et al., 2011), although not all viral symptoms must inevitably have this origin (Díaz-Pendón and Ding, 2008). "
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    ABSTRACT: The large RNA genome of Citrus tristeza virus (CTV; ca. 20 kb) contains 12 open reading frames, with the 3'-terminal one corresponding to a protein of 209 amino acids (p23) that is expressed from an abundant subgenomic RNA. p23, an RNA-binding protein with a putative zinc-finger domain and some basic motifs, is unique to CTV because no homologs have been found in other closteroviruses, including the type species of the genus Beet yellows virus (despite both viruses having many homologous genes). Consequently, p23 might have evolved for the specific interaction of CTV with its citrus hosts. From a functional perspective p23 has been involved in many roles: (i) regulation of the asymmetrical accumulation of CTV RNA strands, (ii) induction of the seedling yellows syndrome in sour orange and grapefruit, (iii) intracellular suppression of RNA silencing, (iv) elicitation of CTV-like symptoms when expressed ectopically as a transgene in several Citrus spp., and (v) enhancement of systemic infection (and virus accumulation) in sour orange and CTV release from the phloem in p23-expressing transgenic sweet and sour orange. Moreover, transformation of Mexican lime with intron-hairpin constructs designed for the co-inactivation of p23 and the two other CTV silencing suppressors results in complete resistance against the homologous virus. From a cellular point of view, recent data indicate that p23 accumulates preferentially in the nucleolus, being the first closterovirus protein with such a subcellular localization, as well as in plasmodesmata. These major accumulation sites most likely determine some of the functional roles of p23.
    Frontiers in Microbiology 05/2013; 4:98. DOI:10.3389/fmicb.2013.00098 · 3.99 Impact Factor
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