RNA Silencing and the Mobile Silencing Signal

Mlotshwa, Sizolwenkosi; Voinnet, Olivier; Mette, Michael Florian; Matzke, Marjori; Vaucheret, Herve H.; Ding, Shou‐Wei; Pruss, Gail J.; Vance, Vicki

doi:10.1105/tpc.001677

Cited by 232 publications

(178 citation statements)

References 96 publications

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“…Other ideas that have been used to explain cross-protection include competition between protective and challenge virus strains for host cells, intracellular replication sites, host translational apparatus and/or other host factors, or inhibitory interactions between the proteins or nucleic acids of the competing viral strains (Hull & Plaskitt, 1970;Palukaitis & Zaitlin, 1984;Sequeira, 1984;Hull, 2002). Mechanisms such as these may explain 'exclusion', in which closely related strains of the same virus infect adjacent cells but do not produce mixed infections within the same host cell (Dietrich & Maiss, 2003;Hull & Plaskitt, 1970 CMV encodes a well studied suppressor of RNA silencing, the 2b protein (Brigneti et al, 1998;Guo & Ding, 2002;Lewsey et al, 2007;Mlotshwa et al, 2002;Zhang et al, 2006). The 2b protein can also act as a symptom determinant; it induces disease symptoms by interfering with microRNA-mediated gene regulation (Lewsey et al, 2007;Zhang et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…CMV encodes a well studied suppressor of RNA silencing, the 2b protein (Brigneti et al, 1998;Guo & Ding, 2002;Lewsey et al, 2007;Mlotshwa et al, 2002;Zhang et al, 2006). The 2b protein can also act as a symptom determinant; it induces disease symptoms by interfering with microRNA-mediated gene regulation (Lewsey et al, 2007;Zhang et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains

Ziebell

Payne

Berry

et al. 2007

Journal of General Virology

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Several plant virus mutants, in which genes encoding silencing suppressor proteins have been deleted, are known to induce systemic or localized RNA silencing against themselves and other RNA molecules containing homologous sequences. Thus, it is thought that many cases of cross-protection, in which infection with a mild or asymptomatic virus mutant protects plants against challenge infection with closely related virulent viruses, can be explained by RNA silencing. We found that a cucumber mosaic virus (CMV) mutant of the subgroup IA strain Fny (Fny-CMVD2b), which cannot express the 2b silencing suppressor protein, cross-protects tobacco (Nicotiana tabacum) and Nicotiana benthamiana plants against disease induction by wild-type Fny-CMV. However, protection is most effective only if inoculation with Fny-CMVD2b and challenge inoculation with wild-type CMV occurs on the same leaf. Unexpectedly, FnyCMVD2b also protected plants against infection with TC-CMV, a subgroup II strain that is not closely related to Fny-CMV. Additionally, in situ hybridization revealed that Fny-CMVD2b and Fny-CMV can co-exist in the same tissues but these tissues contain zones of Fny-CMVD2b-infected host cells from which Fny-CMV appears to be excluded. Taken together, it appears unlikely that cross-protection by Fny-CMVD2b occurs by induction of systemic RNA silencing against itself and homologous RNA sequences in wild-type CMV. It is more likely that protection occurs through either induction of very highly localized RNA silencing, or by competition between strains for host cells or resources. INTRODUCTIONCucumber mosaic virus (CMV) is the type species of the genus Cucumovirus of the family Bromoviridae (Van Regenmortel et al., 2000). Based on serological relationships and sequence criteria, the species is divided into three distinct subgroups: IA, IB and II (Roossinck et al., 1999). CMV has the largest host range of any known plant virus and is transmitted in a non-persistent manner by aphids belonging to over 80 species. Taken together, these factors probably contribute to the worldwide distribution of the virus and its economic importance (Palukaitis et al., 1992;Palukaitis & García-Arenal, 2003). The CMV genome consists of three positive-sense RNA molecules. These are RNAs 1, 2 and 3, which also function as mRNAs for the synthesis of the 1a and 2a replicase proteins, and the 3a movement protein, respectively. During replication, subgenomic mRNAs encoding additional proteins are synthesized. The subgenomic RNA 4, derived from RNA 3, is the mRNA for CMV coat protein (CP) and RNA 4A, which is derived from RNA 2, is the mRNA for the multifunctional 2b protein (Ding et al., 1994). Direct control of CMV or prevention of its transmission by aphids by using insecticides is difficult to achieve. One promising approach for controlling CMV is the use of pathogen-derived transgenes in genetically modified plants (Palukaitis & Zaitlin, 1997;Gaba et al., 2004). Pathogenderived resistance to CMV and other viruses works either through the triggering of...

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains

Ziebell

Payne

Berry

et al. 2007

Journal of General Virology

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“…The antiviral response may be triggered by virusspecific dsRNA intermediates produced during genome replication, by transcription from converging promoters, or through recognition of viral RNAs by host RdRP, as proposed in plants (Voinnet et al, 2000;Szittya et al, 2002). As a counterdefense, viruses encode proteins such as helper component-proteinase (HC-Pro) and Cucumber mosaic virus 2b that suppress RNA silencing at various steps in the pathway (Anandalakshmi et al, 1998;Brigneti et al, 1998;Kasschau and Carrington, 1998;Mlotshwa et al, 2002;Silhavy et al, 2002). The identification of a silencing suppression function typically provides a molecular basis for previously observed defects in viral accumulation and spread of virus mutants that lack a functional suppressor (Li and Ding, 2001;Mlotshwa et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Viral Virulence Protein Suppresses RNA Silencing–Mediated Defense but Upregulates the Role of MicroRNA in Host Gene Expression[W]

et al. 2004

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Small interfering RNAs (siRNAs) and microRNAs (miRNAs) are processed by the ribonuclease Dicer from distinct precursors, double-stranded RNA (dsRNA) and hairpin RNAs, respectively, although either may guide RNA silencing via a similar complex. The siRNA pathway is antiviral, whereas an emerging role for miRNAs is in the control of development. Here, we describe a virulence factor encoded by turnip yellow mosaic virus, p69, which suppresses the siRNA pathway but promotes the miRNA pathway in Arabidopsis thaliana. p69 suppression of the siRNA pathway is upstream of dsRNA and is as effective as genetic mutations in A. thaliana genes involved in dsRNA production. Possibly as a consequence of p69 suppression, p69-expressing plants contained elevated levels of a Dicer mRNA and of miRNAs as well as a correspondingly enhanced miRNA-guided cleavage of two host mRNAs. Because p69-expressing plants exhibited disease-like symptoms in the absence of viral infection, our findings suggest a novel mechanism for viral virulence by promoting the miRNA-guided inhibition of host gene expression.

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“…It is not clear whether viral suppression of intracellular and intercellular silencing plays specific roles in facilitating the cell-to-cell and long-distance virus spread. However, it is of interest to note that virus synergy observed in mixed virus infections, such as potyvirus synergism with potato virus X and CMV, often involves two unrelated viruses that encode distinct suppressors targeting intracellular and intercellular silencing, respectively (22).In this study, we investigated the strategy of citrus tristeza virus (CTV) in counter-defense against the RNA silencing antiviral defense. As the most destructive virus of the citrus industry worldwide, CTV represents the first pathogen of a perennial tree to be examined for the activity in silencing suppression.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome

Folimonov

Shintaku

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

351

248

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Viral infection in both plant and invertebrate hosts requires a virus-encoded function to block the RNA silencing antiviral defense. Here, we report the identification and characterization of three distinct suppressors of RNA silencing encoded by the Ϸ20-kb plus-strand RNA genome of citrus tristeza virus (CTV). When introduced by genetic crosses into plants carrying a silencing transgene, both p20 and p23, but not coat protein (CP), restored expression of the transgene. Although none of the CTV proteins prevented DNA methylation of the transgene, export of the silencing signal (capable of mediating intercellular silencing spread) was detected only from the F1 plants expressing p23 and not from the CP-or p20-expressing F1 plants, demonstrating suppression of intercellular silencing by CP and p20 but not by p23. Thus, intracellular and intercellular silencing are each targeted by a CTV protein, whereas the third, p20, inhibits silencing at both levels. Notably, CP suppresses intercellular silencing without interfering with intracellular silencing. The novel property of CP suggests a mechanism distinct to p20 and all of the other viral suppressors known to interfere with intercellular silencing and that this class of viral suppressors may not be consistently identified by Agrobacterium coinfiltration because it also induces RNA silencing against the infiltrated suppressor transgene. Our analyses reveal a sophisticated viral counter-defense strategy that targets the silencing antiviral pathway at multiple steps and may be essential for protecting CTV with such a large RNA genome from antiviral silencing in the perennial tree host.RNA interference ͉ citrus tristeza virus ͉ virus synergy ͉ antiviral immunity T he discoveries of viral suppressors of RNA silencing play an important role in establishing RNA silencing as a natural antiviral response in both plant and invertebrate hosts (1). Many plant viral proteins have been identified as suppressors of RNA silencing since the initial reports in late 1998 (2-4). RNA silencing suppressors from different virus taxons are structurally diverse. However, they are typically required for long-distance virus spread and influence virulence and accumulation levels in infected plants (5-7). Progress is being made toward understanding the molecular mechanisms involved in viral suppression of RNA silencing (8-11). In RNA silencing assays, plant viral suppressors differ by their ability to suppress intracellular and͞or intercellular silencing (12-16). Intercellular silencing is mediated by the non-cell-autonomous silencing signal that can spread to destroy homologous RNAs in neighboring or distant tissues that do not contain the initial trigger, such as a silencing transgene or a replicating virus (17-19). The differential silencing suppression is best illustrated by the potyviral helper component proteinase (HC-Pro) and the cucumber mosaic virus (CMV) 2b protein. When introduced by genetic crosses into the Nicotiana tabacum line 6b5 carrying a silencing ␤-glucuronidase (GUS) transgen...

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RNA Silencing and the Mobile Silencing Signal

Cited by 232 publications

References 96 publications

A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains

A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains

Viral Virulence Protein Suppresses RNA Silencing–Mediated Defense but Upregulates the Role of MicroRNA in Host Gene Expression[W]

Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome

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