In Planta Recognition of a Double-Stranded RNA Synthesis Protein Complex by a Potexviral RNA Silencing Suppressor

Okano, Yasushi; Senshu, Hiroko; Hashimoto, Masayoshi; Neriya, Yutaro; Netsu, Osamu; Minato, Nami; Yoshida, Tetsuya; Maejima, Kensaku; Oshima, Kenro; Komatsu, Ken; Yamaji, Yutaka

doi:10.1105/tpc.113.120535

Cited by 72 publications

(61 citation statements)

References 81 publications

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“…These VSRs have evolved distinct mechanisms to inhibit SGS3 functions. For example, TYLCV V2 inhibits SGS3 RNA binding activity by directly competing for SGS3 substrates (66), whereas PlAMV TGB1 directly sequesters SGS3/RDR6 bodies by coaggregation with them (23). In this work, we report that TuMV VPg interacts with SGS3 and mediates its degradation.…”

Section: Discussionmentioning

confidence: 80%

“…Several viral proteins, e.g., PlAMV TGB1, TYLCV V2, SPCSV RNase 3, and RSV P2, have been found to target SGS3 to enhance host susceptibility (21)(22)(23)(24). These VSRs have evolved distinct mechanisms to inhibit SGS3 functions.…”

Section: Discussionmentioning

confidence: 99%

“…Many VSRs suppress RNA silencing via sequestration of virus-derived siRNAs and inactivation of AGO proteins (mainly AGO1) (18)(19)(20). In contrast, some other VSRs, such as V2 of Tomato yellow leaf curl virus (TYLCV), P2 of Rice stripe virus (RSV), TGB1 of Plantago asiatica mosaic virus (PlAMV), and the class 1 RNase III endoribonuclease (RNase 3) of Sweet potato chlorotic stunt virus (SPCSV), target other RNA silencing components, e.g., SGS3, to attenuate plant antivirus immunity (21)(22)(23)(24).…”

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confidence: 99%

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The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

Cheng

Wang

2017

J Virol

135

123

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RNA silencing is an innate antiviral immunity response of plants and animals. To counteract this host immune response, viruses have evolved an effective strategy to protect themselves by the expression of viral suppressors of RNA silencing (VSRs). Most potyviruses encode two VSRs, helper component-proteinase (HCPro) and viral genome-linked protein (VPg). The molecular biology of the former has been well characterized, whereas how VPg exerts its function in the suppression of RNA silencing is yet to be understood. In this study, we show that infection by Turnip mosaic virus (TuMV) causes reduced levels of suppressor of gene silencing 3 (SGS3), a key component of the RNA silencing pathway that functions in doublestranded RNA synthesis for virus-derived small interfering RNA (vsiRNA) production. We also demonstrate that among 11 TuMV-encoded viral proteins, VPg is the only one that interacts with SGS3. We furthermore present evidence that the expression of VPg alone, independent of viral infection, is sufficient to induce the degradation of SGS3 and its intimate partner RNA-dependent RNA polymerase 6 (RDR6). Moreover, we discover that the VPg-mediated degradation of SGS3 occurs via both the 20S ubiquitin-proteasome and autophagy pathways. Taken together, our data suggest a role for VPg-mediated degradation of SGS3 in suppression of silencing by VPg.IMPORTANCE Potyviruses represent the largest group of known plant viruses and cause significant losses of many agriculturally important crops in the world. In order to establish infection, potyviruses must overcome the host antiviral silencing response. A viral protein called VPg has been shown to play a role in this process, but how it works is unclear. In this paper, we found that the VPg protein of Turnip mosaic virus (TuMV), which is a potyvirus, interacts with a host protein named SGS3, a key protein in the RNA silencing pathway. Moreover, this interaction leads to the degradation of SGS3 and its interacting and functional partner RDR6, which is another essential component of the RNA silencing pathway. We also identified the cellular pathways that are recruited for the VPg-mediated degradation of SGS3. Therefore, this work reveals a possible mechanism by which VPg sabotages host antiviral RNA silencing to promote virus infection. KEYWORDS RDR6, RNA silencing, SGS3, VPg, VSR, autophagy, potyvirus, ubiquitination T o establish systemic infection, an invading virus must remodel and recruit host elements and overcome resistance responses through complex molecular virushost interactions (1-3). One such essential antiviral response is RNA silencing (4-6), a cellular mechanism conserved from lower eukaryotes to mammals to regulate endogenous gene expression at the transcriptional and posttranscriptional levels (7, 8). To activate antiviral RNA silencing, the viral double-stranded RNAs (dsRNAs), which may

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Section: Discussionmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

Cheng

Wang

2017

J Virol

135

123

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“…The importance of systemic signals in PVX infection is underlined by the fact that the PVX VSR, P25, functions by inhibiting the systemic movement of the silencing signal in N. benthamiana (Voinnet et al, 2000). The PVX P25 protein has not been demonstrated to inhibit this aspect of RNA silencing in Arabidopsis, whereas the P25 protein of PlAMV is thought to do so (Okano et al, 2014). Given that AGO2 seems to be involved in most plant-virus systems tested, this model is likely to extend to other viruses.…”

Section: A Model For Ago2 and Ago5 In Antiviral Defensesmentioning

confidence: 99%

Functional and Genetic Analysis Identify a Role for Arabidopsis ARGONAUTE5 in Antiviral RNA Silencing

2015

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RNA silencing functions as an antiviral defense through the action of DICER-like (DCL) and ARGONAUTE (AGO) proteins. In turn, plant viruses have evolved strategies to counteract this defense mechanism, including the expression of suppressors of RNA silencing. Potato virus X (PVX) does not systemically infect Arabidopsis thaliana Columbia-0, but is able to do so effectively in mutants lacking at least two of the four Arabidopsis DCL proteins. PVX can also infect Arabidopsis ago2 mutants, albeit less effectively than double DCL mutants, suggesting that additional AGO proteins may mediate anti-viral defenses. Here we show, using functional assays, that all Arabidopsis AGO proteins have the potential to target PVX lacking its viral suppressor of RNA silencing (VSR), P25, but that only AGO2 and AGO5 are able to target wild-type PVX. However, P25 directly affects only a small subset of AGO proteins, and we present evidence indicating that its protective effect is mediated by precluding AGO proteins from accessing viral RNA, as well as by directly inhibiting the RNA silencing machinery. In agreement with functional assays, we show that Potexvirus infection induces AGO5 expression and that both AGO2 and AGO5 are required for full restriction of PVX infection in systemic tissues of Arabidopsis.

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“…Alternatively, V2 may compete with SGS3 for dsRNA having 5 0 overhang ends that may be an RDR6/SGS3 substrate/intermediate during vsiRNA amplification (Fukunaga and Doudna 2009;Kumakura et al 2009). Similarly, TRIPLE GENE BOX PROTEIN1 (TGBp1) encoded by PVX was shown to inhibit RDR6/SGS3-dependent dsRNA synthesis (Okano et al 2014). βC1 suppressor of TYLCCNV DNA satellite interacts with the endogenous suppressor of silencing calmodulin-like protein (rgsCAM) in N. benthamiana to repress RDR6 expression .…”

Section: Suppression Of Antiviral Silencing Amplificationmentioning

confidence: 99%

Antiviral Silencing and Suppression of Gene Silencing in Plants

Csorba

Burgyán

2016

Current Research Topics in Plant Virology

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RNA silencing is an evolutionary conserved sequence-specific gene inactivation mechanism that contributes to the control of development, maintains heterochromatin, acts in stress responses, DNA repair and defends against invading nucleic acids like transposons and viruses. In plants RNA silencing functions as one of the main immune systems. RNA silencing process involves the small RNAs and trans factor components like Dicers, Argonautes and RNA-dependent RNA polymerases. To deal with host antiviral silencing responses viruses evolved mechanisms to avoid or counteract this, most notably through expression of viral suppressors of RNA silencing. Due to the overlap between endogenous and antiviral silencing pathways while blocking antiviral pathways viruses also impact endogenous silencing processes. Here we provide an overview of antiviral silencing pathway, host factors implicated in it and the crosstalk between antiviral and endogenous branches of silencing. We summarize the current status of knowledge about the viral counter-defense strategies acting at various steps during virus infection in plants with the focus on representative, well studied silencing suppressor proteins. Finally we discuss future challenges of the antiviral silencing and counter-defense research field.

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In Planta Recognition of a Double-Stranded RNA Synthesis Protein Complex by a Potexviral RNA Silencing Suppressor

Cited by 72 publications

References 81 publications

The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

Functional and Genetic Analysis Identify a Role for Arabidopsis ARGONAUTE5 in Antiviral RNA Silencing

Antiviral Silencing and Suppression of Gene Silencing in Plants

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