Two Plant Viral Suppressors of Silencing Require the Ethylene-Inducible Host Transcription Factor RAV2 to Block RNA Silencing

Endres, Matthew W.; Gregory, Brian D.; Gao, Zhihuan; Foreman, Amy Wahba; Mlotshwa, Sizolwenkosi; Ge, Xijin; Pruss, Gail J.; Ecker, Joseph R.; Bowman, Lewis; Vance, Vicki

doi:10.1371/journal.ppat.1000729

Cited by 130 publications

(96 citation statements)

References 68 publications

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“…TEV HC-Pro was found to interact with rgsCAM in a yeast two-hybrid system. RgsCAM itself is a host suppressor of RNA silencing Anandalakshmi et al, 2000;Endres et al, 2010). Interestingly, geminivirus AL2 protein induces expression and interacts with rgsCAM.…”

Section: Vsr Interactions With Host Factorsmentioning

confidence: 99%

“…It was proposed that RAV2, a transcription factor is required for suppression of silencing mediated by TuMV HC-Pro. RAV2 downstream targets include FIERY1 an endogenous silencing suppressor in Arabidopsis (Gy et al, 2007) and CML38, the likely homologue of rgsCAM in Arabidopsis (Anandalakshmi et al, 2000;Endres et al, 2010). Genome expression analysis reveals that RNA silencing related genes were unaltered in HC-Pro transgenic lines, instead RAV2 was required for HC-Pro-mediated induction of stress and defenserelated genes (Endres et al, 2010).…”

Section: Vsr Interactions With Host Factorsmentioning

confidence: 99%

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viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence

2015

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RNA silencing is a homology-dependent gene inactivation mechanism that regulates a wide range of biological processes including antiviral defense. To deal with host antiviral responses viruses evolved mechanisms to avoid or counteract this, most notably through expression of viral suppressors of RNA silencing. Besides working as silencing suppressors, these proteins may also fulfill other functions during infection. In many cases the interplay between the suppressor function and other "unrelated" functions remains elusive. We will present host factors implicated in antiviral pathways and summarize the current status of knowledge about the diverse viral suppressors' strategies acting at various steps of antiviral silencing in plants. Besides, we will consider the multi-functionality of these versatile proteins and related biochemical processes in which they may be involved in fine-tuning the plant-virus interaction. Finally, we will present the current applications and discuss perspectives of the use of these proteins in molecular biology and biotechnology.

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Section: Vsr Interactions With Host Factorsmentioning

confidence: 99%

Section: Vsr Interactions With Host Factorsmentioning

confidence: 99%

viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence

2015

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“…Among the 11 common potyvirus proteins, HC-Pro and VPg have been shown to be VSRs (32)(33)(34). The molecular mechanisms underlying the functional role of HC-Pro as a VSR have been relatively well understood (35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46). It still remains unclear how VPg interferes with RNA silencing.…”

mentioning

confidence: 99%

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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“…Several reviews of RNA silencing and its role in antiviral defense have been recently published (22)(23)(24)(25). The mechanism by which HCPro acts as an RNA-silencing suppressor (RSS) appears to rely on its capacity to specifically interact with/ sequester virus-derived 21-nucleotide (nt) small RNAs (26)(27)(28) and to interact with the small RNA methyltransferase HEN1 (29) and other host factors (30,31). Interestingly, since its first characterization, HCPro has also been related to several events during viral infection, such as genome amplification, both cell-to-cell and long-distance movements, pathogenicity, and viral synergism (reviewed in references 32 and 33).…”

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confidence: 99%

A Novel Role of the Potyviral Helper Component Proteinase Contributes To Enhance the Yield of Viral Particles

Vallí

Gallo

Calvo

et al. 2014

J Virol

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The helper component proteinase (HCPro) is an indispensable, multifunctional protein of members of the genus Potyvirus and other viruses of the family Potyviridae. This viral factor is directly involved in diverse steps of viral infection, such as aphid transmission, polyprotein processing, and suppression of host antiviral RNA silencing. In this paper, we show that although a chimeric virus based on the potyvirus Plum pox virus lacking HCPro, which was replaced by a heterologous silencing suppressor, caused an efficient infection in Nicotiana benthamiana plants, its viral progeny had very reduced infectivity. Making use of different approaches, here, we provide direct evidence of a previously unknown function of HCPro in which the viral factor enhances the stability of its cognate capsid protein (CP), positively affecting the yield of virions and consequently improving the infectivity of the viral progeny. Site-directed mutagenesis revealed that the ability of HCPro to stabilize CP and enhance the yield of infectious viral particles is not linked to any of its previously known activities and helped us to delimit the region of HCPro involved in this function in the central region of the protein. Moreover, the function is highly specific and cannot be fulfilled by the HCPro of a heterologous potyvirus. The importance of this novel requirement in regulating the sorting of the viral genome to be subjected to replication, translation, and encapsidation, thus contributing to the synchronization of these viral processes, is discussed. IMPORTANCEPotyviruses form one of the most numerous groups of plant viruses and are a major cause of crop loss worldwide. It is well known that these pathogens make use of virus-derived multitasking proteins, as well as dedicated host factors, to successfully infect their hosts. Here, we describe a novel requirement for the proper yield and infectivity of potyviral progeny. In this case, such a function is performed by the extensively studied viral factor HCPro, which seems to use an unknown mechanism that is not linked to its previously described activities. To our knowledge, this is the first time that a factor different from capsid protein (CP) has been shown to be directly involved in the yield of potyviral particles. Based on the data presented here, we hypothesize that this capacity of HCPro might be involved in the coordination of mutually exclusive activities of the viral genome by controlling correct assembly of CP in stable virions.

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Two Plant Viral Suppressors of Silencing Require the Ethylene-Inducible Host Transcription Factor RAV2 to Block RNA Silencing

Cited by 130 publications

References 68 publications

viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence

viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence

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

A Novel Role of the Potyviral Helper Component Proteinase Contributes To Enhance the Yield of Viral Particles

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