Viral RNase3 Co-Localizes and Interacts with the Antiviral Defense Protein SGS3 in Plant Cells

Weinheimer, Isabel; Haikonen, Tuuli; Ala-Poikela, Marjo; Moser, Mirko; Streng, Janne; Rajamäki, Minna-Liisa; Valkonen, Jari P. T.

doi:10.1371/journal.pone.0159080

Cited by 17 publications

(16 citation statements)

References 38 publications

(91 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…RNase III of SPCSV increases the accumulation of SPFMV by suppressing the plants’ RNAi defence system of plants [8, 48]. However, in our study, RNase III transgenic plants infected with SPFMV (R3-F) showed more severe disease symptoms than did those co-infected with SPCSV and SPFMV (Wt-FC) in many aspects of growth (Fig.…”

Section: Discussionmentioning

confidence: 66%

Phenotyping viral infection in sweetpotato using a high-throughput chlorophyll fluorescence and thermal imaging platform

2019

Self Cite

View full text Add to dashboard Cite

BackgroundVirus diseases caused by co-infection with Sweet potato feathery mottle virus (SPFMV) and Sweetpotato chlorotic stunt virus (SPCSV) are a severe problem in the production of sweetpotato (Ipomoea batatas L.). Traditional molecular virus detection methods include nucleic acid-based and serological tests. In this study, we aimed to validate the use of a non-destructive imaging-based plant phenotype platform to study plant-virus synergism in sweetpotato by comparing four virus treatments with two healthy controls.ResultsBy monitoring physiological and morphological effects of viral infection in sweetpotato over 29 days, we quantified photosynthetic performance from chlorophyll fluorescence (ChlF) imaging and leaf thermography from thermal infrared (TIR) imaging among sweetpotatoes. Moreover, the differences among different treatments observed from ChlF and TIR imaging were related to virus accumulation and distribution in sweetpotato. These findings were further validated at the molecular level by related gene expression in both photosynthesis and carbon fixation pathways.ConclusionOur study validated for the first time the use of ChlF- and TIR-based imaging systems to distinguish the severity of virus diseases related to SPFMV and SPCSV in sweetpotato. In addition, we demonstrated that the operating efficiency of PSII and photochemical quenching were the most sensitive parameters for the quantification of virus effects compared with maximum quantum efficiency, non-photochemical quenching, and leaf temperature.

show abstract

Section: Discussionmentioning

confidence: 66%

Phenotyping viral infection in sweetpotato using a high-throughput chlorophyll fluorescence and thermal imaging platform

2019

Self Cite

View full text Add to dashboard Cite

show abstract

“…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).…”

mentioning

confidence: 99%

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

Cheng

Wang

2017

J Virol

139

123

View full text Add to dashboard Cite

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

show abstract

“…As the partner of RDR6, SGS3 can stabilize the 5’ overhang of dsRNAs, prevent their degradation, and recruit them for facilitating RDR6-mediated dsRNA synthesis [ 7 , 8 , 9 , 10 ]. Recent reports have shown that that SGS3 could be targeted by several VSRs or endogenous RNA silencing suppressor [ 11 , 37 , 38 , 39 , 40 , 41 , 42 ]. We showed NbSGS3 is an essential component of PTGS and is closely associated with geminivirus resistance in N. benthamiana .…”

Section: Discussionmentioning

confidence: 99%

SGS3 Cooperates with RDR6 in Triggering Geminivirus-Induced Gene Silencing and in Suppressing Geminivirus Infection in Nicotiana Benthamiana

Wang

Zhou

2017

Viruses

View full text Add to dashboard Cite

RNA silencing has an important role in defending against virus infection in plants. Plants with the deficiency of RNA silencing components often show enhanced susceptibility to viral infections. RNA-dependent RNA polymerase (RDRs) mediated-antiviral defense has a pivotal role in resistance to many plant viruses. In RDR6-mediated defense against viral infection, a plant-specific RNA binding protein, Suppressor of Gene Silencing 3 (SGS3), was also found to fight against some viruses in Arabidopsis. In this study, we showed that SGS3 from Nicotiana benthamiana (NbSGS3) is required for sense-RNA induced post-transcriptional gene silencing (S-PTGS) and initiating sense-RNA-triggered systemic silencing. Further, the deficiency of NbSGS3 inhibited geminivirus-induced endogenous gene silencing (GIEGS) and promoted geminivirus infection. During TRV-mediated NbSGS3 or N. benthamiana RDR6 (NbRDR6) silencing process, we found that their expression can be effectively fine-tuned. Plants with the knock-down of both NbSGS3 and NbRDR6 almost totally blocked GIEGS, and were more susceptible to geminivirus infection. These data suggest that NbSGS3 cooperates with NbRDR6 against GIEGS and geminivirus infection in N. benthamiana, which provides valuable information for breeding geminivirus-resistant plants.

show abstract

Viral RNase3 Co-Localizes and Interacts with the Antiviral Defense Protein SGS3 in Plant Cells

Cited by 17 publications

References 38 publications

Phenotyping viral infection in sweetpotato using a high-throughput chlorophyll fluorescence and thermal imaging platform

Phenotyping viral infection in sweetpotato using a high-throughput chlorophyll fluorescence and thermal imaging platform

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

SGS3 Cooperates with RDR6 in Triggering Geminivirus-Induced Gene Silencing and in Suppressing Geminivirus Infection in Nicotiana Benthamiana

Contact Info

Product

Resources

About