Identification of Silencing Suppressor Protein Encoded by Strawberry Mottle Virus

Overview

Journal Front Plant Sci

Date 2022 Jun 17

PMID 35712581

Authors

Lingjiao Fan

Chengyong He

Dehang Gao

Tengfei Xu

Fei Xing

Jiaqi Yan

Binhui Zhan

Shifang Li

Hongqing Wang

Affiliations

Soon will be listed here.

Abstract

Strawberry mottle virus (SMoV) is associated with strawberry decline disease, causing losses to fruit yield and quality. In this study, using a screening system that enables detection of both local and systemic plant host (RNA silencing) defense responses, we found that Pro2Glu and P28, encoded by SMoV RNA2 genome, functioned to suppress local and systemic RNA silencing triggered by single- but not double-stranded GFP RNA. Subcellular localization assay revealed that both Pro2Glu and P28 were localized to nucleus and cytoplasm. The deletion of 11 amino acid residues at the C-terminus destabilized Pro2Glu protein, and the disruption of two conserved GW motifs deprived Pro2Glu of ability to suppress RNA silencing. Additionally, SMoV Pro2Glu and P28 enhanced the accumulation of potato virus X (PVX) in 22 days post-infiltration, and P28 exacerbated significantly the symptoms of PVX. Collectively, these data indicate that the genome of SMoV RNA2 encodes two suppressors of RNA silencing. This is the first identification of a stramovirus suppressor of RNA silencing.

Citing Articles

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References

Thompson J, Leone G, Lindner J, Jelkmann W, Schoen C . Characterization and complete nucleotide sequence of Strawberry mottle virus: a tentative member of a new family of bipartite plant picorna-like viruses. J Gen Virol. 2001; 83(Pt 1):229-239. DOI: 10.1099/0022-1317-83-1-229. View

Mandadi K, Scholthof K . Plant immune responses against viruses: how does a virus cause disease?. Plant Cell. 2013; 25(5):1489-505. PMC: 3694688. DOI: 10.1105/tpc.113.111658. View

Danielson D, Pezacki J . Studying the RNA silencing pathway with the p19 protein. FEBS Lett. 2013; 587(8):1198-205. DOI: 10.1016/j.febslet.2013.01.036. View

Feng M, Zuo D, Jiang X, Li S, Chen J, Jiang L . Identification of Strawberry vein banding virus encoded P6 as an RNA silencing suppressor. Virology. 2018; 520:103-110. DOI: 10.1016/j.virol.2018.05.003. View

Yang X, Ren Y, Sun S, Wang D, Zhang F, Li D . Identification of the Potential Virulence Factors and RNA Silencing Suppressors of Mulberry Mosaic Dwarf-Associated Geminivirus. Viruses. 2018; 10(9). PMC: 6163789. DOI: 10.3390/v10090472. View

Stewart L, Jarugula S, Zhao Y, Qu F, Marty D . Identification of a maize chlorotic dwarf virus silencing suppressor protein. Virology. 2017; 504:88-95. DOI: 10.1016/j.virol.2016.11.017. View

Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, Belausov E . Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci U S A. 2008; 105(1):157-61. PMC: 2224178. DOI: 10.1073/pnas.0709036105. View

Yaegashi H, Takahashi T, Isogai M, Kobori T, Ohki S, Yoshikawa N . Apple chlorotic leaf spot virus 50 kDa movement protein acts as a suppressor of systemic silencing without interfering with local silencing in Nicotiana benthamiana. J Gen Virol. 2006; 88(Pt 1):316-324. DOI: 10.1099/vir.0.82377-0. View

Parent J, Bouteiller N, Elmayan T, Vaucheret H . Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing. Plant J. 2014; 81(2):223-32. DOI: 10.1111/tpj.12720. View

10.

Kosugi S, Hasebe M, Tomita M, Yanagawa H . Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A. 2009; 106(25):10171-6. PMC: 2695404. DOI: 10.1073/pnas.0900604106. View

11.

Gupta A, Hein G, Graybosch R, Tatineni S . Octapartite negative-sense RNA genome of High Plains wheat mosaic virus encodes two suppressors of RNA silencing. Virology. 2018; 518:152-162. DOI: 10.1016/j.virol.2018.02.013. View

12.

Bustin S, Benes V, Garson J, Hellemans J, Huggett J, Kubista M . The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55(4):611-22. DOI: 10.1373/clinchem.2008.112797. View

13.

Thompson J, Jelkmann W . The Detection and Variation of Strawberry mottle virus. Plant Dis. 2019; 87(4):385-390. DOI: 10.1094/PDIS.2003.87.4.385. View

14.

Pall G, Hamilton A . Improved northern blot method for enhanced detection of small RNA. Nat Protoc. 2008; 3(6):1077-84. DOI: 10.1038/nprot.2008.67. View

15.

Zhan B, Zhao W, Li S, Yang X, Zhou X . Functional Scanning of Apple Geminivirus Proteins as Symptom Determinants and Suppressors of Posttranscriptional Gene Silencing. Viruses. 2018; 10(9). PMC: 6164617. DOI: 10.3390/v10090488. View

16.

Baulcombe D . RNA silencing in plants. Nature. 2004; 431(7006):356-63. DOI: 10.1038/nature02874. View

17.

Sanfacon H, Dasgupta I, Fuchs M, Karasev A, Petrzik K, Thompson J . Proposed revision of the family Secoviridae taxonomy to create three subgenera, "Satsumavirus", "Stramovirus" and "Cholivirus", in the genus Sadwavirus. Arch Virol. 2019; 165(2):527-533. DOI: 10.1007/s00705-019-04468-7. View

18.

Kong L, Wang Y, Yang X, Sunter G, Zhou X . Broad bean wilt virus 2 encoded VP53, VP37 and large capsid protein orchestrate suppression of RNA silencing in plant. Virus Res. 2014; 192:62-73. DOI: 10.1016/j.virusres.2014.08.010. View

19.

Yang X, Guo W, Ma X, An Q, Zhou X . Molecular characterization of tomato leaf curl China virus, infecting tomato plants in China, and functional analyses of its associated betasatellite. Appl Environ Microbiol. 2011; 77(9):3092-101. PMC: 3126389. DOI: 10.1128/AEM.00017-11. View

20.

Perez-Canamas M, Hernandez C . New Insights into the Nucleolar Localization of a Plant RNA Virus-Encoded Protein That Acts in Both RNA Packaging and RNA Silencing Suppression: Involvement of Importins Alpha and Relevance for Viral Infection. Mol Plant Microbe Interact. 2018; 31(11):1134-1144. DOI: 10.1094/MPMI-02-18-0050-R. View