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Table 2 Viral suppressors of RNA silencing (VSRs) encoded by plant-infecting viruses and the corresponding strategies to suppress antiviral RNA silencing

From: Viral suppressors from members of the family Closteroviridae combating antiviral RNA silencing: a tale of a sophisticated arms race in host-pathogen interactions

Family Genus Species Genome VSR Viral strategies to suppress antiviral RNA silencing References
Caulimoviridae Caulimovirus CaMV dsDNA P6 (TAV) Suppresses RNA silencing by DRB4 inactivation and interference with RDR6-dependent trans-acting and secondary vsiRNA pathways Haas et al. (2008) and Shivaprasad et al. (2008)
Geminiviridae Begomovirus TYLCV ssDNA V2 Suppresses antiviral RNA silencing locally by interacting with SGS3 Zrachya et al. (2007) and Glick et al. (2008)
TYLCCNV ssDNA βC1 Interacts with an endogenous suppressor of RNA silencing (rgsCAM) to inhibit RDR6 expression and secondary siRNA production Li et al. (2014)
Curtovirus BCTV ssDNA L2/AL2 Inactivates ADK, suppresses SAMS and SAHH to interfere with the methylation process Buchmann et al. (2009) and Csorba et al. (2015)
Mastrevirus WDV ssDNA Rep Impedes both local and systemic silencing via 21-nt and 24-nt siRNA binding Wang et al. (2014)
Tospoviridae Orthotospovirus GBNV (−)ssRNA NSs Interferes with miRNA biogenesis and suppresses antiviral RNA silencing responses locally Schnettler et al. (2010) and Goswami et al. (2012)
GRSV, INSV, TSWV, TYRV (−)ssRNA NSs Binds to dsRNA duplexes, including siRNA and miRNA, and suppresses local and systemic silencing Schnettler et al. (2010) and Hedil et al. (2015)
Phenuiviridae Tenuivirus RHBV, RSV (−)ssRNA NS3 Suppresses RNA silencing in plants and insects. Binds to RNA/RNA or RNA/DNA duplexes with a length greater than 9 nt and long ssRNA Hemmes et al. (2007) and Shen et al. (2010)
RSV (−)ssRNA P2 Interacts with SGS3 and enhances PVX pathogenicity Du et al. (2011)
Rhabdoviridae Cytorhabdovirus LNYV (−)ssRNA Phosphoprotein (P) Interacts with protein AGO (1, 2, 4), RDR6, and SGS3 to suppress RISC-mediated cleavage and RNA silencing amplification Mann et al. (2016)
Nucleorhabdovirus RYSV (−)ssRNA P6 Suppresses systemic RNA silencing only via inhibiting RDR6-mediated secondary siRNA biosynthesis and enhancing PVX virulence Guo et al. (2013)
Bromoviridae Cucumovirus CMV (+)ssRNA 2b Interacts with RDR proteins, suppresses AGO1 via upregulating miR168, and binds to siRNA as well Goto et al. (2007) and Varallyay and Havelda (2013)
TAV (+)ssRNA 2b Suppresses RNA silencing through the size-selective binding of siRNA Chen et al. (2008)
Ilarvirus AV-2 (+)ssRNA 2b Viral suppressor activity is retained in systemic silencing but not in local silencing Shimura et al. (2013)
Comovirinae Comovirus CPMV (+)ssRNA CP (S) C-terminal 16 amino acids of the CP (S) are predominantly essential for VSR activity Canizares et al. (2004)
Secoviridae Nepovirus ToRSV (+)ssRNA CP Suppresses RNA silencing through AGO1 binding and CP-mediated AGO1 degradation. VSR activity is conserved in the WG motif of CP Karran and Sanfacon (2014)
Reoviridae Phytoreovirus RDV dsRNA PNS10 Suppresses both local and systemic silencing, enhancing viral replication and stability. Downregulation of RDR6 through binding with siRNA Ren et al. (2010)
RGDV dsRNA PNS11, PNS12 PNS11 suppresses RNA silencing through miRNA pathway interference. PNS12 shows nucleus localization and suppresses RNA silencing locally Wu et al. (2011) and Shen et al. (2012)
Oryzavirus RRSV dsRNA PNS6 It is a local VSR, and ablation of the RNA binding region eliminates suppressor activity. Overexpression enhances PVX pathogenicity in N. benthamiana Wu et al. (2010)
Luteoviridae Enamovirus PEMV-1 (+)ssRNA P0 Suppresses local and systemic silencing via destabilization of AGO1 Fusaro et al. (2012)
Polerovirus BWYV, CYDV, CABYV (+)ssRNA P0 Targets AGO proteins through destabilization and the autophagy pathway and suppresses only local silencing Pazhouhandeh et al. (2006), Baumberger et al. (2007), Bortolamiol et al. (2007) and Derrien et al. (2012)
PLRV (+)ssRNA P0 Targets AGO1 and suppresses both local and systemic silencing Fusaro et al. (2012)
CLRDV, SCYLV (+)ssRNA P0 Suppresses local RNA silencing but not systemic silencing Mangwende et al. (2009) and Delfosse et al. (2014)
Potyviridae Ipomovirus SPMMV (+)ssRNA P1 Interacts with AGO1 through WG/GW motifs and inhibits si/miRNA-programmed RISC activity Giner et al. (2010)
CVYV (+)ssRNA P1 It enhances the VSR activity HC-Pro in members of Potyvirus. Its duplicated form, P1b, down-regulates dsRNA formation and suppresses local RNA silencing Valli et al. (2006)
Tritimovirus WSMV (+)ssRNA P1 Suppresses antiviral RNA silencing and downstream GFP siRNA accumulation significantly Young et al. (2012)
Poacevirus TriMV, SCSMV (+)ssRNA P1 Suppresses dsRNA-triggered systemic silencing more efficiently than HC-Pro of TuMV and enhances the pathogenicity of heterologous virus Tatineni et al. (2012)
Potyvirus TEV (+)ssRNA HC-Pro Binds to siRNA and inhibits its 3′ methylation, and suppresses AGO1 through miR168 up-regulation Lakatos et al. (2006) and Varallyay and Havelda (2013)
TuMV (+)ssRNA HC-Pro Interacts with RAV2 to restrict primary siRNA biogenesis, and interferes with the miRNA pathway as well Kasschau et al. (2003) and Endres et al. (2010)
ZYMV (+)ssRNA HC-Pro Binds to siRNA duplexes, interacts and inhibits HEN1 methylation activity Fuellgrabe et al. (2011) and Jamous et al. (2011)
PVY (+)ssRNA HC-Pro Suppresses antiviral RNA silencing through binding with 21–22 nt sRNA of viral sequences Del Toro et al. (2017)
SCMV (+)ssRNA HC-Pro Down-regulates the accumulation of secondary siRNAs and suppresses both sense RNA and dsRNA-induced silencing Zhang et al. (2008)
PVA (+)ssRNA HC-Pro, VPg HC-Pro interferes with host gene expression (SAHH) and interrupts the methionine cycle to suppress RNA silencing. VPg demonstrates SGS3 interaction Rajamaki and Valkonen (2009) and Ivanov et al. (2016)
PRSV (+)ssRNA HC-Pro Interferes with the miRNA pathway and downregulates AGO1 via miR168 upregulation Azad et al. (2014)
PPV (+)ssRNA HcPro-P1 Enhances silencing suppression in a synergistic form (HcPro-P1) Valli et al. (2006)
Rymovirus AgMV, HoMV (+)ssRNA HC-Pro Suppresses RNA silencing with tritimoviruses P1 while its VSR function is still unclear Young et al. (2012)
Tombusviridae Aureusvirus PoLV (+)ssRNA P14 Binds to dsRNAs without size selection and suppresses silencing through sequestering dsRNAs and ds siRNAs Merai et al. (2005)
Tombusvirus CIRV (+)ssRNA P19 Suppresses RNA silencing via binding with siRNA and hampering the 3′ methylation of siRNAs Lozsa et al. (2008) and Rawlings et al. (2011)
CymRSV (+)ssRNA P19 Silencing suppression through AGO1 repression via miR168 upregulation and binding silencing-generated 21–25 nt dsRNA size dependently Silhavy et al. (2002) and Varallyay et al. (2010)
TBSV (+)ssRNA P19 Suppresses antiviral RNA silencing via interacting miRNA pathways at the intermediate level, including miRNA methylation Chapman et al. (2004) and Yu et al. (2006)
CNV (+)ssRNA P20 Its VSR activity is quite similar to TBSV p19 but 50-fold lower than p19 Hao et al. (2011)
Carmovirus TCV (+)ssRNA P38 Targets AGO1 through GW-motifs and modifies DCL usage by increasing DCL1 levels, resulting in considerable DCL3 and DCL4 downregulation. Binds to dsRNA size independently and interferes with primary siRNA biogenesis (effect dependent on interaction with RAV2) Merai et al. (2006), Azevedo et al. (2010) and Endres et al. (2010)
PFBV, HCRSV, PLPV (+)ssRNA CP/ P37 Binds to siRNAs and suppresses RNA silencing with the enhancement of PVX pathogenicity. Mutations in the GW motif affects siRNA binding capability Meng et al. (2006), Martinez-Turino and Hernandez (2009) and Perez-Canamas and Hernandez (2015)
MNSV (+)ssRNA P7B, P42 P7B delays RNA silencing. P42 enhances local spread similar to that of potyviral HC-Pro, probably because of its VSR activity Genoves et al. (2006)
Dianthovirus RCNMV (+)ssRNA MP It is an unknown DCL1 dependent MP and interferes with miRNA biogenesis Takeda et al. (2005)
Closteroviridae Ampelovirus GLRaV-3 (+)ssRNA P19.7 Impedes RNA silencing through siRNA and miRNA pathway interference Gouveia and Nolasco (2012) and Gouveia et al. (2012)
PMWaV-1,-2 (+)ssRNA P61, CP, P20 P61 suppresses RNA silencing systemically, CP subdues both local and systemic silencing, and P20 affects dsRNA-induced local silencing Dey et al. (2015)
Closterovirus BYV (+)ssRNA P21 Interacts with 21 nt or longer ssRNAs and dsRNAs and suppresses dsRNA-induced silencing of GFP mRNA and blocks HEN1 methyltransferase Reed et al. (2003), Lu et al. (2004) and Ye and Patel (2005)
CTV (+)ssRNA CP, P20, P23 CP and p20 suppress antiviral RNA silencing pathways at the intercellular level, while P23 does so at the intracellular level Lu et al. (2004), Fagoaga et al. (2011) and Benitez-Galeano et al. (2015)
RLRaV (+)ssRNA P17 Suppresses antiviral RNA silencing in wild roses He et al. (2015)
Crinivirus CYSDV (+)ssRNA P25 Inhibits siRNA accumulation and suppresses dsRNA- or ssRNA-induced silencing of GFP mRNA Kataya et al. (2009)
CCYV (+)ssRNA P22 Binds with CsSKP1LB and suppresses antiviral RNA silencing Chen et al. (2019)
SPCSV (+)ssRNA RNase3, P22 RNase3 displays endonuclease activity and cleaves siRNAs, but the P22 silencing strategy is still elusive Kreuze et al. (2005) and Cuellar et al. (2008)
LCV (+)ssRNA P23 Enhances degradation of siRNAs and suppresses silencing Kubota and Ng (2016)
ToCV (+)ssRNA P22, CP, CPm P22 counteracts RDR6-mediated antiviral response, CP induces SAHH-interaction, and CPm silencing mechanism is unidentified Canizares et al. (2008), Landeo-Rios et al. (2016a) and Liu et al. (2021)
TICV (+)ssRNA P27 Suppresses S-PTGS and IR-PTGS Mashiko et al. (2019)
Virgaviridae Hordeivirus BSMV, PSLV (+)ssRNA γB Suppresses RNA silencing by preferentially binding to siRNA size selectively Yelina et al. (2002) and Merai et al. (2006)
Pecluvirus PCV (+)ssRNA P15 Binds to siRNA size selectively and interferes with the miRNA pathway to suppress antiviral silencing Dunoyer et al. (2004) and Merai et al. (2006)
Tobamovirus ORMV (+)ssRNA P126 Interferes with the methylation pathway mediated by HEN1 and the accumulation of novel miRNA-like sRNAs Vogler et al. (2007)
TMV (+)ssRNA P126, P122 P126 mechanism of suppression is unclear, while P122 suppresses RNA silencing through siRNA and miRNA binding and downregulates AGO1 via upregulation of miR168 Csorba et al. (2007) and Wang et al. (2012)
ToMV (+)ssRNA P130 Suppresses silencing signals through siRNA binding Kubota et al. (2003)
Tobravirus TRV (+)ssRNA 16 K Blocks local silencing via down streaming of dsRNA biogenesis Martinez-Priego et al. (2008)
Furovirus CWMV, SBWMV (+)ssRNA 19 K (CRP) Suppresses silencing signal, thereby enhancing PVX pathogenicity, and interacts with N-ext/CP Te et al. (2005) and Sun et al. (2013)
Benyviridae Benyvirus BNYVV, BSBMV (+)ssRNA P14 Its VSR activity requires both ZF and NoLS basic residues Chiba et al. (2013)
BNYVV (+)ssRNA P31 Plays a role in root-specific silencing suppression and interacts with PR-10 Rahim et al. (2007) and Wu et al. (2014)
Tymoviridae Tymovirus TYMV (+)ssRNA P69 Inhibits DNA methylation, boosting miRNA and DCL1 upregulation Chen et al. (2004)
CVB (+)ssRNA P12 Its VSR activity is ZF domain-dependent but independent of NLS. Promotes PVX infection Lukhovitskaya et al. (2014)
Alphaflexiviridae Potexvirus PVX, PlAMV, PepMV (+)ssRNA P25 (TGBp1) Suppresses RNA silencing via degrading RNA silencing effector nuclease AGO1, co-aggregation with SGS3/RDR6, CAT1 interaction, and X-body organization Chiu et al. (2010), Tilsner et al. (2012), Mathioudakis et al. (2013) and Okano et al. (2014)
PepMV (+)ssRNA CP Sequesters silencing signals by inhibiting systemic signaling Mathioudakis et al. (2014)
Betaflexiviridae Carlavirus PVM (+)ssRNA CRP, TGBp1 TGBp1 suppresses merely systemic silencing, whereas CRP inhibits both local and systemic silencing Senshu et al. (2011)
SPCFV (+)ssRNA NaBp Suppresses local and systemic silencing, mediated by either sense or dsRNA molecules Deng et al. (2015)
Trichovirus ACLSV (+)ssRNA P50 Suppresses silencing systemically, probably by preventing the movement of silencing signals Yaegashi et al. (2007)
Vitivirus GVA (+)ssRNA P10 Suppresses local and systemic silencing by siRNA binding Zhou et al. (2006)
Citrivirus CLBV (+)ssRNA MP Interferes with silencing pathways via downregulating the biogenesis of dsRNA and siRNA Renovell et al. (2012)
Solemoviridae Sobemovirus RYMV (+)ssRNA P1 Suppresses RNA silencing through reduction of 21–24 nt siRNAs and deregulation of DCL4‐dependent endogenous siRNA pathways Lacombe et al. (2010)
CfMV (+)ssRNA P1, CP P1 shows weak systematic suppression without siRNA binding, while CP suppresses antiviral RNA silencing, but the mechanism of suppression is not clear Sarmiento et al. (2007) and Olspert et al. (2014)
  1. ACLSV Apple chlorotic leaf spot virus, AgMV Agropyron mosaic virus, AV-2 Asparagus virus 2, BCTV Beet curly top virus, BNYVV Beet necrotic yellow vein virus, BSBMV Beet soil-borne mosaic virus, BSMV Barley stripe mosaic virus, BWYV Beet western yellows virus, BYV Beet yellow virus, CABYV Cucurbit aphid borne yellows virus, CaMV Cauliflower mosaic virus, CCYV Cucurbit chlorotic yellow virus, CfMV Cocksfoot mottle virus, CIRV Carnation italian ringspot virus, CLBV Citrus leaf blotch virus, CLRDV Cotton leafroll dwarf virus, CMV Cucumber mosaic virus, CNV Cucumber necrosis virus, CPMV Cowpea mosaic virus, CTV Citrus tristeza virus, CVYV Cucumber vein yellowing virus, CWMV Chinese wheat mosaic virus, CVB Chrysanthemum virus B, CYDV Cereal yellow dwarf virus, CYSDV Cucurbit yellow stunting disorder virus, CymRSV Cymbidium ringspot virus, GBNV Groundnut bud necrosis virus, GLRaV-3 Grapevine leafroll-associated virus 3, GRSV Groundnut ringspot virus, GVA Grapevine virus A, HCRSV Hibiscus chlorotic ringspot virus, HoMV Hordeum mosaic virus, LCV Lettuce chlorosis virus, LNYV Lettuce necrotic yellows virus, MNSV Melon necrotic spot virus, ORMV Oilseed rape mosaic virus, PCV Peanut clump virus, PEMV-1 Pea enation mosaic virus-1, PepMV Pepino mosaic virus, PFBV Pelargonium flower break virus, PlAMV Plantago asiatica mosaic virus, PLPV Pelargonium line pattern virus, PLRV Potato leafroll virus, PMWaV-1,-2 Pineapple mealybug wilt-associated virus 1,-2, PoLV Pothos latent virus, PPV Plum pox potyvirus, PRSV Papaya ringspot virus, PSLV Poa semilatent virus, PVA Potato virus A, PVM Potato virus M, PVX Potato virus X, PVY Potato Virus Y, RCNMV Red clover necrotic mosaic virus, RDV Rice dwarf virus, RGDV Rice gall dwarf virus, RHBV Rice hoja blanca virus, RLRaV Rose leaf rossette-associated virus, RRSV Rice ragged stunt virus, RSV Rice stripe virus, RYMV Rice yellow mottle virus, RYSV Rice yellow stunt rhabdovirus, SBWMV Soil-borne wheat mosaic virus, SCFaV Strawberry chlorotic fleck‐associated virus, SCMV Sugarcane mosaic virus, SCSMV Sugarcane streak mosaic poacevirus, SCYLV Sugarcane yellow leaf virus, SPCSV Sweet potato chlorotic stunt virus, SPMMV Sweet potato mild mottle virus, TAV Tomato aspermy virus, TBSV Tomato bushy stunt virus, TCV Turnip crinkle virus, TEV Tobacco etch virus, TICV Tomato infectious chlorosis virus, TMV Tobacco mosaic virus, ToCV Tomato chlorosis virus, ToMV Tomato mosaic virus, ToRSV Tomato ringspot virus, TriMV Triticum mosaic virus, TRV Tobacco rattle virus, TSWV Tomato spotted wilt virus, TuMV Turnip mosaic virus, TYLCCNV Tomato yellow leaf curl China virus, TYLCV Tomato yellow leaf curl virus, TYRV Tomato yellow ring virus, TYMV Turnip yellow mosaic virus, WDV Wheat dwarf virus, WSMV Wheat streak mosaic virus, ZYMV Zucchini yellow mosaic virus