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

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)