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

Hussain, Muhammad Dilshad; Farooq, Tahir; Chen, Xi; Tariqjaveed, Muhammad; Jiang, Tong; Liu, Sijia; Zhou, Tao

doi:10.1186/s42483-021-00104-y

Review
Open access
Published: 15 November 2021

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

Muhammad Dilshad Hussain¹,
Tahir Farooq²,
Xi Chen¹,
Muhammad Tariqjaveed³,
Tong Jiang¹,
Sijia Liu¹ &
…
Tao Zhou ORCID: orcid.org/0000-0001-7702-8472¹

Phytopathology Research volume 3, Article number: 27 (2021) Cite this article

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Abstract

RNA silencing is an evolutionarily homology-based gene inactivation mechanism and plays critical roles in plant immune responses to acute or chronic virus infections, which often pose serious threats to agricultural productions. Plant antiviral immunity is triggered by virus-derived small interfering RNAs (vsiRNAs) and functions to suppress virus further replication via a sequence-specific degradation manner. Through plant-virus arms races, many viruses have evolved specific protein(s), known as viral suppressors of RNA silencing (VSRs), to combat plant antiviral responses. Numerous reports have shown that VSRs can efficiently curb plant antiviral defense response via interaction with specific component(s) involved in the plant RNA silencing machinery. Members in the family Closteroviridae (closterovirids) are also known to encode VSRs to ensure their infections in plants. In this review, we will focus on the plant antiviral RNA silencing strategies, and the most recent developments on the multifunctional VSRs encoded by closterovirids. Additionally, we will highlight the molecular characters of phylogenetically-associated closterovirids, the interactions of these viruses with their host plants and transmission vectors, and epidemiology.

Background

The viruses of the family Closteroviridae are characterized by their flexuous, exceptionally long filamentous, and non-enveloped particles with lengths of 950–2200 nm and diameters of 10–13 nm. These closterovirids are composed of positive-sense single-stranded RNA (+ssRNA), causing acute or chronic infections in plants and threatening agricultural production systems globally (Martelli 2019; Jones 2021). Generally, closterovirids have a common pattern of genomic organization that possesses variable numbers of open reading frames (ORFs). However, the presence of cellular heat-shock proteins HSP70 homology (HSP70h) with a duplicated and deviated form of coat protein (designated as minor coat protein or CPm) in genome are hallmarks of viruses in this family, distinguishing them from other plant viruses (Agranovsky 2016; Ruiz et al. 2018). Strikingly, their genomic expression strategy is predicated according to the proteolytic processing, such as a + 1 translational/ribosomal frameshifting together with sub-genomic mRNAs. Therefore, strong negative selection and recombination are primary factors influencing their genetic diversity (Rubio et al. 2013; Fuchs et al. 2020).

Presently, according to the 2020 master species list-36 (MSL36) released by the International Committee on Taxonomy of Viruses (ICTV), the Closteroviridae family contains 4 genera (Amplelovirus, Crinivirus, Closterovirus and Velavirus) and 52 identified species, with 7 unassigned species (https://ictv.global/taxonomy). Most closterovirids have evolved from common ancestors and are transmitted through specific insect vectors (arthropods), such as mealybugs (Ampelovirus), aphids (Closterovirus), and whiteflies (Crinivirus). The vector for members of the genus Velarivirus is yet to be identified. However, there is merely an exception for mint vein banding-associated virus (MVBaV). MVBaV is an aphid-borne virus, which is phylogenetically distant from other members of the family (Martelli et al. 2012; Fuchs et al. 2020). The majority of closterovirids cause substantial disease epidemics in combined infections with other plant viruses that may result in synergistic effects. Moreover, the host range and environmental factors determining vector population dynamics have important epidemiological consequences (Tzanetakis et al. 2007, 2013; Quito-Avila et al. 2014).

To improve crop quality and quantity, a study of the progress of viral infection and defense strategies remains most significant. It is obvious from molecular characterization of plant viruses that virus infection process is coordinated with their restricted viral factors, through which viruses interact with host proteins and recruit biological processes crucial for their multiplication and translocation (Tatineni et al. 2012; Castillo-Gonzalez et al. 2015; Liu et al. 2021). On the other hand, plants develop a set of complex antiviral defense system to counter viral infection, including antiviral RNA silencing, systemic acquired resistance (SAR), hypersensitive responses (HR), DNA methylation, ubiquitin–proteasome system (UPS), and hormone signaling pathways such as salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) (Huh et al. 2012; Mandadi and Scholthof 2013; Balint-Kurti 2019; Li and Wang 2019; Tirnaz and Batley 2019; Kamle et al. 2020; Dubiella and Serrano 2021; Zhao and Li 2021).

Recently, significant research has been done to understand the mechanisms and functions of antiviral RNA silencing as well as viral strategies to counter this defense (Jones and Dangl 2006; Shi et al. 2008; Sansregret et al. 2013; Csorba et al. 2015; Jin et al. 2021; Teixeira et al. 2021). Antiviral RNA silencing is a highly conserved regulatory mechanism of gene expression, which plays the most important role in different biological processes associated with host protection against viral infection. Plants recruit this mechanism as a shield against viruses by encoding abundant crucial components, such as RNA-dependent RNA polymerases (RdRps), Dicer ribonucleases (DCLs), Argonaute endonucleases (AGO), double-stranded RNA (dsRNA), and helicases (Lee and Carroll 2018; Muhammad et al. 2019; Lax et al. 2020). In response to this defense strategy, viruses have also evolved to produce various multifunctional proteins that act as VSRs to avoid being silenced and thus ensure successful infections (Daròs 2017; Gaffar and Koch 2019).

Our current review highlights recent progress and breakthroughs in plant-targeting VSRs together with particular strategies and mechanisms aimed at evading antiviral RNA silencing. It also demonstrates mechanistic insights into various VSR strategies by which closterovirids evade antiviral responses of host plants in order to execute successful viral infections. Closterovirids are presented here according to their evolutionary relatedness (Fig. 1) as members of each genus tend to have similar genomic organization, transmission vectors, and host ranges, but diverse modes of infection (Table 1).

Table 1 Closterovirids with their origin, natural hosts, transmission vectors, diverse modes of infection, and disease epidemiology

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Antiviral RNA silencing and plant immunity

Plants and microbial pathogens are fascinatingly engaged in a continuous battle for survival. Plant immunity to non-viral pathogens has revealed well-organized, multi-layered, and sophisticated signaling pathways, which are triggered by the perception of diverse pathogen-associated molecular patterns (PAMPs) to initiate the first layer of defense. This fundamental defense mechanism (PAMP-triggered immunity, PTI) elucidates the entire co-evolutionary arms race between pathogen and host plant. For invading pathogens, they encode virulence factors, named as effectors, to suppress PTI (Shan et al. 2008; Calil and Fontes 2017; Gouveia et al. 2017; Teixeira et al. 2021). Therefore, plants respond to PTI suppression through resistance (R) proteins using a highly precise and effective type of immunity, known as effector-triggered immunity (ETI) (Cui et al. 2015; Hatsugai et al. 2017; Peng et al. 2018). Since this phenomenon represents protein-based rather than RNA-involved defense mechanisms, it was considered that PTI and ETI are remarkably independent of antiviral RNA silencing. The mechanism of antiviral RNA silencing in plants reveals a related process, termed as post-transcriptional gene silencing (PTGS). Recently, biological evidences have indicated that PTGS and transcriptional gene silencing (TGS), induced by endogenic small RNAs (sRNAs), are evolving as significantly crucial drivers of ETI and PTI signaling pathways, as well as R gene expression (Zhai et al. 2011; Baltusnikas et al. 2018; Tan et al. 2020; Sanan-Mishra et al. 2021). Furthermore, several classes of microorganisms, such as plant viruses, bacteria, and oomycetes, have been discovered to produce suppressor proteins as part of their virulence effectors, to suppress RNA silencing in host plants and cause disease (Navarro et al. 2008; He et al. 2019).

The mechanism and localization of antiviral RNA silencing

In plants, an antiviral silencing pathway is triggered by two discrete classes of sRNAs, including microRNAs (miRNAs) and small interfering RNAs (siRNAs), exerting diverse actions such as mRNA degradation, DNA methylation, and translational inhibition (Li and Wang 2019; Tan et al. 2020). Mechanistically, the antiviral RNA silencing model is divided into initiation, effector, and amplification phases (Zhang et al. 2015; Csorba and Burgyán 2016). Plant viruses, containing RNA genomes with defective regulatory stem-loop, are transcribed into complementary dsRNA replication intermediates through viral encoded RdRps. This dsRNA is designed as a virus-associated molecular pattern (VAMP), which is a form of PAMP. During the initiation phase, VAMPs are recognized and cleaved by dsRNA-specific RNases named as DCL enzymes (primarily by DCL4 and secondarily by DCL2), producing 21 to 24-nt double-stranded vsiRNA duplexes (Pumplin and Voinnet 2013). On the other hand, microRNA (MIR) genes encode pre-miRNAs, which are transcribed into primary miRNAs (pri-miRNAs) through RNA polymerase II (Pol II). Subsequently, stem-loop containing pri-miRNAs are processed into mature miRNA duplexes through the RNA III family enzyme DCL1. These miRNA and vsiRNA duplexes are stabilized at their 3′ end, mediated by the HUA Enhancer 1 (HEN1)-dependent methylation process (Burgyan and Havelda 2011; Rogers and Chen 2013; Zhang et al. 2015). Furthermore, stabilized vsiRNA and miRNA duplexes were unzipped and separated into two strands, termed as guide and passenger strand, respectively, by helicase. The guide strand is incorporated into AGO proteins, facilitating the formation of a complex (RNA-induced silencing complex, RISC), while the passenger strand is shattered (Vaucheret 2008; Zhang et al. 2015; Waheed et al. 2021). To complete the effector phase of antiviral RNA silencing, RISCs target vsiRNA or miRNA complementary mRNAs and trigger their PTGS via endonucleolytic cleavage or translational inhibition (Waterhouse and Helliwell 2003; Brodersen et al. 2008; Carbonell and Carrington 2015; Mengistu and Tenkegna 2021). For the amplification of antiviral RNA silencing, AGO-sliced products serve as templates for RdRp (RDR for cellular RdRps) complexes using RNA-helicases (SGS3 and SDE5), the cofactors of RDR-mediated pathways (Vaucheret 2006; Jauvion et al. 2010; Csorba et al. 2015; Tong et al. 2021).

In plant, antiviral RNA silencing spreads between adjacent cells and over long distances via plasmodesmata and phloem, respectively. In local spread of RNA silencing, most probably, silencing molecules (siRNAs, miRNAs) move beyond the production sites to 10–15 cells. However, the activation of local silencing signaling is independent of homologous transcripts. The activity of RDR6 and SDE3 is not essential for the synthesis or detection of silencing signals, but at least three SILENCING MOVEMENT DEFICIENT genes (SMD1-3) are mandatory for cell-to-cell movements (Voinnet 2005; Mermigka et al. 2016). Meanwhile, in the particular scenario of systemic spread of silencing, the amplification process requires RDR6, SDE3 or SDE5 to convert homologous transcripts into new dsRNAs in cells where local silencing signals have been received. These new dsRNAs are processed into secondary siRNAs through DCL4 and movement proceeds across additional 10–15 cells (Fig. 2). Therefore, the local and systemic silencing signaling events are mediated by primary and secondary vsiRNAs synthesis, respectively (Voinnet 2005; Melnyk et al. 2011; Mermigka et al. 2016).

Viral strategies to evade antiviral RNA silencing

PTGS is an important defense mechanism of plants against viral infection. To recruit a successful infection, viruses have evolved diversified strategies, of which the production of VSRs can negatively control PTGS by constraining miRNA and siRNA regulation in plants (Hu et al. 2020). Extensive studies on a large number of plant viruses have demonstrated the multi-functionality of VSRs. In addition to suppress RNA silencing, they also play significant roles as transcriptional activation factors (helicase, protease, and replicase), symptom determinants, as well as helper components in the viral infection process. Therefore, VSRs have evolved independently with no structural similarities, repressing antiviral RNA silencing in hosts by affecting the involved core components (Li and Wang 2019) (Table 2, Fig. 2).

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

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Meddling with methylation cycle and suppressing TGS

DNA viruses such as geminiviruses and their associated betasatellites encode VSRs to suppress TGS through inhibiting or degrading key regulators of the methylation cycle. For example, transcriptional activator protein (TrAP) of beet severe curly top virus (BSCTV), tomato golden mosaic virus (TGMV), and cabbage leaf curl virus (CaLCuV), the pathogenicity factor βC1 of tomato yellow leaf curl China virus (TYLCCNV) and associated betasatellite, C4 protein of cotton leaf curl Multan virus (CLCuMuV), and L2 protein of beet curly top virus (BCTV), as well as AL2 protein of CaLCuV, can compromise the methylation process by impeding its major regulatory enzymes. These enzymes include S-adenosyl methionine synthetase (SAMS), adenosine kinase (ADK), and S-adenosyl homocysteine hydrolase (SAHH), which are also essential for TGS (Fig. 2) (Yang et al. 2011; Csorba et al. 2015; Jackel et al. 2015; Ismayil et al. 2018). Most geminiviruses, such as TGMV and CaLCuV, encode TrAP protein to activate the viral gene transcription by inhibiting the histone methyltransferase KYP/SUVH4 activity (Castillo-Gonzalez et al. 2015; Guerrero et al. 2020). Other geminiviral factors, including Rep, V2, C4, and C5, can also suppress TGS by interfering with methylation factors (Rodríguez-Negrete et al. 2013; Wang et al. 2018).

Binding with dsRNA and cleaving vsiRNA

The binding of VSRs to dsRNA is a general approach for VSRs to suppress RNA silencing. For example, various VSRs such as P38, P14, NS3, and NSs from turnip crinkle virus (TCV), pothos latent virus (PoLV), rice stripe virus (RSV)/rice hoja blanca virus (RHBV), and tomato spotted wilt virus (TSWV)/groundnut bud necrosis virus (GBNV), respectively, bind to dsRNA and inhibit the vsiRNA biogenesis (Fig. 2) (Yang and Li 2018). Strikingly, the sweet potato chlorotic stunt virus (SPCSV)-encoded VSR, RNase3, disables RNA silencing via an endonuclease activity-dependent pathway by cleaving dsRNA and vsiRNA duplexes (Cuellar et al. 2009).

Interfering with RDR and DCL4

The P6 suppressor protein of cauliflower mosaic virus (CaMV) binds with a double-stranded RNA-binding protein 4 (DRB4) to compromise the function of DCL4 in RNA-mediated PTGS. Moreover, P6 can also interfere with RDR6-dependent trans-acting and secondary vsiRNA pathways through interacting with DCL4 and impairing its functions (Haas et al. 2008; Shivaprasad et al. 2008). The TCV-associated P38 protein interacts with AGO1 and alters DCL usage by boosting DCL1 levels, resulting in significant downregulation of DCL3 and DCL4 (Azevedo et al. 2010; Endres et al. 2010).

Binding with HEN and sequestrating vsiRNA

As briefly described above, vsiRNA duplexes undergo methylation mediated by HEN1 before they are loaded onto AGOs. This methylation protects sRNAs from exonuclease degradation, facilitating systemic spread of antiviral RNA silencing signals. To counteract host antiviral RNA silencing, HC-Pro protein of zucchini yellow mosaic virus (ZYMV) binds to HEN1 and inhibits its methyltransferase activity (Jamous et al. 2011). Several VSRs, including 2b protein of cucumber mosaic virus (CMV), p19 protein of tomato bushy stunt virus (TBSV), HC-Pro protein of turnip mosaic virus (TuMV), and p21 protein of beet yellow virus (BYV), can bind to miRNA and vsiRNA duplexes and prevent HEN1-mediated methylation (Burgyan and Havelda 2011; Duan et al. 2012). The sequestration of vsiRNA by VSRs has been demonstrated to inhibit the plant-mediated antiviral RNA silencing pathways.

Degrading AGOs and interfering with RISC assembly

The AGO family is characterized as a critical component of RISC assembly, and plays key regulatory functions during the process of antiviral RNA silencing. Several VSRs interact with AGO1 and suppress RNA silencing response (Müller et al. 2020), such as the Polerovirus F-box P0, the tomato ringspot virus (ToRSV) CP, and the TCV P38; they all target AGO1 and trigger its instability and degradation (Azevedo et al. 2010; Karran and Sanfacon 2014; Derrien et al. 2018). Interestingly, the 16K protein of tobacco rattle virus (TRV) interacts with AGO4 and interferes with the assembly of RISC (Fernandez-Calvino et al. 2016). Similarly, the P1 protein of sweet potato mild mottle virus (SPMMV) suppresses RNA silencing by restricting RNA binding to AGO1, thus negatively regulates RISC assembly (Kenesi et al. 2017).

Interacting with miRNA and upregulating pre-miRNA

The miRNA is a discrete class of sRNA that triggers an antiviral defense against viral infection. However, several VSRs can interact with miRNA pathways to disrupt this antiviral function through upregulation of pre-miRNA. For instance, the rice gall dwarf virus (RGDV) PNS11 protein and the TBSV P19 protein suppress antiviral RNA silencing through interacting with miRNA pathways, including miRNA methylation (Yu et al. 2006; Burgyan and Havelda 2011; Shen et al. 2012). Similarly, HC-Pro from papaya ringspot virus (PRSV) and tobacco etch virus (TEV), and P19 from cymbidium ringspot virus (CymRSV) repress AGO1 accumulation via upregulation of pre-miR168, leading to the suppression of antiviral RNA silencing (Varallyay et al. 2010; Varallyay and Havelda 2013; Azad et al. 2014).

Meddling with the amplification of antiviral RNA silencing

The amplification of RNA silencing is most important for the inhibition of viral infection. Therefore, plant recruits several RDR proteins and RNA-helicases (SGS3 and SDE5), the extremely crucial components in antiviral RNA silencing pathways, to perform this amplification. Plant viruses of different groups encode VSRs to interact with RDR6 and SGS3, resulting in the suppression of RDR-mediated pathways. Some VSRs, such as VPg and HC-Pro from potyviruses, βC1, V2, and AC2 from geminiviruses, P2 from RSV, P6 from rice yellow stunt rhabdovirus (RYSV), and TGBp1 from plantago asiatica mosaic potexvirus (PlAMV), can bind to SGS3 and RDR6, and trigger the suppression of antiviral RNA silencing (Du et al. 2011; Guo et al. 2013; Cheng and Wang 2017) (Table 2, Fig. 2). Among them, V2 of CLCuMuV may also target calmodulin (CaM) to suppress anti-RNAi defense (Wang et al. 2021). In addition, V2 of TYLCV binds to SGS3 and suppresses RNA silencing locally (Glick et al. 2008). Whereas, βC1 protein of TYLCCNV satellite suppresses RDR6 expression and secondary vsiRNA production by upregulating an endogenous suppressor of RNA silencing (rgsCAM) (Li et al. 2014). Moreover, both 2b of CMV and p22 of tomato chlorosis virus (ToCV) interact with RDR6 to inhibit secondary vsiRNA biosynthesis (Landeo-Rios et al. 2016b).

Inhibiting the spread of antiviral RNA silencing

In virus-infected plants, local and systemic spread of silencing signal molecules constitutes the basis of antiviral RNA silencing pathways. To establish successful infection, viruses encode VSRs accordingly to target key regulators of these antiviral pathways. The Rep protein of wheat dwarf virus (WDV) suppresses RNA silencing locally and systemically through binding with vsiRNA duplexes (Wang et al. 2014). The P6 protein of RYSV suppresses systemic RNA silencing by constraining RDR6-mediated biosynthesis of secondary vsiRNAs. Similarly, the CMV-encoded 2b protein block the translocation of RNA silencing signals and inhibit their spread (Guo and Ding 2002). Moreover, the potato virus X (PVX) suppressor protein (p25) inhibits the production of RNA silencing signals and interferes with their propagation (Voinnet et al. 2016).

Viral proteins of closterovirids to counteract antiviral RNA silencing

GLRaV-2 p24 protein as a VSR

The p24 protein of GLRaV-2 is a strong VSR encoded by a cryptic ORF in the viral genome. It can effectively block siRNA accumulation and suppress antiviral RNA silencing (Wang et al. 2019). The N-terminus (amino acids 1–188) of p24 is a main functional region, comprising all predicted α-helicases and β-strands that are most essential for its VSR activity. Moreover, self-interaction, pathogenicity, and silencing suppression of p24 are associated with its hydrophobic residues (135/F38/V85/V89/W149, V162/L169/L170). Specifically, p24 suppresses RNA silencing by adopting an RNA-binding strategy. Substituting two basic amino acid residues at positions 2 and 86, which are involved in RNA-binding, totally negates the VSR activity of p24 (Liu et al. 2016). W54 in the WG/GW-like motif (W54/G55) is also primarily significant for retaining p24 suppressor activity (Li et al. 2018). Furthermore, p24 has no physical interaction with AGO1 of N. benthamiana, and it up-regulates mRNA expression of AGO1 without boosting AGO1 degradation. This impact is specifically correlated with the VSR activity of p24, demonstrating that it may hamper miRNA-directed processes (Li et al. 2018).

GLRaV-3 p19.7 protein as a VSR

The 3′ end monopartite RNA genome of GLRaV-3 encodes a VSR (p19.7) with a molecular weight of around 20 kDa. The p19.7 protein demonstrates VSR activity in various silencing induction systems. This VSR shares several characteristics with p21, a BYV suppressor protein capable of overcoming powerful silencing inducers (Gouveia et al. 2012). In co-infiltration assays, the VSR activity of p19.7 varies among GLRaV-3 variants, resulting in variable levels of accumulation of green fluorescent protein (GFP) mRNA and specific siRNA in the transgenic N. benthamiana line 16c. A comparison analysis of protein sequences demonstrated that the substitutions of a few amino acids in p19.7 may be linked to the variation in its suppression activity (Gouveia and Nolasco 2012).

PMWaV-1 p61 protein as a VSR

The p61 protein is reported to have a systemic silencing suppressor activity up to 18 days post-infiltration (dpi) among the 3′-proximal ORFs of PMWaV-1 that encode p61, p24, CP, and Hsp70, while no protein with local suppressor activity was identified (Dey et al. 2015).

PMWaV-2 p20 and CP proteins as VSRs

It has been stated that the two 3′-proximal ORFs of PMWaV-2 encode CP and p20 proteins, which adversely affect the induction of secondary siRNAs and prevent the systemic spread of antiviral silencing signals. Therefore, CP and p20 proteins affect RNA silencing (both local and systemic) in N. benthamiana, while CPd and p22 proteins solely mitigate systemic silencing. In addition, p20 protein suppresses dsRNA-induced local silencing, specifically, when there are lower levels of dsRNA. Furthermore, it has also been indicated that p20 can boost the infectivity of PVX in N. benthamiana (Dey et al. 2015).

BYV p21 protein as a VSR

The 3′-proximal genomic region of BYV encodes a 21 kDa protein (p21). The p21 protein belongs to an important gene family of alike proteins that are possessed by other viruses in the Closterovirus genus, exhibiting a silencing suppressor role. The p21 is capable of interfering and suppressing dsRNA-induced silencing of GFP mRNA, however, BYSV- and CTV-encoded VSRs, p22 and p20, only show weak suppressor activity as compared to BYV p21. BYV p21 exhibits its VSR functionality in two model systems. In the first system, dsRNA induces a robust silencing of reporter mRNA, while in the second system, weak silencing is initiated via ectopic expression of mRNA from a stronger promoter (Reed et al. 2003). Furthermore, the crystalline structure of p21 shapes an RNA binding octameric ring architecture with a large central cavity of 90 Å diameter and the inner surface of the ring is positively charged. Tombusviruses VSRs, p19 and p21, both inhibit silencing through binding to siRNA directly. Contrastingly, besides interacting with peculiar dimeric-structured p19-siRNA duplex, BYV p21 is also a nucleic acid-binding protein that interacts in vitro with 21 nt or longer ssRNAs and dsRNAs. This p21-adopted precise RNA binding structure highlights various open challenges to study the structure-based interaction mechanism of other VSRs (Ye and Patel 2005).

CTV CP, p20, and p23 proteins as VSRs

Three distinct VSRs such as CP, p20, and p23 are encoded by the 3′-proximal region of large RNA genome of CTV, protecting virus from the antiviral silencing machinery of its perennial woody citrus host (Hajeri et al. 2014). Unlike p20 and other VSRs known to interfere with intercellular silencing, such as CMV 2b and PVX p25, CP is a unique VSR that suppresses antiviral RNA silencing pathways at an intercellular level, and this is not associated with intracellular silencing suppression. CMV 2b and p20 share features in silencing suppression, and are potent suppressors of intercellular silencing but incomplete in suppressing intracellular silencing, however, unlike CMV 2b, the intercellular silencing suppression of p20 is not linked to substantially declined DNA methylation of the target GUS transgene (Lu et al. 2004; Benitez-Galeano et al. 2015). In terms of local silencing suppressor activity, p23 is the most effective VSR among the three aforementioned CTV VSRs, and its localization is restricted to both the plasmodesmata and nucleus. Although p23 is a strong intracellular silencing suppressor like HC-Pro, it does not restrict intercellular silencing and DNA methylation of the target transgene. There are many conserved amino acids in p23 and mutations of E95A/V96A and M99A/L100AA may compromise its VSR activity and stability, furthermore, deletions of Q93A and R143A/E144A completely abolish its VSR activity (Li et al. 2019). Moreover, ectopic expression of p23 enhances CTV accumulation and dispersion in woody hosts and, in addition, promotes systemic infection of the resistant sour orange host (Fagoaga et al. 2011).

RLRaV p17 protein as a VSR

RLRaV encodes a 17 kDa protein (p17). Its BLASTp search results indicate conserved motif characteristics of the viral suppressor p20 superfamily, such as p23 or p20 of RLMV, CTV, and SCFaV. RLRaV uses p17 as a VSR to combat antiviral RNA silencing response in wild roses (Rosa multiflora Thumb) upon the occurrence of wild rose leaf rosette disease (He et al. 2015).

CYSDV p25 protein as a VSR

The papain-like protease proteins, including p25, p5.2, and p22, were hypothesized to have VSR activity. However, only p25 has been identified as a PTGS suppressor of CYSDV. Its VSR strategy is to suppress dsRNA- or ssRNA-induced silencing of GFP mRNA. In plant tissues where silencing is already established, it is unable to prevent silencing signals from spreading locally and restoring GFP expression. Therefore, p25 has no ostensible effects on the accumulation of siRNAs (Kataya et al. 2009).

CCYV p22 protein as a VSR

To combat antiviral RNA silencing, a putative suppressor protein p22 binds with CsSKP1LB, a Cucumis sativus ortholog of S-phase kinase-associated protein 1 (SKP1). It is reported that the F-box-like motif in this protein is most crucial for p22-mediated viral pathogenicity and VSR activity (Chen et al. 2019). CCYV p22 suppresses antiviral RNA silencing at a local level and does not affect local or systemic movement of RNA silencing signals. Moreover, it is comparatively weaker in suppressing local RNA silencing than ToCV p22 and CYSDV p25, the two well-known VSRs of criniviruses (Orfanidou et al. 2019).

LCV p23 protein as a VSR

LCV employs p23 as a sophisticated tool for evasion of host antiviral defense and modulation of disease symptoms. It has been demonstrated that p23 suppresses initiation of local silencing and enhances degradation as well as inhibits accumulation of siRNAs in infiltrated leaves. This protein may also inhibit cell-to-cell and long-distance movement of RNA silencing signals in GFP-transgenic N. benthamiana (line 16c). At an elevated incubation temperature, p23-agroinfiltrated N. benthamiana leaves exhibit localized necrosis and an increased disease severity (within 5 dpi). This is a novelty about the direct temperature effect on VSR, which has been given to p23 of LCV and has never before been reported in other viruses (Kubota and Ng 2016).

SPCSV RNase3 and p22 as VSRs

SPCSV genomic RNA demonstrates variability in gene contents at 3′ proximal ORFs. Therefore, molecular analysis shows heterogeneity at the p22- and RNase3-encoding regions of various SPCSV isolates. The Ugandan SPCSV isolate encodes p22 and RNase3 proteins, which are involved in RNA silencing suppression. RNase3 displays endonuclease activity and cleaves siRNA into ~ 14 nt products, enhancing VSR activity of p22. Furthermore, RNase3 expression alone in sweet potato plants is enough for breaking plant resistance to sweet potato feathery mottle virus (SPFMV) and developing this viral disease (Cuellar et al. 2008).

ToCV p22, CP, and CPm as VSRs

The bipartite genomic RNAs of ToCV encode multiple VSRs with diverse functions to compromise host antiviral defense. Upon heterologous expression, CP and CPm induce obvious systemic symptoms in N. benthamiana, including leaf curling, necrotic mottling, and leaf deformation within 5 dpi (Canizares et al. 2008). Meanwhile, p22 is a strong VSR that preferentially binds to long dsRNAs via a putative zinc finger motif, preventing them from being diced into siRNAs (Landeo-Rios et al. 2016b). By using a ToCV infectious clone based on ToCV-BJ isolate, a consistent expression of p22 was detected in N. benthamiana leaves (Zhao et al. 2013, 2016). Furthermore, p22 interferes with the auxin signaling pathway through binding to SKP1.1 via its C-terminus and disrupting SCF complex formation by competing with transport inhibitor response 1 (TIR1) to promote viral infection (Liu et al. 2021). RdRps play a significant role in antiviral defense, and the RDR6 of N. benthamiana is also involved in defense via combatting ToCV. In rdr6 mutant, p22 is dispensable for ToCV replication, while during systemic infection, p22 counteracts RDR6-mediated antiviral response (Landeo-Rios et al. 2016a). However, the heterologous expression of p22 causes an exacerbation of disease symptoms and ultimately the death of whole plants, although it could not complement suppressor-defective mutant viruses (Landeo-Rios et al. 2017).

TICV-p27 as a VSR

The ORF2 of TICV-RNA1 encodes p27, with a genomic location similar to other criniviruses. It has been reported that p27 can suppress a sense transgene-induced PTGS (S-PTGS) and an inverted repeat-induced PTGS (IR-PTGS) without inhibiting local and systemic movement of RNA silencing signals. Furthermore, upon heterologous expression, p27 induces more severe mosaic and necrosis symptoms with the accumulation of a heterologous virus (Mashiko et al. 2019).

Plant strategies to counter viral suppression of RNA silencing

Plants have evolved counter-suppression pathways to combat viral infection in response to VSR-mediated RNA silencing suppression. Primarily, upon recognizing invading viruses, the plant immune system upregulates the expression of resistance R genes (NBS-LRR), triggering host defensive components (i.e., R proteins, monitor or guard) to guard antiviral RNA silencing response (Shao et al. 2019). In addition to regulating immune system, plants may target VSRs directly to counter the RNA silencing suppression mechanism. For instance, the interaction of the TuMV suppressor protein VPg with SGS3 and RDR6 activates a versatile cellular mechanism in host plants, facilitating the degradation of the RDR6-SGS3-VPg complex through autophagy pathways and ubiquitination to boost host antiviral RNA silencing (Cheng and Wang 2017). Similarly, the calmodulin-like protein in tobacco (rgs-CaM) binds to VSRs, including 2b of CMV and tomato aspermy virus (TAV) and HC-Pro of TuMV, to inhibit RNA silencing suppression through autophagy-mediated degradation of these VSRs (Nakahara et al. 2012). Plants may also trigger antiviral immune responses via regulating the components of RNA silencing pathway, such as dsRNAs. DsRNAs are conserved molecular patterns produced during virus replication and can induce PTI signaling pathway in plants. This dsRNA-mediated antiviral PTI, which requires pattern-recognition co-receptor SERK1 rather than DCLs, elicits antiviral protection independent of RNA silencing. However, the underlying mechanism of the corresponding signaling pathway is still a matter of consideration (Niehl et al. 2016; Niehl and Heinlein 2019). Hence, plant antiviral RNA silencing, viral suppression of RNA silencing, and plant counter-suppression may result in an endless battle of survival between viruses and plants.

Conclusions and future perspectives

It is now evident that antiviral RNA silencing, together with its rudimentary role in antiviral defense, establishes a fundamental regulatory hub in plant immunity to counter large numbers of viral pathogens. However, antiviral RNA silencing pathways should evolve continuously and rapidly due to diverse silencing suppression strategies of VSR. Mostly, viral suppressors hinder RNA silencing pathways by targeting essential elements of siRNAs and miRNAs or proteins like DCLs and AGOs. The interconnections between VSRs and host factors have demonstrated that a single viral suppressor can target several elements in a silencing pathway. For example, potyvirus HC-Pro may interfere with the miRNA pathway via sequestering siRNA biogenesis, downregulating AGO1 expression, and preventing 3′ end methylation of siRNA (Azad et al. 2014; Pollari et al. 2020). Similarly, closterovirid p22 may also compromise the silencing pathway in several ways, including dsRNA binding, counteracting RDR6-mediated antiviral response, accelerating disease symptoms, and ultimately causing plant death upon heterologous expression (Landeo-Rios et al. 2016b) (Fig. 2). Even though investigations into the mechanism of VSR have been on the frontline for more than a decade, many aspects are still indefinable. Interestingly, several VSRs, such as CP, movement protein, protease, and replicase, have analogous functions. Therefore, silencing activities and non-silencing functions should be coordinated to accomplish various tasks and attain optimal infection.

The structure-based interaction mechanism of VSRs is still elusive, although the precise adopted RNA binding octameric ring structure of closterovirid p21 and specific dimeric structured p19-siRNA duplex interaction have revealed various open challenges to investigate structure-based interaction mechanisms of other VSRs (Ye and Patel 2005). In addition, VSRs are supposed to be major contributors to viral disease induction and symptom development due to their negative effects on endogenous small RNA accumulations (Diaz-Pendon et al. 2007). Regardless of the paramount importance of VSRs in counteracting PTGS, their symptom induction is a less-studied aspect of the virus infection process. Furthermore, the direct temperature impact on VSR in modulation of disease symptoms needs more investigations. So far, only p23 of LCV was reported to evade host antiviral defense at elevated temperature (Kubota and Ng 2016).

The molecular characteristics of VSRs are much more complex than we thought. Indeed, the p38 protein of TCV, in addition to dsRNA binding, specifically interferes with the biogenesis of primary vsiRNA through downregulation of DCL4 (Azevedo et al. 2010). Similarly, the p19 protein of CymRSV confiscates vsiRNA through binding with 21–25 nt dsRNA and upregulating miR168 expression, resulting in arrests of antiviral AGO1 translation (Silhavy et al. 2002; Varallyay et al. 2010). Some other VSRs may interact with RNA silencing pathways in multiple ways, which need further investigations.

There are still a lot of lapses in knowledge about plant effectors regarding their silencing mechanisms and mi/siRNA RISC assemblies or some components of plant RISCs, which are potential targets of VSRs. Therefore, VSRs like p38, P1, and P0 may be used as a powerful tool to explore the RISC complexes in future research.

Plant resistant (R) proteins have evolved to recognize strategies of VSRs against RNA silencing. Therefore, the identity of such dedicated proteins, specifically in guarding the RNA silencing components among the plethora of plant R proteins, is an important future question. Presumably, hosts can also neutralize VSRs through appropriate defensive activities that degrade or displace them into inappropriate subcellular compartments. The former probably has explained that the alleles of CMV-encoded VSR 2b protein fail to accumulate in Arabidopsis because of proteolysis, while nuclear re-localization of tombusviral p19 is caused by its interaction with plant ALY protein (Canto et al. 2006; Zhang et al. 2006). These observations of host-directed suppression mechanisms of VSRs and their polymorphic alleles may propose a future direction to study the variations in viral vulnerability between species or subspecies.

Availability of data and materials

Not applicable.

Abbreviations

ADK:: Adenosine kinase
AGO:: Argonaute
BCTV:: Beet curly top virus
BMV:: Brome mosaic virus
BSCTV:: Beet severe curly top virus
BYSV:: Beet yellow stunt virus
BYV:: Beet yellow virus
CaLCuV:: Cabbage leaf curl virus
CaM:: Calmodulin
CaMV:: Cauliflower mosaic virus
CCYV:: Cucurbit chlorotic yellow virus
CLCuMuV:: Cotton leaf curl multan virus
CMV:: Cucumber mosaic virus
CTV:: Citrus tristeza virus
CymRSV:: Cymbidium ringspot virus
CYSDV:: Cucurbit yellow stunting disorder virus
DCL:: Dicer like
DRB4:: Double-RNA binding protein 4
ER:: Endoplasmic reticulum
ETI:: Effector-triggered immunity
GBNV:: Groundnut bud necrosis virus
GLRaV-3:: Grapevine leafroll-associated virus 3
HC-Pro:: Helper component-proteinase
HEN1:: HUA enhancer 1
HSP70h:: Heat-shock proteins HSP70 homology
HR:: Hypersensitive responses
ICTV:: International Committee on Taxonomy of Viruses
IR-PTGS:: Inverted repeat-induced PTGS
LCV:: Lettuce chlorosis virus
miRNAs:: MicroRNAs
MVBaV:: Mint vein banding-associated virus
PAMPs:: Pathogen-associated molecular patterns
PlAMV:: Plantago asiatica mosaic potexvirus
PMWaV-1:: Pineapple mealybug wilt-associated virus 1
PMWaV-2:: Pineapple mealybug wilt-associated virus-2
Pol II:: Polymerase II
PoLV:: Pothos latent virus
pri-miRNAs:: Primary miRNAs
PRSV:: Papaya ringspot virus
PTGS:: Post-transcriptional gene silencing
PTI:: PAMP-triggered immunity
PVX:: Potato virus X
RdRp:: RNA-dependent RNA polymerase
RDR:: Cellular RdRps
RGDV:: Rice gall dwarf virus
RHBV:: Rice hoja blanca virus
RISC:: RNA-induced silencing complex
RLMV:: Raspberry leaf mottle virus
RLRaV:: Rose leaf rossette-associated virus
RSV:: Rice strip virus
RYSV:: Rice yellow stunt rhabdovirus
SAHH:: S-adenosyl homocysteine hydrolase
SAMS:: S-adenosyl methionine synthetase
SAR:: Systemic acquired resistance
siRNAs:: Small interfering RNAs
SKP1:: S-phase kinase associated protein 1
SMD:: Silencing movement deficient
SPCSV:: Sweet potato chlorotic stunt virus
SPFMV:: Sweet potato feathery mottle virus
SPMMV:: Sweet potato mild mottle virus
S-PTGS:: Sense-transgene-induced PTGS
TBSV:: Tomato bushy stunt virus
TCV:: Turnip crinkle virus
TEV:: Tobacco etch virus
TGMV:: Tomato golden mosaic virus
TGS:: Transcriptional gene silencing
TICV:: Tomato infectious chlorosis virus
TIR1:: Transport inhibitor response 1
ToCV:: Tomato chlorosis virus
ToRSV:: Tomato ringspot virus
TrAP:: Transcriptional activator protein
TRV:: Tobacco rattle virus
TSWV:: Tomato spotted wilt virus
TuMV:: Turnip mosaic virus
TYLCCNV:: Tomato yellow leaf curl China virus
UPS:: Ubiquitin proteasome system
VAMP:: Virus-associated molecular pattern
vsiRNAs:: Virus-derived small interfering RNAs
VSR:: Viral suppressor of RNA silencing
WDV:: Wheat dwarf virus
ZYMV:: Zucchini yellow mosaic virus

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Acknowledgements

We would like to express our gratitude and appreciation to Prof. Zaifeng Fan for his valuable suggestions on this manuscript. Please accept our heartfelt apologies to colleagues whose work could not be discussed due to space limitations.

Funding

This work was supported by Beijing Innovation Consortium of Agriculture Research System (Grant Number: BAIC01-2018–2021), the Chinese Universities Scientific Fund (2019TC064), and China Scholarship Council (Award Number: 2017GXZ004561).

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State Key Laboratory for Agro-Biotechnology, and Ministry of Agriculture and Rural Affairs, Key Laboratory for Pest Monitoring and Green Management, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China
Muhammad Dilshad Hussain, Xi Chen, Tong Jiang, Sijia Liu & Tao Zhou
Plant Protection Research Institute and Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China
Tahir Farooq
Department of Plant Pathology, and Ministry of Agriculture and Rural Affairs Key Laboratory of Pest Monitoring and Green Management, and Ministry of Education Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, 100193, China
Muhammad Tariqjaveed

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Muhammad Dilshad Hussain
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Xi Chen
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Tong Jiang
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MDH and TZ conceived the idea and wrote the manuscript. MDH, TF and XC designed and made the Figures and Tables. MT, TJ, TF, SL, and TZ edited and revised the manuscript. All authors read and approved the final manuscript.

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Hussain, M.D., Farooq, T., Chen, X. et al. Viral suppressors from members of the family Closteroviridae combating antiviral RNA silencing: a tale of a sophisticated arms race in host-pathogen interactions. Phytopathol Res 3, 27 (2021). https://doi.org/10.1186/s42483-021-00104-y

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Received: 07 July 2021
Accepted: 04 November 2021
Published: 15 November 2021
DOI: https://doi.org/10.1186/s42483-021-00104-y

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

Abstract

Background

Antiviral RNA silencing and plant immunity

The mechanism and localization of antiviral RNA silencing

Viral strategies to evade antiviral RNA silencing

Meddling with methylation cycle and suppressing TGS

Binding with dsRNA and cleaving vsiRNA

Interfering with RDR and DCL4

Binding with HEN and sequestrating vsiRNA

Degrading AGOs and interfering with RISC assembly

Interacting with miRNA and upregulating pre-miRNA

Meddling with the amplification of antiviral RNA silencing

Inhibiting the spread of antiviral RNA silencing

Viral proteins of closterovirids to counteract antiviral RNA silencing

GLRaV-2 p24 protein as a VSR

GLRaV-3 p19.7 protein as a VSR

PMWaV-1 p61 protein as a VSR

PMWaV-2 p20 and CP proteins as VSRs

BYV p21 protein as a VSR

CTV CP, p20, and p23 proteins as VSRs

RLRaV p17 protein as a VSR

CYSDV p25 protein as a VSR

CCYV p22 protein as a VSR

LCV p23 protein as a VSR

SPCSV RNase3 and p22 as VSRs

ToCV p22, CP, and CPm as VSRs

TICV-p27 as a VSR

Plant strategies to counter viral suppression of RNA silencing

Conclusions and future perspectives

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Phytopathology Research