• Vacuolar (H⁺)-PPases (VPs), are key regulators of active proton (H⁺) transport across membranes using the energy generated from PPi hydrolysis. The VPs also play vital roles in plant responses to ...various abiotic stresses. Their functions in plant responses to pathogen infections are unknown.
• Here, we show that TaVP, a VP of wheat (Triticum aestivum) is important for wheat resistance to Chinese wheat mosaic virus (CWMV) infection. Furthermore, overexpression of TaVP in plants induces the activity of PPi hydrolysis, leading to plants cell death.
• A virus-derived small interfering RNA (vsiRNA-20) generated from CWMV RNA1 can regulate the mRNA accumulation of TaVP in wheat. The accumulation of vsiRNA-20 can suppress cell death induced by TaVP in a dosage-dependent manner. Moreover, we show that the accumulation of vsiRNA-20 can affect PPi hydrolysis and the concentration of H⁺ in CWMV-infected wheat cells to create a more favorable cellular environment for CWMV replication.
• We propose that vsiRNA-20 regulates TaVP expression to prevent cell death and to maintain a weak alkaline environment in cytoplasm to enhance CWMV infection in wheat. This finding may be used as a novel strategy to minimize virus pathogenicity and to develop new antiviral stratagems.
Virus-derived siRNAs (vsiRNAs) generated by the host RNA silencing mechanism are effectors of plant's defense response and act by targeting the viral RNA and DNA in post-transcriptional gene ...silencing (PTGS) and transcriptional gene silencing (TGS) pathways, respectively. Contrarily, viral suppressors of RNA silencing (VSRs) compromise the host RNA silencing pathways and also cause disease-associated symptoms. In this backdrop, reports describing the modulation of plant gene(s) expression by vsiRNAs via sequence complementarity between viral small RNAs (sRNAs) and host mRNAs have emerged. In some cases, silencing of host mRNAs by vsiRNAs has been implicated to cause characteristic symptoms of the viral diseases. Similarly, viroid infection results in generation of sRNAs, originating from viroid genomic RNAs, that potentially target host mRNAs causing typical disease-associated symptoms. Pathogen-derived sRNAs have been demonstrated to have the propensity to target wide range of genes including host defense-related genes, genes involved in flowering and reproductive pathways. Recent evidence indicates that vsiRNAs inhibit host RNA silencing to promote viral infection by acting as decoy sRNAs. Nevertheless, it remains unclear if the silencing of host transcripts by viral genome-derived sRNAs are inadvertent effects due to fortuitous pairing between vsiRNA and host mRNA or the result of genuine counter-defense strategy employed by viruses to enhance its survival inside the plant cell. In this review, we analyze the instances of such cross reaction between pathogen-derived vsiRNAs and host mRNAs and discuss the molecular insights regarding the process of pathogenesis.
The major components of RNA silencing include both transitive and systemic small RNAs, which are technically called secondary sRNAs. Double-stranded RNAs trigger systemic silencing pathways to ...negatively regulate gene expression. The secondary siRNAs generated as a result of transitive silencing also play a substantial role in gene silencing especially in antiviral defense. In this review, we first describe the discovery and pathways of transitivity with emphasis on RNA-dependent RNA polymerases followed by description on the short range and systemic spread of silencing. We also provide an in-depth view on the various size classes of secondary siRNAs and their different roles in RNA silencing including their categorization based on their biogenesis. The other regulatory roles of secondary siRNAs in transgene silencing, virus-induced gene silencing, transitivity, and
-species transfer have also been detailed. The possible implications and applications of systemic silencing and the different gene silencing tools developed are also described. The details on mobility and roles of secondary siRNAs derived from viral genome in plant defense against the respective viruses are presented. This entails the description of other compatible plant-virus interactions and the corresponding small RNAs that determine recovery from disease symptoms, exclusion of viruses from shoot meristems, and natural resistance. The last section presents an overview on the usefulness of RNA silencing for management of viral infections in crop plants.
Abstract
Antiviral RNAi is the main protective measure employed by plants in the fight against viruses. The main steps of this process have been clarified in recent years, primarily relying on the ...extensive genetic resources of Arabidopsis thaliana. Our knowledge of viral diseases of crops, however, is still limited, mainly due to the fact that A. thaliana is a non-host for many agriculturally important viruses. In contrast, Nicotiana benthamiana has an unparalleled susceptibility to viruses and, since it belongs to the Solanaceae family, it is considered an adequate system for modeling infectious diseases of crops such as tomatoes. We used a series of N. benthamiana mutants created by genome editing to analyze the RNAi response elicited by the emerging tomato pathogen, pepino mosaic virus (PepMV). We uncovered hierarchical roles of several Argonaute proteins (AGOs) in anti-PepMV defense, with the predominant contribution of AGO2. Interestingly, the anti-PepMV activities of AGO1A, AGO5, and AGO10 only become apparent when AGO2 is mutated. Taken together, our results prove that hierarchical actions of several AGOs are needed for the plant to build effective anti-PepMV resistance. The genetic resources created here will be valuable assets for analyzing RNAi responses triggered by other agriculturally important pathogenic viruses.
Hierarchical contribution of multiple Argonaute proteins is necessary for the plant to build effective anti-PepMV resistance.
While interferon (IFN) responses are critical for mammalian antiviral defense, induction of antiviral RNA interference (RNAi) is evident. To date, individual functions of the mammalian RNAi and micro ...RNA (miRNA) effector proteins Argonautes 1–4 (AGO1–AGO4) during virus infection remain undetermined. AGO2 was recently implicated in mammalian antiviral defense, so we examined antiviral activity of AGO1, AGO3, or AGO4 in IFN-competent immune cells. Only AGO4-deficient cells are hyper-susceptible to virus infection. AGO4 antiviral function is both IFN dependent and IFN independent, since AGO4 promotes IFN but also maintains antiviral capacity following prevention of IFN signaling or production. We identified AGO-loaded virus-derived short interfering RNAs (vsiRNAs), a molecular marker of antiviral RNAi, in macrophages infected with influenza or influenza lacking the IFN and RNAi suppressor NS1, which are uniquely diminished without AGO4. Importantly, AGO4-deficient influenza-infected mice have significantly higher burden and viral titers in vivo. Together, our data assign an essential role for AGO4 in mammalian antiviral defense.
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•Individual roles for the RNAi/miRNA effector proteins AGO1, AGO3, and AGO4 are elusive•AGO4 is uniquely antiviral in mammalian immune cells•Mammalian AGO4 has evolved to both elicit antiviral RNAi and boost IFN•AGO4 is indispensable for control of influenza in vivo
Functional specificities for the four mammalian RNAi/miRNA effector proteins AGO1–AGO4 remain enigmatic. Adiliaghdam et al. demonstrate a surprising and essential role for AGO4, but not AGO1 or AGO3, in the defense against multiple viral types in immune cells and in vivo.
Main conclusion
This review focuses on different factors involved in promoting symptom recovery in plants post-virus infection such as epigenetics, transcriptional reprogramming, phytohormones with ...an emphasis on RNA silencing as well as role of abiotic factors such as temperature on symptom recovery.
Plants utilize several different strategies to defend themselves in the battle against invading viruses. Most of the viral proteins interact with plant proteins and interfere with molecular dynamics in a cell which eventually results in symptom development. This initial symptom development is countered by the plant utilizing various factors including the plant’s adaptive immunity to develop a virus tolerant state. Infected plants can specifically target and impede the transcription of viral genes as well as degrade the viral transcripts to restrict their proliferation by the production of small-interfering RNA (siRNA) generated from the viral nucleic acid, known as virus-derived siRNA (vsiRNA). To further escalate the degradation of viral nucleic acid, secondary siRNAs are generated. The production of virus-activated siRNA (vasiRNA) from the host genome causes differential regulation of the host transcriptome which plays a major role in establishing a virus tolerant state within the infected plant. The systemic action of vsiRNAs, vasiRNA, and secondary siRNAs with the help of defense hormones like salicylic acid can curb viral proliferation, and thus the newly emerged leaves develop fewer symptoms, maintaining a state of tolerance.
Abstract
Virus-derived small interfering RNAs (vsiRNAs) in plants can target host transcripts to induce symptom development. Southern rice black-streaked dwarf virus (SRBSDV) is the most damaging ...rice-infecting virus, which causes severe stunting and poorly developed roots in rice plants, thereby posing a serious threat to rice production. In this study, we show that a vsiRNA (vsiR-S9-18), generated from SRBSDV genome segment 9, targets the transcription factor ROC1 in rice. SRBSDV infection triggered the production of vsiR-S9-18 and resulted in the downregulation of
ROC1
in rice plants. Transient expression of vsiR-S9-18 in rice protoplasts and tobacco leaves further demonstrated the specific association of vsiR-S9-18 with
ROC1
. Moreover, the
ROC1
-knockout rice plants displayed shortened roots, similar to the phenotype of root growth inhibition caused by SRBSDV infection. We propose that vsiR-S9-18 inhibits root elongation via
ROC1
, which has been proven to regulate root growth. This finding extends our understanding of the role of vsiRNA in viral disease development and is helpful for the development of new antiviral approaches.
Most arthropod-borne viruses produce intermittent epidemics in infected plants. However, the underlying mechanisms of these epidemics are unclear. Here, we demonstrated that rice stripe mosaic virus ...(RSMV), a viral pathogen, significantly increases the mortality of its overwintering vector, the leafhopper species
. Cold-stress assays indicated that RSMV reduces the cold tolerance of leafhoppers, a process associated with the downregulation of leafhopper cuticular protein genes. An RSMV-derived small RNA (vsiR-t00355379) was found to facilitate the downregulation of a leafhopper endocuticle gene that is mainly expressed in the abdomen (named RdABD-5) and is conserved across dipteran species. The downregulation of
expression in
resulted in fewer and thinner endocuticle lamellae, leading to decreased cold tolerance. This effect was correlated with a reduced incidence rate of RSMV in early-planted rice plants. These findings contribute to our understanding of the mechanism by which viral pathogens reduce cold tolerance in arthropod vectors and suggest an approach to managing the fluctuating prevalence of arboviruses.
Increasing arthropod vector dispersal rates have increased the susceptibility of crop to epidemic viral diseases. However, the incidence of some viral diseases fluctuates annually. In this study, we demonstrated that a rice virus reduces the cold tolerance of its leafhopper vector,
. This effect is linked to the virus-derived small RNA-mediated downregulation of a gene encoding a leafhopper abdominal endocuticle protein. Consequently, the altered structural composition of the abdominal endocuticle reduces the overwinter survival of leafhoppers, resulting in a lower incidence of RSMV infection in early-planted rice plants. Our findings illustrate the important roles of RNA interference in virus-vector insect-environment interactions and help explain the annual fluctuations of viral disease epidemics in rice fields.
•Virus/subvirus-derived small interfering RNAs (vsiRNAs) targeting host mRNAs and noncoding RNAs.•Virus-activated but host-derived siRNAs (vasiRNAs) regulating plant endogenous gene ...expression.•Inhibitory effect of miRNAs on viral/subviral RNAs (vRNAs).•siRNA-based interregulation between the viruses and their parasite satellite RNAs (satRNAs).
Host plants deploy the small RNA (sRNA)-directed RNA silencing pathway to resist invasion by acellular microorganisms (viruses/viroids/satellites), and, in turn, this pathway is exploited by pathogenic agents to create an environment conducive to infection. Previous known sRNA-RNA systems consist of host endogenous microRNAs (miRNAs) mediating the regulation of host mRNAs and virus/viroid/satellite-derived small interfering RNAs (vsiRNAs) targeting their genomic RNAs. However, more in-depth explorations have substantially expanded the understanding of the complexity of sRNA-RNA regulatory networks. Here, we review some recently discovered sRNA-mediated regulatory systems. Specifically, in addition to virus-encoded proteins acting as virulence factors, vsiRNAs can serve as important pathogenic determinants targeting host mRNAs and noncoding RNAs to promote virus/viroid/satellite infection and trigger symptoms that may be side effects of infection. Additionally, virus-activated but host-derived siRNAs (vasiRNAs) regulate endogenous plant gene expression related to virus resistance or pathogenicity. The inhibitory effect of miRNAs on plant endogenous mRNAs and viral RNAs (vRNAs) has also been identified. Furthermore, siRNA-based interregulation occurring between viruses and their parasite satellite RNAs (satRNAs) enables coexisting virus-satRNA-plant homoeostasis. Thus, the underlying mechanisms of plant–virus/viroid/satellite competition and symbiosis are largely obscured by these diverse sRNA-RNA combinations. Guided by the intricate regulatory network-based principle at the RNA level, practically applicable and feasible strategies have been developed for the management of plant viruses/viroids/satellites for which effective control measures are lacking.
Parasitoid wasp populations have developed persistent beneficial symbiotic relationships with several viruses through repeated evolution. However, there have been limited reports on RNA viruses in ...parasitoid wasps of tephritid flies, a significant pest group affecting fruits and vegetables. This study explores the diversity of RNA viruses in three parasitoid wasps of tephritid flies and highlights the potential biological significance of specific viruses in
. These findings have important implications for the development of sustainable pest management strategies and the enhancement of artificial rearing techniques for parasitoid wasps.
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