Tracing the Lineage of Two Traits Associated with the Coat Protein of the Tombusviridae: Silencing Suppression and HR Elicitation in Nicotiana Species

Adhab, Mustafa; Ángel, Carlos Ariel; Rodriguez, Andres; Fereidouni, Mohammad; Király, Lóránt; Scheets, Kay; Schoelz, James E.

doi:10.3390/v11070588

Cited by 10 publications

(9 citation statements)

References 68 publications

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“…RNA silencing is a well-established defence response in plantvirus infection (Gaffar & Koch, 2019). In our study, TNVA-siRNA accumulated in the inoculated leaves but did not appear to spread ( Adhab et al, 2019). In this regard, two olive mild mosaic virus (OMMV) proteins (CP and p6) were identified as suppressors of RNAi silencing (Varanda et al, 2018).…”

Section: Discussionmentioning

confidence: 57%

“…In our study, TNVA‐siRNA accumulated in the inoculated leaves but did not appear to spread systemically, suggesting the suppression of antiviral silencing amplification by TNVA. Recent evidence points out the possibility that tombusvirus CPs act as suppressors of RNAi silencing in Nicotiana species (Adhab et al, 2019). In this regard, two olive mild mosaic virus (OMMV) proteins (CP and p6) were identified as suppressors of RNAi silencing (Varanda et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

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Tobacco necrosis virus A overcomes local cell death response in Nicotiana tabacum

et al. 2022

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Plant viruses are categorized as biotrophic pathogens and should not cause death of the infected tissue in a susceptible host. A successful viral infection (compatible interaction) depends on the ability of the virus to take advantage of host factors for its own life cycle and to cope with the antiviral plant defence responses (host susceptibility) either inhibiting biogenesis of viral small interfering RNAs (vsiRNAs)

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Section: Discussionmentioning

confidence: 57%

Section: Discussionmentioning

confidence: 99%

Tobacco necrosis virus A overcomes local cell death response in Nicotiana tabacum

et al. 2022

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“…This result was not unexpected since plants elicit a reactive oxygen species (ROS) burst as an antiviral defense response, and yet RCNMV requires ROS production for efficient replication ( 56 ). It is possible that in wt RCNMV infection, viral RNA and proteins accumulate to a sufficient level to elicit a strong defense response, especially coat protein-mediated HR response ( 57 ), and the virus hijacks one of those defense responses (ROS) to accelerate viral replication. This can be seen as high levels of RNA1 accumulation in wt RCNMV infection compared to RNA1-m1 in RCNMVΔSR1f infection in which the host does not elicit a strong defense or ROS response.…”

Section: Resultsmentioning

confidence: 99%

Effects of the Noncoding Subgenomic RNA of Red Clover Necrotic Mosaic Virus in Virus Infection

Kanodia

Miller

2022

J Virol

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In recent years, a new class of viral noncoding subgenomic (ncsg)RNA has been identified. This RNA is generated as a stable degradation product via an exoribonuclease-resistant (xr) RNA structure, which blocks the progression of 5’→3’ exoribonuclease on viral RNAs in infected cells. Here, we assess the effects of the ncsgRNA of red clover necrotic mosaic virus (RCNMV), called SR1f, in infected plants. We demonstrate: (i) absence of SR1f reduces symptoms and decreases viral RNA accumulation in Nicotiana benthamiana and Arabidopsis thaliana plants; (ii) SR1f has an essential function other than suppression of RNA silencing; and (iii) the cytoplasmic exoribonuclease involved in mRNA turnover, XRN4, is not required for SR1f production or virus infection. A comparative transcriptomic analysis in N. benthamiana infected with wildtype RCNMV or an SR1f-deficient mutant RCNMV revealed that wt RCNMV infection, which produces SR1f and much higher levels of virus, has a greater and more significant impact on cellular gene expression than the SR1f-deficient mutant. Upregulated pathways include plant hormone signaling, plant-pathogen interaction, MAPK signaling, and several metabolic pathways, while photosynthesis-related genes were downregulated. We compare this to host genes known to participate in infection by other tombusvirids. Viral reads revealed a 10 to 100-fold ratio of positive to negative strand, and the abundance of reads of both strands mapping to the 3’ region of RCNMV RNA1 support the premature mechanism of synthesis for the coding sgRNA. These results provide a framework for future studies of the interactions and functions of noncoding RNAs of plant viruses. IMPORTANCE Knowledge of how RNA viruses manipulate host and viral gene expression is crucial to our understanding of infection and disease. Unlike viral protein-host interactions, little is known about the control of gene expression by viral RNA. Here we begin to address this question by investigating the noncoding subgenomic (ncsg)RNA of red clover necrotic mosaic virus (RCNMV), called SR1f. Similar exoribonuclease-resistant RNAs of flaviviruses are well-studied, but the roles of plant viral ncsgRNAs, and how they arise, are poorly understood. Surprisingly, we find the likely exonuclease candidate, XRN4, is not required to generate SR1f, and we assess the effects of SR1f on virus accumulation and symptom development. Finally, we compare the effects of infection by wildtype RCNMV vs an SR1f-deficient mutant on host gene expression in Nicotiana benthamiana , which reveals that ncsgRNAs such as SR1f are key players in virus-host interactions to facilitate productive infection.

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“…Interestingly, a more recent study of phylogeny of the CP of tombusviruses indicated that CP representatives of the family could be divided into four clades. All tested CP members in two separate clades triggered an HR in Nicotiana section Alatae species [ 35 ]. Moreover, a previous study had shown that several members of Nicotiana section Alatae carry functional N′ orthologues [ 34 ] and implied that N′ and N′ orthologues might have been inherited from a common ancestor followed by evolution to confer tobamovirus and tombusvirus resistance to Nicotiana genus species.…”

Section: Coat Proteins (Cp)mentioning

confidence: 99%

“…Recent studies tracing HR induction lineages and silencing suppression associated with the CPs of the Tombusviridae also support the conclusion that SSR and HR elicitation involve independent motifs. Among the four clades in the phylogenetic tree of 54 CPs tombusvirids, two separate CP clades triggered an HR in Nicotiana species of section Alatae but did not have silencing suppressor activity, whereas in one clade the CP functioned as an SSR, but lost the capacity to trigger HR in Nicotiana species [ 35 ].…”

Section: Rna Silencing Suppressors (Rss)mentioning

confidence: 99%

From Player to Pawn: Viral Avirulence Factors Involved in Plant Immunity

Huang

2021

Viruses

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In the plant immune system, according to the ‘gene-for-gene’ model, a resistance (R) gene product in the plant specifically surveils a corresponding effector protein functioning as an avirulence (Avr) gene product. This system differs from other plant–pathogen interaction systems, in which plant R genes recognize a single type of gene or gene family because almost all virus genes with distinct structures and functions can also interact with R genes as Avr determinants. Thus, research conducted on viral Avr-R systems can provide a novel understanding of Avr and R gene product interactions and identify mechanisms that enable rapid co-evolution of plants and phytopathogens. In this review, we intend to provide a brief overview of virus-encoded proteins and their roles in triggering plant resistance, and we also summarize current progress in understanding plant resistance against virus Avr genes. Moreover, we present applications of Avr gene-mediated phenotyping in R gene identification and screening of segregating populations during breeding processes.

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Tracing the Lineage of Two Traits Associated with the Coat Protein of the Tombusviridae: Silencing Suppression and HR Elicitation in Nicotiana Species

Cited by 10 publications

References 68 publications

Tobacco necrosis virus A overcomes local cell death response in Nicotiana tabacum

Tobacco necrosis virus A overcomes local cell death response in Nicotiana tabacum

Effects of the Noncoding Subgenomic RNA of Red Clover Necrotic Mosaic Virus in Virus Infection

From Player to Pawn: Viral Avirulence Factors Involved in Plant Immunity

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