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Effects and role(s) of the noncoding subgenomic RNA of red clover necrotic mosaic virus in virus infection

ABSTRACT: In recent years, a new class of viral noncoding subgenomic (ncsg)RNA has been identified that is generated as a stable degradation product formed via an exonuclease-resistant (xr) RNA structure that blocks the progression of 5’-3’ exonuclease that degrades viral RNAs in infected cells. The xrRNA-derived ncsgRNAs have been implicated in virus pathogenicity, virus movement and transmission, and suppressing antiviral defense responses. Although ncsgRNAs of animal viruses have been studied extensively, research on the role of xrRNA-derived plant viral ncsgRNAs remain scarce. In this study, we assess the effects of the ncsgRNA of red clover necrotic mosaic virus (RCNMV), called SR1f, in infected plants. We demonstrate that the presence of SR1f leads to severe symptoms and increased viral RNA accumulation in Nicotiana benthamiana and Arabidopsis thaliana. We also provide evidence that suppression of RNA silencing is not the primary function of SR1f. Additionally, a comparative transcriptomic analysis in N. benthamiana infected with wildtype RCNMV and an SR1f-deficient mutant RCNMV reveal that wt RCNMV infection that produces SR1f has a greater and significant impact on cellular gene expression resulting in deregulation of several cellular pathways with upregulation of genes mainly involved in plant hormone signaling, plant-pathogen interaction, MAPK signaling, and several metabolic pathways and downregulation of genes involved mainly in photosynthesis.

ORGANISM(S): Nicotiana benthamiana

PROVIDER: GSE178909 | GEO | 2021/06/26

REPOSITORIES: GEO

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Project description:Many virus diseases of economic importance to agriculture result from mixtures of different pathogens invading the host at a given time. This contrasts with the relatively scarce studies available on the molecular events associated with virus-host interactions in mixed infections. In comparison to single infections, co-infection of Nicotiana benthamiana with Potato virus X (PVX) and Potato virus Y (PVY) resulted in increased systemic symptoms (synergism) that led to necrosis of the newly emerging leaves, and the plant death. A comparative transcriptional analysis was undertaken to identify quantitative and qualitative differences in gene expression during this synergistic infection, and to correlate these changes with the severe symptoms it caused. Global transcription profiles of doubly-infected leaves were compared with those from singly-infected leaves using gene ontology enrichment analysis and metabolic pathway annotator software. Functional gene categories altered by the double infection comprise suites of genes regulated coordinately, which are associated with chloroplast functions (down-regulated), protein synthesis and degradation (up-regulated), carbohydrate metabolism (up-regulated), and response to biotic stimulus and stress (up-regulated). The expression of reactive oxygen species-generating enzymes as well as several mitogen-activated protein kinases, were also significantly induced. Accordingly, synergistic infection induced a severe oxidative stress in N. benthamiana leaves, as judged by increases in lipid peroxidation, and by the generation of superoxide radicals in chloroplasts, which correlated with the misregulation of antioxidative genes in microarray data. Interestingly, expression of genes encoding oxylipin biosynthesis was uniquely up-regulated by the synergistic infection. Virus-induced gene silencing of alfa-dioxygenase1 delayed cell death during PVX-PVY infection. Using mock inoculated leaf tissue as a reference, we compare the gene expression profiles of Nicotiana benthamiana plants infected with one of two viruses, Potato virus X (PVX) or Potato virus Y (PVY), or the combination PVX plus PVY. 3 biological replicates per treatment were independently grown and haversted.

Project description:Hypersensitive response-related programmed cell death (PCD) has been extensively analyzed in various plant–virus interactions. However, little is known about changes in gene expression associated with cell death caused by compatible viruses. The synergistic interaction of Potato virus X (PVX) with Plum pox virus (PPV) results in increased symptoms that lead to systemic necrosis (SN) in Nicotiana benthamiana. Here, we performed three transcriptome comparisons in response to i) a PVX recombinant virus expressing the helper component-proteinase (HC-Pro) gene from PPV that leads to SN, ii) a systemic incompatible interaction conferred by the Tobacco mosaic virus (TMV)-resistance gene N (SHR), and iii) the depletion of the PBE subunit of the proteasome that leads to PCD by virus induced gene silencing (VIGS Prot), at early and late stages of infection. Our analysis indicated that the SN response was clustered with SHR by the similarity of their overall gene expression profiles. However, the expression profiles of defence-related and hormone-responsive genes in response to SN were more closely related to the response to VIGS Prot than to that elicited by SHR. This suggests the potential contribution of proteasome dysfunction to the increase in pathogenicity observed in PVX-potyvirus infections We compare the gene expression profiles of Nicotiana benthamiana plants infected with either necrosis-inducing viruses or non-necrosis-inducing viruses, as follow: PVX/HCWT-infected plants versus plants infected with a PVX recombinant virus expressing a PPV HC-Pro mutant (PVX/HCLH) that was unable to induce the SN response (SN comparison), at 7 and 11 days postinoculation (dpi), (ii) TRV:NbPBE-silenced plants versus plants infected with the TRV empty vector (VIGS Prot comparison), at 4 and 8 days after infiltration (dpa), and (iii) TMV-GFP-infected, N-transgenic plants versus wild-type plants infected with TMV-GFP (SHR comparison), at 24 and 72 hours after temperature shift (hts). Per time and treatment, three independent biological replicates were used to monitor differences in gene expression between treatments

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Effects and role(s) of the noncoding subgenomic RNA of red clover necrotic mosaic virus in virus infection

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