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Binding between elongation factor 1A and the 3'-UTR of Chinese wheat mosaic virus is crucial for virus infection.

ABSTRACT: The Chinese wheat mosaic virus (CWMV) genome consists of two positive-strand RNAs that are required for CWMV replication and translation. The eukaryotic translation elongation factor (eEF1A) is crucial for the elongation of protein translation in eukaryotes. Here, we show that silencing eEF1A expression in Nicotiana benthamiana plants by performing virus-induced gene silencing can greatly reduce the accumulation of CWMV genomic RNAs, whereas overexpression of eEF1A in plants increases the accumulation of CWMV genomic RNAs. In vivo and in vitro assays showed that eEF1A does not interact with CWMV RNA-dependent RNA polymerase. Electrophoretic mobility shift assays revealed that eEF1A can specifically bind to the 3'-untranslated region (UTR) of CWMV genomic RNAs. By performing mutational analyses, we determined that the conserved region in the 3'-UTR of CWMV genomic RNAs is necessary for CWMV replication and translation, and that the sixth stem-loop (SL-6) in the 3'-UTR of CWMV genomic RNAs plays a key role in CWMV infection. We conclude that eEF1A is an essential host factor for CWMV infection. This finding should help us to develop new strategies for managing CWMV infections in host plants.

SUBMITTER: Chen X

PROVIDER: S-EPMC8518580 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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Binding between elongation factor 1A and the 3'-UTR of Chinese wheat mosaic virus is crucial for virus infection.

Chen Xuan X He Long L Xu Miaoze M Yang Jin J Li Juan J Zhang Tianye T Liao Qiansheng Q Zhang Hengmu H Yang Jian J Chen Jianping J

Molecular plant pathology 20210817 11

The Chinese wheat mosaic virus (CWMV) genome consists of two positive-strand RNAs that are required for CWMV replication and translation. The eukaryotic translation elongation factor (eEF1A) is crucial for the elongation of protein translation in eukaryotes. Here, we show that silencing eEF1A expression in Nicotiana benthamiana plants by performing virus-induced gene silencing can greatly reduce the accumulation of CWMV genomic RNAs, whereas overexpression of eEF1A in plants increases the accumu ...[more]

PMID: 34405507

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Project description:Wheat streak mosaic virus (WSMV) and Triticum mosaic virus (TriMV) are important viral pathogens of wheat in the Great Plains. These viruses individually or in mixed infections with High Plains wheat mosaic virus cause a devastating wheat streak mosaic (WSM) disease. Although seed transmission of WSMV has been studied, no information is currently available on that of TriMV. Furthermore, no study has explored the implications of mixed infections of WSMV and TriMV on seed transmission of one or both viruses. To study both aspects, seeds from differentially resistant field-grown wheat plants (cv. TAM 304 (susceptible), Joe (WSMV resistant, Wsm2 gene), and Breakthrough (BT) (WSMV and TriMV resistant, Wsm1 gene)) showing characteristic WSM symptoms were collected and analyzed to quantify both viruses using qRT-PCR. The percentage of seeds tested positive for WSMV or TriMV individually and in mixed infection varied with cultivar and virus combinations; 13% of TAM 304 seeds tested positive for WSMV, followed by 8% of BT and 4% of Joe seeds. Similarly, TriMV was detected in 12% of BT seeds, followed by 11% of TAM 304 and 8% of Joe seeds. Lastly, mixed infection was detected in 7% of TAM 304 seeds, followed by 4% in BT, and 2% in Joe. Dissection of field-collected seeds into three parts, embryo, endosperm, and seed coat, revealed both WSMV and TriMV accumulated only in the seed coat. Consistent with seeds, percent infection of WSMV or TriMV in the plants that emerged from infected seeds in each treatment varied with cultivar and virus combinations (WSMV: BT 3%; Joe 2%; TAM 304 9%; TriMV: BT 7%; Joe 8%; and TAM 304 10%). Plants infected with mixed viruses showed more pronounced WSM symptoms compared to individual infections. However, both viruses were present only in a few plants (BT: 2%, Joe: 1%, and TAM 304: 4%). Taken together, this study showed that TriMV was transmitted vertically at a higher frequency than WSMV in resistant cultivars, and the seed transmission of TriMV with WSMV increased the virulence of both pathogens (measured via WSM symptom severity) in the emerged plants. Furthermore, Wsm1 and Wsm2 genes considerably reduced WSMV transmission via infected seeds. However, no such effects were observed on TriMV, especially in progeny plants. These results reiterated the importance of planting clean seeds and highlighted the immediate need to identify/develop new sources of TriMV resistance to effectively manage the recurring WSM epidemic.

Project description:Wheat streak mosaic virus (WSMV; Tritimovirus tritici) and Triticum mosaic virus (TriMV; Poacevirus tritici), the type members of the genera Tritimovirus and Poacevirus, respectively, in the family Potyviridae, are economically important wheat viruses in the Great Plains region of the USA. Co-infection of wheat by WSMV and TriMV results in disease synergism. Wheat transcriptome from singly (WSMV or TriMV) and doubly (WSMV+TriMV) infected upper uninoculated leaves were analyzed by RNA-Seq at 9, 12, and 21 days postinoculation. A total of 31,754 differentially expressed wheat genes were identified among all comparisons. Weighted gene co-expression network analysis resulted in 11 co-expression modules that broadly indicated gene expression profiles attributable to control, single, and double infections. Gene ontology, protein domain and KEGG (Kyoto Encyclopedia of Genes and Genomes) pathway enrichment analysis revealed that genes specifically related to photosynthesis, growth, stress, senescence, and defense were differentially enriched. Analyses of transcription factor families indicated that genes encoding MADS-Box and ARFs were strongly enriched in control plants, moderately repressed in TriMV-infected plants, and more strongly repressed in WSMV- and doubly-infected plants, whereas genes encoding WRKYs and NACs were more enriched in WSMV or doubly infected plants. Synergistic interactions between WSMV and TriMV drastically enhanced disease phenotype compared to individual virus infections. The progression of disease phenotype was correlated to transcriptomic changes, indicating the strong disruption to plant metabolism and likely channeling of energy and metabolites for viral replication. There also appeared to be a connection between viral replication and plastid health, with stronger downregulation of genes needed for chloroplast functions and integrity and increased synergism between TriMV and WSMV. This study provides an overview of transcriptomic changes distinctly influenced by TriMV and WSMV either singly or in combination and provides a good correlation between specific transcription factors and genes associated with metabolism to observed phenotypic changes in plant growth and disease synergism.

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Binding between elongation factor 1A and the 3'-UTR of Chinese wheat mosaic virus is crucial for virus infection.

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Binding between elongation factor 1A and the 3'-UTR of Chinese wheat mosaic virus is crucial for virus infection.

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