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Impact of Wheat Streak Mosaic Virus on Peroxisome Proliferation, Redox Reactions, and Resistance Responses in Wheat.

ABSTRACT: Although peroxisomes play an essential role in viral pathogenesis, and viruses are known to change peroxisome morphology, the role of genotype in the peroxisomal response to viruses remains poorly understood. Here, we analyzed the impact of wheat streak mosaic virus (WSMV) on the peroxisome proliferation in the context of pathogen response, redox homeostasis, and yield in two wheat cultivars, Patras and Pamir, in the field trials. We observed greater virus content and yield losses in Pamir than in Patras. Leaf chlorophyll and protein content measured at the beginning of flowering were also more sensitive to WSMV infection in Pamir. Patras responded to the WSMV infection by transcriptional up-regulation of the peroxisome fission genes PEROXIN 11C (PEX11C), DYNAMIN RELATED PROTEIN 5B (DRP5B), and FISSION1A (FIS1A), greater peroxisome abundance, and activation of pathogenesis-related proteins chitinase, and β-1,3-glucanase. Oppositely, in Pamir, WMSV infection suppressed transcription of peroxisome biogenesis genes and activity of chitinase and β-1,3-glucanase, and did not affect peroxisome abundance. Activity of ROS scavenging enzymes was higher in Patras than in Pamir. Thus, the impact of WMSV on peroxisome proliferation is genotype-specific and peroxisome abundance can be used as a proxy for the magnitude of plant immune response.

SUBMITTER: Mishchenko L

PROVIDER: S-EPMC8508189 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Impact of Wheat Streak Mosaic Virus on Peroxisome Proliferation, Redox Reactions, and Resistance Responses in Wheat.

Mishchenko Lidiya L Nazarov Taras T Dunich Alina A Mishchenko Ivan I Ryshchakova Olga O Motsnyi Ivan I Dashchenko Anna A Bezkrovna Lidiya L Fanin Yaroslav Y Molodchenkova Olga O Smertenko Andrei A

International journal of molecular sciences 20210923 19

Although peroxisomes play an essential role in viral pathogenesis, and viruses are known to change peroxisome morphology, the role of genotype in the peroxisomal response to viruses remains poorly understood. Here, we analyzed the impact of wheat streak mosaic virus (WSMV) on the peroxisome proliferation in the context of pathogen response, redox homeostasis, and yield in two wheat cultivars, Patras and Pamir, in the field trials. We observed greater virus content and yield losses in Pamir than ...[more]

PMID: 34638559

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Project description:BackgroundWheat streak mosaic virus (WSMV) and Triticum mosaic virus (TriMV) are components of the wheat streak mosaic virus disease complex in the Great Plains region of the U.S.A. and elsewhere. Co-infection of wheat with WSMV and TriMV causes synergistic interaction with more severe disease symptoms compared to single infections. Plants are equipped with multiple antiviral mechanisms, of which regulation of microRNAs (miRNAs) is a potentially effective constituent. In this investigation, we have analyzed the total and relative expression of miRNA transcriptome in two wheat cultivars, Arapahoe (susceptible) and Mace (temperature-sensitive-resistant), that were mock-inoculated or inoculated with WSMV, TriMV, or both at 18 °C and 27 °C.ResultsOur results showed that the most abundant miRNA family among all the treatments was miRNA166, followed by 159a and 168a, although the order of the latter two changed depending on the infections. When comparing infected and control groups, twenty miRNAs showed significant upregulation, while eight miRNAs were significantly downregulated. Among them, miRNAs 9670-3p, 397-5p, and 5384-3p exhibited the most significant upregulation, whereas miRNAs 319, 9773, and 9774 were the most downregulated. The comparison of infection versus the control group for the cultivar Mace showed temperature-dependent regulation of these miRNAs. The principal component analysis confirmed that less abundant miRNAs among differentially expressed miRNAs were strongly correlated with the inoculated symptomatic wheat cultivars. Notably, miRNAs 397-5p, 398, and 9670-3p were upregulated in response to WSMV and TriMV infections, an observation not yet reported in this context. The significant upregulation of these three miRNAs was further confirmed with RT-qPCR analysis; in general, the RT-qPCR results were in agreement with our computational analysis. Target prediction analysis showed that the miRNAs standing out in our analysis targeted genes involved in defense response and regulation of transcription.ConclusionInvestigation into the roles of these miRNAs and their corresponding targets holds promise for advancing our understanding of the mechanisms of virus infection and possible manipulation of these factors for developing durable virus resistance in crop plants.

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.

Project description:BackgroundThe September 11, 2001 attacks on the World Trade Center and the Pentagon increased the concern about the potential for terrorist attacks on many vulnerable sectors of the US, including agriculture. The concentrated nature of crops, easily obtainable biological agents, and highly detrimental impacts make agroterrorism a potential threat. Although procedures for an effective criminal investigation and attribution following such an attack are available, important enhancements are still needed, one of which is the capability for fine discrimination among pathogen strains. The purpose of this study was to develop a molecular typing assay for use in a forensic investigation, using Wheat streak mosaic virus (WSMV) as a model plant virus.MethodThis genotyping technique utilizes single base primer extension to generate a genetic fingerprint. Fifteen single nucleotide polymorphisms (SNPs) within the coat protein and helper component-protease genes were selected as the genetic markers for this assay. Assay optimization and sensitivity testing was conducted using synthetic targets. WSMV strains and field isolates were collected from regions around the world and used to evaluate the assay for discrimination. The assay specificity was tested against a panel of near-neighbors consisting of genetic and environmental near-neighbors.ResultEach WSMV strain or field isolate tested produced a unique SNP fingerprint, with the exception of three isolates collected within the same geographic location that produced indistinguishable fingerprints. The results were consistent among replicates, demonstrating the reproducibility of the assay. No SNP fingerprints were generated from organisms included in the near-neighbor panel, suggesting the assay is specific for WSMV. Using synthetic targets, a complete profile could be generated from as low as 7.15 fmoles of cDNA.ConclusionThe molecular typing method presented is one tool that could be incorporated into the forensic science tool box after a thorough validation study. This method incorporates molecular biology techniques that are already well established in research and diagnostic laboratories, allowing for an easy introduction of this method into existing laboratories.Keywordssingle nucleotide polymorphisms, genotyping, plant pathology, viruses, microbial forensics, Single base primer extension, SNaPshot Multiplex Kit.

Project description:Variation within the Type and Sidney 81 strains of wheat streak mosaic virus was assessed by single-strand conformation polymorphism (SSCP) analysis and confirmed by nucleotide sequencing. Limiting-dilution subisolates (LDSIs) of each strain were evaluated for polymorphism in the P1, P3, NIa, and CP cistrons. Different SSCP patterns among LDSIs of a strain were associated with single-nucleotide substitutions. Sidney 81 LDSI-S10 was used as founding inoculum to establish three lineages each in wheat, corn, and barley. The P1, HC-Pro, P3, CI, NIa, NIb, and CP cistrons of LDSI-S10 and each lineage at passages 1, 3, 6, and 9 were evaluated for polymorphism. By passage 9, each lineage differed in consensus sequence from LDSI-S10. The majority of substitutions occurred within NIa and CP, although at least one change occurred in each cistron except HC-Pro and P3. Most consensus sequence changes among lineages were independent, with substitutions accumulating over time. However, LDSI-S10 bore a variant nucleotide (G(6016)) in NIa that was restored to A(6016) in eight of nine lineages by passage 6. This near-global reversion is most easily explained by selection. Examination of nonconsensus variation revealed a pool of unique substitutions (singletons) that remained constant in frequency during passage, regardless of the host species examined. These results suggest that mutations arising by viral polymerase error are generated at a constant rate but that most newly generated mutants are sequestered in virions and do not serve as replication templates. Thus, a substantial fraction of variation generated is static and has yet to be tested for relative fitness. In contrast, nonsingleton variation increased upon passage, suggesting that some mutants do serve as replication templates and may become established in a population. Replicated mutants may or may not rise to prominence to become the consensus sequence in a lineage, with the fate of any particular mutant subject to selection and stochastic processes such as genetic drift and population growth factors.

Dataset Information

Impact of Wheat Streak Mosaic Virus on Peroxisome Proliferation, Redox Reactions, and Resistance Responses in Wheat.

Publications

Impact of Wheat Streak Mosaic Virus on Peroxisome Proliferation, Redox Reactions, and Resistance Responses in Wheat.

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