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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. [ABSTRACT FROM AUTHOR]

Synergistic interactions among unrelated viruses in mixed infections can cause significant yield losses, and viral determinants of these interactions are poorly understood. Wheat ( Triticum aestivum L.) co-infection with wheat curl mite-transmitted wheat streak mosaic virus (WSMV) and Triticum mosaic virus (TriMV) results in disease synergism with a drastically increased symptom phenotype of stunted growth, leaf bleaching, and enhanced titers of both viruses compared with individual virus infections. In this study, we examined the viral determinants responsible for WSMV-TriMV disease synergism through transient expression of select cistrons of WSMV in wheat through TriMV and vice-versa. We found that expression of WSMV P1, NIa, or NIaPro in wheat through TriMV or vice-versa elicited moderate to severe symptoms with a moderate or no increase in virus titer. However, co-expression of P1 and NIaPro of WSMV in wheat through TriMV or vice-versa exhibited a WSMV-TriMV disease synergism-like phenotype with enhanced accumulation of genomic RNA copies and coat protein. Additionally, we found that the P3 of both viruses is dispensable for synergism. HCPro and NIaVPg of WSMV and TriMV are not the primary determinants but might have a minor role in efficient synergism. In co-infected wheat, the accumulation of virus-specific small interfering RNAs (vsiRNAs) was increased, similar to viral genomic RNA copies, despite the presence of two viral RNA-silencing suppressors (VRSS), which function through sequestration of vsiRNAs. Our findings revealed that WSMV-TriMV disease synergism is not caused by the suppression of host posttranscriptional gene silencing by two VRSS proteins in co-infected wheat, and the P1 and NIaPro of both viruses collectively drive synergistic interactions between WSMV and TriMV in wheat. [Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2025., Competing Interests: The author(s) declare no conflict of interest.