Plant Viral Synergism: Co-expression of P1 and NIaPro Cistrons of Wheat Streak Mosaic Virus and Triticum Mosaic Virus Is Required for Synergistic Interaction in Wheat

Synergistic interactions among unrelated viruses in mixed infections can cause significant yield losses, and viral determinants of these interactions are poorly understood. Wheat (<i>Triticum aestivum</i> 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.