Differential synergistic interactions among four different wheat-infecting viruses

Authors: Tatineni, Satyanarayana - Ts; Alexander, Jeffrey; QU, FENG - The Ohio State University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/6/2021
Publication Date: 1/13/2022
Citation: Tatineni, S., Alexander, J.A., Qu, F. 2022. Differential synergistic interactions among four different wheat-infecting viruses. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2021.800318.
DOI: https://doi.org/10.3389/fmicb.2021.800318

Interpretive Summary: Several viruses have been reported to infect wheat, and more than one virus can infect the wheat plants in growers’ fields at the same time. Wheat streak mosaic virus (WSMV) is one of the most economically important viruses on wheat in the Great Plains region. WSMV can co-infect wheat with multiple viruses such as Triticum mosaic virus (TriMV), brome mosaic virus (BMV), and barley stripe mosaic virus (BSMV). These four wheat-infecting viruses are genetically distinct from each other. Plants co-infected by unrelated viruses can induce disease synergism with exacerbated yield loss. This study examined the effect of co-infection of wheat by two, three, or all four of these viruses on disease development and virus levels compared to wheat infected by individual viruses. Wheat co-infected by BMV and BSMV elicited mild to moderate synergism with a drastic reduced BSMV levels. Co-infection of wheat by WSMV or TriMV in combination with BMV or BSMV elicited moderate synergistic disease with little or no change in virus levels. Wheat co-infected by WSMV, TriMV, and BMV or BSMV elicited enhanced disease synergism with differential effects on levels of interacting viruses. Wheat infected by all four viruses elicited very severe synergistic disease resulting in the death of most plants. This study revealed synergistic interactions among WSMV, TriMV, BMV, and BSMV in co-infected wheat resulted in enhanced disease symptoms with the increased number of viruses.

Technical Abstract: Field-grown wheat plants can be co-infected by multiple viruses, including wheat streak mosaic virus (WSMV), Triticum mosaic virus (TriMV), brome mosaic virus (BMV), and barley stripe mosaic virus (BSMV). These viruses belong to four different genera in three different families and are, hence, genetically divergent. However, the impact of potential co-infections with two, three, or all four of them on the viruses themselves, as well as the wheat host, has yet to be examined. This study examined bi-, tri-, and quadripartite interactions among these viruses in wheat for disease development and accumulation of viral genomic RNAs, in comparison with single virus infections. Co-infection with BMV and BSMV resulted in generally mild symptoms with occasional side shoot deformation, but caused a drastic reduction in BSMV titer, suggesting an antagonism-like effect exerted by BMV toward BSMV. However, co-infection of either BMV or BSMV with WSMV or TriMV led to moderately more severe diseases than singly infected wheat, but with a decrease or no significant change in the titers of interacting viruses in the presence of BMV or BSMV, respectively. These results were in stark contrast with exacerbated disease phenotype accompanied with enhanced virus titers caused by WSMV and TriMV co-infection. Co-infections with WSMV, TriMV, and BMV or BSMV resulted in enhanced synergistic disease accompanied with increased accumulation of TriMV and BMV but not WSMV or BSMV. Quadripartite interactions in co-infected wheat by all four viruses resulted in very severe disease synergism, leading to the death of most infected plants, but paradoxically, a drastic reduction in BSMV titer. Our results indicate that interactions among different viruses infecting the same plant host are more complex than previously thought, do not always entail increases in virus titers, and likely involve multiple mechanisms. These findings lay the foundation for additional mechanistic dissections of synergistic interactions among unrelated plant viruses.Field-grown wheat plants can be co-infected by multiple viruses, including wheat streak mosaic virus (WSMV), Triticum mosaic virus (TriMV), brome mosaic virus (BMV), and barley stripe mosaic virus (BSMV). These viruses belong to four different genera in three different families and are, hence, genetically divergent. However, the impact of potential co-infections with two, three, or all four of them on the viruses themselves, as well as the wheat host, has yet to be examined. This study examined bi-, tri-, and quadripartite interactions among these viruses in wheat for disease development and accumulation of viral genomic RNAs, in comparison with single virus infections. Co-infection with BMV and BSMV resulted in generally mild symptoms with occasional side shoot deformation, but caused a drastic reduction in BSMV titer, suggesting an antagonism-like effect exerted by BMV toward BSMV. However, co-infection of either BMV or BSMV with WSMV or TriMV led to moderately more severe diseases than singly infected wheat, but with a decrease or no significant change in the titers of interacting viruses in the presence of BMV or BSMV, respectively. These results were in stark contrast with exacerbated disease phenotype accompanied with enhanced virus titers caused by WSMV and TriMV co-infection. Co-infections with WSMV, TriMV, and BMV or BSMV resulted in enhanced synergistic disease accompanied with increased accumulation of TriMV and BMV but not WSMV or BSMV. Quadripartite interactions in co-infected wheat by all four viruses resulted in very severe disease synergism, leading to the death of most infected plants, but paradoxically, a drastic reduction in BSMV titer. Our results indicate that interactions among different viruses infecting the same plant host are more complex than previously thought, do not always entail increases in virus tit