Asymmetry in synergistic interaction between wheat streak mosaic virus and triticum mosaic virus in wheat

Authors: Tatineni, Satyanarayana - Ts; Alexander, Jeffrey; GUPTA, ADARSH - University Of Nebraska; French, Roy

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/10/2018
Publication Date: 8/14/2018
Citation: Tatineni, S., Alexander, J.A., Gupta, A.K., French, R.C. 2018. Asymmetry in synergistic interaction between wheat streak mosaic virus and triticum mosaic virus in wheat. Molecular Plant-Microbe Interactions. [Online Journal] Available:https://apsjournals.apsnet.org/doi/10.1094/MPMI-07-18-0189-R

Interpretive Summary: Wheat streak mosaic virus (WSMV) and Triticum mosaic virus (TriMV) are economically important viruses infecting wheat in the Great Plains region of the USA. WSMV and TriMV interact synergistically in co-infected wheat with dramatically increased disease severity and yield loss with elevated accumulation of both viruses. Since both these viruses are transmitted by wheat curl mites, double infections in field-grown wheat are common, resulting in disease synergism. Understanding the underlying mechanisms of synergistic interaction between WSMV and TriMV would facilitate developing strategies to minimize losses from disease synergism. This study revealed that WSMV benefited from prior infection of wheat by TriMV during early stages of systemic infection while prior infection of wheat by WSMV negatively affected TriMV systemic infection. However, both viruses benefited from each other during late stages of synergistic interaction with acute symptom phenotype and increased accumulation of both interacting viruses. This study suggests that interactions between WSMV- and TriMV-encoded proteins result in disease synergism and disruption of these interactions most likely prevent synergistic interactions between these viruses.

Technical Abstract: Wheat streak mosaic virus (WSMV) and Triticum mosaic virus (TriMV), distinct members in the family Potyviridae, are economically important wheat-infecting viruses in the Great Plains region. Previously, we reported that co-infection of wheat by WSMV and TriMV cause disease synergism with increased concentration of both viruses. The mechanisms of synergistic interaction between WSMV and TriMV and the effects of prior infection of wheat by either of these ‘synergistically interacting partner’ (SIP) viruses on the establishment of local and systemic infection by the other SIP virus are not known. In this study, using fluorescent protein-tagged viruses, we found that prior infection of wheat by WSMV or TriMV negatively affected the onset and size of local foci elicited by subsequent SIP virus infection compared to those in buffer-inoculated wheat. These data revealed that prior infection of wheat by a SIP virus has no measurable advantage for another SIP virus on the initiation of infection and cell-to-cell movement. In TriMV-infected wheat, WSMV exhibited accelerated long-distance movement and increased accumulation of genomic RNAs compared to those in buffer-inoculated wheat, indicating that TriMV-encoded proteins complemented WSMV for efficient systemic infection. In contrast, TriMV displayed delayed systemic infection in WSMV-infected wheat with fewer genomic RNA copies in early stages of infection compared to those in buffer-inoculated wheat. However, during late stages of infection, TriMV accumulation in WSMV-infected wheat increased rapidly with accelerated long-distance movement compared to those in buffer-inoculated wheat. Taken together, these data suggest that successful establishment of synergistic interaction between unrelated viruses depends on the order of infection of plants by SIP viruses.