The Characterization of the Tobacco-Derived Wild Tomato Mosaic Virus by Employing Its Infectious DNA Clone

SIMPLE SUMMARY: Wild tomato mosaic virus (WTMV, genus Potyvirus, family Potyviridae) is an emerging viral pathogen that endangers Nicotiana tabacum production. The field survey conducted in this study shows that WTMV is becoming an epidemic in China. An infectious DNA clone of the tobacco-derived WTMV is constructed. It can infect wild eggplant, black nightshade, and tobacco plants but can not infect various local pepper varieties. WTMV evolves into three groups that coincide with their original hosts, tobacco, pepper, or wild eggplant. Thus, the tobacco-derived WTMV might divergently evolves to adapt to tobacco other than peppers. We show that WTMV is compatible with the coinfection of cucumber mosaic virus (CMV) or tobacco mosaic virus (TMV) in tobacco but not other potyviruses. Specifically, WTMV can interfere with the infection of other potyvirus species in tobacco, a phenomenon known as superinfection exclusion previously observed within the same potyviral species. This study contributes essential knowledge on the evolution, infectivity, and recent epidemics of WTMV, and provides the key tool for further disease-resistance and field management studies. ABSTRACT: Viral diseases of cultivated crops are often caused by virus spillover from wild plants. Tobacco (N. tabacum) is an important economic crop grown globally. The viral pathogens of tobacco are traditional major subjects in virology studies and key considerations in tobacco breeding practices. A positive-strand RNA virus, wild tomato mosaic virus (WTMV), belonging to the genus potyvirus in the family potyviridae was recently found to infect tobacco in China. In this study, diseased tobacco leaf samples were collected in the Henan Province of China during 2020–2021. Several samples from different locations were identified as WTMV positive. An infectious DNA clone was constructed based on one of the WTMV isolates. By using this clone, we found that WTMV from tobacco could establish infections on natural reservoir hosts, demonstrating a possible route of WTMV spillover and overwintering in the tobacco field. Furthermore, the WTMV infection was found to be accompanied by other tobacco viruses in the field. The co-inoculation experiments indicate the superinfection exclusion (SIE) between WTMV and other potyvirus species that infect tobacco. Overall, our work reveals novel aspects of WTMV evolution and infection in tobacco and provides an important tool for further studies of WTMV.