Impacts of coingesting two tomato-infecting begomoviruses on virus infection in Bemisia tabaci and vector transmission

Abstract

In agricultural fields where many viruses are prevalent, plants are commonly coinfected with multiple viruses. Whiteflies, vectors of plant viruses, can acquire two viruses by probing on two infected plants sequentially or on a coinfected plant. Although the coingestion of two viruses by a common vector is supposed to influence vector transmission and virus epidemiology, these effects still require more comprehensive research. In this study, we investigated the impact of coingesting two begomoviruses on virus infection in Bemisia tabaci Middle East–Asia Minor 1 (MEAM1). Whiteflies underwent two successive acquisition access periods through feeding on plants infected with tomato leaf curl Taiwan virus (ToLCTV), tomato yellow leaf curl Thailand virus (TYLCTHV), or both. The amounts of virus in the midgut, hemolymph, primary salivary glands (PSGs), and saliva of the whiteflies were determined through quantitative real-time polymerase chain reaction. Transmission assays were conducted to evaluate the impact of coingesting ToLCTV and TYLCTHV on the whitefly-mediated transmission of both viruses. Our results revealed that the preingestion of TYLCTHV was antagonistic to the infection of ToLCTV in the whitefly midgut. Regardless of the ingestion sequence, the amounts of TYLCTHV in the midgut, hemolymph, PSGs, and saliva of whitefly, as well as its transmission rate, were higher than those of ToLCTV. This study provides valuable insights into the intricate interactions between two tomato begomoviruses (ToLCTV and TYLCTHV) within B. tabaci and improves our understanding of the complex tripartite interplay involving virus–virus–vector relationships and the implications for plant virus transmission.