Viruses that cause tomato yellow leaf curl disease are part of a group of viruses of the genus Begomovirus, family Geminiviridae. Tomato-infecting begomoviruses cause epidemics in tomato crops in tropical, subtropical, and Mediterranean climates, and they are exclusively transmitted by Bemisia tabaci in the field. The objective of the present study was to examine the transmission biology of the tomato yellow leaf curl Thailand virus (TYLCTHV) by B. tabaci, including virus-infected tissues, virus translocation, virus replication, and transovarial transmission. The results demonstrated that the virus translocates from the alimentary gut to the salivary glands via the hemolymph, without apparent replication when acquired by B. tabaci. Furthermore, the virus was detected in 10% of the first-generation progeny of viruliferous females, but the progeny was unable to cause the viral infection of host plants. There was no evidence of transovarial transmission of TYLCTHV in B. tabaci. When combined with the current literature, our results suggest that B. tabaci transmits TYLCTHV in a persistent-circulative mode. The present study enhances our understanding of virus–vector interaction and the transmission biology of TYLCTHV in B. tabaci.

Tomato yellow leaf curl disease poses one of the most severe threats to tomato production worldwide. This disease is associated with a group of closely related tomato yellow leaf curl viruses. These viruses can be transmitted by the sweet potato whitefly (Bemisia tabaci) in a persistent-circulative mode. Virus particles can infect the midgut and filter chamber of whiteflies feeding on infected plants, circulate in the hemolymph, and eventually infect the primary salivary gland (PSG) of whiteflies. Later, the whiteflies feed on healthy plants, and viral particles are introduced into the plants through their saliva. Virus–vector interactions play a crucial role in the efficiency and dynamics of virus transmission. In this study, we assessed the effects of the acquisition time and viral load of source plants on infections of two tomato begomoviruses, tomato yellow leaf curl Thailand virus (TYLCTHV) and tomato leaf curl Taiwan virus (ToLCTV), in B. tabaci Middle East–Asia Minor 1. We found that more viruses were acquired and accumulated in the whitefly midgut and PSG before reaching a plateau when the acquisition time increased and when the source plant had a higher viral load. The midgut and PSG acquired and accumulated more TYLCTHV than ToLCTV with the same acquisition time and regardless of the viral loads in coinfected source plants. These results not only help us to understand virus–vector interactions but also help in developing integrated disease management strategies.

Tomato yellow leaf curl disease, caused by a group of closely related tomato yellow leaf curl viruses, is a major threat to tomato cultivation worldwide. These viruses are primarily transmitted by the sweet potato whitefly (Bemisia tabaci) in a persistent-circulative manner, wherein the virus circulates in the body of B. tabaci and infects its tissues. The complex relationship between viruses and whiteflies significantly influences virus transmission, with studies showing varying effects of the former on the life history and feeding preference of the latter. Whether these effects are direct or indirect, and whether they are negative, neutral, or positive, appears to depend on the specific interactions between virus and whitefly species. The tomato yellow leaf curl Thailand virus (TYLCTHV) and the tomato leaf curl Taiwan virus (ToLCTV) are two prevalent begomoviruses in fields in Taiwan. This study examined the direct and indirect effects of TYLCTHV and ToLCTV on the life history traits (longevity, fecundity, nymph survival, and nymph developmental time) and feeding preference of B. tabaci Middle East–Asia Minor 1 (MEAM1). The results revealed that TYLCTHV had no effects on these life history traits or the feeding preference of MEAM1 whiteflies. Although ToLCTV did not directly affect the longevity and fecundity of MEAM1 whiteflies, their fecundity and the nymph developmental time were negatively affected by feeding on ToLCTV-infected plants. In addition, ToLCTV infection also altered the feeding preference of MEAM1 whiteflies. The different effects of virus infection may contribute to the lower prevalence of ToLCTV compared to TYLCTHV in fields in Taiwan.