The Plant Virus Tomato Spotted Wilt Orthotospovirus Benefits Its Vector Frankliniella occidentalis by Decreasing Plant Toxic Alkaloids in Host Plant Datura stramonium

The transmission of insect-borne viruses involves sophisticated interactions between viruses, host plants, and vectors. Chemical compounds play an important role in these interactions. Several studies reported that the plant virus tomato spotted wilt orthotospovirus (TSWV) increases host plant quality for its vector and benefits the vector thrips Frankliniella occidentalis. However, few studies have investigated the chemical ecology of thrips vectors, TSWV, and host plants. Here, we demonstrated that in TSWV-infected host plant Datura stramonium, (1) F. occidentalis were more attracted to feeding on TSWV-infected D. stramonium; (2) atropine and scopolamine, the main tropane alkaloids in D. stramonium, which are toxic to animals, were down-regulated by TSWV infection of the plant; and (3) F. occidentalis had better biological performance (prolonged adult longevity and increased fecundity, resulting in accelerated population growth) on TSWV-infected D. stramonium than on TSWV non-infected plants. These findings provide in-depth information about the physiological mechanisms responsible for the virus’s benefits to its vector by virus infection of plant regulating alkaloid accumulation in the plant.