Antagonistic Plant Defense System Regulated by Phytohormones Assists Interactions Among Vector Insect, Thrips and a Tospovirus

The western flower thrips (Frankliniella occidentalis) is a polyphagous herbivore that causes serious damage to many agricultural plants. In addition to causing feeding damage, it is also a vector insect that transmits tospoviruses such as Tomato spotted wilt virus (TSWV). We previously reported that thrips feeding on plants induces a jasmonate (JA)-regulated plant defense, which negatively affects both the performance and preference (i.e. host plant attractiveness) of the thrips. The antagonistic interaction between a JA-regulated plant defense and a salicylic acid (SA)-regulated plant defense is well known. Here we report that TSWV infection allows thrips to feed heavily and multiply on Arabidopsis plants. TSWV infection elevated SA contents and induced SA-regulated gene expression in the plants. On the other hand, TSWV infection decreased the level of JA-regulated gene expression induced by thrips feeding. Importantly, we also demonstrated that thrips significantly preferred TSWV-infected plants to uninfected plants. In JA-insensitive coi1-1 mutants, however, thrips did not show a preference for TSWV-infected plants. In addition, SA application to wild-type plants increased their attractiveness to thrips. Our results suggest the following mechanism: TSWV infection suppresses the anti-herbivore response in plants and attracts its vector, thrips, to virus-infected plants by exploiting the antagonistic SA-JA plant defense systems.