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

Abstract

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.

Herbivore exploits orally secreted bacteria to suppress plant defenses

“…For example, Tomato spotted wilt virus vectored by western flower thrips (Frankliniella occidentalis) decreased JA-regulated defenses through induction of the SA-signaling pathway, benefitting the insect vector (36). Phytoplasmas secreted the protein SAP11 to down-regulate lipoxygenase and inhibit JA biosynthesis, which increases survival and fecundity of the leafhopper vector and phytoplasma transmission (37).…”

Intervention of Phytohormone Pathways by Pathogen Effectors

“…TSWV induces increased SA levels and SAmediated defenses, leading to a suppression of JA-mediated defenses. Consequently, WFT prefer feeding on TSWV-infected plants because the JA pathway provides resistance to WFT ( Figure 5) (Abe et al, 2012). However, in contrast to the previously discussed P6 effector of cauliflower mosaic virus, which may modulate SA-JA antagonism via NPR1, the mechanism involved in TSWV-mediated modulation of this phenomenon is currently unknown.…”

Plants, viruses and the environment: Ecology and mutualism

“…Thrip-damaged Arabidopsis plants produce jasmonic acid (JA), which is involved in the plants' resistance to thrips and probably explains why juveniles are negatively impacted. TSWV-infected plants produce salicylic acid (SA), which counteracts the JA response, and makes plants a better host of thrips (Abe et al, 2012). The positive response of insects on virus-infected plants can extend to other insects as well.…”