In response to herbivore damage, several plant species emit volatiles that attract natural predators of the attacking herbivores. Using spider mites (Tetranychus urticae) and predatory mites (Phytoseiulus persimilis), it has been shown that not only the attacked plant but also neighbouring plants are affected, becoming more attractive to predatory mites and less susceptible to spider mites. The mechanism involved in such interactions, however, remains elusive. Here we show that uninfested lima bean leaves activate five separate defence genes when exposed to volatiles from conspecific leaves infested with T. urticae, but not when exposed to volatiles from artificially wounded leaves. The expression pattern of these genes is similar to that produced by exposure to jasmonic acid. At least three terpenoids in the volatiles are responsible for this gene activation; they are released in response to herbivory but not artificial wounding. Expression of these genes requires calcium influx and protein phosphorylation/dephosphorylation.

We compared volatiles from lima bean leaves (Phaseolus lunatus) infested by either beet armyworm (Spodoptera exigua), common armyworm [Mythimna (Pseudaletia) separata], or two-spotted spider mite (Tetranychus urticae). We also analyzed volatiles from the leaves treated with jasmonic acid (JA) and/or methyl salicylate (MeSA). The volatiles induced by aqueous JA treatment were qualitatively and quantitatively similar to those induced by S. exigua or M. separata damage. Furthermore, both S. exigua and aqueous JA treatment induced the expression of the same basic PR genes. In contrast, gaseous MeSA treatment, and aqueous JA treatment followed by gaseous MeSA treatment, induced volatiles that was qualitatively and quantitatively more similar to the T. urticae-induced volatiles than those induced by aqueous JA treatment. In addition, T. urticae damage resulted in the expression of the acidic and basic PR genes that were induced by gaseous MeSA treatment and by aqueous JA treatment, respectively. Based on these data, we suggest that in lima bean leaves, the JA-related signaling pathway is involved in the production of caterpillar-induced volatiles, while both the SA-related signaling pathway and the JA-related signaling pathway are involved in the production of T. urticae-induced volatiles.

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.

Background: The western flower thrips (Frankliniella occidentalis [Pergande]) is one of the most important insect herbivores of cultivated plants. However, no pesticide provides complete control of this species, and insecticide resistance has emerged around the world. We previously reported the important role of jasmonate (JA) in the plant's immediate response to thrips feeding by using an Arabidopsis leaf disc system. In this study, as the first step toward practical use of JA in thrips control, we analyzed the effect of JA-regulated Arabidopsis defense at the whole plant level on thrips behavior and life cycle at the population level over an extended period. We also studied the effectiveness of JA-regulated plant defense on thrips damage in Chinese cabbage (Brassica rapa subsp. pekinensis).