Airborne host–plant manipulation by whiteflies via an inducible blend of plant volatiles

Significance Plants respond to herbivory and pathogenic infection with the synthesis of various defense compounds, including volatile compounds that are emitted into the environment. These volatiles can be perceived by neighboring plants and “prime” them for an attack by the specific attacker. We found that whitefly-infested tomato plants release volatiles that prime a defense against pathogens in neighboring plants, which goes at the cost of defenses against insect herbivores, making the neighboring plants more suitable for whitefly development. This apparent ability of whiteflies to manipulate plant defense responses through induced volatile emissions could explain the rapid spread of this invasive pest, and a good understanding of the mechanisms that are involved may lead to novel pest control strategies.
The whitefly Bemisia tabaci is one of the world’s most important invasive crop pests, possibly because it manipulates plant defense signaling. Upon infestation by whiteflies, plants mobilize salicylic acid (SA)-dependent defenses, which mainly target pathogens. In contrast, jasmonic acid (JA)-dependent defenses are gradually suppressed in whitefly-infested plants. The down-regulation of JA defenses make plants more susceptible to insects, including whiteflies. Here, we report that this host–plant manipulation extends to neighboring plants via airborne signals. Plants respond to insect attack with the release of a blend of inducible volatiles. Perception of these volatiles by neighboring plants usually primes them to prepare for an imminent attack. Here, however, we show that whitefly-induced tomato plant volatiles prime SA-dependent defenses and suppress JA-dependent defenses, thus rendering neighboring tomato plants more susceptible to whiteflies. Experiments with volatiles from caterpillar-damaged and pathogen-infected plants, as well as with synthetic volatiles, confirm that whiteflies modify the quality of neighboring plants for their offspring via whitefly-inducible plant volatiles.