Interference with phytohormone signaling by whiteflies differentially affects plant attractiveness to a larval and an egg parasitoid of the cabbage white butterfly

In response to egg deposition or feeding by insect herbivores, plants release specific blends of volatiles that attract natural enemies of the herbivores. In nature, plants are often simultaneously attacked by multiple herbivores that may induce different signaling pathways, thus affecting the volatile blends and interfering with the attraction of natural enemies. The mechanisms underlying such interference remain largely unknown. Here, we show that co-infestation of Arabidopsis thaliana plants with the whitefly Bemisia tabaci reduces the volatile emissions induced by Pieris rapae caterpillars, resulting in reduced attraction of the larval parasitoid Cotesia rubecula. Hormone and gene expression analyses, followed by assays with various Arabidopsis mutants, revealed that this interference by B. tabaci is the result of antagonistic crosstalk between jasmonic acid and salicylic acid, involving the transcription factor NPR1 but not WRKY70. In contrast, B. tabaci co-infestation had no impact on the attraction of an egg parasitoid to egg-induced volatiles of P. rapae. These differential effects of the whitefly on the behavior of the two parasitoids were confirmed in greenhouse assays. This study provides new insight into the molecular mechanisms underlying the recruitment of different parasitoids by plants and could help in developing effective biocontrol strategies.