Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription

Summary 1. Plants face threats from a variety of herbivorous insects and can use induced responses to defend themselves against these attackers. Induced responses are mediated by signal transduction involving phytohormones, such as jasmonic acid (JA) and salicylic acid (SA). Cross-talk between signal transduction pathways triggered by attackers with contrasting feeding styles allows plants to fine-tune defences. A central question in this emerging field is to understand how responses to single attackers interfere with responses to other attackers, especially by integratively addressing molecular and ecological aspects. 2. We examined the plant-mediated interactions between the leaf-chewing Pieris brassicae and the phloem-sucking Brevicoryne brassicae, and their respective parasitoids Cotesia glomerata and Diaeretiella rapae, when feeding simultaneously, sequentially or in isolation on the brassicaceous ecological model plant Brassica oleracea. We analysed the underlying defence mechanisms in the plant. Levels of the phytohormones JA and SA transcriptional responses of a number of selected defence-related genes and secondary plant compounds were quantified at different time points during the single and multiple infestations. 3. The caterpillars developed faster and reached a larger body mass on plants previously attacked by aphids. Aphids initially developed faster on plants with caterpillars, although the moment of moulting to adults was independent of the presence of caterpillars. Both parasitoid species performed better under multiple-infestation scenarios than in single-herbivore situations. 4. On plants attacked by aphids, the JA levels were tenfold lower than on undamaged plants or plants with caterpillars. Additionally, the low transcript levels of LOX and MYC, genes coding for a JA biosynthesis-related enzyme and a transcription factor, respectively, in aphid-infested plants, suggest that the facilitation of the caterpillar performance was mediated by interference in signal transduction. Levels of carbon and nitrogen and secondary plant compounds (glucosinolates) did not differ significantly between treatments, suggesting that these compounds did not mediate the facilitation. 5. Our data show that the leaf chewer and phloem feeder asymmetrically interact not via competition as would be expected from interspecific herbivores but instead via facilitation; the phloem feeder attenuated JA-related plant defences, thus facilitating the growth and development of the leaf chewers. In linear bitrophic systems, interactions between JA and SA signalling pathways have been proposed to allow plants to fine-tune their defences, but if facilitation frequently occurs in interspecific interguild interactions among herbivores this may represent an important constraint for plant defences. Such a constraint might be reduced if, as in our model system, parasitoids also benefit from interactions between interguild hosts and nonhosts, but parasitoids are rarely considered in model molecular systems to assess the impact of herbivore-induced plant defences.