A pathogen may cause infected plants to promote the performance of its transmitting vector, which accelerates the spread of the pathogen. This positive effect of a pathogen on its vector via their shared host plant is termed indirect mutualism. For example, terpene biosynthesis is suppressed in begomovirus-infected plants, leading to reduced plant resistance and enhanced performance of the whiteflies (Bemisia tabaci) that transmit these viruses. Although begomovirus-whitefly mutualism has been known, the underlying mechanism is still elusive. Here, we identified βC1 of Tomato yellow leaf curl China virus, a monopartite begomovirus, as the viral genetic factor that suppresses plant terpene biosynthesis. βC1 directly interacts with the basic helix-loop-helix transcription factor MYC2 to compromise the activation of MYC2-regulated terpene synthase genes, thereby reducing whitefly resistance. MYC2 associates with the bipartite begomoviral protein BV1, suggesting that MYC2 is an evolutionarily conserved target of begomoviruses for the suppression of terpene-based resistance and the promotion of vector performance. Our findings describe how this viral pathogen regulates host plant metabolism to establish mutualism with its insect vector.

Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids. In nature, plants often release volatiles in response to damage by herbivores (e.g., by caterpillars), and these can indirectly help defend the plants. Indeed, it is well documented that volatiles can recruit the natural enemies of herbivores, such as predators and parasitoid wasps, whose offspring feed on and develop within their caterpillar hosts. However, such induced plant odours can also be detected by other organisms. One important group of organisms, hyperparasitoids, the enemies of the parasitoids that indirectly benefit the plants, have not been included in this trophic web because so little is known about their foraging behaviour. Here, using a combination of laboratory and field experiments, we demonstrate that hyperparasitoid wasps also take advantage of the odours that plants produce in response to the feeding by caterpillars. The larvae of parasitic wasps developing inside the caterpillar alter the composition of the oral secretions of their herbivorous host and thereby affect the cocktail of volatiles the plant produces. The hyperparasitoids on the lookout for their parasitoid prey can preferentially detect infected caterpillars, although not all parasitoid wasps gave away their presence through this host–plant interaction. We conclude that herbivore-induced plant volatiles can affect the interaction among parasitoids and their enemies and thereby may reduce the indirect defence accrued for the plant.

Plants release volatiles induced by herbivore feeding that may affect the diversity and composition of plant-associated arthropod communities. However, the specificity and role of plant volatiles induced during the early phase of attack, i.e. egg deposition by herbivorous insects, and their consequences on insects of different trophic levels remain poorly explored. In olfactometer and wind tunnel set-ups, we investigated behavioural responses of a specialist cabbage butterfly (Pieris brassicae) and two of its parasitic wasps (Trichogramma brassicae and Cotesia glomerata) to volatiles of a wild crucifer (Brassica nigra) induced by oviposition of the specialist butterfly and an additional generalist moth (Mamestra brassicae). Gravid butterflies were repelled by volatiles from plants induced by cabbage white butterfly eggs, probably as a means of avoiding competition, whereas both parasitic wasp species were attracted. In contrast, volatiles from plants induced by eggs of the generalist moth did neither repel nor attract any of the tested community members. Analysis of the plant’s volatile metabolomic profile by gas chromatography-mass spectrometry and the structure of the plant-egg interface by scanning electron microscopy confirmed that the plant responds differently to egg deposition by the two lepidopteran species. Our findings imply that prior to actual feeding damage, egg deposition can induce specific plant responses that significantly influence various members of higher trophic levels.

Summary: The effects of plant competition for light on the emission of plant volatile organic compounds (VOCs) were studied by investigating how different light qualities that occur in dense vegetation affect the emission of constitutive and methyl‐jasmonate‐inducedVOCs. Arabidopsis thalianaColumbia (Col‐0) plants andPieris brassicaecaterpillars were used as a biological system to study the effects of light quality manipulations onVOCemissions and attraction of herbivores.VOCs were analysed using gas chromatography–mass spectrometry and the effects of light quality, notably the red : far red light ratio (R : FR), on expression of genes associated withVOCproduction were studied using reverse transcriptase–quantitativePCR. The emissions of both constitutive and methyl‐jasmonate‐induced green leaf volatiles and terpenoids were partially suppressed under lowR : FRand severe shading conditions. Accordingly, theVOC‐based preference of neonates of the specialist lepidopteran herbivoreP. brassicaewas significantly affected by theR : FRratio. We conclude thatVOC‐mediated interactions among plants and between plants and organisms at higher trophic levels probably depend on light alterations caused by nearby vegetation. Studies on plant–plant and plant–insect interactions throughVOCs should take into account the light quality within dense stands when extrapolating to natural and agricultural field conditions.