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When plants are exposed to ozone they exhibit changes in both primary and secondary metabolism, which may affect their interactions with herbivorous insects. Here we investigated the performance and preferences of the specialist herbivore Pieris brassicae on the wild plant Brassica nigra under elevated ozone conditions. The direct and indirect effects of ozone on the plant-herbivore system were studied. In both cases ozone exposure had a negative effect on P. brassicae development. However, in dual-choice tests larvae preferentially consumed plant material previously fumigated with the highest concentration tested, showing a lack of correlation between larval preference and performance on ozone exposed plants. Metabolomic analysis of leaf material subjected to combinations of ozone and herbivore-feeding, and focussing on known defence metabolites, indicated that P. brassicae behaviour and performance were associated with ozone-induced alterations to glucosinolate and phenolic pools. 

Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O-3), a global anthropogenic pollutant, directly affects living organisms and ecosystems, including plant-herbivore interactions. In this study, we investigate the stress responses of Brassica nigra (wild black mustard) exposed consecutively to O-3 and the specialist herbivore Pieris brassicae. Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O-3 and herbivory responses. O-3 stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O-3 to herbivory induced characteristic plant defense responses, including a decrease in central metabolism, induction of the jasmonic acid/ethylene pathways, and emission of volatiles. Omics network and pathway analyses predicted a link between glycerol and central energy metabolism that influences the osmotic stress response and stomatal closure. Further physiological measurements confirmed that while O-3 stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O-3, resulting in a phenotype similar to that observed after herbivory alone. This study clarifies the consequences of multiple stress interactions on a plant metabolic system and also illustrates how omics data can be integrated to generate new hypotheses in ecology and plant physiology.

Plant responses to dual herbivore attack are increasingly studied, but effects on the metabolome have largely been restricted to volatile metabolites and defence-related non-volatile metabolites. However, plants subjected to stress, such as herbivory, undergo major changes in both primary and secondary metabolism. Using a naturally occurring system, we investigated metabolome-wide effects of single or dual herbivory on Brassica nigra plants by Brevicoryne brassicae aphids and Pieris brassicae caterpillars, while also considering the effect of aphid density. Metabolomic analysis of leaf material showed that single and dual herbivory had strong effects on the plant metabolome, with caterpillar feeding having the strongest influence. Additionally, aphid-density-dependent effects were found in both the single and dual infestation scenarios. Multivariate analysis revealed treatment-specific metabolomic profiles, and effects were largely driven by alterations in the glucosinolate and sugar pools. Our work shows that analysing the plant metabolome as a single entity rather than as individual metabolites provides new insights into the subcellular processes underlying plant defence against multiple herbivore attackers. These processes appear to be importantly influenced by insect density.

In order to defend, plants rely on quick metabolic reconfigurations. Here weinvestigated plant herbivore-induced responses asking: 1) how exposure to methyljasmonate(MeJA) and herbivory alter plant defence and growth metabolism, and 2)are herbivore-induced responses concentrated in tissues with higher fitness value, aspredicted by the optimal defence (OD) theory? We analysed the leaf metabolome of black mustard (B. nigra) in response to MeJAand/or feeding by specialist caterpillars of the large white cabbage butterfly (Pierisbrassicae). Shifts in defence-related (secondary) and growth-related (primary)metabolites were initially evaluated on fully expanded mature leaves and thenfollowed across leaf ontogeny. MeJA enhanced herbivore induced-responses and increased the plant resistanceagainst sequential herbivory. Responses were focused in young leaves andcharacterized by changes in defence- (glucosinolates, phenolics) and growth- (aminoacids, sugars, organic acids) metabolism, including asymmetric accumulation ofcentral tricarboxylic acid cycle (TCA) intermediates. MeJA application enhanced the plant resistance towards herbivory and, consistentlywith the OD theory, herbivore-induced responses were prioritized in young leaves.However, shifts in the plant were not limited to higher defences but affected growthmetabolism including regulation of energy pathways and increased leaf senescence.These effects deserve attention by future ecological and applied research on plantinsectinteractions.