The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.

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Organisms make the best of their mother's oviposition choices and utilize specific feeding options that meet energetic requirements and cope with environmental constraints. This is particularly true for leaf-miner insects that develop enclosed in the two epidermis layers of a single leaf for their entire larval life. Cytokinins (CKs) play a central role in plant physiology -including regulation of senescence and nutrient translocation -and, as such, can be the specific target of plant exploiters that manipulate plant primary metabolism. 'Green-islands' are striking examples of a CKinduced phenotype where green areas are induced by plant pathogens/insects in otherwise yellow senescent leaves. Here, we document how the leaf-miner caterpillar Phyllonorycter blancardella, working through an endosymbiotic bacteria, modifies phytohormonal profiles, not only on senescing (photosynthetically inactive) but also on normal (photosynthetically active) leaf tissues of its host plant (Malus domestica). This leaf physiological manipulation allows the insect to maintain sugar-rich green tissues and to create an enhanced nutritional microenvironment in an otherwise degenerating context. It also allows them to maintain a nutritional homeostasis even under distinct leaf environments. Our study also highlights that only larvae harboring bacterial symbionts contain significant amounts of CKs that are most likely not plant-derived. This suggests that insects are able to provide CKs to the plant through their symbiotic association, thus extending further the role of insect bacterial symbionts in plant-insect interactions.

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