From shoots to roots: transport and metabolic changes in tomato after simulated feeding by a specialist lepidopteran

Upon herbivory, plants can swiftly reallocate newly acquired resources to different tissues within a plant. Although the herbivore-induced movement of resources is apparent, the movement direction and the role of the remobilized resources are not well understood. Here, we used a two-pronged approach combining radioisotope and metabolomic techniques to shed light on whole-plant resource reallocation and changes in primary metabolism within the tomato, Solanum lycopersicum (L.) (Solanaceae), model in response to simulated herbivory by the specialist Manduca sexta (L.) (Lepidoptera: Sphingidae). Manduca sexta regurgitant applied to damaged leaves, but not mechanical damage alone, increased 11C-photosynthate allocation to roots but did not affect 11CO2 fixation and leaf export. Changes in primary metabolite concentrations occurred mostly in sink tissues (apex and roots) as well as in damaged leaves. Both damage treatments (with and without M. sexta regurgitant application) resulted in increased concentrations of primary metabolites relative to undamaged plants in the apex and decreased concentrations in the roots, but there were also extensive changes specific to each damage treatment. Mechanical damage alone led to changes consistent with water stress caused by tissue damage. Manduca sexta led to metabolite increases in the apex consistent with an increase in glucose breakdown, metabolite increases in damaged leaves consistent with starch degradation, and metabolite decreases in roots suggesting a high use of metabolites. A possible explanation for the observed patterns in the aboveground tissues might be an increase in carbohydrate degradation to support defense production in attacked leaves and vulnerable developing leaves, and/or subsequent remobilization to belowground tissues to support high carbohydrate demand for respiration, enhanced nutrient uptake, and storage.