Manipulation of plant primary metabolism by leaf-mining larvae in the race against leaf senescence

Plants are often considered as suboptimal food for phytophagous insects, requiring them to employ various adaptive mechanisms to overcome food nutritional imbalances. This could include host-plant manipulation and/or symbiotic associations. The extensive reconfiguration of plant primary metabolism upon herbivory, as well as its impact on herbivores, have been largely overlooked, while studies investigating secondary metabolites is extensive. Here, we document how the apple leaf-mining caterpillar Phyllonorycter blancardella, a highly-specialized insect which completes development within a restricted area of a single Malus domestica leaf over successive different larval feeding modes, maintains nutrient-rich green tissues in its feeding area on green and senescent leaves. For this purpose, we quantified a large number of compounds involved in plant primary metabolism: starch, total soluble sugars, five individual sugars, twenty protein-bound amino acids and twenty free amino acids. Plant alteration can be observed not only on senescing (photosynthetically inactive) but also normal (photosynthetically active) leaf tissues of its host-plant to compensate for detrimental environmental variations. Our results show a differential control of the primary metabolism depending on the larva developmental stage, itself correlated to the fluid-feeding and tissue-feeding modes. Our results also suggest that leaf amino acid alterations favor a faster insect development. Finally, chemical scores indicate that the most growth-limiting essential amino acids are also common to other phytophagous insects and large herbivores, suggesting that these limitations are a general consequence of using plants as food source. We discuss the possible mechanisms responsible for these different manipulative capacities, as well as their ecological implications.