Leaf-mining by Phyllonorycter blancardella reprograms the host-leaf transcriptome to modulate phytohormones associated with nutrient mobilization and plant defense

This study has been supported by the ANR Grant No. ANR-05-JCJC-0203-01 and the Region Centre Project 201000047141International audiencePhytohormones have long been hypothesized to play a key role in the interactions betweenplant-manipulating organisms and their host–plants such as insect–plant interactions that lead to gallor ‘green-islands’ induction. However, mechanistic understanding of how phytohormones operate inthese plant reconfigurations is lacking due to limited information on the molecular and biochemical phytohormonalmodulation following attack by plant-manipulating insects. In an attempt to fill this gap, thepresent study provides an extensive characterization of how the leaf-miner Phyllonorycter blancardellamodulates the major phytohormones and the transcriptional activity of plant cells in leaves of Malusdomestica.We show here, that cytokinins strongly accumulate in mined tissues despite a weak expressionof plant cytokinin-related genes. Leaf-mining is also associated with enhanced biosynthesis of jasmonicacid precursors but not the active form, a weak alteration of the salicylic acid pathway and a clear inhibitionof the abscisic acid pathway. Our study consolidates previous results suggesting that insects mayproduce and deliver cytokinins to the plant as a strategy to manipulate the physiology of the leaf to createa favorable nutritional environment. We also demonstrate that leaf-mining by P. blancardella leads to astrong reprogramming of the plant phytohormonal balance associated with increased nutrient mobilization,inhibition of leaf senescence and mitigation of plant direct and indirect defens