Leaf-mining by Phyllonorycter blancardella reprograms the host-leaf transcriptome to modulate phytohormones associated with nutrient mobilization and plant defense
Résumé
Phytohormones have long been hypothesized to play a key role in the interactions between
plant-manipulating organisms and their host–plants such as insect–plant interactions that lead to gall
or ‘green-islands’ induction. However, mechanistic understanding of how phytohormones operate in
these plant reconfigurations is lacking due to limited information on the molecular and biochemical phytohormonal
modulation following attack by plant-manipulating insects. In an attempt to fill this gap, the
present study provides an extensive characterization of how the leaf-miner Phyllonorycter blancardella
modulates the major phytohormones and the transcriptional activity of plant cells in leaves of Malus
domestica.We show here, that cytokinins strongly accumulate in mined tissues despite a weak expression
of plant cytokinin-related genes. Leaf-mining is also associated with enhanced biosynthesis of jasmonic
acid precursors but not the active form, a weak alteration of the salicylic acid pathway and a clear inhibition
of the abscisic acid pathway. Our study consolidates previous results suggesting that insects may
produce and deliver cytokinins to the plant as a strategy to manipulate the physiology of the leaf to create
a favorable nutritional environment. We also demonstrate that leaf-mining by P. blancardella leads to a
strong reprogramming of the plant phytohormonal balance associated with increased nutrient mobilization,
inhibition of leaf senescence and mitigation of plant direct and indirect defense