Endogenous rhythmic growth and ectomycorrhizal fungi modulate priming of antiherbivore defences in subsequently formed new leaves of oak trees

Abstract

Abstract Priming of plant defences provides increased plant protection against herbivores and reduces the allocation costs of defence. Defence priming in woody plants remains obscure, in particular, due to plant development traits such as endogenous rhythmic growth. By using bioassays with oak microcuttings (Quercus robur) and combining transcriptomic and metabolomic analyses, we investigated how leaf herbivory by Lymantria dispar and root inoculation with the ectomycorrhizal fungus Piloderma croceum prime oak defences. We further investigated how defence priming is modulated by the rhythmic growth of the oaks. A first herbivory challenge in oak leaves primed newly grown leaves for enhanced induction of jasmonic acid (JA)‐related direct defences, or enhanced emission of volatiles, depending on the specific growth stage at which the plants were first challenged. Root inoculation with Piloderma abolished the enhanced induction of JA‐related defences and volatile emission. Synthesis: Our results indicate that a first herbivore attack primes direct and indirect defences of newly formed oak leaves and that the specific display of defence priming is regulated by rhythmic growth, and modulated by the interaction Piloderma. Our results show that the priming memory in oaks can be transmitted to the next growth cycle, to the leaves of the new shoot unit.