Modulation of the leaf transcriptome of Quercus robur by specialist and generalist herbivorous insects

Plants deploy complex transcriptional responses to herbivores yet differences in the responses to generalist versus specialist insects, especially in long-lived tree species, are still poorly understood. Here, we analysed the transcriptional responses in Quercus robur L. leaves to infestation by two chewing insect species: the specialist moth Tortrix viridana L. and the generalist moth Lymantria dispar L. Regardless of insect species, we observed extensive gene induction. Key regulators such as the transcription factors MYC2, JAZ and ERF1, primarily activate defence gene expression via jasmonate and ethylene pathways after feeding by the generalist or the specialist. A total of 1591 genes were differentially expressed between the two herbivore treatments. Feeding by L. dispar triggered a broader transcriptional response, stronger activating pathways related to jasmonate, abscisic acid, auxin and ethylene signalling, as well as genes involved in terpene synthesis, monooxygenase activity and phloem development. In contrast, T. viridana induced a more specialized profile, including genes associated with serine-type endopeptidase activity, cell wall and cell wall organization, such as those encoding hydroxyproline-rich glycoproteins or pectin esterase inhibitors. This suggests a role of cell wall-related defences in response to specialist herbivores. Network analysis of Arabidopsis thaliana (L.) Heynh. homologues highlighted MYC2 as a central regulatory hub in both responses. Activation of MYC2 triggers downstream responses, including the induction of secondary metabolism genes, e.g., QrTPS1 encoding a functional sesquiterpene synthase, with germacrene D as its primary product. Transcriptional differences between resistant and susceptible oak genotypes were more pronounced following specialist than generalist herbivore feeding. These results provide insights into genome-scale herbivore-specific and genotype-mediated defence programmes at the transcriptome level and highlight promising gene targets for future functional genomics and natural variation studies in a keystone forest tree.