Multi-omics dissection of mode-specific growth–defence reprogramming to insect herbivores in Populus hopeiensis

Abstract

How woody perennials coordinate growth–defence reprogramming in response to herbivores with contrasting feeding modes remains insufficiently understood. Here, we integrated transcriptomic, metabolomic, and volatilomic analyses to compare the responses of Populus hopeiensis to chewing herbivory and piercing–sucking herbivory. Chewing and piercing–sucking treatments induced both shared and distinct defence-associated responses. Short-term chewing herbivory was associated with rapid transcriptional reprogramming towards defence, including jasmonate- and ethylene-related signalling, mitogen-activated protein kinase (MAPK) cascades, phenylpropanoid/flavonoid metabolism, and repression of photosynthesis-related functions. In contrast, the 19 h piercing–sucking treatment was associated with broader transcriptomic and metabolic restructuring, particularly involving lipid- and amino acid-related pathways. Metabolomic data further indicated that chewing herbivory was more closely linked to phenylpropanoid- and flavonoid-associated metabolite changes, whereas piercing–sucking herbivory induced a wider metabolic response. Volatilomic profiling, which was performed only for the chewing treatments, identified characteristic volatile organic compound (VOC) changes, and co-expression analysis highlighted several WRKY and MYB transcription factors as candidate regulatory hubs. Overall, these results provide a multi-omics view of herbivory-associated growth–defence reprogramming in P. hopeiensis and identify candidate genes and pathways for future functional studies of insect resistance in woody plants.