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

Herbivore attack is a major constraint on growth and survival in long-lived woody plants, yet the early molecular events coordinating defence reprogramming remain incompletely understood. Here, we integrated transcriptomic, metabolomic and volatilomic profiling to dissect early defence responses of Populus hopeiensis, a desert-adapted woody species, subjected to chewing and piercing–sucking herbivory. Short-term feeding and standardized mechanical wounding triggered a rapid shift from growth- to defence-associated transcriptional programmes, including activation of jasmonate–ethylene signalling and MAPK cascades, and strong induction of phenylpropanoid and flavonoid pathway genes, accompanied by repression of photosynthesis- and ribosome-related genes.Multi-omics integration revealed distinct, mode-specific defence signatures. Chewing stress preferentially enhanced phenylpropanoid-derived phenolics and proteinase inhibitors, consistent with strengthened direct defences against leaf-chewing larvae. By contrast, prolonged piercing–sucking stress was associated with broader remodelling of lipid and oxylipin metabolism and phytohormone networks, together with the emission of characteristic volatile organic compound blends that may contribute to indirect or systemic defences. Co-expression network analysis further highlighted several WRKY and MYB transcription factors as candidate regulatory hubs linking hormone signalling with downstream defence metabolism. Collectively, these results provide a systems-level framework for how feeding mode shapes hormonal signalling, specialized metabolism and volatile emission in P. hopeiensis, and identify candidate molecular targets for improving insect resistance in woody plants.