Integrated transcriptomic and metabolomic analysis reveals differential molecular mechanisms underlying resistance of native and invasive Phytolacca americana against Spodoptera litura herbivory.

BACKGROUND: In response to herbivory from insects, plants have evolved complex defense strategies. Alien plants often escape control by specialist insects in their introduced range. This release from herbivory pressure may lead to a reallocation of the defensive strategies of alien plants, thereby promoting their invasiveness. However, the molecular mechanisms underlying this resource reallocation process remain unclear. In the present study, we used Phytolacca americana as a model species, and combined transcriptomic and metabolomic analyses to investigate the molecular basis of its invasion success under the herbivory by Spodoptera litura.

RESULTS: Herbivore assays with S. litura revealed that constitutive resistance was comparable between native and invasive P. americana, while induced resistance was significantly lower in invasive P. americana. In the native population, differentially expressed genes and differential abundance metabolites upon S. litura herbivory were mainly enriched in α‑linolenic acid metabolism, the primary pathway for jasmonic acid (JA) formation, whereas in the invasive population, they were predominantly enriched in biosynthesis of amino acids. Notably, the invasive population maintains the synthesis of certain defense metabolites like isoquercitrin, suggesting a defense strategy reconfiguration rather than a complete loss.

CONCLUSIONS: Collectively, these findings suggest that invasive P. americana may employ a strategic resource reallocation from induced defense to growth metabolism, while JA-mediated induced defense was activated in native P. americana. Our results provide support for the Shifting Defense Hypothesis and advance the mechanisms of plant invasion adaptation.