Abstract
Plants are naturally exposed to multiple biotic interactions that can simultaneously influence their growth, metabolism, and defense responses. Plant growth-promoting rhizobacteria (PGPR) can influence plant growth and defense, yet their role in shaping plant responses to belowground herbivory remains poorly understood. This study examines how inoculation with Bacillus velezensis GB03 and root herbivory by Diabrotica speciosa affect growth, specialized metabolism, and hormonal signaling in sweet basil (Ocimum basilicum), considering responses in both roots and shoots. GB03 promoted plant growth, whereas root herbivory reduced biomass and strongly activated jasmonate-related signaling. Both GB03 inoculation and herbivory altered specialized metabolism, increasing essential oil accumulation, phenolic content, and volatile organic compound emission, although these responses differed between roots and shoots. The combined treatment produced the strongest response for several specialized-metabolism traits, particularly essential oil and eugenol accumulation and shoot phenolic content. Importantly, the effects of herbivory on shoot phenolic accumulation, root volatile emission, and jasmonic acid levels depended on the inoculation status of the plants, indicating that GB03 selectively modified specific responses to root herbivory. These findings reveal a complex interplay between beneficial rhizobacteria and belowground herbivores, in which GB03 not only promotes plant growth and modifies basal metabolism but also reshapes specific local and systemic responses to herbivore attack. Understanding these interactions may contribute to the development of sustainable strategies that exploit beneficial microorganisms to improve plant performance and modulate specialized metabolism in aromatic crops.