Herbivory-triggered assemblage of sunflower rhizosphere microbiome enhances herbivore tolerance through plant–soil feedback

Rhizosphere microbial communities are key drivers of plant immunity and stress responses, and plants recruit beneficial microorganisms under stress. Herbivorous insects pose a major agricultural challenge, yet how leaf herbivory influences root-associated microbiomes and whether these changes generate plant–soil feedbacks that alter plant defense phenotypes remain poorly understood. With a two-phase greenhouse bioassay, we investigated how leaf herbivory with Spodoptera exigua affects sunflower rhizosphere microbiome (Conditioning Phase) and whether herbivory-induced microbial shifts modulate plant defense traits via plant–soil feedback (Feedback Phase). Herbivory triggered significant changes in bacterial community structure and dynamics, as well as in microbiome functional profile, whereas effects on fungal community were weaker. Several bacterial taxa and functional groups were enriched, co-occurrence networks became more complex, and community assembly showed increased stochasticity. Herbivore-driven microbial legacies increased plant nutrient content and photosynthetic pigments via plant–soil feedback. After subsequent infestation, resistance-related traits and herbivore performance were unaffected, but tolerance-related traits were significantly altered. Plants grown with a herbivory-conditioned microbiome were smaller but exhibited reduced biomass loss after attack, indicating enhanced compensatory growth. Overall, herbivory reshaped the sunflower rhizosphere microbiome and generated a soil legacy that enhances plant tolerance, highlighting the role of microbiome-mediated plant–soil feedbacks in plant adaptation to herbivory.