A root symbiont rewires tomato polyamine network to enhance herbivore resistance

ABSTRACT Plants rely on specialized metabolites to defend against herbivores, yet how root-associated symbiotic microbes influence their regulation, coordination, and overall contribution to defense remains widely unknown. We hypothesized that symbiotic microbes can reprogram specialized metabolic networks, thereby enhancing herbivore resistance, with a particular focus here on polyamine metabolic network. Using the fungal symbiotic endophyte Trichoderma harzianum, tomato, and the herbivore Spodoptera exigua, we combined greenhouse bioassays with molecular, genetic, and metabolomic analyses to investigate how Trichoderma symbiosis reshapes the plant polyamine metabolic network, and affects plant-herbivore interactions. We found that in the absence of the root symbiosis, herbivory primarily activated polyamine uptake transport and catabolism, reflecting a stress-driven turnover response. Trichoderma symbiosis markedly reconfigured the polyamine network. Symbiosis primed uptake transport and catabolic responses, enhanced polyamine flux through activation of the ornithine decarboxylase pathway, and redirected polyamines into conjugated metabolites with anti-herbivore activity. Genetic analyses and dietary supplementation bioassays confirmed that this metabolic rewiring contributes to Trichoderma-induced resistance to herbivory, linking primary metabolic routes to the accumulation of specialized defense compounds. Our study highlights root symbionts as key modulators of plant metabolism, showing that specialized metabolite diversity can be shaped by symbiotic interactions. Competing Interest Statement The authors have declared no competing interest. Footnotes Minor changes have been made, including the grouping of figures and the addition of new analyses. Some typographical errors have also been corrected. The main conclusions of the paper remain unchanged.