Purpose Continuous cropping of tomato (Solanum lycopersicum Mill.) causes soil degradation, accumulating Ralstonia solanacearum that induce Ralstonia wilt notably in plastic shed soils. Arbuscular mycorrhizal (AM) fungi play a crucial role in protecting hosts against such soil-borne pathogens, but comprehensive understanding of the soil-plant defense systems upon mycorrhization is not clear yet, especially at the later period of fruit production. The aim of this study was to investigate the underlining mechanisms in both soil and plant. Materials and methods A 10-week greenhouse pot experiment with four treatments, including control and inoculation with Funneliformis caledonium (Fc), R. solanacearum (Rs), and both strains (Rs + Fc), was carried out on a sterilized soil. Pots with two tomato plants each were randomly arranged with six replicates per treatment. The wilt severity; the tissue biomass and nutrient content; the root mycorrhizal colonization and total phenolic compounds; the leaf peroxidase (POD), polyphenol oxidase (PPO), and phenylalanine ammonia lyase (PAL) activities; and soil AM fungi and R. solanacearum abundances, soil pH, organic C and nutrient concentrations, and phosphatase activity were all tested. Both redundancy analysis (RDA) and structural equation modeling (SEM) were performed to illustrate plant overall performance among treatments and to elucidate the major influencing pathways of AM fungi. Results and discussion The additional inoculation with F. caledonium resulted in significant decreases of soil R. solanacearum abundance and Olsen-P concentration, as well as increases of soil pH, organic C concentration, and phosphatase activity, as compared to the soil only inoculated with R. solanacearum. Mycorrhizal inoculation also increased root total phenolic compound content, and leaf POD and PPO activities, but reduced shoot/root K ratio in plants under the attack of R. solanacearum, thereby alleviating Ralstonia wilt severity by 65.7% and yield loss by 46.5%. The RDA and SEM results revealed significant variation in plant overall performance among treatments, and the contribution of AM fungi in suppressing tomato Ralstonia wilt and yield damage particularly via ameliorating soil quality and alleviating plant metabolic pressure. Conclusions This study verified the bio-protection of AM fungi in both soil and plant systems against tomato Ralstonia wilt. Mycorrhization shifted the soil environment and suppressed soil R. solanacearum population, and also modulated plant nutrient translocation, increased phenolic compounds synthetization, and activated defense enzymes. Through establishing the integrated defense systems in both rhizosphere and plant, AM fungi alleviated the severity of Ralstonia disease and ameliorated yield damage in tomato.
