This study evaluated the effects and underlying mechanisms of different combinations of plant symbiotic microbes, comprising arbuscular mycorrhizal fungi (AMF), plant growth-promoting rhizobacteria (PGPR), and Trichoderma spp., on tomato Fusarium crown and root rot (TFCRR) resistance. A total of 54 treatments were applied in a greenhouse pot experiment to tomato (Solanum lycopersicum) seedlings inoculated with or without Funneliformis mosseae (Fm), Rhizophagus intraradices (Ri), Trichoderma virens l40012 (Tv), Trichoderma harzianum l40015 (Th), Bacillus subtilis PS1-3 (Bs), Pseudomonas fluorescens PS2-6 (Pf), and Fusarium oxysporum f. sp. radicis-lycopersici (Fo). The symbioses on the tomato root system were well developed, and the composite symbiont generated by AMF + Trichoderma spp. was observed for the first time. Compared with other treatments, Ri + Bs + Tv and Fm + Pf + Tv stimulated the greatest improvements in tomato growth and yield. The combination Ri + Pf + Th + Fo resulted in the strongest biocontrol effects on TFCRR, followed by the treatments Th + Pf + Fo and Ri + Th + Fo. Compared with the Fo treatment, most inoculation treatments improved photosynthetic performance and significantly increased defense enzyme activity in tomato plants, of which the treatment Ri + Pf + Th + Fo showed the highest enzyme activity. Metabolome analysis detected changes in a total of 1,266 metabolites. The number of up-regulated metabolites in tomato plants inoculated with Ri + Pf + Th and Ri + Pf + Th + Fo exceeded that of the Fo treatment, whereas the number of down-regulated metabolites showed the opposite trend. It is concluded that AMF + Trichoderma + PGPR is the most effective combination to promote resistance to TFCRR in tomato. The up-regulation and down-regulation of metabolites regulated by symbiotic microbial genes may be an important mechanism by which root symbiotic microorganisms promote plant growth, increase yield, and improve disease resistance.

Watermelon (Citrullus lanatus) is susceptible to wilt disease caused by Fusarium oxysporum f. sp niveum (FON). AMF colonization alleviates watermelon wilt and regulates the composition of root exudates, but the effects of mycorrhizal watermelon root exudates on watermelon Fusarium wilt is not well understood. Root exudates of watermelon inoculated with AMF (Funeliformis mosseae or Glomus versiformme) were collected in this study. Then the root exudates of control plants and mycorrhizal plants were used to irrigate watermelon in continuous cropping soil, respectively. Meanwhile, the watermelon growth, antioxidant enzyme activity, rhizosphere soil enzyme activities and bacterial community composition, as well as the control effect on FON were analyzed. The results indicated that mycorrhizal watermelon root exudates promoted the growth of watermelon seedlings and increased soil enzyme activities, actinomyces, and the quantity of bacteria in rhizosphere soil. The proportion of Proteobacteria and Bacteroides was decreased, and the proportion of Actinobacteria, Firmicutes, and Chloroflexi in rhizosphere soil was increased when the seedlings were watered with high concentrations of mycorrhizal root exudates. The dominant bacterial genera in rhizosphere soil were Kaistobacter, Rhodanobacter, Thermomonas, Devosia, and Bacillus. The root exudates of mycorrhizal watermelon could reduce the disease index of Fusarium wilt by 6.7–30%, and five ml/L of watermelon root exudates inoculated with F. mosseae had the strongest inhibitory effect on watermelon Fusarium wilt. Our results suggest mycorrhizal watermelon root exudates changed the composition of bacteria and soil enzyme activities in rhizosphere soil, which increase the resistance of watermelon to Fusarium wilt and promoted the growth of plants in continuous cropping soil.

Root-knot nematodes (RKNs) are among the most destructive pests in protected watermelon production under continuous cropping systems. Although both pepper rotation and arbuscular mycorrhizal fungi (AMF) inoculation have shown potential for suppressing RKNs and promoting plant growth, their combined effects remain unclear. This study conducted greenhouse pot experiments using continuously cropped watermelon soil over two consecutive cycles. In the first cycle, chili pepper (Capsicum annuum) or watermelon (Citrullus lanatus) was planted, followed by watermelon cultivation in the second cycle with inoculation of Funneliformis mosseae or Glomus versiforme. Compared with continuous watermelon cropping, both rotation and AMF inoculation improved root vitality, osmotic regulation, antioxidant enzyme activities, and photosynthetic performance, thereby enhancing watermelon growth and resistance to RKNs. Among all treatments, chili pepper rotation combined with Glomus versiforme showed the best performance, increasing shoot fresh weight by 31% and reducing disease index (DI), gall index (GI), and egg mass index (EI) by 30.8%, 77.0%, and 57.1%, respectively. In addition, the populations of second-stage juveniles (J2) in soil and roots and adult females in roots decreased by 85.4%, 55.5%, and 50.8%, respectively. High-throughput sequencing results showed that the combined treatment enriched several potentially beneficial microbial taxa, including Ochrobactrum, Bacillus, Acinetobacter, and Delftia. In addition, it enriched predicted metabolic pathways that may be associated with plant growth promotion and stress tolerance. Overall, pepper rotation combined with Glomus versiforme inoculation represents a promising, environmentally friendly strategy for the management of watermelon root-knot nematode disease.