Watermelon (Citrullus lanatus) is one of the most popular fruit crops. However, Fusarium wilt (FW) is a serious soil-borne disease caused by Fusarium oxysporum f. sp. niveum (FON) that severely limits the development of the watermelon industry. Trichoderma spp. is an important plant anti-pathogen biocontrol agent. The results of our previous study indicated that Trichoderma asperellum M45a (T. asperellum M45a) could control FW by enhancing the relative abundance of plant growth-promoting rhizobacteria (PGPR) in the rhizosphere of watermelon. However, there are few studies on its mechanism in the pathogen resistance of watermelon. Therefore, transcriptome sequencing of T. asperellum M45a-treated watermelon roots combined with metabolome sequencing of the rhizosphere soil was performed with greenhouse pot experiments. The results demonstrated that T. asperellum M45a could stably colonize roots and significantly increase the resistance-related enzymatic activities (e.g., lignin, cinnamic acid, peroxidase and peroxidase) of watermelon. Moreover, the expression of defense-related genes such as MYB and PAL in watermelon roots significantly improved with the inoculation of T. asperellum M45a. In addition, KEGG pathway analysis showed that a large number of differentially expressed genes were significantly enriched in phenylpropane metabolic pathways, which may be related to lignin and cinnamic acid synthesis, thus further inducing the immune response to resist FON. Furthermore, metabolic analysis indicated that four differential metabolic pathways were enriched in M45a-treated soil, including six upregulated compounds and one down-regulated compound. Among them, galactinol and urea were significantly positively correlated with Trichoderma. Hence, this study provides insight into the biocontrol mechanism of T. asperellum M45a to resist soil-borne diseases, which can guide its industrial application.

Abstract Fusarium wilt (FW) caused by Fusarium oxysporum f. sp. niveum (FON) is a soil-borne disease that seriously limits watermelon production. In the present study, the Trichoderma asperellum (T. asperellum) M45a was shown to be an effective biocontrol agent against Fusarium wilt (FW). In a pot experiment, the application of 105 cfu/g of T. asperellum M45a granules had better control effect on FW at the blooming period (up to 67.44%) from soils subjected to five years of continuous cropping with watermelon, while the average length of watermelon vine was also significantly improved(P < 0.05). Additionally, the acid phosphatase (ACP), cellulase (CL), catalase (CAT) and sucrase (SC) activities in the M45a-inoculation group were significantly higher than in the control (CK) group, and the soil nutrients (total N, NO3-N, and available P) transformation was significantly increased. Moreover, T. asperellum M45a inoculation reduced fungal diversity and increased bacterial diversity, especially enhancing the relative abundance of PGPR (plant growth promoting rhizobacteria), such as Trichoderma, Sphingomonas, Pseudomonas, Actinomadura and Rhodanobacter. Through functional prediction, the relative abundance of Ectomycorrhizal, Endophyte, Animal pathotroph and saprotroph in fungal community was determined to be significantly lower than observed in the M45a-treated soil. Correlation analysis revealed that Sphingomonas, Pseudomonas and Trichoderma had the most differences in microorganisms abundance, positively correlated with ACP, CL, CAT and SC. These findings will provide ecological fungicide advice for microecological control of FW in continuous cropping watermelon.

Fusarium wilt (FW) caused by Fusarium oxysporum f. sp. niveum (FON) is a soil-borne disease that seriously limits watermelon production. In the present study, the Trichoderma asperellum ( T. asperellum ) M45a was shown to be an effective biocontrol agent against Fusarium wilt (FW). In a pot experiment, the application of 10 5 cfu/g of T. asperellum M45a granules had better control effect on FW at the blooming period (up to 67.44%) from soils subjected to five years of continuous cropping with watermelon, while the average length of watermelon vine was also significantly improved(P<0.05). Additionally, the acid phosphatase (ACP), cellulase (CL), catalase (CAT) and sucrase (SC) activities in the M45a-inoculation group were significantly higher than in the control (CK) group, and the soil nutrients (total N, NO3-N, and available P) transformation was significantly increased. Moreover, T. asperellum M45a inoculation reduced fungal diversity and increased bacterial diversity, especially enhancing the relative abundance of PGPR (plant growth promoting rhizobacteria), such as Trichoderma, Sphingomonas , Pseudomonas , Actinomadura and Rhodanobacter . Through functional prediction, the relative abundance of Ectomycorrhizal, Endophyte, Animal pathotroph and saprotroph in fungal community was determined to be significantly lower than observed in the M45a-treated soil. Correlation analysis revealed that Sphingomonas , Pseudomonas and Trichoderma had the most differences in microorganisms abundance, positively correlated with ACP, CL, CAT and SC. These findings will provide ecological fungicide advice for microecological control of FW in continuous cropping watermelon.