Crop rotation is a common practice aimed at enhancing both plant disease suppression and crop productivity under open field condition. The objective of the present study was to evaluate the effects of tomato-wheat rotation on Fusarium wilt suppression and shoot growth on tomato in comparison to tomato monoculture. The following factors were determined and integrated through a transdisciplinary approach: (i) soil chemical parameters; (ii) abundance, composition, richness and diversity of soil fungal and bacterial communities; (iii) soil biochemical and enzymatic indicators; (iv) abundance of Fusarium oxysporum isolates in rhizosphere under tomato cultivation and evaluation of the pathogenicity of the isolates; (v) suppressive response of the bulk soil samples against a selected pathogenic strain of Fusarium oxysporum f. sp. lycopersici on tomato; and (vi) tomato shoot growth. The integrated approach included soil amplicon sequencing by metabarcoding analyses carried out by Illumina MiSeq platform in association with the standard procedure for soil analyses. In addition, the pathogenicity of F. oxysporum from the tomato rhizosphere and the suppressive response of the soil bulk to Fusarium wilt were performed by bioassays under greenhouse condition. The results showed that, if durum wheat was rotated with cherry tomato for at least four consecutive years, it had the following beneficial effects: (i) increased suppressive response of the bulk soil samples against F. oxysporum f. sp. lycopersici, (ii) decreased abundance of the F. oxysporum isolates in tomato rhizosphere, (iii) decreased pathogenicity of the F. oxysporum isolates, and (iv) increased tomato shoot growth. The increased abundance of certain microbial groups belonging to potential biocontrol agents against fusaria-related wilt including Bacillales (Bacillus and Paenibacillus), Pseudomonadales (Pseudomonas), Streptomycetales (Streptomyces), Eurotiales (Aspergillus and Penicillium) and Mortierellales (Mortierella), as well as the highest tomato shoot growth, coincided with the end of the second wheat rotation cycle. There were significant Spearman cross-correlations and two-way ANOVA interactions among the microbiome variables with the (i) soil chemical parameters, (ii) abundance and pathogenicity of the F. oxysporum isolates in tomato rhizosphere, (iii) soil suppression to Fusarium wilt, and (iv) tomato shoot growth. The results indicate that a soil managed under tomato-wheat rotation displays increased suppressive response against Fusarium wilt and improved shoot growth in tomato plants by changing the microbial composition and chemical parameters of the soil.
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