The continuous cropping of banana in the same field may result in a serious soil-borne Fusarium wilt disease and a severe yield decline, a phenomenon known as soil sickness. Although soil microorganisms play key roles in maintaining soil health, the alternations of soil microbial community and relationship between these changes and soil sickness under banana monoculture are still unclear. Bacterial and fungal communities in the soil samples collected from banana fields with different monoculture spans were profiled by sequencing of the 16S rRNA genes and internal transcribed spacer using the MiSeq platform to explore the relationship between banana monoculture and Fusarium wilt disease in the present study. The results showed that successive cropping of banana was significantly correlated with the Fusarium wilt disease incidence. Fungal communities responded more obviously and quickly to banana consecutive monoculture than bacterial community. Moreover, a higher fungal richness significantly correlated to a higher banana Fusarium wilt disease incidence but a lower yield. Banana fungal pathogenic genus of Fusarium and Phyllosticta were closely associated with banana yield depletion and disease aggravation. Potential biocontrol agents, such as Funneliformis, Mortierella, Flavobacterium, and Acidobacteria subgroups, exhibited a significant correlation to lower disease occurrence. Further networks analysis revealed that the number of functionally interrelated modules decreased, the composition shifted from bacteria- to fungi-dominated among these modules, and more resources-competitive interactions within networks were observed after banana long-term monoculture. Our results also showed that bacterial and fungal communities were mainly driven by soil organic matter. Overall, the findings indicated that the bacterial and fungal community structures altered significantly after banana long-term monoculture, and the fungal richness, abundance of Fusarium, interactions between and within bacteria and fungi in ecological networks, and soil organic matter were associated with banana soil-borne Fusarium wilt disease.

Background The development of suppressive soils is a promising strategy to protect plants against soil-borne diseases in a sustainable and viable manner. The use of crop rotation and the incorporation of plant residues into the soil are known to alleviate the stress imposed by soil pathogens through dynamics changes in soil biological and physicochemical properties. However, relatively little is known about the extent to which specific soil amendments of plant residues trigger the development of plant-protective microbiomes. Here, we investigated how the incorporation of pineapple residues in soils highly infested with the banana Fusarium wilt disease alleviates the pathogen pressure via changes in soil microbiomes. Results The addition of above- and below-ground pineapple residues in highly infested soils significantly reduced the number of pathogens in the soil, thus resulting in a lower disease incidence. The development of suppressive soils was mostly related to trackable changes in specific fungal taxa affiliated with Aspergillus fumigatus and Fusarium solani, both of which displayed inhibitory effects against the pathogen. These antagonistic effects were further validated using an in vitro assay in which the pathogen control was related to growth inhibition via directly secreted antimicrobial substances and indirect interspecific competition for nutrients. The disease suppressive potential of these fungal strains was later validated using microbial inoculation in a well-controlled pot experiment. Conclusions These results mechanistically demonstrated how the incorporation of specific plant residues into the soil induces trackable changes in the soil microbiome with direct implications for disease suppression. The incorporation of pineapple residues in the soil alleviated the pathogen pressure by increasing the relative abundance of antagonistic fungal taxa causing a negative effect on pathogen growth and disease incidence. Taken together, this study provides a successful example of how specific agricultural management strategies can be used to manipulate the soil microbiome towards the development of suppressive soils against economically important soil-borne diseases.

Summary Crop rotation can assemble distinct core microbiota as functionally specific barriers against the invasion of banana Fusarium oxysporum pathogens. However, the taxonomic identity of rotation‐unique core taxa and their legacy effects are poorly understood under field conditions. Pepper and eggplant rotations were employed to reveal rotation crop‐ and banana‐unique antagonistic core taxa by in situ tracking of the soil microbiome assembly patterns for 2 yr. The rotation crop‐unique antagonistic taxa were isolated and functionally verified by culture‐dependent techniques, high‐throughput sequencing, and pot experiments. Pepper and eggplant rotations resulted in eight and one rotation‐unique antagonistic core taxa out of 12 507 microbial taxa, respectively. These nine antagonistic taxa were retained the following year and significantly decreased banana wilt disease incidence via legacy effects, although the cultivated strains were exclusively of the genera Bacillus and Pseudomonas. The fermentation broth and volatiles of these two taxa showed strong antagonistic activity, and pot experiments demonstrated high suppression of wilt disease and significant promotion of banana growth. Our study provides a mechanistic understanding of the identification of rotation crop‐unique antagonistic taxa and highlights the importance of targeted cultivation of beneficial microorganisms for optimizing crop rotation‐based scenarios in support of banana agriculture sustainability.

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Banana Fusarium wilt-suppressive soils are effective against pathogen invasion, yet soil physicochemical factors responsible for conducive or suppressive behavior have not been reported. Here, we investigated the changes in banana biomass, disease incidence (DI), soil culturable microbes and physicochemical properties by incorporating pepper and banana residues into conducive and suppressive soils. Before the incorporation of any residues, the suppressive soil significantly increased banana biomass and decreased DI compared to the conducive soil. The biomass of the suppressive soil was significantly higher than that of the conducive soil after the incorporation of either pepper or banana residues. Compared with the control (CK), the incorporation of pepper residues to both soils significantly reduced DI, while banana residues had the opposite effect. Additionally, both conducive and suppressive soils supplemented with pepper residues significantly reduced the amounts of culturable Fusarium oxysporum and increased the amounts of beneficial Pseudomonas and Bacillus. The pepper residue extracts significantly inhibited the growth of F. oxysporum mycelium. Soil alkali-hydrolyzable nitrogen (AN) responded most strongly to residue application to suppressive soil. The AN factor was significantly and positively correlated with banana biomass; however, there was no direct and significant negative correlation with DI. Further analysis of the results showed that elevated AN content could stimulate the amounts of culturable Bacillus in the soil, and Bacillus antagonized the proliferation of pathogen and thus indirectly and effectively reduced banana DI. In conclusion, soil AN content can indirectly improve the disease suppression ability of pepper-residue-mediated suppressive soil by manipulating the soil microbiome.