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Rice spikelet rot disease (RSRD) caused by Fusarium proliferatumseriously reduces rice yield and produces mycotoxins that threaten human health. The root symbiotic endophytic fungus Phomopsis liquidambarisreduces RSRD incidence and fumonisins accumulation in grain by 21.5 and 9.3%, respectively, while the mechanism of disease resistance remains largely elusive. Here, we found that B3 significantly reduced the abundance of pathogen from 79.91 to 2.84% and considerably enriched resistant microbes Pseudomonasand Proteobacteriain the spikelet microbial community. Further study revealed that B3 altered the metabolites of spikelets, especially hordenine and l-aspartic acid, which played a key role in reshaping the microbiome and supporting the growth of the functional core microbe Pseudomonas, and inhibited the pathogen growth and mycotoxin production. This study provided a feasibility of regulating the function of aboveground microbial communities by manipulating plant subsurface tissues to control disease and mycotoxin pollutants in agricultural production.

Plant-associated microbiomes play important roles in plant health and productivity. However, despite fruits being directly linked to plant productivity, little is known about the microbiomes of fruits and their potential association with fruit health. Here, by integrating 16S rRNA gene, ITS high-throughput sequencing data, and microbiological culturable approaches, we reported that roots and fruits (pods) of peanut, a typical plant that bears fruits underground, recruit different bacterial and fungal communities independently of cropping conditions and that the incidence of pod disease under monocropping conditions is attributed to the depletion of Bacillusgenus and enrichment of Aspergillusgenus in geocarposphere. On this basis, we constructed a synthetic community (SynCom) consisting of three Bacillusstrains from geocarposphere soil under rotation conditions with high culturable abundance. Comparative transcriptome, microbiome profiling, and plant phytohormone signaling analysis reveal that the SynCom exhibited more effective Aspergillusgrowth inhibition and pod disease control than individual strain, which was underpinned by a combination of molecular mechanisms related to fungal cell proliferation interference, mycotoxins biosynthesis impairment, and jasmonic acid–mediated plant immunity activation. Overall, our results reveal the filter effect of plant organs on the microbiome and that depletion of key protective microbial community promotes the fruit disease incidence.