Continuous monocultures alter the composition and function of root-associated microbiota, and thus compromise crop health and productivity. In comparison, little is known about how leaf-associated microbiota respond to continuous monocultures. Here, we profiled root and leaf-associated microbiota of peanut plants under monocropping and rotation conditions. Additionally, their protective effects against root pathogen Fusarium oxysporum and leaf pathogen Alternaria alstroemeriae were evaluated. We found that monocropping increased root and leaf disease severity. Meanwhile, the peanut growth and productivity were inhibited by monocropping. Microbiota analysis revealed that monocropping reduced rhizosphere microbial population and diversity, while increased leaf epiphytic microbial population and did not influence leaf epiphytic microbial diversity. Cropping conditions had a greater impact on the microbiota composition of leaf epiphytes than that of the rhizosphere. Moreover, in vitro and in vivo experiments, combined with correlation analyses showed that monocropping weakened the antagonistic activity of rhizosphere microbiota against F. oxysporum and root rot disease. This effect may be associated with the depletion of Bacillus sp. and Sphingomonas sp.. By contrast, leaf epiphytic microbiota under monocropping exhibited greater inhibition of A. alstroemeriae growth and leaf spot control. Together, our results demonstrated a differential response pattern of root and leaf-associated microbiota to continuous monocultures.
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