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We identified a promising compound—4-MU, as a useful tool, to facilitate the drought tolerance of apple dwarfing rootstock by regulating rhizosphere microbial diversity and root architecture.The dwarfing rootstocks-mediated high-density apple orchard is becoming the main practice management. Currently, dwarfing rootstocks are widely used worldwide, but their shallow root system and drought sensitivity necessitate high irrigation requirements. Here, the root transcriptome and metabolome of dwarfing (M9-T337, a drought-sensitive rootstock) and vigorous rootstocks (Malus sieversii, a drought-tolerant species, is commonly used as a rootstock) showed that a coumarin derivative, 4-Methylumbelliferon (4-MU), was found to accumulate significantly in the roots of vigorous rootstock under drought condition. When exogenous 4-MU was applied to the roots of dwarfing rootstock under drought treatment, the plants displayed increased root biomass, higher root-to-shoot ratio, greater photosynthesis, and elevated water use efficiency. In addition, diversity and structure analysis of the rhizosphere soil microbial community demonstrated that 4-MU treatment increased the relative abundance of putatively beneficial bacteria and fungi. Of these, Pseudomonas, Bacillus, Streptomyces, and Chryseolineabacterial strains and Acremonium, Trichoderma, and Phomafungal strains known for root growth, or systemic resistance against drought stress, were significantly accumulated in the roots of dwarfing rootstock after 4-MU treatment under drought stress condition. Taken together, we identified a promising compound—4-MU, as a useful tool, to strengthen the drought tolerance of apple dwarfing rootstock.