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Summary: In plants under drought stress, sugar content in roots increases, which is important for drought resistance. However, the molecular mechanisms for controlling the sugar content in roots during response to drought remain elusive. Here, we found that the MdDOF3‐MdHT1.2 module‐mediated glucose influx into the root is essential for drought resistance in apple (Malus × domestica). Drought induced glucose uptake from the rhizosphere and up‐regulated the transcription of hexose transporter MdHT1.2. Compared with the wild‐type plants, overexpression of MdHT1.2 promoted glucose uptake from the rhizosphere, thereby facilitating sugar accumulation in root and enhancing drought resistance, whereas silenced plants showed the opposite phenotype. Furthermore, ATAC‐seq, RNA‐seq and biochemical analysis demonstrated that MdDOF3 directly bound to the promoter of MdHT1.2 and was strongly up‐regulated under drought. Overexpression of MdDOF3 in roots improved MdHT1.2‐mediated glucose transport capacity and enhanced plant resistance to drought, but MdDOF3‐RNAihr apple plants showed the opposite phenotype. Moreover, overexpression of MdDOF3 in roots did not attenuate drought sensitivity in MdHT1.2‐RNAi plants, which was correlated with a lower glucose uptake capacity and glucose content in root. Collectively, our findings deciphered the molecular mechanism through which glucose uptake from the rhizosphere is mediated by MdDOF3‐MdHT1.2, which acts to modulate sugar content in root and promote drought resistance. [ABSTRACT FROM AUTHOR]