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SUMMARY: Hydrogen sulfide (H2S) promotes plant tolerance against various environmental cues, and d‐cysteine desulfhydrase (DCD) is an enzymatic source of H2S to enhance abiotic stress resistance. However, the role of DCD‐mediated H2S production in root growth under abiotic stress remains to be further elucidated. Here, we report that DCD‐mediated H2S production alleviates osmotic stress‐mediated root growth inhibition by promoting auxin homeostasis. Osmotic stress up‐regulated DCD gene transcript and DCD protein levels and thus H2S production in roots. When subjected to osmotic stress, a dcd mutant showed more severe root growth inhibition, whereas the transgenic lines DCDox overexpressing DCD exhibited less sensitivity to osmotic stress in terms of longer root compared to the wild‐type. Moreover, osmotic stress inhibited root growth through repressing auxin signaling, whereas H2S treatment significantly alleviated osmotic stress‐mediated inhibition of auxin. Under osmotic stress, auxin accumulation was increased in DCDox but decreased in dcd mutant. H2S promoted auxin biosynthesis gene expression and auxin efflux carrier PIN‐FORMED 1 (PIN1) protein level under osmotic stress. Taken together, our results reveal that mannitol‐induced DCD and H2S in roots promote auxin homeostasis, contributing to alleviating the inhibition of root growth under osmotic stress. Significance Statement: Hydrogen sulfide (H2S) promotes plant tolerance against various environmental stress resistance. However, the role of H2S in root development under abiotic stress remains to be further elucidated. Here, we report that d‐cysteine desulfhydrase‐mediated H2S accumulation alleviates root growth inhibition under osmotic stress by promoting auxin homeostasis. [ABSTRACT FROM AUTHOR]