Cell-specific–resolved coordination of mitochondrial metabolism and DNA damage responses underpins aluminium responses in plant roots

Aluminium (Al) toxicity is a major constraint on crop productivity in acidic soils (pH < 5.5), severely impairing root growth and function. While organic acid (OA)-mediated chelation and DNA damage response (DDR)-mediated control of cell division are recognized as key tolerance mechanisms, their integration at the cellular level remains poorly understood. Here, we employed Translating Ribosome Affinity Purification (TRAP) to achieve cell-type-specific gene expression profiling of Arabidopsis thaliana roots, enabling the dissection of molecular responses in whole roots, the quiescent centre, and cortical tissues under Al stress. Our results reveal a spatially resolved reprogramming in which mitochondrial metabolism, particularly tricarboxylic acid (TCA) cycle activity, is preferentially induced in differentiated tissues, whereas meristematic regions display limited metabolic adjustment. In parallel, genes associated with cell cycle regulation and DNA damage checkpoints exhibit pronounced, cell-type-dependent modulation, indicating a coordinated DDR-driven control of root growth dynamics. These findings uncover a previously underexplored functional interplay between mitochondrial metabolic pathways and DDR signaling in mediating intracellular Al detoxification. By linking metabolic reprogramming with cell cycle regulation in a spatially resolved manner, this study provides new mechanistic insights into plant tolerance to Al toxicity. Such knowledge advances our understanding of plant adaptation to hazardous soil conditions and offers potential targets for developing crops with enhanced resilience to Al stress.