Vacuolar sequestration and glandular trichome secretion underlie cultivar-dependent cadmium accumulation in tobacco

Cadmium (Cd) is a toxic element that poses significant health risks to humans. Tobacco smoke is a primary source of human Cd exposure, aside from dietary intake. However, the mechanisms governing Cd accumulation and translocation among tobacco cultivars remain insufficiently understood. This study initially screened the Cd accumulation potential of 83 cultivars grown in China. The results revealed that KY14, K326, Yunyan99, G28, and Basma1 had higher Cd translocation ability, while 47 cultivars including Maxopka had lower Cd translocation ability. It then comparatively studied vacuolar compartmentalization, cell wall binding, glandular trichome secretion, and Cd in mainstream smoke between two contrasting cultivars under 20 μM Cd stress. K326 exhibited weaker root retention due to lower thiols contents, reduced expression of tonoplast transporter genes, and decreased uronic acid, lignin, and phenylalanine ammonia-lyase activity, facilitating Cd translocation to leaves. K326 leaves showed higher secretory detoxification ability due to the enhancement of long-stalked glandular trichome, and thus had the capacity to accommodate more Cd. Conversely, Maxopka roots immobilized Cd through enhanced vacuolar sequestration and cell wall binding, limiting its translocation. Structural equation modeling further identified CAX2 , MTP1 , and LTP1 to be key regulators modulating Cd accumulation in leaves. Ultimately, Cd concentrations in mainstream smoke were markedly higher in K326 than in Maxopka. These results elucidate the mechanisms underlying varietal differences in Cd translocation and offer strategies for reducing Cd accumulation in crops and its entry into the food chain. • Smoking is a source of cadmium (Cd) exposure in human beings. • Cd translocation factor ranged from 0.12 to 1.51 among 83 tobacco cultivars. • K326 roots had weaker vacuolar compartmentalization and cell wall binding capacities. • K326 leaves demonstrated enhanced secretory glandular trichomes excretion capacities. • K326’s mainstream smoke contained 2.63 times more Cd than Maxopka.