Stomatal width and vascular bundle anatomy govern foliar uptake and phloem transport of atmospheric Pb in wheat

Abstract

Foliar uptake of atmospheric particulate matter-bound lead (APM-Pb) is a primary pathway for Pb accumulation in wheat grains. However, the dynamic mechanisms governing stomatal uptake of APM-Pb and its subsequent translocation to grains remain unclear. Short and long-term hydroponic experiments using low and high Pb-accumulating wheat cultivars (LW and HW) verified that open stomata are crucial for APM-Pb uptake and translocation to spikes, particularly for submicron APM-Pb (< 1 μm). Wider stomata in HW contributed more to flag leaf Pb accumulation (85.24%) than in LW (26.39%). Fluorescence and TEM-EDX analyses revealed that submicron APM-Pb entered stomatal guard cells on the adaxial surface and transferred to vascular bundles and the abaxial surface within 6 h. Following foliar uptake of APM-Pb, grain Pb accumulation rates exhibited an “N-shaped” trajectory, with a significant cultivar difference only at the milky stage (FS2), when the rate in HW was 3.03-fold that in LW. At FS2, node 1 and rachis restricted Pb translocation to grains. Pb concentrations in LW phloem sap were 7.35- and 5.34-fold lower than in HW at node 1 and the rachis, suppressing transport to grains while promoting allocation to roots. Larger transit (TVB) and diffuse vascular bundle (DVB) areas in LW node 1 promoted Pb retention, while smaller nodal (NVB) and intermediate vascular bundle (IVB) areas in LW rachis limited phloem transport to grain. These findings elucidate the mechanisms of APM-Pb from stomata uptake to translocation into grains and identify key anatomical targets for breeding low-Pb wheat cultivars in contaminated areas.