Stomatal closure of tomato under drought is driven by an increase in soil-root hydraulic resistance

The fundamental question as to what triggers stomatal closure during soil drying remains contentious. Thus, we urgently need to improve our understanding of stomatal response to water deficits in soil and atmosphere. Here, we investigated the role of soil-plant hydraulic conductance (K_sp ) on transpiration (E) and stomatal regulation. We used a root pressure chamber to measure the relation between E, leaf xylem water potential (ψ_leaf-x ) and soil water potential (ψ_soil ) in tomato. Additional measurements of ψ_leaf-x were performed with unpressurized plants. A soil-plant hydraulic model was used to simulate E(ψ_leaf-x ) for decreasing ψ_soil . In wet soils, E(ψ_leaf-x ) had a constant slope, while in dry soils, the slope decreased, with ψ_leaf-x rapidly and nonlinearly decreasing for moderate increases in E. The ψ_leaf-x measured in pressurized and unpressurized plants matched well, which indicates that the shoot hydraulic conductance did not decrease during soil drying and that the decrease in K_sp is caused by a decrease in soil-root conductance. The decrease of E matched well the onset of hydraulic nonlinearity. Our findings demonstrate that stomatal closure prevents the drop in ψ_leaf-x caused by a decrease in K_sp and elucidate a strong correlation between stomatal regulation and belowground hydraulic limitation.