Leaf hydraulic maze; Differential effect of ABA on vascular bundle-sheath, palisade, and spongy mesophyll controlling hydraulic conductance

Leaf hydraulic conductance (Kleaf) facilitates the movement of water for transpiration, enabling continual CO2 uptake while the plant maintains its water status. We hypothesized that bundle-sheath and mesophyll cells play key roles in regulating the radial flow of water out of the xylem under optimal and stress conditions. To examine that hypothesis, we generated transgenic Arabidopsis plants that were insensitive to abscisic acid (ABA) in their bundle sheath (BSabi) or mesophyll (MCabi) cells. Both BSabi and MCabi plants showed greater Kleaf and transpiration under optimal conditions. Yet, the stomatal apertures, stomatal indices and vein densities of the BSabi plants were similar to those of WT plants. MCabi plants had larger stomatal apertures, a higher stomatal index and greater vascular diameter and biomass, relative to the WT and BSabi. In response to xylem-fed ABA, both transgenic and WT plants reduced their Kleaf and transpiration. However, leaf water potential was reduced only in the WT. The membrane osmotic water permeability (Pf) of the WTs spongy mesophyll was higher than that of its palisade mesophyll. Moreover, only the spongy cells reduced their Pf in response to ABA. ABA-insensitive spongy mesophyll cells had a low Pf; whereas ABA-insensitive bundle-sheath cells had a higher Pf. Palisade cells maintained a low Pf at all ABA levels. ABA increased the symplastic water pathway, but its contribution to Kleaf was negligible. We suggest that the bundle sheath-spongy mesophyll pathway may control Kleaf to maintain steady-state conditions in the palisade cells and optimal whole-leaf water-use efficiency.