What determines leaf hydraulic decline to dehydration? A novel method for partitioning xylem and outside-xylem hydraulic vulnerability

Background/Question/Methods

The decline in the leaf hydraulic conductance (K_leaf; the capacity for water flow through the leaf per pressure driving force) with dehydration has potential impacts on photosynthetic rate and whole plant growth for plants in moist soil and during drought. Previous studies have shown that K_leaf declines as leaf water potential becomes increasingly negative, but unlike in stems, a strong decline is observed even with mild dehydration. While this decline has been typically attributed to cavitation occurring in leaf veins, recent studies have shown aquaporin deactivation and/or cell shrinkage in the outside xylem pathways can also play an important role. However, no studies have yet characterized vulnerability responses of the xylem and outside-xylem pathways and their respective impacts on K_leaf. We hypothesized that outside-xylem hydraulic conductance (K_ox) decline in leaf dehydration is substantial, that it drives K_leaf decline under mild dehydration, and that it correlates with other aspects of leaf structure and drought tolerance, such as leaf shrinkage and osmotic potential at full turgor and turgor loss point. We developed a new method to measure xylem hydraulic conductance (K_x) as the leaf dehydrates on the bench. Briefly, leaf minor veins are cut under water for leaves of a range of water potentials, placed in a vacuum chamber connected by tubing to a water source on a balance, and K_x is determined as the slope of flow rate against pressure determined for a range of levels of partial vacuum. K_x vulnerability curves were obtained by plotting K_x against initial leaf water potential for six diverse species ranging in their drought tolerance. K_ox vulnerability curves were determined from the K_leaf and K_x vulnerability curves (because 1 / K_leaf = 1/ K_x + 1/ K_ox).  

Results/Conclusions

In all species the outside-xylem pathways played a much stronger role in shaping K_leaf vulnerability than xylem pathways. The decline of K_ox correlated across species with shrinkage of leaves during dehydration and with osmotic potential. Species with higher resistances in their outside xylem pathways in fact showed lower vulnerability to K_leaf dehydration because the decline of K_ox causes an increasing bottleneck in leaf water transport, protecting the xylem from reaching air-seeding pressures and thus reducing K_x decline. This study shows for the first time that in contrast to stems, for leaves, decline of hydraulic conductance with dehydration is less driven by xylem processes such as cavitation, but mainly driven by the vulnerability of the outside-xylem pathways.