How does leaf anatomy influence water transport outside the xylem?
Leaf anatomy and leaf hydraulic conductance (Kleaf) vary greatly across species, but the links between the two remain largely unexplored. In particular, we know very little about the mechanism of variations in outside-xylem hydraulic conductance (Kox). We explored the role of leaf anatomy in Kox by creating a novel computational model of water flow beyond the xylem, parameterising this model with measurements of leaf anatomy across 14 species, and using the model to address several questions: (1) Where are the major resistances located outside the xylem (in which tissues, and in which type of flow pathways), and in particular, how much resistance is located in the bundle sheath (BS)? (2) How do bundle sheath extensions (BSEs) affect Kox? (3) How do other cell and tissue anatomical traits influence Kox and Kleaf? (4) Can these influences explain previously described correlations of anatomical traits with Kleaf? (5) What is the role of gas phase transport in determining Koxunder different temperature regimes?
Our results suggest the epidermis and BSEs are much more conductive than the mesophyll, mostly due to airspaces in the mesophyll, and that apoplastic pathways support a large majority of outside-xylem water transport. The gas phase contributes a significant minority of transport when large vertical temperature gradients occur. The contribution of the BS to outside-xylem resistance is large if the BS apoplast is suberized, but moderate or small otherwise. BSEs enhance Kox substantially; however, Kox is disproportionately higher in heterobaric species (which possess BSEs) than in homobaric species (which lack BSEs), indicating that other features that enhance Kox, such as vein length per unit leaf area (VLA), are correlated with the presence of BSEs. The increase in Kox with VLA results partly from reduced flow distance from the xylem to the epidermis, as previously predicted, but also from greater bundle sheath surface area per unit leaf area. Our results illuminate the mechanistic basis of Kox and Kleaf and identify targets for intensive study -- particularly the intrinsic hydraulic conductivity of cell walls and membranes, which we predict to have much greater than anticipated influence on leaf and plant water transport, and thus on ecological specialization.