How Does Leaf Anatomy Influence Water Transport outside the Xylem?

Abstract

Leaves are arguably the most complex and important physicobiological systems in the ecosphere. Yet, water transport outside the leaf xylem remains poorly understood, despite its impacts on stomatal function and photosynthesis. We applied anatomical measurements from 14 diverse species to a novel model of water flow in an areole (the smallest region bounded by minor veins) to predict the impact of anatomical variation across species on outside-xylem hydraulic conductance (K ox ). Several predictions verified previous correlational studies: (1) vein length per unit area is the strongest anatomical determinant of K ox , due to effects on hydraulic pathlength and bundle sheath (BS) surface area; (2) palisade mesophyll remains well hydrated in hypostomatous species, which may benefit photosynthesis, (3) BS extensions enhance K ox ; and (4) the upper and lower epidermis are hydraulically sequestered from one another despite their proximity. Our findings also provided novel insights: (5) the BS contributes a minority of outside-xylem resistance; (6) vapor transport contributes up to two-thirds of K ox ; (7) K ox is strongly enhanced by the proximity of veins to lower epidermis; and (8) K ox is strongly influenced by spongy mesophyll anatomy, decreasing with protoplast size and increasing with airspace fraction and cell wall thickness. Correlations between anatomy and K ox across species sometimes diverged from predicted causal effects, demonstrating the need for integrative models to resolve causation. For example, (9) K ox was enhanced far more in heterobaric species than predicted by their having BS extensions. Our approach provides detailed insights into the role of anatomical variation in leaf function.

The Sites of Evaporation within Leaves

“…Cowan (1977) predicted that vertical T gradients between the illuminated upper mesophyll and the cooler lower epidermis could drive evaporation and vapor transport toward the lower epidermis, which Sheriff (1979) corroborated by observing condensation on the lower epidermis in transpiring leaves when the epidermis was cooler than the leaf center. More recent simulations by Rockwell et al (2014), Buckley (2015), and Buckley et al (2015) supported the notion that even small vertical T gradients (on the order of 0.1°C) between illuminated palisade mesophyll and transpiring epidermis could drive substantial vapor transport toward the lower epidermis. Together, these studies suggested that the mesophyll may, in fact, support a great deal of evaporation in illuminated leaves.…”

“…We tested the impact of these assumptions by repeating simulations using different assumed degrees of suppression of BS apoplastic transport by cell wall suberization or lignification (from 0% to 100% suppression), different values for R a (1.5-4.5 nm), and different values of P m (8-200 mm s 21 ), which accounts for differences in the role of aquaporins. Background, justification, and discussion of these parameter defaults and ranges can be found in the report of Buckley et al (2015). Unless noted otherwise, all simulations were repeated for the 14 species listed in Table III, with results averaged across species, and environmental and gas-exchange parameters were set at the following default values: PPFD = 1,500 mmol m 22 s 21 incident on the adaxial surface (we assumed PPFD = 0 at the abaxial surface), T air = 25°C, w air = 15 mmol mol 21 (0.015 mol mol 21 ), g s = 0.4 mol m 22 s 21 , and g bw = 3 mol m 22 s 21 .…”

“…As we recently found that these parameters can strongly influence the partitioning of water flow among transport modes (apoplastic, transmembrane and transcellular, and gas phase; Buckley et al, 2015), we tested whether variation in these parameters also affected where evaporation is predicted to occur within the leaf. The model predicted that any change in these parameters that enhanced liquid phase transport relative to vapor transport (i.e., increases in P m or R a ) increased the percentage of total evaporation that occurs from the epidermis and reduced evaporation from locations closer to the xylem (Fig.…”

“…For several biophysical and anatomical parameters whose values are not well characterized, we assumed similar default values to those used for the simulations presented by Buckley et al (2015); that is, we reduced cell wall thicknesses measured by light microscopy by 80%, assumed that BS apoplastic transport was not at all suppressed by suberization or lignification, assumed that horizontal connectivity among palisade mesophyll cells was limited to the thickness of cell walls, assumed that the R a was 3 nm, and assumed that the P m was 40 mm s 21 . We tested the impact of these assumptions by repeating simulations using different assumed degrees of suppression of BS apoplastic transport by cell wall suberization or lignification (from 0% to 100% suppression), different values for R a (1.5-4.5 nm), and different values of P m (8-200 mm s 21 ), which accounts for differences in the role of aquaporins.…”

“…However, most previous studies of the evaporating sites have been confined to single species or have used generic models that are not suitable for exploring the effects of species variation in leaf internal anatomy. To overcome these limitations, we used an anatomically and biophysically explicit model of coupled heat and water transport outside the xylem, MOFLO 2.0 (an extension of the MOFLO model; Buckley et al, 2015), parameterized for 14 diverse angiosperm species (Table III), to analyze the sites of evaporation within leaves in relation to anatomy and environmental conditions. Our objectives were to map the distribution of net evaporation across tissues within a single leaf areole, to determine how that distribution is affected by leaf anatomy and environmental conditions, and to explore the implications of the evaporating sites for measurements and inferences across plant physiology.…”