Hydraulic Analysis of Water Flow through Leaves of Sugar Maple and Red Oak

Abstract

Leaves constitute a substantial fraction of the total resistance to water flow through plants. A key question is how hydraulic resistance within the leaf is distributed among petiole, major veins, minor veins, and the pathways downstream of the veins. We partitioned the leaf hydraulic resistance (R leaf ) for sugar maple (Acer saccharum) and red oak (Quercus rubra) by measuring the resistance to water flow through leaves before and after cutting specific vein orders. Simulations using an electronic circuit analog with resistors arranged in a hierarchical reticulate network justified the partitioning of total R leaf into component additive resistances. On average 64% and 74% of the R leaf was situated within the leaf xylem for sugar maple and red oak, respectively. Substantial resistance-32% and 49%-was in the minor venation, 18% and 21% in the major venation, and 14% and 4% in the petiole. The large number of parallel paths (i.e. a large transfer surface) for water leaving the minor veins through the bundle sheath and out of the leaf resulted in the pathways outside the venation comprising only 36% and 26% of R leaf . Changing leaf temperature during measurement of R leaf for intact leaves resulted in a temperature response beyond that expected from changes in viscosity. The extra response was not found for leaves with veins cut, indicating that water crosses cell membranes after it leaves the xylem. The large proportion of resistance in the venation can explain why stomata respond to leaf xylem damage and cavitation. The hydraulic importance of the leaf vein system suggests that the diversity of vein system architectures observed in angiosperms may reflect variation in whole-leaf hydraulic capacity.Water flow through the leaf is one of the most important but least understood components of the whole-plant hydraulic system. The leaf hydraulic resistance (R leaf ) constitutes a significant hydraulic bottleneck, correlates with leaf structure, and apparently constrains gas exchange (Tyree and Zimmermann, 2002;Sack et al., 2003b;Sack and Tyree, 2004). R leaf is an aggregate measure; once past the petiole, water flows through a reticulate network of veins, across the bundle sheath cells, and through or around mesophyll cells before evaporation and diffusion from the stomata (Esau, 1965). Recent work has focused primarily on measurement of R leaf and its functional correlates. Few studies have attempted to determine quantitatively how the various components of the water flow pathway through the leaf contribute to its total resistance.Partitioning of R leaf is a crucial step for understanding leaf hydraulic design. Cavitation in the leaf vein xylem can substantially increase R leaf , as can physical damage to major veins; both drive reductions of leaf water potential and gas exchange Nardini et al., 2001Cochard et al., 2002;Huve et al., 2002;Sack et al., 2003a). These observations suggest that a large proportion of R leaf is situated in the veins. However, a number of studies have reported that most of the leaf resista...

Viewing leaf structure and evolution from a hydraulic perspective

“…A possible involvement of aquaporins in modulating the extra-xylary hydraulic resistance of leaves has also been demonstrated (Cochard et al 2007;Kaldenhoff et al 2008;Heinen et al 2009). The bulk of evidence indicates that the resistance to water flow through leaves acclimated to light is split evenly between the leaf xylem network and the mesophyll apoplast (Sack et al 2004;Nardini et al 2005;Sack and Holbrook 2006).…”

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

“…Cuts were made between about 95% of tertiary veins, yielding 5 to 33 cuts mm 22 depending on sample size (larger leaves have their major veins spaced farther apart, so that fewer but longer cuts were made; Sack et al, 2012;. These cuts were enough for water to move directly out of minor veins and not through outside-xylem pathways (Sack et al, 2004;Nardini et al, 2005). After minor veins were cut, leaves were connected by tubing to a water source on a balance and placed in a vacuum chamber.…”

“…Representing circular bands of tissue as single nodes is equivalent to assuming that the areole is radially symmetrical. Areole radius was computed from VLA following previous models that considered the vein system as a square grid with unit edge length x; this implies that each areole is uniquely associated with a vein length of 2x and an area of x 2 , so VLA = 2x/x 2 = 2/x (Cochard et al, 2004;Sack et al, 2004). Equating this area with that of a circle of radius, r areole (p 3 r 2 areole = x 2 ), gives r areole = x/p 0.5 = 2/(VLA 3 p 0.5 ).…”

Partitioning hydraulic resistance in Sorghum bicolor leaves reveals unique correlations with stomatal conductance during drought

“…Leaf resistance in dicot leaves has been previously partitioned into xylary and extra-xylary components that range widely across species; the relative proportion of these two resistances in leaves range from 26 to 80% of total leaf resistance (Martre et al 2001;Cochard et al 2004b;Sack et al 2004;. Across a range of species and environmental conditions, both xylary and extra-xylary resistance have been linked to maximum rates of gas exchange (Sack et al 2002;Sack and Frole 2006;Brodribb et al 2007), but the role of these two leaf resistances for regulating stomatal responses to decreasing soil moisture has not been investigated.…”