The contributions of apoplastic, symplastic and gas phase pathways for water transport outside the bundle sheath in leaves

Abstract

Water movement from the xylem to stomata is poorly understood. There is still no consensus about whether apoplastic or symplastic pathways are more important, and recent work suggests vapour diffusion may also play a role. The objective of this study was to estimate the proportions of hydraulic conductance outside the bundle sheath contributed by apoplastic, symplastic and gas phase pathways, using a novel analytical framework based on measurable anatomical and biophysical parameters. The calculations presented here suggest that apoplastic pathways provide the majority of conductance outside the bundle sheath under most conditions, whereas symplastic pathways contribute only a small proportion. The contributions of apoplastic and gas phase pathways vary depending on several critical but poorly known or highly variable parameters namely, the effective Poiseuille radius for apoplastic bulk flow, the thickness of cell walls and vertical temperature gradients within the leaf. The gas phase conductance should increase strongly as the leaf centre becomes warmer than the epidermis - providing up to 44% of vertical water transport for a temperature gradient of 0.2 K. These results may help to explain how leaf water transport is influenced by light absorption, temperature and differences in leaf anatomy among species.

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

“…Eijkel and Van Den Berg (2005) note that "friction is seen to increase from the macroscopic [continuum-derived] value when the separation between two surfaces becomes less than, roughly, ten molecular layers," or approximately 3 nm in this case. This is identical to the low end of the range estimated by Buckley (2015) for the diameter of channels for water flow created by spaces between adjacent microfibrils or bundles of microfibrils in the apoplast (3-20 nm), based on published measurements of cell wall microstructure (McCann et al, 1990;Fleischer et al, 1999;Fahlén and Salmén, 2005;Kennedy et al, 2007), which suggests that the continuum approximation is probably reasonable for apoplastic transport.…”

“…Apoplastic tracer studies (Canny, 1986) and the discovery of aquaporins (Agre et al, 1993;Chrispeels and Agre 1994) have promoted the view in recent years that transmembrane flow may dominate outside-xylem transport (Tyree et al, 1981(Tyree et al, , 1999Sack and Tyree, 2005), at least in the light, when aquaporins may be activated (Cochard et al, 2007). However, a theoretical study by Buckley (2015) that used membrane permeability values from published studies carried out on illuminated leaves concluded that apoplastic transport should dominate. MOFLO extends upon that study and similarly predicted that that apoplastic bulk flow contributes the majority of K ox (68% on average across species), thus dominating both transmembrane and gas-phase pathways under most conditions.…”

“…The framework developed by Buckley (2015) included a term for diffusive resistance across the cellular interior (transcellular resistance) in series with transmembrane resistance. Further thought and discussions with colleagues led us to conclude that any water transport across the cellular interior probably occurs mostly by bulk flow, provided that the flow area consists of channels much greater than the 0.31-nm lattice spacing of water.…”

“…List of parameters Variables and parameters referred to in this study, other than leaf anatomical parameters (Table IV) or unknown parameters (Table III) the consequences of these features for stomatal regulation (Meidner, 1976;Tyree and Yianoulis, 1980). More recent work has led to new insights, as well as new questions, about the nature and role of vaporphase water transport within the leaf, highlighting the need to better represent the anatomical structure of the mesophyll and surrounding airspaces in models (Rockwell et al, 2014;Buckley, 2015). The latter study made steps toward a more anatomically explicit model of leaf water flow and presented an analysis of the effects of epidermal and mesophyll anatomy on partitioning of flow among apoplastic, symplastic, and gas-phase transport modes.…”

“…A new approach was needed to refine and test hypotheses for the influence of anatomy on water flow outside the xylem. The objective of this study was to test hypothesized relationships between leaf anatomy and outside-xylem water transport by extending the framework of Buckley (2015) to create a new, spatially explicit model of outsidexylem water transport, MOFLO (mesophyll and outsidexylem flow), that includes all leaf tissues, including BS and BSEs. MOFLO computes K ox and its BS and outside-BS components (K b and K ob , respectively) by simulating steady-state water transport outside the xylem in an areole (the smallest region of a leaf bounded by minor veins).…”