Dynamic surface tension of xylem sap lipids

Abstract

The surface tension of xylem sap has been traditionally assumed to be close to that of the pure water because decreasing surface tension is thought to increase vulnerability to air seeding and embolism. However, xylem sap contains insoluble lipid-based surfactants, which also coat vessel and pit membrane surfaces, where gas bubbles can enter xylem under negative pressure in the process known as air seeding. Because of the insolubility of amphiphilic lipids, the surface tension influencing air seeding in pit pores is not the equilibrium surface tension of extracted bulk sap but the local surface tension at gas–liquid interfaces, which depends dynamically on the local concentration of lipids per surface area. To estimate the dynamic surface tension in lipid layers that line surfaces in the xylem apoplast, we studied the time-dependent and surface area-regulated surface tensions of apoplastic lipids extracted from xylem sap of four woody angiosperm plants using constrained drop surfactometry. Xylem lipids were found to demonstrate potent surface activity, with surface tensions reaching an equilibrium at ~25 mN m-1 and varying between a minimum of 19 mN m-1 and a maximum of 68 mN m-1 when changing the surface area between 50 and 160% around the equilibrium surface area. It is concluded that xylem lipid films in natural conditions most likely range from nonequilibrium metastable conditions of a supersaturated compression state to an undersaturated expansion state, depending on the local surface areas of gas–liquid interfaces. Together with findings that maximum pore constrictions in angiosperm pit membranes are much smaller than previously assumed, low dynamic surface tension in xylem turns out to be entirely compatible with the cohesion–tension and air-seeding theories, as well as with the existence of lipid-coated nanobubbles in xylem sap, and with the range of vulnerabilities to embolism observed in plants.

Lipids in xylem sap of woody plants across the angiosperm phylogeny

“…However, layers of phospho‐ and galactolipids on conduit surfaces and in pit membranes (Figure 4) will reduce the surface tension at gas–water interfaces substantially below that of pure water, with the dynamic surface tension depending on the local concentration of lipids at the surface (Zuo et al ., 2004; Kwan and Borden, 2010). Measurements of xylem lipids extracted from four of the species studied in this paper found average equilibrium surface tensions to be about 25 mN m −1 , roughly a third of the surface tension of pure water (Yang et al ., 2020). These findings are entirely compatible with the air seeding pressure required to force air through pore constrictions in angiosperm pit membranes.…”

No gas source, no problem: Proximity to pre‐existing embolism and segmentation affect embolism spreading in angiosperm xylem by gas diffusion

“…xylem sap interfaces are affected by the dynamic surface tension of xylem sap lipids (Schenk et al, 2020;Yang, M Michaud, Jansen, Schenk, & Zuo, 2020) and how surfactant-coated nanobubbles affect the gas concentration of xylem sap and embolism formation (Jansen et al, 2018;Park, Go, Ryu, & Lee, 2019;Schenk et al, 2017;Schenk, Steppe, & Jansen, 2015).…”

An increase in xylem embolism resistance of grapevine leaves during the growing season is coordinated with stomatal regulation, turgor loss point and intervessel pit membranes

“…How seasonal changes in electron density of pit membranes (Fig. 8) affect embolism resistance is currently unknown and would require further research on the functional role of xylem sap lipids (Schenk et al, 2015(Schenk et al, , 2018Yang et al, 2020).…”