- Award ID(s):
- 1754850
- NSF-PAR ID:
- 10142216
- Date Published:
- Journal Name:
- IAWA Journal
- Volume:
- 40
- Issue:
- 4
- ISSN:
- 2294-1932
- Page Range / eLocation ID:
- 673 to 702
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract Pit membranes between xylem vessels play a major role in angiosperm water transport. Yet, their three‐dimensional (3D) structure as fibrous porous media remains unknown, largely due to technical challenges and sample preparation artefacts. Here, we applied a modelling approach based on thickness measurements of fresh and fully shrunken pit membranes of seven species. Pore constrictions were also investigated visually by perfusing fresh material with colloidal gold particles of known sizes. Based on a shrinkage model, fresh pit membranes showed tiny pore constrictions of ca. 20 nm, but a very high porosity (i.e. pore volume fraction) of on average 0.81. Perfusion experiments showed similar pore constrictions in fresh samples, well below 50 nm based on transmission electron microscopy. Drying caused a 50% shrinkage of pit membranes, resulting in much smaller pore constrictions. These findings suggest that pit membranes represent a mesoporous medium, with the pore space characterized by multiple constrictions. Constrictions are much smaller than previously assumed, but the pore volume is large and highly interconnected. Pores do not form highly tortuous, bent, or zigzagging pathways. These insights provide a novel view on pit membranes, which is essential to develop a mechanistic, 3D understanding of air‐seeding through this porous medium.
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Summary Embolism spreading in angiosperm xylem occurs via mesoporous pit membranes between vessels. Here, we investigate how the size of pore constrictions in pit membranes is related to pit membrane thickness and embolism resistance.
Pit membranes were modelled as multiple layers to investigate how pit membrane thickness and the number of intervessel pits per vessel determine pore constriction sizes, the probability of encountering large pores, and embolism resistance. These estimations were complemented by measurements of pit membrane thickness, embolism resistance, and number of intervessel pits per vessel in stem xylem (
n = 31, 31 and 20 species, respectively).The modelled constriction sizes in pit membranes decreased with increasing membrane thickness, explaining the measured relationship between pit membrane thickness and embolism resistance. The number of pits per vessel affected constriction size and embolism resistance much less than pit membrane thickness. Moreover, a strong relationship between modelled and measured embolism resistance was observed.
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One of the more surprising occurrences of bulk nanobubbles is in the sap inside the vascular transport system of flowering plants, the xylem. In plants, nanobubbles are subjected to negative pressure in the water and to large pressure fluctuations, sometimes encompassing pressure changes of several MPa over the course of a single day, as well as wide temperature fluctuations. Here, we review the evidence for nanobubbles in plants and for polar lipids that coat them, allowing nanobubbles to persist in this dynamic environment. The review addresses how the dynamic surface tension of polar lipid monolayers allows nanobubbles to avoid dissolution or unstable expansion under negative liquid pressure. In addition, we discuss theoretical considerations about the formation of lipid-coated nanobubbles in plants from gas-filled spaces in the xylem and the role of mesoporous fibrous pit membranes between xylem conduits in creating the bubbles, driven by the pressure gradient between the gas and liquid phase. We discuss the role of surface charges in preventing nanobubble coalescence, and conclude by addressing a number of open questions about nanobubbles in plants.more » « less
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Abstract In previous research, xylem sap of angiosperms has been found to include low concentrations of nanoparticles and polar lipids. A major goal of this study was to test predictions arising from the hypothesis that the nanoparticles consist largely of polar lipids from the original cell content of vessel elements. These predictions included that polar lipid and nanoparticle concentrations would be correlated, that they both do not pass through pit membranes and that they do not vary seasonally because they originate from living vessel element cells. We collected xylem sap of six temperate angiosperm species over the whole year to consider seasonal variation. Concentrations of nanoparticles and lipids in xylem sap and contamination control samples were measured with a NanoSight device and mass spectrometry. We found that the concentration of nanoparticles and polar lipids was (i) diluted when an increasing amount of sap was extracted, (ii) significantly correlated to each other for three species, (iii) affected by vessel anatomy, (iv) very low and largely different in chemical composition from contamination controls and (v) hardly variable among seasons. Moreover, there was a minor freezing–thawing effect with respect to nanoparticle amount and size. Xylem sap lipids included polar galactolipids and phospholipids in all species and neutral triacylglycerols in two species. These findings support the predictions and, by implication, the underlying hypothesis that nanoparticles in xylem sap consist of polar lipids from the original cell content of living vessel element cells. Further research is needed to examine the formation and stability of nanoparticles concerning lipid composition and multiphase interactions among gas, liquid and solid phases in xylem conduits of living plants.