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.
Lipids have been observed attached to lumen‐facing surfaces of mature xylem conduits of several plant species, but there has been little research on their functions or effects on water transport, and only one lipidomic study of the xylem apoplast. Therefore, we conducted lipidomic analyses of xylem sap from woody stems of seven plants representing six major angiosperm clades, including basal magnoliids, monocots and eudicots, to characterize and quantify phospholipids, galactolipids and sulfolipids in sap using mass spectrometry. Locations of lipids in vessels of
- NSF-PAR ID:
- 10452593
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 105
- Issue:
- 6
- ISSN:
- 0960-7412
- Page Range / eLocation ID:
- p. 1477-1494
- 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 The resistance of xylem conduits to embolism is a major factor defining drought tolerance and can set the distributional limits of species across rainfall gradients. Recent work suggests that the proximity of vessels to neighbors increases the vulnerability of a conduit. We therefore investigated whether the relative vessel area of xylem correlates with intra- and inter-generic variation in xylem embolism resistance in species pairs or triplets from the genera Acer, Cinnamomum, Ilex, Quercus and Persea, adapted to environments differing in aridity. We used the optical vulnerability method to assess embolism resistance in stems and conducted anatomical measurements on the xylem in which embolism resistance was quantified. Vessel lumen fraction (VLF) correlated with xylem embolism resistance across and within genera. A low VLF likely increases the resistance to gas movement between conduits, by diffusion or advection, whereas a high VLF enhances gas transport thorough increased conduit-to-conduit connectivity and reduced distances between conduits and therefore the likelihood of embolism propagation. We suggest that the rate of gas movement due to local pressure differences and xylem network connectivity is a central driver of embolism propagation in angiosperm vessels.
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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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Premise Belowground functional traits play a significant role in determining plant water‐use strategies and plant performance, but we lack data on root traits across communities, particularly in the tropical savanna biome, where vegetation dynamics are hypothesized to be strongly driven by tree–grass functional differences in water use.
Methods We grew seedlings of 21 tree and 18 grass species (
N = 5 individuals per species) from the southern African savanna biome under greenhouse conditions and collected fine‐root segments from plants for histological analysis. We identified and measured xylem vessels in 539 individual root cross sections. We then quantified six root vascular anatomy traits and tested them for phylogenetic signals and tree–grass differences in trait values associated with vessel size, number, and hydraulic conductivity.Results Grass roots had larger root xylem vessels than trees, a higher proportion of their root cross‐sectional area comprised vessels, and they had higher estimated axial conductivities than trees, while trees had a higher number of vessels per root cross‐sectional area than grasses did. We found evidence of associations between trait values and phylogenetic relatedness in most of these traits across tree species, but not grasses.
Conclusions Our findings support the hypothesis that grass roots have higher water transport capacity than tree roots in terms of maximum axial conductivity, consistent with the observation that grasses are more “aggressive” water users than trees under conditions of high soil moisture availability. Our study identifies root functional traits that may drive differential responses of trees and grasses to soil moisture availability.
