Air spreading through wetted cellulose membranes: Implications for the safety function of hydraulic valves in plants

Park, Jooyoung; Go, Taesik; Ryu, Jeongeun; Lee, Sang Joon

doi:10.1103/physreve.100.032409

Cited by 13 publications

(11 citation statements)

References 37 publications

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“…Further research is clearly needed to investigate how gas diffusion may contribute to the very high gas solubility of xylem sap (Schenk et al, 2016), whether oversolubility occurs as a of result nanoconfined spaces such as pit membranes and cell walls (Coasne & Farrusseng, 2019; Ho et al, 2015; Pera‐Titus et al, 2009), how gas‐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).…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

Section: Vulnerability Segmentation May Reflect Hydraulic Segmentatmentioning

confidence: 99%

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

Guan

Pereira

McAdam

et al. 2021

Plant Cell & Environment

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Embolism spreading in dehydrating angiosperm xylem is driven by gas movement between embolized and sap-filled conduits. Here we examine how the proximity to pre-existing embolism and hydraulic segmentation affect embolism propagation.Based on the optical method, we compare xylem embolism resistance between detached leaves and leaves attached to branches, and between intact leaves and leaves with cut minor veins, for six species. Embolism resistance of detached leaves was significantly lower than that of leaves attached to stems, except for two species, with all vessels ending in their petioles. Cutting of minor veins showed limited embolism spreading in minor veins near the cuts prior to major veins. Moreover, despite strong agreement in the overall embolism resistance of detached leaves between the optical and pneumatic method, minor differences were observed during early stages of embolism formation. We conclude that embolism resistance may represent a relative trait due to an open-xylem artefact, with embolism spreading possibly affected by the proximity and connectivity to pre-existing embolism as a gas source, while hydraulic segmentation prevents such artefact. Since embolism formation may not rely on a certain pressure difference threshold between functional and embolized conduits, we speculate that embolism is facilitated by pressure-driven gas diffusion across pit membranes.bordered pits, drought stress, optical method, pneumatic method, vessel networkXylem sap in plants is frequently transported under negative pressure (Dixon & Joly, 1895;. Under conditions of low soil water content and/or high transpiration rates, the tensile force of xylem sap may increase considerably, which could lead to interruption of water transport in tracheary elements by large gas bubbles (embolism). Understanding the frequency and mechanism behind embolism formation in plant species is important because the amount of embolized conduits may affect the transport of xylem sap, and therefore photosynthesis (

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Section: Discussionmentioning

confidence: 99%

Section: Vulnerability Segmentation May Reflect Hydraulic Segmentatmentioning

confidence: 99%

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

Guan

Pereira

McAdam

et al. 2021

Plant Cell & Environment

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“…To summarize that hypothesis briefly, gas penetrating from embolized conduits into pit membranes of sap‐filled conduits may snap off nanobubbles inside confined, lipid‐coated pore spaces, resulting in the creation of lipid‐coated nanobubbles (Figure 5), which have in fact been found and visualized in xylem sap (Schenk et al ., 2017). The key to this hypothesis is that both the low dynamic surface tension of lipids and the snapping off of bubbles at pore constrictions inside fibrous pit membranes would limit bubble sizes (Park et al ., 2019) and keep them below a critical threshold that prevents bubble expansion into embolism (Schenk et al ., 2015; Schenk et al ., 2017). This process could happen under normal xylem water potentials and would allow xylem to operate without spreading embolisms via air seeding from gas‐filled conduits.…”

Section: Discussionmentioning

confidence: 99%

Lipids in xylem sap of woody plants across the angiosperm phylogeny

et al. 2021

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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 Laurus nobilis were imaged using transmission electron microscopy and confocal microscopy. Xylem sap contained the galactolipids di-and monogalactosyldiacylglycerol, as well as all common plant phospholipids, but only traces of sulfolipids, with total lipid concentrations in extracted sap ranging from 0.18 to 0.63 nmol ml À1 across all seven species. Contamination of extracted sap from lipids in cut living cells was found to be negligible. Lipid composition of sap was compared with wood in two species and was largely similar, suggesting that sap lipids, including galactolipids, originate from cell content of living vessels. Seasonal changes in lipid composition of sap were observed for one species. Lipid layers coated all lumen-facing vessel surfaces of L. nobilis, and lipids were highly concentrated in inter-vessel pits. The findings suggest that apoplastic, amphiphilic xylem lipids are a universal feature of angiosperms. The findings require a reinterpretation of the cohesion-tension theory of water transport to account for the effects of apoplastic lipids on dynamic surface tension and hydraulic conductance in xylem.

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“…Third, it is also possible that drought-induced embolism spreading does not occur via mass flow of air-water menisci across intervessel pit membranes, as suggested by the air-seeding hypothesis. The discovery of surfactant-coated nanobubbles in xylem sap provides a complementary mechanism of the mass flow of gas, and highlights the importance of amphiphilic, insoluble lipids associated with pit membranes, and bubble snap-off by pore constrictions (Schenk et al, 2015, Schenk et al, 2021Kaack et al, 2019;Park et al, 2019). Moreover, diffusion of gas molecules between an embolised and an adjacent vessel could represent an additional way in which gas entry could trigger embolism formation (Guan et al, 2021), which might be largely dependent on R MIN_mean and less so on R MIN_max .…”

Section: The Most Narrow Pore Constriction Becomes Strongly Reduced In Size With Increasing Pit Membrane Thicknessmentioning

confidence: 99%

Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms

et al. 2021

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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.Pore constrictions provide a mechanistic explanation for why pit membrane thickness determines embolism resistance, which suggests that hydraulic safety can be uncoupled from hydraulic efficiency. Although embolism spreading remains puzzling and encompasses more than pore constriction sizes, angiosperms are unlikely to have leaky pit membranes, which enables tensile transport of water.

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Air spreading through wetted cellulose membranes: Implications for the safety function of hydraulic valves in plants

Cited by 13 publications

References 37 publications

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

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

Lipids in xylem sap of woody plants across the angiosperm phylogeny

Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms

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