Lipids in xylem sap of woody plants across the angiosperm phylogeny

Abstract

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.

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

“…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 .…”

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).…”

Xylem Parenchyma—Role and Relevance in Wood Functioning in Trees

“…Recently, new agents called surfactants, which reduce the surface tension of water, have been identified to influence the internal flow within the xylem [ 153 , 154 , 155 ]. The presence of an artificial surfactant in the xylem sap strongly alters xylem vulnerability to cavitation in both conifer and angiosperm species [ 156 , 157 ].…”

“…The presence of an artificial surfactant in the xylem sap strongly alters xylem vulnerability to cavitation in both conifer and angiosperm species [ 156 , 157 ]. Furthermore, surfactants have been found in the xylem sap of woody representatives of major angiosperm clades [ 153 , 154 , 155 , 158 ]. In situ studies by Losso et al [ 159 ] on hydraulic safety in conifers ( Picea abies and Pinus mugo ) indicate that solutions with low surface tension cause higher vulnerability to drought-induced xylem embolism [ 159 ].…”

“…In situ studies by Losso et al [ 159 ] on hydraulic safety in conifers ( Picea abies and Pinus mugo ) indicate that solutions with low surface tension cause higher vulnerability to drought-induced xylem embolism [ 159 ]. In contrast, Schenk et al [ 153 , 154 , 155 ] hypothesised that insoluble lipid-based surfactants increase the hydraulic safety in angiosperms, mostly by coating hydrophobic surfaces and nanobubbles, and thereby keeping the latter below the critical size at which bubbles expand to form embolism [ 153 , 154 , 155 ]. A similar mechanism of surfactant action was observed in Populus nigra L., and it was suggested that woody tissue assimilates play a role in the synthesis of xylem surfactants, which is facilitated by VACs [ 160 ].…”