Gas diffusion kinetics drive embolism spread in angiosperm xylem: evidence from flow-centrifuge experiments and modelling

Abstract

Understanding xylem embolism formation is challenging due to dynamic changes and multiphase interactions in conduits. If embolism spread involves gas movement in xylem, we hypothesise that it is affected by time. We measured hydraulic conductivity (Kh) in flow-centrifuge experiments over one hour at a given pressure and temperature for stem samples of three angiosperm species. Temporal changes in Kh at 5, 22, and 35 degrees C, and at various pressures were compared to modelled gas pressure changes in a recently embolised vessel in the centre of a centrifuge sample. Temporal changes in Kh at 22 degrees C showed maximum relative increases between 6% and 40%, and maximum decreases between 41% and 61% at low and high centrifugal speed, respectively. Logarithmic changes in Kh were species-specific, and most pronounced during the first 15 minutes. Embolism formation started near the edges of centrifuge samples and gradually increased at the centre. Moreover, measured decreases in Kh strongly correlated with modelled increases in gas concentration in a recently embolised vessel. Although embolism is mostly pressure-driven, our experimental and modelled data indicate that time, conduit characteristics, and temperature are involved due to their role in gas diffusion. Gas diffusion, however, does not cover the entire process of embolism spread.

Angiosperms follow a convex trade‐off to optimize hydraulic safety and efficiency

“…2a), we cannot discard the possibility that the velocity for changes in gas concentration, at a scale of seconds or minutes as determined by A p and T PM , could be important for embolism initiation. The mechanisms of embolism initiation are still largely unknown (Schenk et al, 2015;Kaack et al, 2021) and the mechanistic role of gas concentration is not clear, despite its correlation to embolism equilibration with the atmospheric pressure (Wang et al, 2015;Silva et al, 2023). Our model makes no assumption about the mechanism of embolism initiation, either via nucleation or rapid expansion of an existing nanobubble, and instead addresses the consequences of that rapidly expanding void as it turns into a large, gas-filled bubble.…”

Time-based shifts in xylem vulnerability curves of angiosperms based on the flow-centrifuge method

“…Experiment 1: Investigating temporal dynamics of hydraulic conductivity during one hour of spinning This experiment aimed to investigate the temporal variation in K h during 1 hour-long spin times. We specifically wanted to test whether the temporal dynamics of hydraulic conductivity for stem samples of Acer pseudoplatanus , Betula pendula , and Carpinus betulus would align with those previously reported for Corylus avellana , Fagus sylvatica , and Prunus avium by Silva et al (2023). Samples were subjected to a controlled rotational speed and temperature of 22°C while measuring K h over a one-hour duration.…”

“…Silva et al (2023) reported that a sample that was spun for one hour at a fixed Ψ, could exhibit temporal increases in K h ranging between +6% and +40% at low centrifugal speed, but K h may decrease between -41% and -61% at high centrifugal speeds. Interestingly, these changes were significantly larger than previously reported reductions of K h by accumulation of contaminants or gas bubbles on pit membranes (Canny et al 2007, Espino and Schenk 2011, Krieger and Schymanski 2023).…”

“…Consequently, considering the spin period component may improve the precision of VCs and associated parameters. Accurate estimations of K h and K max are important to estimate embolism resistance, as K max values measured at low centrifugal speed may increase over time, while values of K h measured at high centrifugal speed may decrease over time (Silva et al 2023). Decreasing values of K h and/or increasing measurements of K max over time (Equation 1), may significantly change the K h /K max ratio.…”

“…We hypothesised that longer spin times would shift VCs towards higher Ψ values, leading to reduced values of embolism resistance. Furthermore, we expected that these potential VC shifts (including P 50 values) would be species specific, as the variability in K h over time differs among angiosperm species (Silva et al 2023).…”