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

Abstract

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 (

A Unit Pipe Pneumatic model to simulate gas kinetics during measurements of embolism in excised angiosperm xylem

“…Therefore, the purpose of this study is to provide a theoretical background for pneumatic measurements, with the aim of proving that the theoretical kinetics of pressure change via diffusion of gases axially through intervessel pit membranes follows the proportion of embolized vascular tissue, either on a volume basis or hydraulic conductance basis. The model presented in this paper complements experimental evidence in recent papers (Pereira et al, 2020(Pereira et al, , 2021Guan et al, 2021;Paligi et al, submitted).…”

“…Comparison of the Pneumatic with hydraulic and other non-hydraulic methods has provided strong agreement for a substantial number of angiosperm species and samples ( Fig. S1 and Table S2; Pereira et al, 2016Pereira et al, , 2020Pereira et al, , 2021Zhang et al, 2018, Sergent et al, 2020Guan et al, 2021;Paligi et al, submitted). This agreement is especially strong when the above-mentioned caveats are considered.…”

“…The Pneumatic method involves measuring the kinetics of gas movement down the axis of a stem while independently measuring the stem water potential with a stem hygrometer (thermocouple psychrometer connected to a stem) or by measuring the balance pressure of excised leaves with a pressure chamber. Since 2016, the Pneumatic method has been used to estimate the vulnerability curves (VCs) of woody species where the interpretation of what is measured is based on qualitative arguments, or by comparing pneumatic VCs to VCs measured by more conventional hydraulic (Pereira et al, 2016(Pereira et al, , 2020(Pereira et al, , 2021Zhang et al, 2018, Sergent et al, 2020Chen et al, 2020) and non-hydraulic techniques (Sergent et al, 2020;Chen et al, 2020;Guan et al, 2021).…”

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

“…Here, we use the broader term 'embolism spreading' or 'propagation' instead of 'air-seeding' because embolism spreading includes both mass flow and diffusion of gas across pit membranes. Air-seeding, however, is limited to mass flow only, and embolism formation may not be caused only by mass flow of gas (Guan et al, 2021). Also, 'embolism' is used instead of the term 'cavitation', because the triggering process leading to embolism is unlikely to be due to the formation of a void by phase transition from liquid to gas, but most likely caused by pre-existing bubbles (Hölttä et al, 2002;Schenk et al, 2017).…”

Accuracy of the pneumatic method for estimating xylem vulnerability to embolism in temperate diffuse-porous tree species

“…Table S2) lower for the pneumatic method, which also resulted in a lower agreement in the estimates of P 12P and P 88P . Similar conclusions were found based on a pneumatic modelling approach (Yang et al ., 2021), and based on experimental evidence by comparing the pneumatic and the optical method (Pereira et al ., 2020; Guan et al ., 2021). A mechanistic explanation for the difference in P 12 and P 88 values is provided by the open-xylem artefact, which suggests that embolism spreading could be enhanced by the proximity to gas under atmospheric pressure in the open-cut conduits (Guan et al ., 2021).…”