Xylem embolism and bubble formation during freezing suggest complex dynamics of pressure-tension in Betula pendula stems

Freeze-thaw-induced embolism is a key limiting factor for perennial plants in frost-exposed environments. Gas bubbles are formed during freezing, when the low chemical potential of the ice reaches a critical cavitation threshold and expand during thawing. However, when water freezes, its volume increases by 9%, generating local pressures, which can limit the formation of bubbles. To characterize local dynamic of pressure-tension and physical state of the sap during freeze-thaw cycles, we simultaneously used ultrasonic acoustic emissions analysis and synchrotron-based High Resolution Computed Tomography on the diffuse-porous species Betula pendula. Visualization of individual air-filled vessels was performed to measure freeze-thaw induced embolism after successive freeze-thaw cycles down to -10C or -20C during the leafy and the leafless periods. We also measured the distribution of gas bubbles and made additional continuous monitoring of embolism spreading using a dedicated cooling system that allowed X-ray scanning during freezing and thawing. Experiments confirmed that ultrasonic emissions occurred after the onset of ice formation, together with bubble formation, whereas the development of embolism took place after thawing in all cases. The pictures of frozen tissues indicated that upon freezing the balance between negative pressure generated by the low water potential of the ice and the positive pressure induced by the volumetric increase of ice can provoke inward flow from the cell wall toward the lumen of the vessels. We found no evidence that wider vessels within a tissue were more prone to embolism although the occurrence of gas bubbles in larger conduits would make them prone to earlier embolism. These results highlight the need to monitor local pressure as well as ice and air distribution during xylem freezing to understand the mechanism leading to frost-induced embolism.Comment: 41 pages, 7 figures, 4 supplementary figure

Hydraulically nonfunctional xylem areas in Alpine shrubs

International audienc

Freezing and thawing in woody species: ice formation in relation with cavitation and freeze-thaw induced embolism

Freezing is a limiting factor for plant life, as it can cause damage on living tissues and embolism formation in xylem conduits. Ice formation in plant tissues is usually detected by exotherm analysis or infra-red thermography, whereas freeze-thaw induced embolism is measured through loss of hydraulic conductivity (PLC). We used a nondestructive method based on ultrasonic acoustic emissions (UE) generated by the freezing xylem. However, the exact source(s) of UE has not been identified up to now, especially in angiosperm species, in which xylem tissues are composed of several diverse cell types. We report recent advances on how UE detection could enable insights into: (i) Ice nucleation and propagation (Charrier et al., 2015), (ii) Presence of ice within xylem (Charrier et al., 2014a), (iii) Loss of hydraulic conductivity after a freeze-thaw cycle (Charrier et al., 2014b), (iv) Damages generated on living cells (Kasuga et al., 2015). Results indicate that cavitation events are generated at the ice front leading to UE. Species-specific cavitation thresholds are thus reached during freezing due to the temperature-dependent decrease of ice water potential, while bubble expansion and the resulting PLC occur during thawing. Contrarily to drought-induced embolism, UE analysis during freeze-thaw cycles may allow to distinguish between cavitation and embolism stages, according to the freezing and thawing processes, respectively. Ultrasonic emission analysis enabled new insights into the complex process of xylem freezing and might be used to monitor ice propagation in a whole plant in natura in relation with stress intensities and physiology (Charrier et al., 2017)

Ice scream: what do trees tell during freezing?

Freezing is a limiting factor for plant life, as it can cause damage on living tissues and embolism formation in xylem conduits. Ice formation in plant tissues is usually detected by exotherm analysis or infra-red thermography, whereas freeze-thaw induced embolism is measured through loss of hydraulic conductivity (PLC). We used a nondestructive method based on ultrasonic acoustic emissions (UE) generated by the freezing xylem. However, the exact source(s) of UE has not been identified up to now, especially in angiosperm species, in which xylem tissues are composed of several diverse cell types. We report recent advances on how UE detection could enable insights into: We report recent advances on how UE detection could inform on: (i)Ice nucleation and propagation (Charrier et al., 2015), (ii)Presence of ice within xylem (Charrier et al., 2014a), (iii)Loss of hydraulic conductivity after a freeze-thaw cycle (Charrier et al., 2014b), (iv)Damages generated on living cells (Kasuga et al., 2015). Results indicate that cavitation events are generated at the ice front leading to UE. Species-specific cavitation thresholds are thus reached during freezing due to the temperature-dependent decrease of ice water potential, while bubble expansion (embolism) and the resulting PLC occur during thawing. Contrarily to drought-induced embolism, UE analysis during freeze-thaw cycles can allow to split between cavitation and embolism stages: on freezing and thawing, respectively. Ultrasonic emission analysis enabled new insights into the complex process of xylem freezing and might be used to monitor ice propagation in a whole plant in natura in relation with stress intensities and physiology (Charrier et al., 2017)

Ultrasonic acoustic emission within the angiosperms

Ultrasonic acoustic emission within the angiosperms. Colloque de la société autrichienne de biologie végétal

Effects of snow cover change on freezing induced xylem dysfunctions in subalpine woody species

International audienc

Effects of snow cover change on freezing induced xylem dysfunctions in subalpine woody species

International audienc

Hydraulic efficiency and safety of conifer needles

absen

Émissions acoustiques ultrasoniques dans le xylème d'angiospermes soumis à des congélations répétées

absen

Freeze-Thaw Stress: Effects of Temperature on Hydraulic Conductivity and Ultrasonic Activity in Ten Woody Angiosperms

Freeze-thaw events can affect plant hydraulics by inducing embolism. This study analyzed the effect of temperature during the freezing process on hydraulic conductivity and ultrasonic emissions (UE). Stems of 10 angiosperms were dehydrated to a water potential at 12% percentage loss of hydraulic conductivity (PLC) and exposed to freeze-thaw cycles. The minimal temperature of the frost cycle correlated positively with induced PLC, whereby species with wider conduits (hydraulic diameter) showed higher freeze-thaw-induced PLC. Ultrasonic activity started with the onset of freezing and increased with decreasing subzero temperatures, whereas no UE were recorded during thawing. The temperature at which 50% of UE were reached varied between −9.1°C and −31.0°C across species. These findings indicate that temperatures during freezing are of relevance for bubble formation and air seeding. We suggest that species-specific cavitation thresholds are reached during freezing due to the temperature-dependent decrease of water potential in the ice, while bubble expansion and the resulting PLC occur during thawing. UE analysis can be used to monitor the cavitation process and estimate freeze-thaw-induced PLC