Dynamic changes in gas solubility of xylem sap reiterate the enigma of plant water transport under negative pressure

Despite a long research history, we do not fully understand why plants are able to transport xylem sap under negative pressure without constant failure. Microbubble formation via direct gas entry is assumed to cause hydraulic failure, while the concentration of gas dissolved in xylem sap is traditionally supposed to be constant, following Henry's law. Here, the concentration of soluble gas in xylem sap was estimated in vivo using well-watered Citrus plants under varying levels of air temperature and photoperiodic exposure, and compared to modelled data. The gas concentration in xylem sap showed non-equilibrium curves, with a minimum over-or undersaturation of 5% compared to gas solubility based on Henry's law. A similar diurnal pattern was obtained from the gas concentration in the cut-open conduits and discharge tube, and oversolubility was strongly associated with decreasing xylem water potentials during transpiration. Although our model did not explain the daily changes in gas solubility for an anisobaric situation, oversolubility characterises nanoconfined liquids, such as sap inside cell walls. Thus, plants are able to transport sap under negative pressure with relatively high amounts of dissolved gas, providing them with a buffering capacity to prevent hydraulic failure, despite diurnal changes in pressure and temperature.

Catastrophic Hydraulic Failure and Tipping Points in Plants

Water inside plants forms a continuous chain from water in soils to the water evaporating from leaf surfaces. Failures in this chain result in reduced transpiration and photosynthesis and these failures are caused by soil drying and/or cavitation-induced xylem embolism. Xylem embolism and plant hydraulic failure share a number of analogies to “catastrophe theory” in dynamical systems. These catastrophes are often represented in the physiological and ecological literature as tipping points or alternative stable states when control variables exogenous (e.g. soil water potential) or endogenous (e.g. leaf water potential) to the plant are allowed to slowly vary. Here, plant hydraulics viewed from the perspective of catastrophes at multiple spatial scales is considered with attention to bubble expansion (i.e. cavitation), organ-scale vulnerability to embolism, and whole-plant biomass as a proxy for transpiration and hydraulic function. The hydraulic safety-efficiency tradeoff, hydraulic segmentation and maximum plant transpiration are examined using this framework. Underlying mechanisms for hydraulic failure at very fine scales such as pit membranes, intermediate scales such as xylem network properties and at larger scales such as soil-tree hydraulic pathways are discussed. Lacunarity areas in plant hydraulics are also flagged where progress is urgently needed.

Seasonal Drought Induces Hydraulic Dysfunction, Not Carbohydrate Depletion, for Robinia Pseudoacacia in a Semi-humid Forest

BackgroundShifts in rainfall patterns that are associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. However, causes of forest decline and their physiological mechanisms remain unclear, particularly the roles of carbon metabolism and xylem function. To explore the response of hydraulic architecture and non-structural carbohydrates (NSC) traits under seasonal drought, we conducted a manipulation experiment in a Robinia pseudoacacia plantation in 2015 and 2016 in Loess Plateau of China. Sap-flow, leaf area index, water potential, non-structural carbohydrate concentrations, and hydraulics in different organs were measured. ResultsThe mean pre-dawn and midday leaf water potential after two growing seasons of drought stress was significantly lower (-2.2 MPa and -2.7 MPa, respectively) than those of control trees (-1.5 MPa and -2.0 MPa, respectively). Drought stress accelerated the loss of conductivity, and promoted the formation of narrow hydraulic safety margins, which indicated that hydraulic failure could be a good predictor of “physiological drought” in trees when subjected to two growing seasons of drought. Both sugar and starch concentrations in stems and roots were similar in all trees throughout the drought period, which indicated that trees maintained good coordination between carbon supply and demand when confronted with two growing seasons of drought.ConclusionsOur results emphasized that hydraulic failure plays the predominant role in causing tree death during highly intense drought, while whether "carbon starvation" occurs during tree mortality remains to be tested in longer (multi-year) but less intense drought.

Tree Mortality Risks Under Climate Change in Europe: Assessment of Silviculture Practices and Genetic Conservation Networks

General Context: Climate change can positively or negatively affect abiotic and biotic drivers of tree mortality. Process-based models integrating these climatic effects are only seldom used at species distribution scale.Objective: The main objective of this study was to investigate the multi-causal mortality risk of five major European forest tree species across their distribution range from an ecophysiological perspective, to quantify the impact of forest management practices on this risk and to identify threats on the genetic conservation network.Methods: We used the process-based ecophysiological model CASTANEA to simulate the mortality risk of Fagus sylvatica, Quercus petraea, Pinus sylvestris, Pinus pinaster, and Picea abies under current and future climate conditions, while considering local silviculture practices. The mortality risk was assessed by a composite risk index (CRIM) integrating the risks of carbon starvation, hydraulic failure and frost damage. We took into account extreme climatic events with the CRIMmax, computed as the maximum annual value of the CRIM.Results: The physiological processes' contributions to CRIM differed among species: it was mainly driven by hydraulic failure for P. sylvestris and Q. petraea, by frost damage for P. abies, by carbon starvation for P. pinaster, and by a combination of hydraulic failure and frost damage for F. sylvatica. Under future climate, projections showed an increase of CRIM for P. pinaster but a decrease for P. abies, Q. petraea, and F. sylvatica, and little variation for P. sylvestris. Under the harshest future climatic scenario, forest management decreased the mean CRIM of P. sylvestris, increased it for P. abies and P. pinaster and had no major impact for the two broadleaved species. By the year 2100, 38–90% of the European network of gene conservation units are at extinction risk (CRIMmax=1), depending on the species.Conclusions: Using a process-based ecophysiological model allowed us to disentangle the multiple drivers of tree mortality under current and future climates. Taking into account the positive effect of increased CO2 on fertilization and water use efficiency, average mortality risk may increase or decrease in the future depending on species and sites. However, under extreme climatic events, our process-based projections are as pessimistic as those obtained using bioclimatic niche models.

Comprehensive Assessment of the Effect of Water Pressure on the Development of Cracks in Gravity Concrete Dams

In recent years, extensive studies have been conducted to ensure the safety and stability of concrete dams. The development of numerical methods in considering more factors affecting the response of dams and also increasing the accuracy of calculation methods has played an important role in ensuring the safety of concrete dams. Therefore, one of the most important points in the design and analysis of concrete dams is to predict the location of cracks, expand it, investigate the phenomenon of hydraulic failure, consider the pressure caused by the infiltration of reservoir water into cracks and joints in static and dynamic states, and find solutions prevention of dam destruction due to this phenomenon. In the study of the effect of tensile strength, with increasing tensile strength, the reservoir water level increases at the beginning of cracking and the final reservoir water level increases, but there is no linear relationship between tensile strength and the two responses. In general, in examining the refractive energy parameter in each of the states with and without taking into account the water pressure inside the crack, the results of the mentioned models are slightly different from each other, but comparing the results shows that in nonlinear analysis considering water pressure inside the crack failure energy change has a greater impact on the results of these models.

Hydraulic segmentation does not protect stems from acute water loss during fire

The heat plume associated with fire has been hypothesized to cause sufficient water loss from trees to induce embolism and hydraulic failure. However, it is unclear whether the water transport path remains sufficiently intact during scorching or burning of foliage to sustain high water loss. We measured water uptake by branches of Magnolia grandiflora while exposing them to a range of fire intensities, and examined factors influencing continued water uptake after fire. Burning caused a 22-fold mean increase in water uptake, with greatest rates of water loss observed at burn intensities that caused complete consumption of leaves. Such rapid uptake is possible only with steep gradients in water potential, which would likely result in substantial cavitation of xylem and loss of conductivity in intact stems. Water uptake continued after burning was complete, and was greatest following burn intensities that killed leaves but did not consume them. This post-fire uptake was mostly driven by rehydration of the remaining tissues, rather than evaporation from the tissues. Our results indicate that the fire-plume hypothesis can be expanded to include a wide range of burning conditions experienced by plants. High rates of water loss are sustained during burning, even when leaves are killed or completely consumed.

Seasonal and long-term consequences of esca on grapevine stem xylem integrity

Hydraulic failure has been extensively studied during drought-induced plant dieback, but its role in plant-pathogen interactions is under debate. During esca, a grapevine (Vitis vinifera) disease, symptomatic leaves are prone to irreversible hydraulic dysfunctions but little is known about the hydraulic integrity of perennial organs over the short- and long-term. We investigated the effects of esca on stem hydraulic integrity in naturally infected plants within a single season and across season(s). We coupled direct (ks) and indirect (kth) hydraulic conductivity measurements, and tylose and vascular pathogen detection with in vivo X-ray microtomography visualizations. We found xylem occlusions (tyloses), and subsequent loss of stem ks, in all of the shoots with severe symptoms (apoplexy) and in more than 60% of the shoots with moderate symptoms (tiger-stripe), and no tyloses in shoots that were currently asymptomatic. In vivo stem observations demonstrated that tyloses were observed only when leaf symptoms appeared, and resulted in more than 50% PLC in 40% of symptomatic stems, unrelated to symptom age. The impact of esca on xylem integrity was only seasonal and no long-term impact of disease history was recorded. Our study demonstrated how and to what extent a vascular disease such as esca, affecting xylem integrity, could amplify plant mortality by hydraulic failure.