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Vulnerability of xylem to cavitation and embolism
... The susceptibility of each tree sample to xylem cavitation was measured using the air-injection method (Tyree and Sperry 1989;Cochard et al. 1992;Sperry et al. 1996;Barotto et al. 2018). Prior to measurement, the two cut ends of sample branches were trimmed with a sharp razor blade while immersed in distilled water and the samples were rehydrated overnight in 10 mM KCl solution in a refrigerator. ...
... Vulnerability curves (Tyree and Sperry 1989) were drawn by fitting the Weibull function to the relationships between applied pressure and PLC (Neufeld et al. 1992;Lopez et al. 2005). The Weibull function is given as PLC = 100 − 100 · exp (-Ψ xylem /b) c , where Ψ xylem is the tension considered as equal in absolute value to the positive pressure applied in the pressure sleeve, and b and c are the applied pressure at 63% PLC and the slope of the negative inflection point, respectively. ...
Key message
Repeated defoliation soon after full leaf expansion reduces xylem hydraulic transport safety in beech trees.
Abstract
Japanese beech trees undergo branch dieback and eventual mortality following years of repeated leaf loss due to leaf-feeding insects attacking immediately after full leaf expansion. To study the impact of recurrent defoliation on beech debilitation and mortality, we investigated xylem hydraulic transport safety and observed the xylem vessel architecture in field-grown medium-sized Japanese beech trees that had been artificially defoliated repeatedly for 4 years immediately after full leaf expansion. Multiple years of defoliation immediately after full leaf expansion increased the susceptibility to xylem cavitation (P50 value; − 4.46 ± 0.38 MPa (mean ± SD) for non-defoliated control beeches, and − 2.32 ± 0.20 MPa for defoliated beeches), despite a decrease in their vessel diameter and an increase in their vessel density. In defoliated beech, many irregularly shaped, axially wrinkled and partially cracked vessels, mountain-folded intervessel pits, and fibers with thin and less-lignified cell walls were observed. The intervessel double-wall thickness of the defoliated beech was thinner than that of the control beech. Furthermore, the size and shape of intervessel pits did not change in defoliated beech, but the density of intervessel pits and the total number and total area of intervessel pits per 1 mm of vessel length increased. We conclude that the increased susceptibility to xylem cavitation caused by repeated defoliation immediately after full leaf expansion may be due to an increased total area of intervessel pits with thin pit membranes per unit vessel wall area, in addition to cell wall alteration and vessel deformation and damage.
... Globally, forests are threatened by rising temperatures and droughts, which push plants past their physiological thresholds, leading to hydraulic failure (Choat et al., 2012;Adams et al., 2017;Brodribb et al., 2020;Tavares et al., 2023). As water availability declines, leaves lose turgor pressure and air embolisms can spread through the xylem (Tyree & Sperry, 1989;Brodersen et al., 2019). Resistance to embolism formation and spread, therefore, has been an important component of xylem evolution and diversification into ever-drier habitats (Pittermann et al., 2010(Pittermann et al., , 2012Larter et al., 2017;Skelton et al., 2021;Bouda et al., 2022). ...
Drought‐induced xylem embolism is a primary cause of plant mortality. Although c. 70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked.
We quantified the vulnerability to drought‐induced embolism, pressure–volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads.
Compared with other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than noncycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads.
Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits – particularly vessels – may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.
... Several previous studies documented an increased risk of forest mortality due to extreme drought events (Klein & Henrik 2018;Hajek et al. 2022). Continuous water transport supply from roots to stems and leaves through xylem can be interrupted by embolism, or the blockage of conduits by air (Tyree & Sperry 1989). Embolism is tightly linked to drought-induced mortality in plants . ...
The vulnerability of plant xylem to embolism can be described as the water potential at which xylem conductivity is lost by 50% (P50). According to the traditional hypothesis of hydraulic vulnerability segmentation, the difference in vulnerability to embolism between branches and roots is positive (P50 root−branch > 0). It is not clear whether this occurs broadly across species or how segmentation might vary across aridity gradients. We compiled hydraulic and anatomical datasets from branches and roots across 104 woody species (including new measurements from 10 species) in four biomes to investigate the relationships between P50 root–branch and environmental factors associated with aridity. We found a positive P50 root–branch relationship across species, and evidence that P50 root–branch increases with aridity. Branch xylem hydraulic conductivity transitioned from more efficient (e.g., wider conduit, higher hydraulic conductivity) to safer (e.g., narrower conduit, more negative P50) in response to the increase of aridity, while root xylem hydraulic conductivity remained unchanged across aridity gradients. Our results demonstrate that the hydraulic vulnerability difference between branches and roots is more positive in species from arid regions, largely driven by modifications to branch traits.
... Embolism forms when increasing negative pressure in the xylem breaches a threshold that results in the invasion of the conduit by gas crossing the pit membranes (Avila et al., 2022;Kaack et al., 2021;Tyree & Sperry, 1989). As drought progresses, critical levels of embolism directly associate with drought-induced damage and mortality (Brodribb et al., 2021;Cardoso et al., 2020;Hammond et al., 2019;Urli et al., 2013). ...
The stems of some herbaceous species can undergo basal secondary growth, leading to a continuum in the degree of woodiness along the stem. Whether the formation of secondary growth in the stem base results in differences in embolism resistance between the base and the upper portions of stems is unknown. We assessed the embolism resistance of leaves and the basal and upper portions of stems simultaneously within the same individuals of two divergent herbaceous species that undergo secondary growth in the mature stem bases. The species were Solanum lycopersicum (tomato) and Senecio minimus (fireweed). Basal stem in mature plants of both species displayed advanced secondary growth and greater resistance to embolism than the upper stem. This also resulted in significant vulnerability segmentation between the basal stem and the leaves in both species. Greater embolism resistance in the woodier stem base was found alongside decreases in the pith-to-xylem ratio, increases in the proportion of secondary xylem, and increases in lignin content. We show that there can be considerable variation in embolism resistance across the stem in herbs and that this variation is linked to the degree of secondary growth present. A gradient in embolism resistance across the stem in herbaceous plants could be an adaptation to ensure reproduction or basal resprouting during episodes of drought late in the lifecycle.
... Embolism resistance of xylem tissue represents a useful trait to understand plant water 54 relations, and has been linked with xylem anatomy, plant physiology (photosynthetic productivity, 55 growth and reproduction), ecological distribution, and drought-induced mortality (Brodribb et al. while the loss of a critical amount of conductivity can initiate runaway embolism, resulting in partial or 59 even complete failure of the water transport system (Tyree and Sperry 1988, 1989, Tyree et al. 1998 Hacke and Sperry 2001, Choat et al. 2012). Considering that embolism resistance is a key trait in 61 distinguishing the ability of a species to tolerate drought and frost, it is crucial to have appropriate 62 methods available to quantify embolism resistance at the intra-and interspecific level for a wide range 63 of vegetation types Choat 2016, Sergent et al. 2020). ...
Centrifuges provide a fast and standard approach to quantify embolism resistance of xylem in vulnerability curves (VCs). Traditionally, embolism formation in centrifuge experiments is assumingly driven by centrifuge speed, and thus pressure, but unaffected by spin time. Here, we explore to what extent embolism resistance is not only pressure but also spin time dependent, and hypothesise that time-stable hydraulic conductivity (Kh) values could shift VCs. We quantified time-based shifts in flow-centrifuge VCs and their parameter estimations for six angiosperm species by measuring Kh at regular intervals over 15 minutes of spinning at a particular speed before a higher speed was applied to the same sample. We compared various VCs per sample based on cumulative spin time, and modelled the relationship between Kh, xylem water potential (psi), and spin time. Time-based changes of Kh showed considerable increases and decreases at low and high centrifuge speeds, respectively, which generally shifted VCs towards more positive psi values. Values corresponding to 50% loss of hydraulic conductivity (P50) increased up to 0.72 MPa in Acer pseudoplatanus, and on average by 8.5% for all six species compared to VCs that did not consider spin time. By employing an asymptotic exponential model, we estimated time-stable Kh, which improved the statistical significance of VCs in 5 of the 6 species studied. This model also revealed the instability of VCs at short spin times, and showed that embolism formation in flow-centrifuges followed a saturating exponential growth curve. Although pressure remains the major determinant of embolism formation, spin time should be considered in flow-centrifuge VCs to avoid overestimation of embolism resistance. This spin-time artefact is species-specific, and likely based on relatively slow gas diffusion associated with embolism spreading. It can be minimized by determining time-stable Kh values for each centrifuge speed, without considerably extending the experimental time to construct VCs.
... Droughts are becoming more severe, harsh, and frequent as the climate continues to warm [5]. The manner in which forests react to drought is influenced by various factors, including the flow and distribution of water in the soil-plantatmosphere continuum [6]. There is significant evidence that vegetation water content (VWC) can serve as a useful measure of water status as it is directly linked to the moisture content of living fuel [1]. ...
In this study, we conducted an empirical investigation on mobile Global Navigation Satellite System (GNSS) Transmissometry (GNSS-T) measurements to explore vegetation optical depth (VOD). Our approach involved using a dual-receiver setup, with one receiver located in open terrain to capture direct signals as a reference and another deployed on an unmanned ground vehicle (UGV) to sample vegetation across expansive forested regions. Noteworthy findings reveal the negligible influence of ground multipath effects within these forested terrains, effectively resulting in sampling the forest canopy rather than the ground itself as the receiver moves. The UGV-based method also uncovers VOD fluctuations inside the forest, offering insights into spatial distribution and the influence of satellite position on VOD measurements. The study further examines the effect of tree heterogeneity and seasonal dynamics on the VOD estimates. This empirical study contributes to our understanding of the VOD mapping capabilities of the mobile GNSS-T approach and can potentially lead to non-intrusive quantification of Vegetation Water Content (VWC) at a landscape scale in forest terrains. These results are significant for advancing our knowledge of forest ecosystem dynamics and sustainable resource management.
Species mixture is promoted as a crucial management option to adapt forests to climate change. However, there is little consensus on how tree diversity affects tree water stress, and the underlying mechanisms remain elusive. By using a greenhouse experiment and a soil-plant-atmosphere hydraulic model, we explored whether and why mixing the isohydric Aleppo pine (Pinus halepensis, drought avoidant) and the anisohydric holm oak (Quercus ilex, drought tolerant) affects tree water stress during extreme drought. Our experiment showed that the intimate mixture strongly alleviated Q. ilex water stress while it marginally impacted P. halepensis water stress. Three mechanistic explanations for this pattern are supported by our modelling analysis. First, the difference in stomatal regulation between species allowed Q. ilex trees to benefit from additional soil water in mixture, thereby maintaining higher water potentials and sustaining gas exchange. By contrast, P. halepensis exhibited earlier water stress and stomatal regulation. Second, P. halepensis trees showed stable water potential during drought, although soil water potential strongly decreased, even when grown in a mixture. Model simulations suggested that hydraulic isolation of the root from the soil associated with decreased leaf cuticular conductance was a plausible explanation for this pattern. Third, the higher predawn water potentials for a given soil water potential observed for Q. ilex in mixture can - according to model simulations - be explained by increased soil-to-root conductance, resulting from higher fine root length. This study brings insights into the mechanisms involved in improved drought resistance of mixed species forests.
Drought conditions caused by soil moisture stress and/or high vapour pressure deficit pose a challenge to many terrestrial ecosystem models (TEMs). The Canadian LAnd Surface Scheme Including biogeochemical Cycles (CLASSIC) employs an empirical approach to link soil moisture stress with stomatal conductance. Such soil moisture-based empirical approaches typically perform poorly during drought. Here, we implemented an explicit plant hydraulics parameterization, i.e., Stomatal Optimization based on Xylem hydraulics (SOX), in CLASSIC, thereby connecting the soil-plant-atmosphere continuum through plant hydraulic traits. Performance of the resulting CLASSIC$_{SOX}$ was evaluated against carbon and water fluxes measured with eddy covariance at eight boreal forest flux tower sites in North America. Compared to CLASSIC, CLASSIC$_{SOX}$ better simulated gross primary productivity (GPP) across all sites, i.e., coefficient of determination (R$^{2}$) increased (0.51 to 0.59), root mean square error (RMSE) and bias decreased (1.85 to 1.54 g C m$^{-2}$ d$^{-1}$) and (-0.99 to -0.58 g C m$^{-2}$ d$^{-1}$), respectively. Under drought conditions, identified using the Palmer drought severity index, GPP simulated with CLASSIC$_{SOX}$ improved compared to CLASSIC, i.e., R$^{2}$ increased (0.51 to 0.60), and RMSE and bias decreased (1.79 to 1.46 g C m$^{-2}$ d$^{-1}$) and (-0.97 to -0.53 g C m$^{-2}$ d$^{-1}$), respectively. In contrast, CLASSIC$_{SOX}$ simulated evapotranspiration worsened, i.e., R$^{2}$ decreased (0.61 to 0.42), RMSE increased (0.54 to 0.62 mm d$^{-1}$), and bias changed direction (0.09 to -0.09 mm d$^{-1}$). As evaporation is a highly parameterized process in CLASSIC, it likely needs to be re-parameterized to account for the SOX transpiration behaviour.
Hydraulic testing of isolated sapwood from mature tree trunks is time-consuming and prone to errors, whereas the measurement of compression strength is a standardized and rapid wood technological application. In this study, we aimed to analyze if compression stress perpendicular to the grain relates to hydraulic vulnerability of mature Norway spruce (Picea abies) trunk wood with an expected narrow vulnerability range. The sample-set comprised 52 specimens originating from 34 trees harvested in Sweden. Before mechanical testing, the P50, i.e., the water potential resulting in 50 % of hydraulic conductivity loss, was estimated on small sapwood beams employing the air injection method. Compression strength perpendicular to the grain was defined as the first peak of a stress-strain curve (peak stress) when the wood is subjected to radial compression. Peak stress ranged between 1,65 MPa and 5,07 MPa, P50 between-2,98 MPa and-1,98 MPa. We found a good correlation between the peak stress and P50 (r = 0,80; P < 0,0001). This provides further evidence that peak stress in radial compression and P50 are both extremely dependent on the characteristics of the "weakest" wood part, i.e., the highly conductive earlywood. We conclude that the radial compression strength is a good proxy for P50 of mature Norway spruce trunk wood.
Development of plants and animals depends on the formation of complex vascular systems for the delivery of water, nutrients, and hormonal signals. This review clarifies major controlling mechanisms that regulate vascular differentiation, regeneration, adaptation, and evolution of plants, which were discovered during the past 50 years. Hypotheses and evidence on the hormonal mechanisms that regulate vascular differentiation are discussed, focusing on phloem and xylem relationships, control of vessel width, fiber differentiation, leaf and flower development, root initiation, evolution of ring-porous wood, parasitism, gall formation, cancer development and prevention.
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