Grapevine species from varied native habitats exhibit differences in embolism formation/repair associated with leaf gas exchange and root pressure

Drought induces xylem embolism formation, but grapevines can refill non‐functional vessels to restore transport capacity. It is unknown whether vulnerability to embolism formation and ability to repair differ among grapevine species. We analysed in vivo embolism formation and repair using x‐ray computed microtomography in three wild grapevine species from varied native habitats (Vitis riparia, V. arizonica, V. champinii) and related responses to measurements of leaf gas exchange and root pressure. Vulnerability to embolism formation was greatest in V. riparia, intermediate in V. arizonica and lowest in V. champinii. After re‐watering, embolism repair was rapid and pronounced in V. riparia and V. arizonica, but limited or negligible in V. champinii even after numerous days. Similarly, root pressure measured after re‐watering was positively correlated with drought stress severity for V. riparia and V. arizonica (species exhibiting embolism repair) but not for V. champinii. Drought‐induced reductions in transpiration were greatest for V. riparia and least in V. champinii. Recovery of transpiration after re‐watering was delayed for all species, but was greatest for V. champinii and most rapid in V. arizonica. These species exhibit varied responses to drought stress that involve maintenance/recovery of xylem transport capacity coordinated with root pressure and gas exchange responses.     

Elevated growth temperatures alter hydraulic characteristics in trembling aspen (Populus tremuloides) seedlings: implications for tree drought tolerance

Although climate change will alter both soil water availability and evaporative demand, our understanding of how future climate conditions will alter tree hydraulic architecture is limited. Here, we demonstrate that growth at elevated temperatures (ambient +5 °C) affects hydraulic traits in seedlings of the deciduous boreal tree species Populus tremuloides, with the strength of the effect varying with the plant organ studied. Temperature altered the partitioning of hydraulic resistance, with greater resistance attributed to stems and less to roots in warm‐grown seedlings (P < 0.02), and a 46% (but marginally significant, P = 0.08) increase in whole plant conductance at elevated temperature. Vulnerability to cavitation was greater in leaves grown at high than at ambient temperatures, but vulnerability in stems was similar between treatments. A soil–plant–atmosphere (SPA) model suggests that these coordinated changes in hydraulic physiology would lead to more frequent drought stress and reduced water‐use efficiency in aspen that develop at warmer temperatures. Tissue‐specific trade‐offs in hydraulic traits in response to high growth temperatures would be difficult to detect when relying solely on whole plant measurements, but may have large‐scale ecological implications for plant water use, carbon cycling and, possibly, plant drought survival.     

Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism

We investigated the common assumption that severing stems and petioles under water preserves the hydraulic continuity in the xylem conduits opened by the cut when the xylem is under tension. In red maple and white ash, higher percent loss of conductivity (PLC) in the afternoon occurred when the measurement segment was excised under water at native xylem tensions, but not when xylem tensions were relaxed prior to sample excision. Bench drying vulnerability curves in which measurement samples were excised at native versus relaxed tensions showed a dramatic effect of cutting under tension in red maple, a moderate effect in sugar maple, and no effect in paper birch. We also found that air injection of cut branches (red and sugar maple) at pressures of 0.1 and 1.0 MPa resulted in PLC greater than predicted from vulnerability curves for samples cut 2 min after depressurization, with PLC returning to expected levels for samples cut after 75 min. These results suggest that sampling methods can generate PLC patterns indicative of repair under tension by inducing a degree of embolism that is itself a function of xylem tensions or supersaturation of dissolved gases (air injection) at the moment of sample excision. Implications for assessing vulnerability to cavitation and levels of embolism under field conditions are discussed.     

A method for measuring hydraulic conductivity and embolism in xylem

Abstract Hydraulic conductivity of the xylem is computed as the quotient of mass flow rate and pressure gradient. Measurements on excised plant stems can be difficult to interpret because of time-dependent reductions in flow rate, and because of variable degrees of embolism. Using Acer saccharum Marsh. stems, we found that certain perfusing solutions including dilute fixatives (e.g. 0.05% formaldehyde) and acids with pH below 3 (e.g. 10 mol m^?3 oxalic) prevent long-term decline in conductivity. Xylem embolism can be quantified by expressing the initial conductivity as a percentage of the maximum obtained after flow-impeding air emboli have been removed by repeated high-pressure (175 kPa) flushes. Correlation between microbial contamination and declining conductivity suggests that long-term (> 4h) declines are caused by microbial growth within the vessels. Unpredictable trends in short-term (< 4h) measurements may be caused by movements of air emboli in vessels and/or participate matter.     

Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels

Diel variation in specific hydraulic conductivity (k_s) was recorded in petioles of two savanna tree species, Schefflera macrocarpa and Caryocar brasiliense, from central Brazil. These two species have compound leaves with long petioles (10–30 cm). In both species, petiole k_s decreased sharply with increasing transpiration rates and declining leaf water potentials (ψ_L) during the morning. Petiole k_s increased during the afternoon while the plants were still transpiring and the water in the non‐embolized vessels was still under tension. Dye experiments confirmed that in both species diel variation in k_s was associated with embolism formation and repair. When transpiration was prevented in individual leaves, their petiole k_s and water potential remained close to their maximum values during the day. When minimum daily ψ_L on selected branches was experimentally lowered by 0.2–0.6 MPa, the rate of k_s recovery during the afternoon was slower in comparison with control branches. Several field manipulations were performed to identify potential mechanisms involved in the refilling of embolized petiole vessels. Removal of the cortex or longitudinal incisions in the cortex prevented afternoon recovery of k_s and refilling of embolized vessels. When distilled water was added to petiole surfaces that had been abraded to partially remove the cuticle, k_s increased sharply during the morning and early afternoon. Evidence of starch to sugar conversion in the starch sheath cells surrounding the vascular bundles of the petioles was observed during periods of rapid transpiration when the abundance of starch granules in the starch sheath cells surrounding the vascular bundles decreased. Consistent with this, petiole sugar content was highest in the early afternoon. The most parsimonious explanation of the field observations and the experimental results was that an increase in osmotically active solutes in cells outside the vascular bundles at around midday leads to water uptake by these cells. However, the concurrent increase in tissue volume is partially constrained by the cortex, resulting in a transient pressure imbalance that may drive radial water movement in the direction of the embolized vessels, thereby refilling them and restoring water flow. This study thus presents evidence that embolism formation and repair are two distinct phenomena controlled by different variables. The degree of embolism is a function of tension, and the rate of refilling a function of internal pressure imbalances.     

Cavitation resistance and seasonal hydraulics differ among three arid Californian plant communities

Vulnerability to water stress-induced cavitation was measured on 27 woody shrub species from three arid plant communities including chaparral, coastal sage and Mojave Desert scrub. Dry season native embolism and pre-dawn water potential, and both wet and dry season xylem specific hydraulic conductivity (Ks) were measured. Cavitation resistance, estimated as water potential at 50% loss in conductivity (Psi50), was measured on all species during the wet season and on a subset of species during the dry season. Cavitation resistance varied with sampling season, with 8 of 13 sampled species displaying significant seasonal shifts. Native embolism and water potential were useful in identification of species displaying seasonal shifts. The Ks was not different among sites or seasons. The Psi50 varied among species and communities. Within communities, interspecific variation may be partially explained by differences in rooting depth or leaf habit (evergreen, semi-deciduous, deciduous). Communities diverged in their Psi50 with chaparral species displaying the greatest cavitation resistance regardless of sampling season. The greater cavitation resistance of chaparral species is surprising, considering the greater aridity of the Mojave Desert site. Adaptation to arid environments is due to many plant traits, and aridity does not necessarily lead to convergence in cavitation resistance.     

Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo

The ability of juvenile Laurus nobilis and Acer negundo plants to refill embolized xylem vessels was tested under conditions of soil drought when xylem sap pressure was substantially negative, thus violating the expected condition that pressure must rise to near atmospheric for refilling. Intact potted plants were dried to a stem water potential (Σ_W) corresponding with approximately 80% loss of hydraulic conductivity (PLC) in shoots. Then plants were re‐watered and kept at a less negative target Ψ_W for 1–48 h. The Ψ_W was measured continuously with stem psychrometers. Rewatered L. nobilis held at the target Ψ_W for 1 h showed no evidence for refilling unless Ψ_W was within a few tenths of a MPa of zero. In contrast, re‐watered L. nobilis held for 24 and 48 h at water potentials well below zero showed a significant reduction in PLC. The recovery was highly variable, being complete in some stem segments, and scarcely evident in others. Embolism repair was accompanied by a significant but moderate decrease in the osmotic potential (Ψ) of the bulk xylem sap (Ψ = ?67 kPa in recovering plants versus ?31 kPa in controls). In contrast, embolized and re‐watered A. negundo plants held for 24 h at target Ψ_W of ?0·9 and ?0·3 MPa showed no embolism reversal. The mechanism allowing L. nobilis plants to refill under negative pressure is unknown, but does not appear to operate in A. negundo, and is slower to act for drought‐induced embolism than when embolism was artificially induced by air injection as previously shown for L. nobilis.     

Interpretation of seasonal changes of xylem embolism and plant hydraulic resistance in Fagus sylvatica

The annual course of xylem embolism in twigs of adult beech trees was monitored, and compared to concurrent changes of tree water status and hydraulic resistances. Xylem embolism was quantified in 1-year-old apical twigs by the hydraulic conductivity as a percentage of the maximum measured after removal of air emboli. Tree and root hydraulic resistances were estimated from water potential differences and sap flux measurements. The considerable degree of twig embolism found in winter (up to 90% loss of hydraulic conductivity) may be attributed to the effect of freeze-thaw cycles in the xylem. A partial recovery from winter embolism occurred in spring, probably because of the production of new functional xylem. Xylem embolism fluctuated around 50% throughout the summer, without significant changes. Almost complete refilling of apical twigs was observed early in autumn. A significant negative correlation was found between xylem embolism and precipitation; thus, an active role of rainfall in embolism reversion is hypothesized. Tree and root hydraulic resistances were found to change throughout the growing period. A marked decrease of hydraulic resistance preceded the refilling of apical twigs in the autumn. Most of the decrease in total tree resistance was estimated to be located in the root compartment.     

Effects of tree height on branch hydraulics, leaf structure and gas exchange in California redwoods

We examined changes in branch hydraulic, leaf structure and gas exchange properties in coast redwood ( Sequoia sempervirens ) and giant sequoia ( Sequoiadendron giganteum ) trees of different sizes. Leaf-specific hydraulic conductivity ( k _L) increased with height in S. sempervirens but not in S. giganteum , while xylem cavitation resistance increased with height in both species. Despite hydraulic adjustments, leaf mass per unit area (LMA) and leaf carbon isotope ratios ( δ ¹³C) increased, and maximum mass-based stomatal conductance ( g _mass) and photosynthesis ( A _mass) decreased with height in both species. As a result, both A _mass and g _mass were negatively correlated with branch hydraulic properties in S. sempervirens and uncorrelated in S. giganteum . In addition, A _mass and g _mass were negatively correlated with LMA in both species, which we attributed to the effects of decreasing leaf internal CO₂ conductance ( g _i). Species-level differences in wood density, LMA and area-based gas exchange capacity constrained other structural and physiological properties, with S. sempervirens exhibiting increased branch water transport efficiency and S. giganteum exhibiting increased leaf-level water-use efficiency with increasing height. Our results reveal different adaptive strategies for the two redwoods that help them compensate for constraints associated with growing taller, and reflect contrasting environmental conditions each species faces in its native habitat.     

Water deficits and hydraulic limits to leaf water supply

Many aspects of plant water use -- particularly in response to soil drought -- may have as their basis the alteration of hydraulic conductance from soil to canopy. The regulation of plant water potential (Psi) by stomatal control and leaf area adjustment may be necessary to maximize water uptake on the one hand, while avoiding loss of hydraulic contact with the soil water on the other. Modelling the changes in hydraulic conductance with pressure gradients in the continuum allows the prediction of water use as a function of soil environment and plant architectural and xylem traits. Large differences in water use between species can be attributed in part to differences in their 'hydraulic equipment' that is presumably optimized for drawing water from a particular temporal and spatial niche in the soil environment. A number of studies have identified hydraulic limits as the cause of partial or complete foliar dieback in response to drought. The interactions between root:shoot ratio, rooting depth, xylem properties, and soil properties in influencing the limits to canopy water supply can be used to predict which combinations should optimize water use in a given circumstance. The hydraulic approach can improve our understanding of the coupling of canopy processes to soil environment, and the adaptive significance of stomatal behaviour.     

8种木本植物木质部栓塞变化与生理生态指标关系的研究 I.与植物木质部水势的关系

以自然状况下生长良好的耐旱树种刺槐（Robinia pseudoacacia L.）、元宝枫（Acer truncatum Bge）、沙棘（Hippophae rhamnoides L.）、白榆（Ulmus pumila L.）、油松（Pinus tabulaeformis Carr.）、白皮松（Pinus bungeana Zucc.ex Endl.）及中生树种女贞（Ligustrum lucidum Ait.）、柳树（Salix matsudana Koidz.f.pendula Schneid.）为研究对象,用压力室法测定木质部水势,用冲洗法测定木质部栓塞程度,研究不同生长季节木质部栓塞与水势间的火系。结果表明：针叶树油松、白皮松在各个季节水势均较高,水势变化幅度较小,木质部不易发生栓塞,这与其木质部由管胞构成,对木质部栓塞不敏感,在干旱时采用高水势延迟脱水的耐旱策略有关。阔叶树刺槐、元宝枫、沙棘、白榆、女贞和柳树的木质部栓塞现象是其在每天正常生长过程中不可避免的“平常事件”,是它们适应干旱的一种方式。它们的木质部栓塞程度与水势表现出了相反的变化趋势,即同一树种在同一季节内水势值越低,木质部栓塞程度越大,但在不同树种及同一树种的不同季节不存在这种关系。由此可见,植物木质部栓塞对水势的敏感程度（即木质部栓塞脆弱性）主要由树种的木质部结构决定,同时受到树种特性、树木生长发育时期、外界环境因子的影响,木质部栓塞的脆弱性也具有季节变化特征。     

Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance

Hydraulic conductance of leaves (K(leaf)) typically decreases with increasing water stress and recent studies have proposed different mechanisms responsible for decreasing K(leaf) . We measured K(leaf) concurrently with ultrasonic acoustic emissions (UAEs) in dehydrating leaves of several species to determine whether declining K(leaf) was associated with xylem embolism. In addition, we performed experiments in which the surface tension of water in the leaf xylem was reduced by using a surfactant solution. Finally, we compared the hydraulic vulnerability of entire leaves with the leaf lamina in three species. Leaf hydraulic vulnerability based on rehydration kinetics and UAE was very similar, except in Quercus garryana. However, water potentials corresponding to the initial decline in K(leaf) and the onset of UAE in Q. garryana were similar. In all species tested, reducing the surface tension of water caused K(leaf) to decline at less negative water potentials compared with leaves supplied with water. Microscopy revealed that as the fraction of embolized xylem increased, K(leaf) declined sharply in Q. garryana. Measurements on leaf discs revealed that reductions in lamina hydraulic conductance with dehydration were not as great as those observed in intact leaves, suggesting that embolism was the primary mechanism for reductions in K(leaf) during dehydration.     

Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values

Diurnal changes in percentage loss of hydraulic conductivity (PLC), with recorded values being higher at midday than on the following morning, have been interpreted as evidence for the occurrence of cycles of xylem conduits' embolism and repair. Recent reports have suggested that diurnal PLC changes might arise as a consequence of an experimental artefact, that is, air entry into xylem conduits upon cutting stems, even if under water, while under substantial tension generated by transpiration. Rehydration procedures prior to hydraulic measurements have been recommended to avoid this artefact. In the present study, we show that xylem rehydration prior to hydraulic measurements might favour xylem refilling and embolism repair, thus leading to PLC values erroneously lower than those actually experienced by transpiring plants. When xylem tension relaxation procedures were performed on stems where refilling mechanisms had been previously inhibited by mechanical (girdling) or chemical (orthovanadate) treatment, PLC values measured in stems cut under native tension were the same as those measured after sample rehydration/relaxation. Our data call for renewed attention to the procedures of sample collection in the field and transport to the laboratory, and suggest that girdling might be a recommendable treatment prior to sample collection for PLC measurements.     

自然和人工生境被子植物枝木质部结构与功能差异

水是植物生存与生长的基础条件, 水分有效性影响植物木质部解剖结构、水力功能, 使之形成特定的适应特征。因此, 对比自然与人工生境中同一植物的水力功能与解剖结构差异, 有助于理解植物对水分环境的适应机理。该研究以湿润区三角槭(Acer buergerianum)、青冈(Cyclobalanopsis glauca)和女贞(Ligustrum lucidum)为研究材料, 对比分析了自然和人工生境中各物种的栓塞抗性(导水率损失50%时的水势(P₅₀))、输水效率(比导率(K_s))和解剖结构(导管直径(D)、导管壁厚(T)、导管密度(N)、木质部密度(WD)、厚度跨度比(t/b)²)特征, 探究了同生境种内与跨生境、跨物种水平的效率-安全权衡关系, 量化分析了水力功能与解剖结构的关系。结果发现: 1) 3种被子植物在自然生境中K_s更大, P₅₀更小, 与其更大的D、更小的(t/b)²有关。2)同生境种内K_s与P₅₀不存在权衡。3)功能性状和解剖结构相关分析表明: 同生境种内D与P₅₀不存在显著的相关关系; 除自然生境女贞外, T、(t/b)²均与P₅₀正相关。相对于人工生境, 在水分有效性低或无额外浇灌的自然生境中, 植物通过增大导管直径显著提高其输水效率, 从而避免水势下降、降低潜在栓塞风险。     

The relationship between xylem conduit diameter and cavitation caused by freezing

The centrifuge method for measuring the resistance of xylem to cavitation by water stress was modified to also account for any additional cavitation that might occur from a freeze-thaw cycle. A strong correlation was found between cavitation by freezing and mean conduit diameter. On the one extreme, a tracheid-bearing conifer and diffuse-porous angiosperms with small-diameter vessels (mean diameter <30 μm) showed no freezing-induced cavitation under modest water stress (xylem pressure = −0.5 MPa), whereas species with larger diameter vessels (mean >40 μm) were nearly completely cavitated under the same conditions. Species with intermediate mean diameters (30–40 μm) showed partial cavitation by freezing. These results are consistent with a critical diameter of 44 μm at or above which cavitation would occur by a freeze–thaw cycle at −0.5 MPa. As expected, vulnerability to cavitation by freezing was correlated with the hydraulic conductivity per stem transverse area. The results confirm and extend previous reports that small-diameter conduits are relatively resistant to cavitation by freezing. It appears that the centrifuge method, modified to include freeze–thaw cycles, may be useful in separating the interactive effects of xylem pressure and freezing on cavitation.