Stomatal factors and vulnerability of stem xylem to cavitation in poplars

The relationships between the vulnerability of stem xylem to cavitation, stomatal conductance, stomatal density, and leaf and stem water potential were examined in six hybrid poplar (P38P38, Walker, Okanese, Northwest, Assiniboine and Berlin) and balsam poplar (Populus balsamifera) clones. Stem xylem cavitation resistance was examined with the Cavitron technique in well-watered plants grown in the greenhouse. To investigate stomatal responses to drought, plants were subjected to drought stress by withholding watering for 5 (mild drought) and 7 (severe drought) days and to stress recovery by rewatering severely stressed plants for 30 min and 2 days. The clones varied in stomatal sensitivity to drought and vulnerability to stem xylem cavitation. P38P38 reduced stomatal conductance in response to mild stress while the balsam poplar clone maintained high leaf stomatal conductance under more severe drought stress conditions. Differences between the severely stressed clones were also observed in leaf water potentials with no or relatively small decreases in Assiniboine, P38P38, Okanese and Walker. Vulnerability to drought-induced stem xylem embolism revealed that balsam poplar and Northwest clones reached loss of conductivity at lower stem water potentials compared with the remaining clones. There was a strong link between stem xylem resistance to cavitation and stomatal responsiveness to drought stress in balsam poplar and P38P38. However, the differences in stomatal responsiveness to mild drought suggest that other drought-resistant strategies may also play a key role in some clones of poplars exposed to drought stress.     

Xylem embolism and drought-induced stomatal closure in maize

Water relations during drought and xylem vulnerability to embolism were studied on four maize ( Zea mays L.) genotypes having contrasting grain yields under drought conditions. Drought provoked a drop in xylem pressure, leaf water potential and whole-plant transpiration. Transpiration was reduced to a minimum value when xylem pressures reached ca. -1.6 MPa. This value corresponded to the threshold xylem pressure below which xylem embolism developed to a substantial degree in leaf midribs. Therefore, xylem embolism always remained low in leaf veins, even when plants exhibited clear water-stress symptoms. This suggests that stomatal closure during drought contains xylem embolism to a minimum value. Cavitation resistance was not related to grain yield under drought conditions for the four genotypes evaluated. However, it can be speculated that an increase in cavitation resistance by cultural practices or genetic selection may increase drought survival in maize.     

Cavitation resistance of peduncle,petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora

Variation in resistance of xylem to embolism among flowers, leaves, and stems strongly influences the survival and reproduction of plants. However, little is known about the vulnerability to xylem embolism under drought stress and their relationships to the anatomical traits of pits among reproductive and vegetative organs. In this study, we investigated the variation in xylem vulnerability to embolism in peduncles, petioles, and stems in a woody plant, Magnolia grandiflora. We analyzed the relationships between water potentials that induced 50% embolism (P₅₀) in peduncles, petioles, and stems and the conduit pit traits hypothesized to influence cavitation resistance. We found that peduncles were more vulnerable to cavitation than petioles and stems, supporting the hypothesis of hydraulic vulnerability segmentation that leaves and stems are prioritized over flowers during drought stress. Moreover, P₅₀ was significantly correlated with variation in the dimensions of inter-vessel pit apertures among peduncles, petioles and stems. These findings highlight that measuring xylem vulnerability to embolism in reproductive organs is essential for understanding the effect of drought on plant reproductive success and mortality under drought stress.     

Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas)

The impact of water deficit on stomatal conductance (g(s)), petiole hydraulic conductance (K(petiole)), and vulnerability to cavitation (PLC, percentage loss of hydraulic conductivity) in leaf petioles has been observed on field-grown vines (Vitis vinifera L. cv. Chasselas). Petioles were highly vulnerable to cavitation, with a 50% loss of hydraulic conductivity at a stem xylem water potential (Ψ(x)) of -0.95?MPa, and up to 90% loss of conductivity at a Ψ(x) of -1.5?MPa. K(petiole) described a daily cycle, decreasing during the day as water stress and evapotranspiration increased, then rising again in the early evening up to the previous morning's K(petiole) levels. In water-stressed vines, PLC increased sharply during the daytime and reached maximum values (70-90%) in the middle of the afternoon. Embolism repair occurred in petioles from the end of the day through the night. Indeed, PLC decreased in darkness in water-stressed vines. PLC variation in irrigated plants showed the same tendency, but with a smaller amplitude. The Chasselas cultivar appears to develop hydraulic segmentation, in which petiole cavitation plays an important role as a 'hydraulic fuse', thereby limiting leaf transpiration and the propagation of embolism and preserving the integrity of other organs (shoots and roots) during water stress. In the present study, progressive stomatal closure responded to a decrease in K(petiole) and an increase in cavitation events. Almost total closure of stomata (90%) was measured when PLC in petioles reached >90%.     

Relationships between stomatal behavior,xylem vulnerability to cavitation and leaf water relations in two cultivars of Vitis vinifera

Current understanding of physiological mechanisms governing stomatal behavior under water stress conditions is still incomplete and controversial. It has been proposed that coordination of stomatal kinetics with xylem vulnerability to cavitation [vulnerability curve (VC)] leads to different levels of isohydry/anisohydry in different plant species/cultivars. In this study, this hypothesis is tested in Vitis vinifera cultivars displaying contrasting stomatal behavior under drought stress. The cv Montepulciano (MP, near‐isohydric) and Sangiovese (SG, anisohydric) were compared in terms of stomatal response to leaf and stem water potential, as possibly correlated to different petiole hydraulic conductivity (k_petiole) and VC, as well as to leaf water relations parameters. MP leaves showed almost complete stomatal closure at higher leaf and stem water potentials than SG leaves. Moreover, MP petioles had higher maximum k_petiole and were more vulnerable to cavitation than SG. Water potential at the turgor loss point was higher in MP than in SG. In SG, the percentage reduction of stomatal conductance (PLg_s) under water stress was almost linearly correlated with corresponding percentage loss of k_petiole (PLC), while in MP PLg_s was less influenced by PLC. Our results suggest that V. vinifera near‐isohydric and anisohydric genotypes differ in terms of xylem vulnerability to cavitation as well as in terms of k_petiole, and that the coordination of these traits leads to their different stomatal responses under water stress conditions.     

Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem

Although cavitation and refilling cycles could be common in plants, it is unknown whether these cycles weaken the cavitation resistance of xylem. Stem or petiole segments were tested for cavitation resistance before and after a controlled cavitation-refilling cycle. Cavitation was induced by centrifugation, air drying of shoots, or soil drought. Except for droughted plants, material was not significantly water stressed prior to collection. Cavitation resistance was determined from "vulnerability curves" showing the percentage loss of conductivity versus xylem pressure. Two responses were observed. "Resilient" xylem (Acer negundo and Alnus incana stems) showed no change in cavitation resistance after a cavitation-refilling cycle. In contrast, "weakened" xylem (Populus angustifolia, P. tremuloides, Helianthus annuus stems, and Aesculus hippocastanum petioles) showed considerable reduction in cavitation resistance. Weakening was observed whether cavitation was induced by centrifugation, air dehydration, or soil drought. Observations from H. annuus showed that weakening was proportional to the embolism induced by stress. Air injection experiments indicated that the weakened response was a result of an increase in the leakiness of the vascular system to air seeding. The increased air permeability in weakened xylem could result from rupture or loosening of the cellulosic mesh of interconduit pit membranes during the water stress and cavitation treatment.     

Relationship of Xylem Embolism to Xylem Pressure Potential, Stomatal Closure, and Shoot Morphology in the Palm Rhapis excelsa

Xylem failure via gas embolism (cavitation) induced by water stress was investigated in the palm Rhapis excelsa (Thumb.) Henry. Xylem embolism in excised stems and petioles was detected using measurements of xylem flow resistance: a decrease in resistance after the removal of flow-impeding embolisms by a pressure treatment indicated their previous presence in the axis. Results supported the validity of the method because increased resistance in an axis corresponded with: (a) induction of embolism by dehydration, (b) increased numbers of cavitations as detected by acoustic means, (c) presence of bubbles in xylem vessels. The method was used to determine how Rhapis accommodates embolism; results suggested four ways. (a) Embolism was relatively rare because pressure potentials reach the embolism-inducing value of about −2.90 megapascals only during prolonged drought. (b) When embolism did occur in nature, it was confined to the relatively expendable leaf xylem; the stem xylem, which is critical for shoot survival, remained fully functional. (c) Even during prolonged drought, the extent of embolism is limited by complete stomatal closure, which occurred at the xylem pressure potential of −3.20 ± 0.18 megapascals. (d) Embolism is potentially reversible during prolonged rains, since embolisms dissolved within 5 h at a pressure potential of 0.00 megapascals (atmospheric), and xylem sap can approach this pressure during rain.     

Poplar vulnerability to xylem cavitation acclimates to drier soil conditions

Xylem vulnerability to cavitation differs between tree species according to their drought resistance, more xerophilous species being more resistant to xylem cavitation. Variability in xylem vulnerability to cavitation is also found within species, especially between in situ populations. The origin of this variability has not been clearly identified. Here we analyzed the response of xylem hydraulic traits of Populus tremula×Populus alba trees to three different soil water regimes. Stem xylem vulnerability was scored as the xylem water potential causing 12, 50 and 88% loss of conductivity (P₁₂, P₅₀ and P₈₈). Vulnerability to cavitation was found to acclimate to growing conditions under different levels of soil water content, with P₅₀ values of ?1.82, ?2.03 and ?2.45 MPa in well‐watered, moderately water‐stressed and severely water‐stressed poplars, respectively. The value of P₁₂, the xylem tension at which cavitation begins, was correlated with the lowest value of midday leaf water potential (ψm) experienced by each plant, the difference between the two parameters being approximately 0.5 MPa, consistent with the absence of any difference in embolism level between the different water treatments. These results support the hypothesis that vulnerability to cavitation is a critical trait for resistance to drought. The decrease in vulnerability to cavitation under growing conditions of soil drought was correlated with decreased vessel diameter, increased vessel wall thickness and a stronger bordered pit field (t/b)². The links between these parameters are discussed.     

Are leaves ‘freewheelin'? Testing for a Wheeler‐type effect in leaf xylem hydraulic decline

A recent study found that cutting shoots under water while xylem was under tension (which has been the standard protocol for the past few decades) could produce artefactual embolisms inside the xylem, overestimating hydraulic vulnerability relative to shoots cut under water after relaxing xylem tension (Wheeler et al. 2013). That study also raised the possibility that such a ‘Wheeler effect’ might occur in studies of leaf hydraulic vulnerability. We tested for such an effect for four species by applying a modified vacuum pump method to leaves with minor veins severed, to construct leaf xylem hydraulic vulnerability curves. We tested for an impact on leaf xylem hydraulic conductance (K_x) of cutting the petiole and minor veins under water for dehydrated leaves with xylem under tension compared with dehydrated leaves after previously relaxing xylem tension. Our results showed no significant ‘cutting artefact’ for leaf xylem. The lack of an effect for leaves could not be explained by narrower or shorter xylem conduits, and may be due to lesser mechanical stress imposed when cutting leaf petioles, and/or to rapid refilling of emboli in petioles. These findings provide the first validation of previous measurements of leaf hydraulic vulnerability against this potential artefact.     

木本植物木质部栓塞脆弱性研究新进展

木质部空穴化和栓塞是木本植物在干旱等条件下遭受水分胁迫时产生的木质部输水功能障碍, 在全球气候变化的大背景下, 栓塞脆弱性对干旱响应的研究已成为热点和重要内容。近年来有关木质部栓塞脆弱性与植物输水结构和耐旱性的关系已有大量研究并取得一定成果, 但是, 不同学者在不同地区对不同材料的研究结果存在很大不同。该文就近年来这一研究领域取得的成果及争议问题进行了概括和总结, 主要涉及木质部栓塞脆弱性(P₅₀)及脆弱曲线的建立方法、木质部栓塞脆弱性与木质部结构(导管直径、导管长度、纹孔膜、木质部密度、纤维及纤维管胞)间的关系和木质部栓塞脆弱性与耐旱性的关系, 并对未来工作进行展望, 提出在未来的工作中应对同一树种使用Cochard Cavitron离心机法、Sperry离心机技术与传统方法建立的脆弱曲线进行比较验证、计算P₅₀值、分析植物个体器官水平差异(根、茎、叶)、测定树种生理生态指标, 探索植物栓塞脆弱性与输水结构和耐旱性的关系, 从而评估不同类型植物在未来气候变化下的耐旱能力。     

A review of new research progress on the vulnerability of xylem embolism of woody plants

Xylem cavitation/embolism is the blockage of xylem conduits when woody plants suffer from water stress under drought and other environmental conditions, the study of embolism has become a hot and key topic under global climate change. Recent researches on the relationship between the vulnerability of xylem embolism and hydraulic architecture/drought tolerance have made some progress, however, scholars reached different conclusions based on results from different regions or different materials. This paper reviews the current achievements and controversial viewpoints, which includes indicator of xylem embolism vulnerability (P₅₀), method of vulnerability curve establishment, the relationship between embolism vulnerability and hydraulic architecture (vessel diameter, vessel length, pit area, wood density, fiber and fiber tracheid) and the relationship between embolism vulnerability and drought tolerance of woody plants. Future studies should use Cochard Cavitron centrifuge and Sperry centrifuge coupled with traditional methods to establish vulnerability curves, calculate P₅₀, analyze the difference among different organisms (root, stem, leaf), and measure physiological and ecological indexes. Future studies should be aimed to explore the relationship between the vulnerability of xylem embolism and hydraulic architecture/drought tolerance and to assess drought tolerance ability of different species under future climate change.     

Cavitation,stomatal conductance,and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought

Seedling shrubs in the Mediterranean semi-arid climate are subjected to intense droughts during summer. Thus, seedlings often surpass their limits of tolerance to water stress, resulting in the loss of hydraulic conductivity due to xylem cavitation. The response in terms of stomatal conductance, vulnerability to cavitation, leaf dieback, and survival were analysed in two co-occurring seedlings of mastic tree (Pistacia lentiscus L.) and kermes oak (Quercus coccifera L.) during an intense drought period. Both species reacted to drought with steep decreases in stomatal conductance before the critical water potential brought about the onset of cavitation events. Q. coccifera showed wider safety margins for avoiding runaway embolism than P. lentiscus and these differences could be related to the particular drought strategy displayed by each species: water saver or water spender. The limits for survival, resprout capacity and leaf dieback were also analysed in terms of loss of conductivity. By contrast with previous studies, the species showing higher seedling survival in the presence of drought also showed higher susceptibility to cavitation and operated with a lower safety margin for cavitation. Both species showed a leaf specific conductivity (LSC) threshold below which leaf biomass had to be regulated to avoid runaway embolism. However, each species displayed a different type of response: P. lentiscus conserved total leaf area up to 100% loss of LSC, whereas Q. coccifera continuously adjusted leaf biomass throughout the drought period in order to maintain the LSC very close to the maximum values recorded without loss of conductivity. Both species maintained the capacity for survival until the loss of conductivity was very nearly 100%.     

Vulnerability to embolism differs in roots and shoots and among three Mediterranean conifers: consequences for stomatal regulation of water loss?

We investigated the potential links between stomatal control of transpiration and the risk of embolism in root and shoot xylem of seedlings of three Mediterranean conifers (Cupressus sempervirens, Pinus halepensis and P. nigra) grown in a greenhouse under semi-controlled conditions. We measured the intrinsic vulnerability to embolism in roots and current year shoots by the air injection method. Root and shoot segments were subjected to increasing pressures, and the induced loss of hydraulic conductivity recorded. The three species displayed very different vulnerabilities in shoots, with P. nigra being much more vulnerable than P. halepensis and C. sempervirens. Roots were distinctly more vulnerable than shoots in C. sempervirens and P. halepensis (50% loss of conductivity induced at 3.0 MPa and 1.7 MPa higher xylem water potential in roots vs shoots). In P. nigra, no significant difference of vulnerability between shoots and roots was found. Seedlings were subjected to soil drought, and stomatal conductance, twig hydraulic conductivity and needle water potential were measured. The water potential resulting in almost complete stomatal closure (90%) was very close to the threshold water potential inducing loss of conductivity (10%) in twigs in P nigra, resulting in a very narrow safety margin between stomatal closure and embolism induction. The safety margin was larger in P. halepensis and greatest in C. sempervirens. Unexpectedly, this water potential threshold produced a 30–50% loss of conductivity in 3–5 mm diameter roots, depending on the species. The implications of this finding are discussed.     

Drought-Induced Xylem Dysfunction in Petioles,Branches, and Roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn

Variation in vulnerability to xylem cavitation was measured within individual organs of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Cavitation was quantified by three different techniques: (a) measuring acoustic emissions, (b) measuring loss of hydraulic conductance while air-dehydrating a branch, and (c) measuring loss of hydraulic conductance as a function of positive air pressure injected into the xylem. All of these techniques gave similar results. In Populus, petioles were more resistant than branches, and branches were more resistant than roots. This corresponded to the pattern of vessel width: maximum vessel diameter in 1- to 2-year-old roots was 140 [mu]m, compared to 65 and 45 [mu]m in rapidly growing 1-year-old shoots and petioles, respectively. Cavitation in Populus petioles started at a threshold water potential of -1.1 MPa. The lowest leaf water potential observed was -0.9 MPa. In Alnus, there was no relationship between vessel diameter and the cavitation response of a plant organ. Although conduits were narrower in petioles than in branches, petioles were more vulnerable to cavitation. Cavitation in petioles was detected when water potential fell below -1.2 MPa. This value equaled midday leaf water potential in late June. As in Populus, roots were the most vulnerable organ. The significance of different cavitation thresholds in individual plant organs is discussed.     

Interrelationships between water use and growth traits in biomass-producing willows

Abstract Water use, drought response and growth were examined under controlled conditions in four interbreeding willow species from different geographical origins (two clones of Salix viminalis L., one clone of S. viminalis × S. schwerenii E. Wolf and one clone of S. purpurea L.). The levels of soil water depletion that plants could sustain without wilting varied markedly between the clones. The level of drought resistance expressed this way was positively related to resistance to xylem cavitation, negatively related to the maximum stomatal conductance, and positively related to early stomatal closure. The rate of stomatal closure, however, was negatively related to the resistance to xylem cavitation. Prior to drought, there were no significant differences between leaf-specific hydraulic conductances of the clones when whole plants were considered. However, there were differences if the roots and shoots were considered separately. Drought resistance was negatively related to maximum growth yields. This is probably because resources were diverted away from leaf production to the production of denser wood (wood density was positively related to cavitation resistance), and, for one clone, to the growth of a larger root system. In addition, because the level of drought resistance was negatively related to the maximum stomatal conductance, growth may have been adversely affected as a result of reduced photosynthesis. Given its high water extraction ability, one of the clones started to wilt sooner than expected, although only lateral shoots were affected. This appeared to indicate a strategy of sacrificing expendable shoots.     

Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L.

Differences in the seasonal variation in stem water potential between the two shrub species Sorbus aucuparia and Sambucus nigra were related with their vulnerability to xylem cavitation. It was also demonstrated indirectly that the two species differ in the extent to which they reverse cavitation. Seasonal variation in stem water potential was investigated during three growing seasons with in situ stem psychrometers. Sorbus experienced wide water potential variations and reached a minimum of -4.2 MPa during drought. Under the same microclimatic conditions, Sambucus experienced consistent stem water potentials with a minimum of -1.7 MPa. The relationship between percentage loss in hydraulic conductivity (PLC) and water potential (hydraulic vulnerability curve) of the two species differed in shape: a flat curve with nearly total loss of conductivity at -6 MPa was found for SORBUS: Sambucus showed a steep vulnerability curve with 90% loss conductivity at -2.2 MPa. Thus, Sambucus is extremely vulnerable to cavitation, but Sorbus is an almost invulnerable species. This different cavitation resistance adjusted the ranges of field stem water potential that the species experienced. Finally, seasonal courses of naturally occurring (native) embolism were compared with calculated PLC courses. This comparison indicates that Sorbus did not refill embolized xylem vessels whereas Sambucus reversed embolism. It was concluded that species which are highly vulnerable to cavitation and drought-induced embolism need refilling of embolized vessels as well as isohydric water potential patterns as two strategies of survival.     

Unraveling the Effects of Plant Hydraulics on Stomatal Closure during Water Stress in Walnut

The objectives of the study were to identify the relevant hydraulic parameters associated with stomatal regulation during water stress and to test the hypothesis of a stomatal control of xylem embolism in walnut (Juglans regia x nigra) trees. The hydraulic characteristics of the sap pathway were experimentally altered with different methods to alter plant transpiration (Eplant) and stomatal conductance (gs). Potted trees were exposed to a soil water depletion to alter soil water potential (Psisoil), soil resistance (Rsoil), and root hydraulic resistances (Rroot). Soil temperature was changed to alter Rroot alone. Embolism was created in the trunk to increase shoot resistance (Rshoot). Stomata closed in response to these stresses with the effect of maintaining the water pressure in the leaf rachis xylem (P(rachis)) above -1.4 MPa and the leaf water potential (Psileaf) above -1.6 MPa. The same dependence of Eplant and gs on P(rachis) or Psileaf was always observed. This suggested that stomata were not responding to changes in Psisoil, Rsoil, Rroot, or Rshoot per se but rather to their impact on P(rachis) and/or Psileaf. Leaf rachis was the most vulnerable organ, with a threshold P(rachis) for embolism induction of -1.4 MPa. The minimum Psileaf values corresponded to leaf turgor loss point. This suggested that stomata are responding to leaf water status as determined by transpiration rate and plant hydraulics and that P(rachis) might be the physiological parameter regulated by stomatal closure during water stress, which would have the effect of preventing extensive developments of cavitation during water stress.     

Wood anatomy constrains stomatal responses to atmospheric vapor pressure deficit in irrigated, urban trees

Plant transpiration is strongly constrained by hydraulic architecture, which determines the critical threshold for cavitation. Because species vary greatly in vulnerability to cavitation, hydraulic limits to transpiration and stomatal conductance have not generally been incorporated into ecological and climate models. We measured sap flow, leaf transpiration, and vulnerability to cavitation of a variety of tree species in a well-irrigated but semi-arid urban environment in order to evaluate the generality of stomatal responses to high atmospheric vapor pressure deficit (D). We found evidence of broad patterns of stomatal responses to humidity based on systematic differences in vulnerability to cavitation. Ring-porous taxa consistently had vulnerable xylem and showed strong regulation of transpiration in response to D, while diffuse-porous taxa were less vulnerable and transpiration increased nearly linearly with D. These results correspond well to patterns in the distribution of the taxa, such as the prevalence of diffuse-porous species in riparian ecosystems, and also provide a means of representing maximum transpiration rates at varying D in broad categories of trees.     

Plant resistance to drought depends on timely stomatal closure

Stomata play a significant role in the Earth's water and carbon cycles, by regulating gaseous exchanges between the plant and the atmosphere. Under drought conditions, stomatal control of transpiration has long been thought to be closely coordinated with the decrease in hydraulic capacity (hydraulic failure due to xylem embolism). We tested this hypothesis by coupling a meta‐analysis of functional traits related to the stomatal response to drought and embolism resistance with simulations from a soil–plant hydraulic model. We report here a previously unreported phenomenon: the existence of an absolute limit by which stomata closure must occur to avoid rapid death in drought conditions. The water potential causing stomatal closure and the xylem pressure at the onset of embolism formation were equal for only a small number of species, and the difference between these two traits (i.e. safety margins) increased continuously with increasing embolism resistance. Our findings demonstrate the need to revise current views about the functional coordination between stomata and hydraulic traits and provide a mechanistic framework for modeling plant mortality under drought conditions.