Embolism recovery strategies and nocturnal water loss across species influenced by biogeographic origin

Drought‐induced tree mortality is expected to increase in future climates with the potential for significant consequences to global carbon, water, and energy cycles. Xylem embolism can accumulate to lethal levels during drought, but species that can refill embolized xylem and recover hydraulic function may be able to avoid mortality. Yet the potential controls of embolism recovery, including cross‐biome patterns and plant traits such as nonstructural carbohydrates (NSCs), hydraulic traits, and nocturnal stomatal conductance, are unknown. We exposed eight plant species, originating from mesic (tropical and temperate) and semi‐arid environments, to drought under ambient and elevated CO₂ levels, and assessed recovery from embolism following rewatering. We found a positive association between xylem recovery and NSCs, and, surprisingly, a positive relationship between xylem recovery and nocturnal stomatal conductance. Arid‐zone species exhibited greater embolism recovery than mesic zone species. Our results indicate that nighttime stomatal conductance often assumed to be a wasteful use of water, may in fact be a key part of plant drought responses, and contribute to drought survival. Findings suggested distinct biome‐specific responses that partially depended on species climate‐of‐origin precipitation or aridity index, which allowed some species to recover from xylem embolism. These findings provide improved understanding required to predict the response of diverse plant communities to drought. Our results provide a framework for predicting future vegetation shifts in response to climate change.     

植物干旱胁迫下水分代谢、碳饥饿与死亡机理

植物在生长发育过程中受众多环境因子共同作用。随着全球气候变化,气温升高、降水量下降等问题频繁出现。目前气象学家一致预测未来环境变暖会使干旱更加频繁剧烈,这一环境改变使植物死亡更加严重。植物在水分胁迫、特别是干旱胁迫条件下,体内水分代谢与碳代谢会发生失衡现象:光合速率降低、蒸腾速率降低,带来生长降低;为维持植物新陈代谢,植物呼吸作用必然下调。在长期干旱胁迫条件下植物体内碳水化合物储存发生失衡现象,这种失衡使植物陷入碳饥饿现象。另外,由于水分失衡而出现的木质部栓塞和空穴会进一步加剧水分运输障碍,而修复空穴则需要大量非结构性碳水化合物(NSC),这使植物陷入两难选择。总结了植物干旱胁迫下,碳饥饿与水分代谢、植物死亡关系的相关研究,对未来的研究方向和重点提出建议,以期对未来的植物死亡研究提供帮助。     

Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange

In woody plants, photosynthetic capacity is closely linked to rates at which the plant hydraulic system can supply water to the leaf surface. Drought‐induced embolism can cause sharp declines in xylem hydraulic conductivity that coincide with stomatal closure and reduced photosynthesis. Recovery of photosynthetic capacity after drought is dependent on restored xylem function, although few data exist to elucidate this coordination. We examined the dynamics of leaf gas exchange and xylem function in Eucalyptus pauciflora seedlings exposed to a cycle of severe water stress and recovery after re‐watering. Stomatal closure and leaf turgor loss occurred at water potentials that delayed the extensive spread of embolism through the stem xylem. Stem hydraulic conductance recovered to control levels within 6 h after re‐watering despite a severe drought treatment, suggesting an active mechanism embolism repair. However, stomatal conductance did not recover after 10 d of re‐watering, effecting tighter control of transpiration post drought. The dynamics of recovery suggest that a combination of hydraulic and non‐hydraulic factors influenced stomatal behaviour post drought.     

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.     

木本植物木质部的冻融栓塞应对研究进展

冻融栓塞在中高纬度地区木本植物中普遍存在。抗冻融栓塞能力对在寒冷环境中木本植物的生长和安全越冬十分关键, 这直接决定植物分布范围。冻融栓塞是由于冰中气体溶解度低, 木质部水分在低温下冷冻, 使之前水中溶解的气体逸出到导管中, 随后木质部中的冰融化又使气泡扩张而引发的栓塞现象。木质部解剖结构的差异会影响植物的抗冻融栓塞能力, 植物还可以通过调节木质部正压、代谢耗能等方式主动修复冻融栓塞, 也可通过增加树液溶质含量等逃避冷冻, 以减少低温损伤。然而, 与干旱栓塞相比, 目前对木质部冻融栓塞的形成以及植物响应和调节机制的理解不足。为此, 该文首先综述了木质部冻融栓塞的形成机制和植物的逃避、忍耐、修复等3种冻融栓塞的应对策略, 然后总结了木质部抗低温胁迫能力的生理表现、影响因子和评价指标, 并在此基础上讨论了低温抗性、干旱抗性和水力效率之间的多元权衡关系, 最后提出今后该领域中的5个优先研究问题: (1)不同植物冰冻的最低温度阈值; (2)是否存在应对低温胁迫的水力脆弱性分割机制; (3)冻融栓塞修复与代谢消耗的关系; (4)低温抗性、干旱抗性和水力效率之间的权衡关系; (5)抗冻融栓塞性状是否能够纳入经济性状谱系。     

荒漠河岸林植物木质部导水与栓塞特征及其对干旱胁迫的响应

 以同处于干旱区的塔里木河下游(铁干里克)和黑河下游(乌兰图格)断面为研究区, 比较了荒漠河岸林主要建群种胡杨(Populus euphratica)、柽柳(Tamarix spp.)、疏叶骆驼刺(Alhagi sparsifolia)和花花柴(Karelinia caspia)在长期遭受不同干旱胁迫下的根、枝条木质部导水力和栓塞化程度的变化特征, 并分析了木质部导水对干旱胁迫的响应及适应策略。结果表明: 1) 黑河下游荒漠河岸林植物的导水能力显著高于塔里木河下游, 其中柽柳、胡杨、疏叶骆驼刺和花花柴根木质部的初始比导率(K_s0)分别高11.97、6.74、7.10和3.73倍, 枝条的K_s0分别高9.48、3.65、2.07和1.88倍, 地下水埋深导致的干旱胁迫程度不同是诱发荒漠植物导水能力差异的根本原因; 2)柽柳耐干旱能力最强, 适应范围较宽, 而花花柴、疏叶骆驼刺的耐旱性相对较弱, 适生范围较窄, 这可能与植物的根系分布有关; 3)干旱胁迫较轻时, 枝条木质部是荒漠河岸林植物水分传输的主要阻力部位, 干旱胁迫严重时, 根木质部是限制植株水流的最大阻碍部位; 4)荒漠河岸林植物主要通过调节枝条木质部的水流阻力来适应干旱胁迫, 且其适应策略与干旱胁迫程度有关, 干旱胁迫轻时, 植物通过限制枝条木质部水流来协调整株植物的均匀生长; 干旱胁迫严重时, 植物通过牺牲劣势枝条、增强优势枝条水流来提高植株整体生存的机会。     

Intraspecific variation in embolism resistance and stem anatomy across four sunflower (Helianthus annuus L.) accessions

Drought‐induced xylem embolism is a key process closely related to plant mortality during extreme drought events. However, this process has been poorly investigated in crop species to date, despite the observed decline of crop productivity under extreme drought conditions. Interspecific variation in hydraulic traits has frequently been reported, but less is known about intraspecific variation in crops. We assessed the intraspecific variability of embolism resistance in four sunflower (Helianthus annuus L.) accessions grown in well‐watered conditions. Vulnerability to embolism was determined by the in situ flow‐centrifuge method (cavitron), and possible trade‐offs between xylem safety, xylem efficiency and growth were assessed. The relationship between stem anatomy and hydraulic traits was also investigated. Mean P ₅₀ was ?3 MPa, but significant variation was observed between accessions, with values ranging between ?2.67 and ?3.22 MPa. Embolism resistance was negatively related to growth and positively related to xylem‐specific hydraulic conductivity. There is, therefore, a trade‐off between hydraulic safety and growth but not between hydraulic safety and efficiency. Finally, we found that a few anatomical traits, such as vessel density and the area of the vessel lumen relative to that of the secondary xylem, were related to embolism resistance, whereas stem tissue lignification was not. Further investigations are now required to investigate the link between the observed variability of embolism resistance and yield, to facilitate the identification of breeding strategies to improve yields in an increasingly arid world.     

Dwarf shrub hydraulics: two Vaccinium species (Vaccinium myrtillus,Vaccinium vitis‐idaea) of the European Alps compared

Vaccinium myrtillus and Vaccinium vitis‐idaea are two dwarf shrubs widespread in the European Alps. We studied the hydraulics of these species hypothesizing that (1) the hydraulic architecture of dwarf shrubs differs from trees, (2) hydraulic properties reflect the species' ecological amplitude and (3) hydraulic properties vary spatially and seasonally. Key hydraulic parameters (osmotic potential, turgor loss point, xylem hydraulic conductivity, vulnerability to drought‐induced embolism, stomata closure, drought‐induced cell damage and embolism repair) and related wood anatomical traits (conduit diameter and conduit wall reinforcement) were analyzed at four sites in Tyrol, Austria. Both species exhibited low hydraulic safety as well as low hydraulic efficiency. Fifty percentage embolism accumulated at ?2.08 (V. myrtillus) and ?1.97 MPa (V. vitis‐idaea), 88% stomata closure was at ?2.19 and ?2.35 MPa, respectively. After drought, both species showed embolism repair on re‐watering. Site‐specific variation within species was low, while seasonal changes in embolism resistance and turgor loss point were observed. Results indicate that studied Vaccinium species have a high risk for embolism formation. This is balanced by refilling capacities, which are probably based on the small growth height of dwarf shrubs. V. vitis‐idaea, which occurs on drier sites, showed more efficient repair and a lower turgor loss point than V. myrtillus.     

Amazonia trees have limited capacity to acclimate plant hydraulic properties in response to long‐term drought

The fate of tropical forests under future climate change is dependent on the capacity of their trees to adjust to drier conditions. The capacity of trees to withstand drought is likely to be determined by traits associated with their hydraulic systems. However, data on whether tropical trees can adjust hydraulic traits when experiencing drought remain rare. We measured plant hydraulic traits (e.g. hydraulic conductivity and embolism resistance) and plant hydraulic system status (e.g. leaf water potential, native embolism and safety margin) on >150 trees from 12 genera (36 species) and spanning a stem size range from 14 to 68 cm diameter at breast height at the world's only long‐running tropical forest drought experiment. Hydraulic traits showed no adjustment following 15 years of experimentally imposed moisture deficit. This failure to adjust resulted in these drought‐stressed trees experiencing significantly lower leaf water potentials, and higher, but variable, levels of native embolism in the branches. This result suggests that hydraulic damage caused by elevated levels of embolism is likely to be one of the key drivers of drought‐induced mortality following long‐term soil moisture deficit. We demonstrate that some hydraulic traits changed with tree size, however, the direction and magnitude of the change was controlled by taxonomic identity. Our results suggest that Amazonian trees, both small and large, have limited capacity to acclimate their hydraulic systems to future droughts, potentially making them more at risk of drought‐induced mortality.     

How do fires kill plants? The hydraulic death hypothesis and Cape Proteaceae “fire-resisters”

The actual mechanism which causes plant death after having been burned has been poorly studied. One possibility is that fire causes direct, or indirect, fatal damage to plant hydraulic systems. If true, this suggests that burned plants ultimately die of drought. This hypothesis was tested on the post-fire response of a “fire-resister” species of the Cape Proteaceae, as well as by analysing its morphology. Fire-resisters are plants which are incapable of resprouting, but nevertheless survive some fires. Mortality of the studied fire-resister appears to be compatible with a hydraulic death hypothesis because i) most post-fire mortality occurred within days, ii) it occurred from the base-upwards and iii) correlated negatively with stem diameter rather than plant height. Higher levels of survival of the fire-resister is probably due to absolutely thicker bark than co-occurring re-seeder species of the same age. Since this bark has not evolved to protect buds, it has probably evolved to protect stem hydraulic systems.     

干旱对陆地生态系统生产力的影响

该文综述了干旱对陆地生态系统生产力的影响,分析了其影响机制,并总结了植被对干旱的响应与适应及其机理机制。干旱通过抑制光合作用来降低陆地生态系统总初级生产力,干旱还可以降低生态系统的自养呼吸和异养呼吸。同时干旱还可以通过影响其它干扰形式来间接影响陆地生态系统生产力,如增加火干扰的发生频率和强度,增加植物的死亡率,增加病虫害的发生等。在生态系统水平上干旱可以降低碳固定,减弱碳汇功能,甚至把生态系统从碳汇改变成碳源。目前生态系统水平上的干旱影响研究主要通过两种方法实现,一种是模型模拟,另一种就是大型模拟实验。作为陆地生态系统生产力的实现者,在干旱胁迫条件下,植物也会采取积极的适应策略以减弱干旱对生态系统生产力的影响,其适应策略主要分以下3种:在一些周期性发生干旱的地区,植物会调整生长期以避开干旱或通过休眠来减弱干旱所造成的伤害;还有一些植物会通过调节体内的代谢过程,改变一些生理特性来抵御干旱;而长期生活在干旱条件下的植物则通过进化来改变了自身的生理生化代谢过程,形成耐旱机制。目前,植物对干旱响应的分子学机制,以及生态系统水平上对干旱的响应和适应仍然是薄弱的领域,也必然成为未来研究的重点。     

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.     

X‐ray microtomography (micro‐CT): a reference technology for high‐resolution quantification of xylem embolism in trees

As current methods for measuring xylem embolism in trees are indirect and prone to artefacts, there is an ongoing controversy over the capacity of trees to resist or recover from embolism. The debate will not end until we get direct visualization of the vessel content. Here, we propose desktop X‐ray microtomography (micro‐CT) as a reference direct technique to quantify xylem embolism and thus validate more widespread measurements based upon either hydraulic or acoustic methods. We used desktop micro‐CT to measure embolism levels in dehydrated or centrifuged shoots of laurel – a long‐vesseled species thought to display daily cycles of embolism formation and refilling. Our direct observations demonstrate that this Mediterranean species is highly resistant to embolism and is not vulnerable to drought‐induced embolism in a normal range of xylem tensions. We therefore recommend that embolism studies in long‐vesseled species should be validated by direct methods such as micro‐CT to clear up any misunderstandings on their physiology.     

Water transport properties of seven woody species from the semi-arid Mu Us Sandy Land,China

Maintenance of water transport is very important for plant growth and survival. We studied seven woody species that inhabit the semi-arid Mu Us Sandy Land, China, to understand their strategies for maintaining hydraulic function. We evaluated water transport properties, including cavitation resistance, hydraulic recovery, and water loss regulation by stomatal control, which are associated with xylem structural and leaf physiological traits. We also discussed the water-use characteristics of these species by comparing them with those of species in other regions. Species with tracheids had higher levels of xylem resistance to cavitation and a smaller midday transpiration rate than the other species studied. Although species with vessels were less resistant to cavitation, some recovered hydraulic conductivity within 12 h of rehydration. Species with xylem tracheids could maintain their hydraulic function through resistance to cavitation and by relaxing xylem tension. Although species with vessels had less resistant xylem, they could maintain hydraulic function through hydraulic recovery even when xylem dysfunction occurred. Additionally, the species studied here were less resistant to cavitation than species in semi-arid environments, and equally or less resistant than species in humid environments. Rather than allow hydraulic dysfunction due to drought-induced dehydration, they may develop water absorption systems to avoid or recover quickly from hydraulic dysfunction. Thus, not only stem cavitation resistance to drought but also stem–root coordination should be considered when selecting plants for the revegetation of arid regions.     

Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation

Relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co‐occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar g_s temporal dynamics in response to drought. Further, whereas P. edulis exhibited chronic embolism, J. monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies.     

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.     

不同水分条件下两个树种木质部栓塞对P素添加的响应

 在两种水分供给(干旱胁迫和适宜水分,土壤含水量分别为田间持水量的30%～40%和70%～80%)下,研究了耐旱树种元宝枫(Acer truncatum)和 中生树种女贞(Ligustrum lucidum )木质部栓塞(以导水率(Percentage loss of hydraulic conductivity, PLC)损失程度衡量)对P素添加的 响应。结果发现,两个树种PLC的日变化均呈现出先上升后降低的规律,表明木质部栓塞的形成与恢复是植物体的一种平常事件;除适宜水分条 件的女贞外,P素可以显著提高元宝枫和遭受干旱胁迫时女贞的PLC;两种水分条件下,干旱胁迫时元宝枫木质部栓塞明显高于适宜水分供给时 。女贞的PLC在两种水分状况下无显著差异;树种间,干旱胁迫促进了元宝枫木质部的栓塞形成,明显高于同等水分条件下的女贞。该研究结果 证实了“木质部限流耐旱假设”。     

Drought resistance of Quercus pubescens as a function of root hydraulic conductance, xylem embolism and hydraulic architecture

Water relations, xylem embolism, root and shoot hydraulic conductance of both young plants in the field and potted seedlings of Quercus pubescens have been studied with the aim of investigating whether these variables may account for the well known adaptation of this oak species to arid habitats. Our data revealed that Q. pubescens is able to maintain high leaf relative water contents under water stress conditions. In fact, relative water contents measured in summer (July) did not differ from those recorded in April. This was apparently achieved by compensating water loss by an equal amount of water uptake. Such a drought avoidance strategy was made possible by the recorded high hydraulic efficiency of stems and roots under water stress. In fact, root hydraulic conductance of field-grown plants was maintained high in summer when the percentage loss of hydraulic conductance of stems was lowest. The hydraulic architecture of young plants of Q. pubescens measured in terms of partitioning of hydraulic resistances along the water pathway revealed that the highest hydraulic resistance was located in stems of the current year's growth. This hydraulic architecture is interpreted as consistent with the adaptation of Q. pubescens to arid habitats as a consequence of the recorded seasonal changes in water relation parameters as well as in root and stem hydraulics.     

Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?

Severe droughts have been associated with regional-scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, prediction remains difficult because the physiological mechanisms underlying drought survival and mortality are poorly understood. We developed a hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality. Multiple mechanisms may cause mortality during drought. A common mechanism for plants with isohydric regulation of water status results from avoidance of drought-induced hydraulic failure via stomatal closure, resulting in carbon starvation and a cascade of downstream effects such as reduced resistance to biotic agents. Mortality by hydraulic failure per se may occur for isohydric seedlings or trees near their maximum height. Although anisohydric plants are relatively drought-tolerant, they are predisposed to hydraulic failure because they operate with narrower hydraulic safety margins during drought. Elevated temperatures should exacerbate carbon starvation and hydraulic failure. Biotic agents may amplify and be amplified by drought-induced plant stress. Wet multidecadal climate oscillations may increase plant susceptibility to drought-induced mortality by stimulating shifts in hydraulic architecture, effectively predisposing plants to water stress. Climate warming and increased frequency of extreme events will probably cause increased regional mortality episodes. Isohydric and anisohydric water potential regulation may partition species between survival and mortality, and, as such, incorporating this hydraulic framework may be effective for modeling plant survival and mortality under future climate conditions.