Xylem Recovery Research Articles

A one-way ticket: Wheat roots do not functionally refill xylem emboli following rehydration

Abstract Understanding xylem embolism spread in roots is essential for predicting the loss of function across root systems during drought. However, the lasting relevance of root embolism to plant recovery depends on whether roots can refill xylem emboli and resume function after rehydration. Using MicroCT and optical and dye staining methods, we investigated embolism repair in rehydrated intact roots of wheat (Triticum aestivum L. ‘Krichauff’) exposed to a severe water deficit of −3.5 MPa, known to cause approximately 30% total root network embolism in this species. Air emboli in the xylem vessels of intact roots remained clearly observable using MicroCT after overnight rehydration. This result was verified by xylem staining of the root system and optical quantification of emboli, both of which indicated a lack of functional root xylem recovery 60 h following soil re-saturation. The absence of root xylem refilling in wheat has substantial implications for how we understand plant recovery after drought. Our findings suggest that xylem embolism causes irreversible damage to the soil–root hydraulic connection in affected parts of the root network.

Optimal stomatal drought response shaped by competition for water and hydraulic risk can explain plant trait covariation.

The classical theory of stomatal optimization stipulates that stomata should act to maximize photosynthesis while minimizing transpiration. This theory, despite its remarkable success in reproducing empirical patterns, does not account for the fact that the available water to plants is dynamically regulated by plants themselves, and that plants compete for water in most locations. Here, we develop an alternative theory in which plants maximize the expected carbon gain under stochastic rainfall in a competitive environment. We further incorporate xylem hydraulic limitation as an additional constraint to transpiration and evaluate its impacts on stomatal optimization by incorporating the direct carbon cost of xylem recovery and the opportunity cost of reduced future photosynthesis as a result of irrecoverable xylem damage. We predict stomatal behaviour to be more conservative with a higher cost induced by xylem damage. By varying the unit carbon cost and extent of xylem recovery, characterizing the direct and opportunity cost of xylem damage, respectively, our model can reproduce several key patterns of stomatal-hydraulic trait covariations. By addressing the key elements of water limitation in plant gas exchange simultaneously, including plants' self-regulation of water availability, competition for water and hydraulic risk, our study provides a comprehensive theoretical basis for understanding stomatal behaviour.

Repair of severe winter xylem embolism supports summer water transport and carbon gain in flagged crowns of the subalpine conifer Abies veitchii.

Xylem embolism induced by winter drought is a serious dysfunction in evergreen conifers growing at wind-exposed sites in the mountains. Some coniferous species can recover from winter embolism. The aim of this study was to determine whether wind direction influences embolism formation and/or repair dynamics on short windward and long leeward branches of asymmetrical `flagged' crowns. We analyzed the effect of branch orientation on percentage loss of xylem conductive area (PLC), leaf functional traits and the xylem:leaf area ratio for subalpine, wind-exposed flagged-crown Abies veitchii trees in the northern Yatsugatake Mountains of central Japan. In late winter, the shoot water potential was below -2.5MPa, and the PLC exceeded 80% in 2-year-old branches, independent of branch orientation within a flagged crown. Both of these parameters almost fully recovered by summer. At branch internodes 4years of age and older, seasonal changes in PLC were not found in either windward or leeward branches, but the PLC was higher in less leafy windward branches. The leaf nitrogen content and water-use efficiency of mature leaves were comparable between windward branches and leafy leeward branches. The ratio of xylem conductive area to total leaf area was the same for windward and leeward branches. These results indicate that the repair of winter xylem embolism allows leaf physiological functions to be maintained under sufficient leaf water supply, even on winter-wind-exposed branches. This permits substantial photosynthetic carbon gain during the following growing season on both windward and leeward branches. Thus, xylem recovery from winter embolism is a key trait for the survival of harsh winters and to support productivity on the individual level in flagged-crown A. veitchii trees.

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.

Traits of stem anatomy of some herbaceous members of the family Polygonaceae Juss.

The stem anatomy of the vine Fallopia convolvulus (L.) A. Love and that of the self-supporting plant Polygonum patulum M. Bieb. is described. Two groups of tracheary system—few wide elements and many narrow ones—are present in the xylem of the herbaceous vine. The maximum vessel diameters are far greater in Fallopia convolvulus than in Polygonum patulum. Such traits are typical of woody lianas and their self-supporting relatives. The cambium can give rise to wide vessels inward of separate phloem strands in Fallopia convolvulus. The newly formed vessels may substitute for the injured ones. This favors xylem recovery from a drought-induced embolism.

Traits to stay, traits to move: a review of functional traits to assess sensitivity and adaptive capacity of temperate and boreal trees to climate change

The integration of functional traits into vulnerability assessments is a promising approach to quantitatively capture differences in species sensitivity and adaptive capacity to climate change, allowing the refinement of tree species distribution models. In response to a clear need to identify traits that are responsive to climate change and applicable in a management context, we review the state of knowledge of the main mechanisms, and their associated traits, that underpin the ability of boreal and temperate tree species to persist and (or) shift their distribution in a changing climate. We aimed to determine whether current knowledge is sufficiently mature and available to be used effectively in vulnerability assessments. Marshalling recent conceptual advances and assessing data availability, our ultimate objective is to guide modellers and practitioners in finding and selecting sets of traits that can be used to capture differences in species’ ability to persist and migrate. While the physiological mechanisms that determine sensitivity to climate change are relatively well understood (e.g., drought-induced cavitation), many associated traits have not been systematically documented for North American trees and differences in methodology preclude their widespread integration into vulnerability assessments (e.g., xylem recovery capacity). In contrast, traits traditionally associated with the ability to migrate and withstand fire are generally well documented, but new key traits are emerging in the context of climate change that have not been as well characterized (e.g., age of optimum seed production). More generally, lack of knowledge surrounding the extent and patterns in intraspecific trait variation, as well as co-variation and interaction among traits, limit our ability to use this approach to assess tree adaptive capacity. We conclude by outlining research needs and potential strategies for the development of trait-based knowledge applicable in large-scale modelling efforts, sketching out important aspects of trait data organization that should be part of a coordinated effort by the forest science community.

Mechanisms of xylem embolism repair in woody plants: Research progress and questions

To maintain long-distance water transport in woody plants is critical for their survival, growth and development. Water under tension is in a metastable state and prone to cavitation and embolism, which leads to loss of hydraulic conductance, reduced productivity, and eventually plant death. In face to water stress-induced cavitation, plants either reduce frequency of embolism occurrence through cavitation resistance with specialized anatomical struc- ture, or/and form a metabolically active embolism repair mechanism. For the xylem embolism and repair, how- ever, there are controversies regarding the occurring frequency, conditions and underlying mechanisms. In this review paper, we first examined the process, temporal dynamics and frequency of xylem embolism and repair. Then, we summarized hypotheses for the mechanisms of the novel refilling in xylem embolism repair, including the osmotic hypothesis, the reverse osmotic hypothesis, the phloem-driven refilling hypothesis, and the phloem unloading hypothesis. We further compared differences in xylem embolism and repair between conifers and an- giosperms tree species, and examined the trade-offs between cavitation resistance and xylem recovery perform- ance. Finally, we proposed four priorities in future research in this field: (1) to improve measuring technology of xylem embolism; (2) to test hypotheses for the mechanisms of the novel refilling in xylem embolism repair and the signal triggering xylem refilling; (3) to explore species-specific trait differences related to xylem embolism and repair and their underlying trade-off relationships; and (4) to enhance studies on the relationship between the involvement of carbon metabolism and aquaporins expression in xylem embolism and repair.

Xylem recovery from drought-induced embolism: where is the hydraulic point of no return?

Xylem recovery from drought-induced embolism: where is the hydraulic point of no return?

Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species

Woody species hydraulically vulnerable to xylem cavitation may experience daily xylem embolism. How such species cope with the possibility of accumulated embolism is unclear. In this study, we examined seven temperate woody species to assess the hypothesis that low cavitation resistance (high vulnerability to cavitation) is compensated by high recovery performance via vessel refilling. We also evaluated leaf functional and xylem structural traits. The xylem recovery index (XRI), defined as the ratio of xylem hydraulic conductivity in plants rewatered after soil drought to that in plants under moist conditions, varied among species. The xylem water potential causing 50% loss of hydraulic conductivity (Ψ50) varied among the species studied, whereas only a slight difference was detected with respect to midday xylem water potential (Ψmin), indicating smaller hydraulic safety margins (Ψmin - Ψ50) for species more vulnerable to cavitation. Cavitation resistance (|Ψ50|) was negatively correlated with XRI across species, with cavitation-vulnerable species showing a higher performance in xylem recovery. Wood density was positively correlated with cavitation resistance and was negatively correlated with XRI. These novel results reveal that coordination exists between cavitation resistance and xylem recovery performance, in association with wood functional traits such as denser wood for cavitation-resistant xylem and less-dense but water-storable wood for refillable xylem. These findings provide insights into long-term maintenance of water transport in tree species growing under variable environmental conditions.

Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale.

Recent large-scale studies of tree growth in the Iberian Peninsula reported contrasting positive and negative effects of temperature in Mediterranean angiosperms and conifers. Here we review the different hypotheses that may explain these trends and propose that the observed contrasting responses of tree growth to temperature in this region could be associated with a continuum of trait differences between angiosperms and conifers. Angiosperm and conifer trees differ in the effects of phenology in their productivity, in their growth allometry, and in their sensitivity to competition. Moreover, angiosperms and conifers significantly differ in hydraulic safety margins, sensitivity of stomatal conductance to vapor-pressure deficit (VPD), xylem recovery capacity or the rate of carbon transfer. These differences could be explained by key features of the xylem such as non-structural carbohydrate content (NSC), wood parenchymal fraction or wood capacitance. We suggest that the reviewed trait differences define two contrasting ecophysiological strategies that may determine qualitatively different growth responses to increased temperature and drought. Improved reciprocal common garden experiments along altitudinal or latitudinal gradients would be key to quantify the relative importance of the different hypotheses reviewed. Finally, we show that warming impacts in this area occur in an ecological context characterized by the advance of forest succession and increased dominance of angiosperm trees over extensive areas. In this context, we examined the empirical relationships between the responses of tree growth to temperature and hydraulic safety margins in angiosperm and coniferous trees. Our findings suggest a future scenario in Mediterranean forests characterized by contrasting demographic responses in conifer and angiosperm trees to both temperature and forest succession, with increased dominance of angiosperm trees, and particularly negative impacts in pines.

Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel).

Xylem recovery from embolism was studied in stems of Laurus nobilis L. that were induced to cavitate by combining negative xylem pressures with positive air pressures applied with a pressure collar. Xylem refilling was measured 2 and 20 min and 15 h after air pressure release in January, March and June when increasing percentages of wood parenchyma cells with high starch content (HSC-VAC) were counted (from 0% in January to 87.3% in June). In January, no xylem repair was measured. In June, stems refilled by 75% of previous conductivity loss with a parallel decrease of HSC-VAC. Xylem refilling was tested for stems with phloem either intact or excised by 20 and 50% and with phloem inactivated by girdling stems at both sides of the embolised segment. Stems with 50% of the cortex removed showed some recovery 15 h after embolism. Girdled stems did not recover from embolism and no starch depolymerisation was measured. Girdled stems where a radial mechanical pressure was applied for 20 min after embolism refilled in the same way as stems with intact phloem. Our conclusion is that phloem may export some signal for starch depolymerisation and this, in turn, would drive sugar efflux into embolised conduits with consequent osmotic water flows and refilling.

Mechanisms of xylem recovery from winter embolism in Fagus sylvatica.

Hydraulic conductivity in the terminal branches of mature beech trees (Fagus sylvatica L.) decreased progressively during winter and recovered in the spring. The objective of this study was to determine the mechanisms involved in recovery. Two periods of recovery were identified. The first recovery of hydraulic conductivity occurred early in the spring, before bud break, and was correlated with the occurrence of positive xylem pressure at the base of the tree trunk. Active refilling of the embolized vessels caused the recovery. The second recovery of hydraulic conductivity occurred after bud break and was correlated with the onset of cambial activity. Formation of new functional vessels, leading to an increase in xylem diameter, was largely responsible for the increase in xylem conductivity. The two mechanisms were complementary: active refilling of embolized vessels occurred mostly in the root and the trunk, whereas formation of new functional vessels occurred mainly in young terminal shoots.

Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism.

Xylem recovery from cavitation-induced embolism was studied in l-yr-old twigs of Laurus mibilis L. Cavitation was induced by applying pre-established pressure differentials (AP0,1 ) across the pit membranes of xylem conduits. ΔP0 ) were 1.13, 1.75 and 2.26 MPa, corresponding to about 50, 77 und 100% of the measured leaf water potential at the rurgor loss point ΔP0,1 were obtained either by increasing xylem tensions or by applying positive pressures from outside, or by a combination of the two. The percentage loss of hydraulic conductivity (PLC) did not change, regardless of how the ΔP0-1 were obtained. This confirmed that xylem cavitation was nucleated by microbubbles from outside the vessels. Positive pressures, however, amplified (up to 75%) and sped up the xylem refilling (20 min) in comparison with that measured in unpressurized twigs (c.50% in 15 h). Twigs girdled proximally to their pressurized segment 1 nun after the desired pressure value had been reached, did not recover from embolism. The later the twigs were girdled with respect to when they were tested for PLC, the higher was their recovery from embolism, suggesting that some messenger was transported in the phloem which stimulated xylem refilling. Indol-3-acetic acid (1AA] applied to the exposed cortex of both pressurized and unpressurized twigs, induced an almost complete recovery from PLC. We hypothesize that the refilling of cavitated xylem might be a result of an auxin-induced increase in the phloem loading with solutes. This would cause radial transport of solutes to cavitated xylem conduits via the rays, thus decreasing their osmotic potential and making them refill. No positive xylem pressure potentials were measured during xylem recovery from PLC.