Bubbles of gas trapped in the xylem during freezing are a major cause of damage for trees growing at high altitudes or latitudes, as the bubbles may cause embolism during thawing. Yet the factors ...controlling bubble formation upon freeze–thaw cycles remain poorly understood. Especially the size of the bubbles formed in the ice is crucial for winter embolism formation. We used high‐resolution X‐ray microtomography combined with freezing experiments to investigate the size and shape of 68,343 gas bubbles in frozen conduits in branches of Betula pendula. We also studied how conduit size, tree water status (−0.2 MPa vs. −0.6 MPa) and bark permeability to gases (decreased by Vaseline‐coating) affect the gas bubbles characteristics. High‐resolution X‐ray images allowed us to detect gas bubbles down to 1.0 μm in diameter and revealed that not only small spherical gas bubbles but also gaseous volumes of various shapes and sizes were found from the frozen xylem indicating that gas bubbles may have started to grow already during the freezing propagation. Most of the gas bubbles were found in fibers, but the rare gas bubbles found in the vessels were larger than those in the fibers. Bubble volume increased with conduit volume in both fibers and vessels, but conduit size alone could not explain gas bubble volume. Low water potential and restriction of gas escape from the branch seem to cause more, larger, and less spherical bubbles and thus increase the risk of embolism formation. These findings open new research avenues for further studies of winter embolism formation.
ABSTRACT
Carbon uptake and transpiration in plant leaves occurs through stomata that open and close. Stomatal action is usually considered a response to environmental driving factors. Here we show ...that leaf gas exchange is more strongly related to whole tree level transport of assimilates than previously thought, and that transport of assimilates is a restriction of stomatal opening comparable with hydraulic limitation. Assimilate transport in the phloem requires that osmotic pressure at phloem loading sites in leaves exceeds the drop in hydrostatic pressure that is due to transpiration. Assimilate transport thus competes with transpiration for water. Excess sugar loading, however, may block the assimilate transport because of viscosity build‐up in phloem sap. Therefore, for given conditions, there is a stomatal opening that maximizes phloem transport if we assume that sugar loading is proportional to photosynthetic rate. Here we show that such opening produces the observed behaviour of leaf gas exchange. Our approach connects stomatal regulation directly with sink activity, plant structure and soil water availability as they all influence assimilate transport. It produces similar behaviour as the optimal stomatal control approach, but does not require determination of marginal cost of water parameter.
Requiring stomata to open such that assimilate transport from leaves is maximized reproduces known plant responses of stomatal conductance to various environmental conditions, above and below ground, in a single theoretical framework. The model agrees with field observations and produces similar behavior than the optimal stomatal control approach. However, here no marginal cost of water is needed but the stomatal behavior results from axial and radial water flows and the osmotic competition for water between phloem and the transpiration stream.
The quantification of cambial growth over short time periods has been hampered by problems to discern between growth and the swelling and shrinking of a tree stem. This paper presents a model, which ...separates cambial growth and reversible water‐potential induced diurnal changes from simultaneously measured whole stem and xylem radial variations, from field‐measured Scots pine trees in Finland. The modelled growth, which includes osmotic concentration changes, was compared with (direct) dendrometer measurements and microcore samples. In addition, the relationship of modelled growth and dendrometer measurements to environmental factors was analysed. The results showed that the water‐potential induced changes of tree radius were successfully separated from stem growth. Daily growth predicted by the model exhibited a high correlation with the modelled daily changes of osmotic concentration in phloem, and a temperature dependency in early summer. Late‐summer growth saw higher dependency on water availability and temperature. Evaluation of the model against dendrometer measurements showed that the latter masked a true environmental signal in stem growth due to water‐potential induced changes. The model provides better understanding of radial growth physiology and offers potential to examine growth dynamics and changes due to osmotic concentration, and how the environment affects growth.
Understanding stomatal regulation is fundamental to predicting the impact of changing environmental conditions on vegetation. However, the influence of soil temperature (ST) and soil water content ...(SWC) on canopy conductance (gs) through changes in belowground hydraulic conductance (kbg) remains poorly understood, because kbg has seldom been measured in field conditions. Our aim was to (a) examine the dependence of kbg on ST and SWC, (b) examine the dependence of gs on kbg and (c) test a recent stomatal optimization model according to which gs and soil‐to‐leaf hydraulic conductance are strongly coupled. We estimated kbg from continuous sap flow and xylem diameter measurements in three boreal species. kbg increased strongly with increasing ST when ST was below +8°C, and typically increased with increasing SWC when ST was not limiting. gs was correlated with kbg in all three species, and modelled and measured gs were well correlated in Pinus sylvestris (a model comparison was only possible for this species). These results imply an important role for kbg in mediating linkages between the soil environment and leaf gas exchange. In particular, our finding that ST strongly influences kbg in mature trees may help us to better understand tree behaviour in cold environments.
Soil temperature and water content are important factors influencing belowground hydraulic conductance and canopy conductance in mature boreal trees.
Background and AimsTree models simulate productivity using general gas exchange responses and structural relationships, but they rarely check whether leaf gas exchange and resulting water and ...assimilate transport and driving pressure gradients remain within acceptable physical boundaries. This study presents an implementation of the cohesion–tension theory of xylem transport and the Münch hypothesis of phloem transport in a realistic 3-D tree structure and assesses the gas exchange and transport dynamics.MethodsA mechanistic model of xylem and phloem transport was used, together with a tested leaf assimilation and transpiration model in a realistic tree architecture to simulate leaf gas exchange and water and carbohydrate transport within an 8-year-old Scots pine tree. The model solved the dynamics of the amounts of water and sucrose solute in the xylem, cambium and phloem using a fine-grained mesh with a system of coupled ordinary differential equations.Key ResultsThe simulations predicted the observed patterns of pressure gradients and sugar concentration. Diurnal variation of environmental conditions influenced tree-level gradients in turgor pressure and sugar concentration, which are important drivers of carbon allocation. The results and between-shoot variation were sensitive to structural and functional parameters such as tree-level scaling of conduit size and phloem unloading.ConclusionsLinking whole-tree-level water and assimilate transport, gas exchange and sink activity opens a new avenue for plant studies, as features that are difficult to measure can be studied dynamically with the model. Tree-level responses to local and external conditions can be tested, thus making the approach described here a good test-bench for studies of whole-tree physiology.
Accurate modelling of drought-induced mortality is challenging. A steady-state model is presented integrating xylem and phloem transport, leaf-level gas exchange and plant carbohydrate consumption ...during drought development.
A Bayesian analysis of parameter uncertainty based on expert knowledge and a literature review is carried out. The model is tested by combining six data compilations covering 170 species using information on sensitivities of xylem conductivity, stomatal conductance and leaf turgor to water potential.
The possible modes of plant failure at steady state are identified (i.e. carbon (C) starvation, hydraulic failure and phloem transport failure). Carbon starvation occurs primarily in the parameter space of isohydric stomatal control, whereas hydraulic failure is prevalent in the space of xylem susceptibility to embolism. Relative to C starvation, phloem transport failure occurs under conditions of low sensitivity of photosynthesis and high sensitivity of growth to plant water status.
These three failure modes are possible extremes along two axes of physiological vulnerabilities, one characterized by the balance of water supply and demand and the other by the balance between carbohydrate sources and sinks. Because the expression of physiological vulnerabilities is coordinated, we argue that different failure modes should occur with roughly equal likelihood, consistent with predictions using optimality theory.
Trees must simultaneously balance their CO2 uptake rate via stomata, photosynthesis, the transport rate of sugars and rate of sugar utilization in sinks while maintaining a favourable water and ...carbon balance. We demonstrate using a numerical model that it is possible to understand stomatal functioning from the viewpoint of maximizing the simultaneous photosynthetic production, phloem transport and sink sugar utilization rate under the limitation that the transpiration-driven hydrostatic pressure gradient sets for those processes. A key feature in our model is that non-stomatal limitations to photosynthesis increase with decreasing leaf water potential and/or increasing leaf sugar concentration and are thus coupled to stomatal conductance. Maximizing the photosynthetic production rate using a numerical steady-state model leads to stomatal behaviour that is able to reproduce the well-known trends of stomatal behaviour in response to, e.g., light, vapour concentration difference, ambient CO2 concentration, soil water status, sink strength and xylem and phloem hydraulic conductance. We show that our results for stomatal behaviour are very similar to the solutions given by the earlier models of stomatal conductance derived solely from gas exchange considerations. Our modelling results also demonstrate how the 'marginal cost of water' in the unified stomatal conductance model and the optimal stomatal model could be related to plant structural and physiological traits, most importantly, the soil-to-leaf hydraulic conductance and soil moisture.
Measurements of diurnal diameter variations of the xylem and phloem are a promising tool for studying plant hydraulics and xylem-phloem interactions in field conditions. However, both the theoretical ...framework and the experimental verification needed to interpret phloem diameter data are incomplete. In this study, we analytically evaluate the effects of changing the radial conductance between the xylem and the phloem on phloem diameter variations and test the theory using simple manipulation experiments. Our results show that phloem diameter variations are mainly caused by changes in the radial flow rate of water between the xylem and the phloem. Reducing the hydraulic conductance between these tissues decreases the amplitude of phloem diameter variation and increases the time lag between xylem and phloem diameter variation in a predictable manner. Variation in the amplitude and timing of diameter variations that cannot be explained by changes in the hydraulic conductance, could be related to changes in the osmotic concentration in the phloem.
Abstract
The size-related xylem adjustments required to maintain a constant leaf-specific sapwood conductance (KLEAF) with increasing height (H) are still under discussion. Alternative hypotheses are ...that: (i) the conduit hydraulic diameter (Dh) at any position in the stem and/or (ii) the number of sapwood rings at stem base (NSWr) increase with H. In addition, (iii) reduced stem elongation (ΔH) increases the tip-to-base conductance through inner xylem rings, thus possibly the NSWr contributing to KLEAF. A detailed stem analysis showed that Dh increased with the distance from the ring apex (DCA) in all rings of a Picea abies and a Fagus sylvatica tree. Net of DCA effect, Dh did not increase with H. Using sapwood traits from a global dataset, NSWr increased with H, decreased with ΔH, and the mean sapwood ring width (SWrw) increased with ΔH. A numerical model based on anatomical patterns predicted the effects of H and ΔH on the conductance of inner xylem rings. Our results suggest that the sapwood/heartwood transition depends on both H and ΔH, and is set when the carbon allocation to maintenance respiration of living cells in inner sapwood rings produces a lower gain in total conductance than investing the same carbon in new vascular conduits.
The sapwood/heartwood transition is hydraulically determined by the combined effects of conduit widening, tree height, and height growth rate on the contribution of inner rings to the total xylem conductance.
Model–data comparisons of plant physiological processes provide an understanding of mechanisms underlying vegetation responses to climate. We simulated the physiology of a piñon pine–juniper woodland ...(Pinus edulis–Juniperus monosperma) that experienced mortality during a 5 yr precipitation-reduction experiment, allowing a framework with which to examine our knowledge of drought-induced tree mortality. We used six models designed for scales ranging from individual plants to a global level, all containing state-of-the-art representations of the internal hydraulic and carbohydrate dynamics of woody plants. Despite the large range of model structures, tuning, and parameterization employed, all simulations predicted hydraulic failure and carbon starvation processes co-occurring in dying trees of both species, with the time spent with severe hydraulic failure and carbon starvation, rather than absolute thresholds per se, being a better predictor of impending mortality. Model and empirical data suggest that limited carbon and water exchanges at stomatal, phloem, and below-ground interfaces were associated with mortality of both species. The model–data comparison suggests that the introduction of a mechanistic process into physiology-based models provides equal or improved predictive power over traditional process-model or empirical thresholds. Both biophysical and empirical modeling approaches are useful in understanding processes, particularly when the models fail, because they reveal mechanisms that are likely to underlie mortality. We suggest that for some ecosystems, integration of mechanistic pathogen models into current vegetation models, and evaluation against observations, could result in a breakthrough capability to simulate vegetation dynamics.
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