Fulton E. Rockwell

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.

Cavitation and its discontents: opportunities for resolving current controversies

An understanding of cavitation and the spread of embolism in plant xylem can be viewed from the perspective of physical models of air seeding, the potential for artifacts to interact with natural variation in xylem structure, and new technologies that could lead to their resolution. Cavitation has long been recognized as a key constraint on the structure and functional integrity of the xylem. Yet, recent results call into question how well we understand cavitation in plants. Here, we consider embolism formation in angiosperms at two scales. The first focuses on how air-seeding occurs at the level of pit membranes, raising the question of whether capillary failure is an appropriate physical model. The second addresses methodological uncertainties that affect our ability to infer the formation of embolism and its reversal in plant stems. Overall, our goal is to open up fresh perspectives on the structure-function relationships of xylem.

The competition between liquid and vapor transport in transpiring leaves

The competition between internal liquid and vapor transport in transpiring leaves is sensitive to environmental drivers, the sites of evaporation in leaves varying with both leaf structure and external conditions. In leaves, the transpirational flux of water exits the veins as liquid and travels toward the stomata in both the vapor and liquid phases before exiting the leaf as vapor. Yet, whether most of the evaporation occurs from the vascular bundles (perivascular), from the photosynthetic mesophyll cells, or within the vicinity of the stomatal pore (peristomatal) remains in dispute. Here, a one-dimensional model of the competition between liquid and vapor transport is developed from the perspective of nonisothermal coupled heat and water molecule transport in a composite medium of airspace and cells. An analytical solution to the model is found in terms of the energy and transpirational fluxes from the leaf surfaces and the absorbed solar energy load, leading to mathematical expressions for the proportions of evaporation accounted for by the vascular, mesophyll, and epidermal regions. The distribution of evaporation in a given leaf is predicted to be variable, changing with the local environment, and to range from dominantly perivascular to dominantly peristomatal depending on internal leaf architecture, with mesophyll evaporation a subordinate component. Using mature red oak (Quercus rubra) trees, we show that the model can be solved for a specific instance of a transpiring leaf by combining gas-exchange data, anatomical measurements, and hydraulic experiments. We also investigate the effect of radiation load on the control of transpiration, the potential for condensation on the inside of an epidermis, and the impact of vapor transport on the hydraulic efficiency of leaf tissue outside the xylem.

Reversible Deformation of Transfusion Tracheids in Taxus baccata Is Associated with a Reversible Decrease in Leaf Hydraulic Conductance

The reversible collapse of leaf transfusion tracheids of Taxus baccata under desiccation is related to reversible declines in leaf hydraulic conductance, suggesting a circuit breaker-like function that protects the xylem from excessive tensions. Declines in leaf hydraulic conductance (Kleaf) with increasing water stress have been attributed to cavitation of the leaf xylem. However, in the leaves of conifers, the reversible collapse of transfusion tracheids may provide an alternative explanation. Using Taxus baccata, a conifer species without resin, we developed a modified rehydration technique that allows the separation of declines in Kleaf into two components: one reversible and one irreversible upon relaxation of water potential to −1 MPa. We surveyed leaves at a range of water potentials for evidence of cavitation using cryo-scanning electron microscopy and quantified dehydration-induced structural changes in transfusion tracheids by cryo-fluorescence microscopy. Irreversible declines in Kleaf did not occur until leaf water potentials were more negative than −3 MPa. Declines in Kleaf between −2 and −3 MPa were reversible and accompanied by the collapse of transfusion tracheids, as evidenced by cryo-fluorescence microscopy. Based on cryo-scanning electron microscopy, cavitation of either transfusion or xylem tracheids did not contribute to declines in Kleaf in the reversible range. Moreover, the deformation of transfusion tracheids was quickly reversible, thus acting as a circuit breaker regulating the flux of water through the leaf vasculature. As transfusion tissue is present in all gymnosperms, the reversible collapse of transfusion tracheids may be a general mechanism in this group for the protection of leaf xylem from excessive loads generated in the living leaf tissue.

Stomatal Closure, Basal Leaf Embolism, and Shedding Protect the Hydraulic Integrity of Grape Stems

Grape stomata are regulated to close before xylem cavitation. If the plant continues to dehydrate, basal leaf embolism and shedding protect the hydraulic integrity of younger leaves and the stem. The time scale of stomatal closure and xylem cavitation during plant dehydration, as well as the fate of embolized organs, are under debate, largely due to methodological limitations in the evaluation of embolism. While some argue that complete stomatal closure precedes the occurrence of embolism, others believe that the two are contemporaneous processes that are accompanied by daily xylem refilling. Here, we utilize an optical light transmission method to continuously monitor xylem cavitation in leaves of dehydrating grapevine (Vitis vinifera) in concert with stomatal conductance and stem and petiole hydraulic measurements. Magnetic resonance imaging was used to continuously monitor xylem cavitation and flow rates in the stem of an intact vine during 10 d of dehydration. The results showed that complete stomatal closure preceded the appearance of embolism in the leaves and the stem by several days. Basal leaves were more vulnerable to xylem embolism than apical leaves and, once embolized, were shed, thereby preventing further water loss and protecting the hydraulic integrity of younger leaves and the stem. As a result, embolism in the stem was minimal even when drought led to complete leaf shedding. These findings suggest that grapevine avoids xylem embolism rather than tolerates it.

Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation

Reversible collapse of the xylem in the smallest vein orders of red oak leaves buffers major veins from cavitation over time scales relevant to stomatal responses. We report a novel form of xylem dysfunction in angiosperms: reversible collapse of the xylem conduits of the smallest vein orders that demarcate and intrusively irrigate the areoles of red oak (Quercus rubra) leaves. Cryo-scanning electron microscopy revealed gradual increases in collapse from approximately −2 MPa down to −3 MPa, saturating thereafter (to −4 MPa). Over this range, cavitation remained negligible in these veins. Imaging of rehydration experiments showed spatially variable recovery from collapse within 20 s and complete recovery after 2 min. More broadly, the patterns of deformation induced by desiccation in both mesophyll and xylem suggest that cell wall collapse is unlikely to depend solely on individual wall properties, as mechanical constraints imposed by neighbors appear to be important. From the perspective of equilibrium leaf water potentials, petioles, whose vessels extend into the major veins, showed a vulnerability to cavitation that overlapped in the water potential domain with both minor vein collapse and buckling (turgor loss) of the living cells. However, models of transpiration transients showed that minor vein collapse and mesophyll capacitance could effectively buffer major veins from cavitation over time scales relevant to the rectification of stomatal wrong-way responses. We suggest that, for angiosperms, whose subsidiary cells give up large volumes to allow large stomatal apertures at the cost of potentially large wrong-way responses, vein collapse could make an important contribution to these plants’ ability to transpire near the brink of cavitation-inducing water potentials.

Iso/Anisohydry: A Plant–Environment Interaction Rather Than a Simple Hydraulic Trait

Plants are frequently classified as isohydric or anisohydric in an attempt to portray their water relations strategy or ecological niche. However, despite the popularity of the iso/anisohydric classification, the underlying biology remains unclear. We use here a simple hydraulic model and the extensive literature on grapevine hydraulics to illustrate that the iso/anisohydric classification of a plant depends on the definition used and the environment in which it is grown, rather than describing an intrinsic property of the plant itself. We argue that abandoning the iso/anisohydric terminology and returning to a more fundamental hydraulic framework would provide a stronger foundation for species comparisons and ecological predictions.

Leaf hydraulics II: Vascularized tissues

Current models of leaf hydration employ an Ohms law analogy of the leaf as an ideal capacitor, neglecting the resistance to flow between cells, or treat the leaf as a plane sheet with a source of water at fixed potential filling the mid-plane, neglecting the discrete placement of veins as well as their resistance. We develop a model of leaf hydration that considers the average conductance of the vascular network to a representative areole (region bounded by the vascular network), and represent the volume of tissue within the areole as a poroelastic composite of cells and air spaces. Solutions to the 3D flow problem are found by numerical simulation, and these results are then compared to 1D models with exact solutions for a range of leaf geometries, based on a survey of temperate woody plants. We then show that the hydration times given by these solutions are well approximated by a sum of the ideal capacitor and plane sheet times, representing the time for transport through the vasculature and tissue respectively. We then develop scaling factors relating this approximate solution to the 3D model, and examine the dependence of these scaling factors on leaf geometry. Finally, we apply a similar strategy to reduce the dimensions of the steady state problem, in the context of peristomatal transpiration, and consider the relation of transpirational gradients to equilibrium leaf water potential measurements.

Modelled hydraulic redistribution by sunflower (Helianthus annuus L.) matches observed data only after including night-time transpiration

The movement of water from moist to dry soil layers through the root systems of plants, referred to as hydraulic redistribution (HR), occurs throughout the world and is thought to influence carbon and water budgets and ecosystem functioning. The realized hydrologic, biogeochemical and ecological consequences of HR depend on the amount of redistributed water, whereas the ability to assess these impacts requires models that correctly capture HR magnitude and timing. Using several soil types and two ecotypes of sunflower (Helianthus annuus L.) in split-pot experiments, we examined how well the widely used HR modelling formulation developed by Ryel et al. matched experimental determination of HR across a range of water potential driving gradients. H. annuus carries out extensive night-time transpiration, and although over the last decade it has become more widely recognized that night-time transpiration occurs in multiple species and many ecosystems, the original Ryel et al. formulation does not include the effect of night-time transpiration on HR. We developed and added a representation of night-time transpiration into the formulation, and only then was the model able to capture the dynamics and magnitude of HR we observed as soils dried and night-time stomatal behaviour changed, both influencing HR.

Leaf Hydraulic Architecture and Stomatal Conductance: A Functional Perspective

Mechanistic modeling of water transport from petiole to stomata provides new perspectives on optimality in vascular and mesophyll transport properties.