Evaporation-driven internal hydraulic redistribution alleviates root drought stress: Mechanisms and modeling.

Many tree species have developed extensive root systems that allow them to survive in arid environments by obtaining water from a large soil volume. These root systems can transport and redistribute soil water during drought by hydraulic redistribution (HR). A recent study revealed the phenomenon of evaporation-driven hydraulic redistribution (EDHR), which is driven by evaporative demand (transpiration). In this study, we confirmed the occurrence of EDHR in Chinese white poplar (Populus tomentosa) through root sap flow measurements. We utilized microcomputed tomography technology to reconstruct the xylem network of woody lateral roots and proposed conceptual models to verify EDHR from a physical perspective. Our results indicated that EDHR is driven by the internal water potential gradient within the plant xylem network, which requires 3 conditions: high evaporative demand, soil water potential gradient, and special xylem structure of the root junction. The simulations demonstrated that during periods of extreme drought, EDHR could replenish water to dry roots and improve root water potential up to 38.9% to 41.6%. This highlights the crucial eco-physiological importance of EDHR in drought tolerance. Our proposed models provide insights into the complex structure of root junctions and their impact on water movement, thus enhancing our understanding of the relationship between xylem structure and plant hydraulics.

An undiscovered facet of hydraulic redistribution driven by evaporation-a study from a Populus tomentosa plantation.

Maintaining the activity and function of the shallow root system of plants is essential for withstanding drought stress, but the associated mechanism is poorly understood. By investigating sap flow in 14 lateral roots (LRs) randomly selected from trees of a Chinese white poplar (Populus tomentosa) plantation receiving three levels of irrigation, an unknown root water transport mode of simultaneous daytime bi-directional water flow was discovered. This mode existed in five LRs confined to the surface soil without attached sinker roots. In the longer term, the bi-directional water flow was correlated with the soil water content. However, within the day, it was associated with transpiration. Our data demonstrated that bi-directional root sap flow occurred during the day, and was driven by evaporative demand, further suggesting the existence of circumferential water movement in the LR xylem. We named this phenomenon evaporation-driven hydraulic redistribution (EDHR). A soil-root water transport model was proposed to encapsulate this water movement mode. EDHR may be a crucial drought-tolerance mechanism that allows plants to maintain shallow root survival and activity by promoting root water recharge under extremely dry conditions.

Root grafts matter for inter-tree water exchange - a quantification of water translocation between root grafted mangrove trees using field data and model based indication.

BACKGROUND AND AIMS: Trees interconnected through functional root grafts can exchange resources, but the effect of exchange on trees remains under debate. A mechanistic understanding of resources exchange via functional root grafts will help understand their ecological implications for tree water exchange for individual trees, groups of trees, and forest stands. METHODS: To identify the main patterns qualitatively describing the movement of sap between grafted trees, we reviewed available literature on root grafting in woody plants that focus on tree allometry and resource translocation via root grafts. We then extended the BETTINA model, which simulates mangrove (Avicennia germinans) tree growth on the individual tree scale, in order to synthesize the available empirical information. Using allometric data from a field study in mangrove stands, we simulated potential water exchange and analyzed movement patterns between grafted trees. KEY RESULTS: In the simulations, relative water exchange ranged between -9.17 and 20.3 %, and was driven by gradients of water potential, i.e. differences in tree size and water availability. Moreover, the exchange of water through root grafts alters the water balance of trees and their feedback with the soil: grafted trees that receive water from their neighbors reduce their water uptake. CONCLUSIONS: Our individual-tree modelling study is a first theoretical attempt to quantify root graft-mediated water exchange between trees. Our findings indicate that functional root grafts represent a vector of hydraulic redistribution, helping to maintain the water balance of grafted trees. This non-invasive approach can serve as a fundament for designing empirical studies to better understand the role of grafted root interaction networks on a broader scale.

Root grafts matter for inter-tree water exchange - a quantification of water translocation between root grafted mangrove trees using field data and model-based indications.

BACKGROUND AND AIMS: Trees interconnected through functional root grafts can exchange resources, but the effect of exchange on trees remains under debate. A mechanistic understanding of resource exchange via functional root grafts will help understand their ecological implications for tree water exchange for individual trees, groups of trees and forest stands. METHODS: To identify the main patterns qualitatively describing the movement of sap between grafted trees, we reviewed the available literature on root grafting in woody plants that focus on tree allometry and resource translocation via root grafts. We then extended the BETTINA model, which simulates mangrove (Avicennia germinans) tree growth on the individual tree scale, to synthesize the available empirical information. Using allometric data from a field study in mangrove stands, we simulated potential water exchange and analysed movement patterns between grafted trees. KEY RESULTS: In the simulations, relative water exchange ranged between -9.17 and 20.3 %, and was driven by gradients of water potential, i.e. differences in tree size and water availability. Moreover, the exchange of water through root grafts alters the water balance of trees and their feedback with the soil: grafted trees that receive water from their neighbours reduce their water uptake. CONCLUSIONS: Our individual-tree modelling study is a first theoretical attempt to quantify root graft-mediated water exchange between trees. Our findings indicate that functional root grafts represent a vector of hydraulic redistribution, helping to maintain the water balance of grafted trees. This non-invasive approach can serve as a basis for designing empirical studies to better understand the role of grafted root interaction networks on a broader scale.

Stem-mediated hydraulic redistribution in large roots on opposing sides of a Douglas-fir tree following localized irrigation.

*Increasing evidence about hydraulic redistribution and its ecological consequences is emerging. Hydraulic redistribution results from an interplay between competing plant and soil water potential gradients. In this work, stem-mediated hydraulic redistribution was studied in a 53-year-old Douglas-fir tree during a period of drought. *Sap flux density measurements using the heat field deformation method were performed at four locations: in two large opposing roots and on two sides of the tree stem. Hydraulic redistribution was induced by localized irrigation on one of the measured roots, creating heterogeneous soil water conditions. *Stem-mediated hydraulic redistribution was detected during night-time conditions when water was redistributed from the wet side of the tree to the nonirrigated dry side. In addition to stem-mediated hydraulic redistribution, bidirectional flow in the dry root was observed, indicating radial sectoring in the xylem. *It was observed that, through stem-mediated hydraulic redistribution, Douglas-fir was unable to increase its transpiration despite the fact that sufficient water was available to one part of the root system. This resulted from the strong water potential gradient created by the dry soil in contact with the nonirrigated part of the root system. A mechanism of stem-mediated hydraulic redistribution is proposed and its possible implications are discussed.

Variability with xylem depth in sap flow in trunks and branches of mature olive trees.

Knowledge of sap flow variability in tree trunks is important for up-scaling transpiration from the measuring point to the whole-tree and stand levels. Natural variability in sap flow, both radial and circumferential, was studied in the trunks and branches of mature olive trees (Olea europea L., cv Coratina) by the heat field deformation method using multi-point sensors. Sapwood depth ranged from 22 to 55 mm with greater variability in trunks than in branches. Two asymmetric types of sap flow radial patterns were observed: Type 1, rising to a maximum near the mid-point of the sapwood; and Type 2, falling continuously from a maximum just below cambium to zero at the inner boundary of the sapwood. The Type 1 pattern was recorded more often in branches and smaller trees. Both types of sap flow radial patterns were observed in trunks of the sample trees. Sap flow radial patterns were rather stable during the day, but varied with soil water changes. A decrease in sap flow in the outermost xylem was related to water depletion in the topsoil. We hypothesized that the variations in sap flow radial pattern in a tree trunk reflects a vertical distribution of water uptake that varies with water availability in different soil layers.

Mechanisms underlying the long-term survival of the monocot Dracaena marginata under drought conditions.

Efficient water management is essential for the survival of vascular plants under drought stress. While interrelations among drought stress, plant anatomy and physiological functions have been described in woody dicots, similar research is very limited for non-palm arborescent and shrubby monocots despite their generally high drought tolerance. In this study, potted transplants of Dracaena marginata Lam. in primary growth stage were exposed to several short- and long-term drought periods. Continuous measurements of sap flow and stem diameter, the evaluation of capacitance and leaf conductance, the quantification of non-structural carbohydrates (NSC), and organ-specific anatomical analyses were performed to reveal the mechanisms promoting plant resistance to limited soil moisture. The plants showed sensitive stomata regulation in the face of drying soil, but only intermediate resistance to water loss through cuticular transpiration. The water losses were compensated by water release from stem characterized by densely interconnected, parenchyma-rich ground tissue and considerable hydraulic capacitance. Our results suggest that the high concentration of osmotically active NSC in aboveground organs combined with the production of root pressures supported water uptake and the restoration of depleted reserves after watering. The described anatomical features and physiological mechanisms impart D. marginata with high resistance to irregular watering and long-term water scarcity. These findings should help to improve predictions with respect to the impacts of droughts on this plant group.

Vertical and horizontal water redistribution in Norway spruce (Picea abies) roots in the Moravian Upland.

Hydraulic redistribution (HR) by roots of large Norway spruce (Picea abies (L.) Karst.) trees was investigated by means of sap flow measurements made with the heat field deformation method. Irrigation was applied to a limited portion of the root system to steepen gradients of water potential in the soil and thus enhance rates of HR. On completion of the sap flow measurements, and to aid in their interpretation, the structure of the root system of seven of the investigated trees was exposed to a depth of 30 cm with a supersonic air-stream (air-spade). Before irrigation, vertical redistribution of water was observed in large coarse roots and some adjacent small lateral roots. Immediately after localized irrigation, horizontal redistribution of water from watered roots to dry roots via the stem base was demonstrated. The amount of horizontal distribution depended on the position of the receiving roots relative to the watered roots and the absorbing area of the watered root. No redistribution from watered roots via dry soil to roots of neighboring trees was detected. Responses of sap flow to localized irrigation were more pronounced in small lateral roots than in large branching roots where release and uptake of water are integrated. Sap flow measurements with multi-point sensors along radii in large lateral roots demonstrated water extraction from different soil horizons. We conclude that synchronous measurements of sap flow in both small and large lateral roots are needed to study water absorption and transport in tree root systems.

Kinetic studies on the tensile state of water in trees.

The solar-powered generation and turnover of tensile, cohesive water in trees is described as a kinetic phenomenon of irreversible thermodynamics. A molecular kinetic model for tensile water formation and turnover is presented, which is found to be mathematically equivalent with an autocatalytic reaction (Brusselator). It is also shown to be consistent with the van der Waals equation for real liquid-gas systems, which empirically considers intermolecular forces. It can therefore be used to explain both the irreversible thermodynamics and the kinetics of the tensile liquid state of water. A nonlinear bistable evaporation behavior of tensile water is predicted, which has not yet been experimentally characterized in trees. Conventional sap flow techniques in combination with infrared imaging of heat flow around a local heat source were used to study the dynamics and energetics of water transport of trees during the eclipse of August 11, 1999. The evaporative "pulling force" in a tree was demonstrated with infrared techniques and shown to respond within seconds. While the ambient temperature during the eclipse did not drop by more than 2 degrees C, evaporative water transport was reduced by a factor of up to 2-3. The expected hysteresis (with an up to 50% decrease in energy-conversion-related entropy production) was measured, reflecting a bistable mode of conversion of solar energy into tensile water flow. This nonlinear (autocatalytic) phenomenon, together with tensile molecular order, damped the oscillating behavior of xylem tensile water, and its occasional all-or-none rupture (cavitation) can thus be explained by the nonlinear nature of intermolecular forces active in the water conduit/parenchyma environment. This characterizes the physical chemistry and energetics of tensile water in trees as an active-solar-energy-driven self-organizing process. Water is handled in the form of microcanonical ensembles and transformed into a stretched, metastable icelike state with stronger hydrogen bonding and increased heat of evaporation. The discussed model may open new opportunities for research and understanding toward innovative water technologies.

A comparative structural and functional study of leaf traits and sap flow in Dracaena cinnabari and Dracaena draco seedlings.

Water relations for two remote populations of Dracaena tree species from the dragon tree group, Dracaena cinnabari Balfour f. and Dracaena draco (L.) L., were studied to test our hypothesis that morphological and anatomical differences in leaf structure may lead to varied functional responses to changing environmental conditions. Sap flow measurements were performed using the heat field deformation method for four Dracaena seedlings grown in one glasshouse and two greenhouses, and leaf traits related to plant-water relationships were characterised. All traits studied confirmed that D. cinnabari leaves are more xeric in their morpho-anatomical structure compared with D. draco leaves. No radial sap flow variability was detected in D. draco plant stems, whereas sap flow was found to be higher in the inner part of D. cinnabari stems. The regular occurrence of reverse sap flow at night in both Dracaena species was consistent with a staining experiment. Vapour pressure deficit (VPD) was found to be the main driver for transpiration for both Dracaena species. However, the relationship between VPD and sap flow appeared to be different for each species, with a clockwise or no hysteresis loop for D. draco and a counter-clockwise hysteresis loop for D. cinnabari. This resulted in a shorter transpiration cycle in D. cinnabari. The observed superior water-saving strategy of D. cinnabari corresponds to its more xeric morpho-anatomical leaf structure compared with D. draco.

Radial patterns of sap flow in woody stems of dominant and understory species: scaling errors associated with positioning of sensors.

We studied sap flow in dominant coniferous (Pinus sylvestris L.) and broadleaf (Populus canescens L.) species and in understory species (Prunus serotina Ehrh. and Rhododendron ponticum L.) by the heat field deformation (HFD) method. We attempted to identify possible errors arising during flow integration and scaling from single-point measurements to whole trees. Large systematic errors of -90 to 300% were found when it was assumed that sap flow was uniform over the sapwood depth. Therefore, we recommend that the radial sap flow pattern should be determined first using sensors with multiple measuring points along a stem radius followed by single-point measurements with sensors placed at a predetermined depth. Other significant errors occurred in the scaling procedure even when the sap flow radial pattern was known. These included errors associated with uncertainties in the positioning of sensors beneath the cambium (up to 15% per 1 mm error in estimated xylem depth), and differences in environmental conditions when the radial profile applied for integration was determined over the short term (up to 47% error). High temporal variation in the point-to-area correction factor along the xylem radius used for flow integration is also problematic. Compared with midday measurements, measurements of radial variation of sap flow in the morning and evening of sunny days minimized the influence of temporal variations on the point-to-area correction factor, which was especially pronounced in trees with a highly asymmetric sap flow radial pattern because of differences in functioning of the sapwood xylem layers. Positioning a single-point sensor at a depth with maximum sap flow is advantageous because of the high sensitivity of maximum sap flow to water stress conditions and changes in micro-climate, and because of the lower random errors associated with the positioning of a single-point sensor along the xylem radius.

Hydraulic connectivity from roots to branches depicted through sap flow: analysis on a Quercus suber tree.

The topology of the xylem network is likely to affect the transport of water, propagation of embolism and plant survival and growth. Few studies have been conducted on the hydraulics of the entire water pathway in trees. We evaluated the hydraulic connections from roots to branches in a mature Quercus suber L. tree, through sap flow responses upon branch severing. Sap flow was recorded in branches, stem and roots by the heat field deformation (HFD) method. Results showed that roots, except for the taproot, were hydraulically connected to all branches, but the rest of the tree (stem, branches and taproot) was highly sectored. In the large roots that showed an integrated response to branch severing, the outer xylem was preferentially connected to the same side branch and the inner xylem to the opposite branch. The hydraulic sectoriality in branches, stem and taproot may be regarded as an adaptive trait to water stress. The integrated hydraulic structure of roots is advantageous under patchy soil conditions, but may allow the spread of root diseases. The HFD sap flow method proved extremely useful to calculate xylem flux connectivity between different organs of a large tree, providing a comprehensive picture of its hydraulic architecture.

Instrumental methods for studies of structure and function of root systems of large trees.

New methods using different physical principles have been successfully applied in studies of root systems of large trees. The ground-penetrating radar technique provides 3D images of coarse roots (starting with a diameter of about 20 mm) from the soil surface down to a depth of several metres. This can even be done under layers of undisturbed materials such as concrete, asphalt and water. Fine roots cannot be visualized by this method, but the total rooted volume of soil can be determined. The differential electric conductance method has been used for fast measurement of conducting (absorbing) root surfaces. However, more testing is needed. Both these methods are non-invasive. The results can be verified by an almost harmless excavation of whole root systems, including fine roots, using the ultrasonic air-stream (air-spade) method. This method is suitable for all studies, as well as practical operations on roots or objects in their vicinity, where a gentle approach is required. Sap flow measurements on their own or in tandem with soil moisture monitoring play a leading role in studying root function and hydraulic redistribution of flow in the soil. The water absorption function of roots can be studied by measuring sap flow on individual root branches directly (as on crown branches) and also indirectly, by measuring the radial pattern of sap flow in different sapwood depths at the base of a stem. Root zone architecture can also be estimated indirectly by studying its functionality. The heat field deformation method with multi-point sensors has been found to be very convenient for this purpose. A combination of several such methods is recommended whenever possible, in order to obtain detailed information about the root systems of trees.

Radial variation in sap flow in five laurel forest tree species in Tenerife, Canary Islands.

Variations in radial patterns of xylem water content and sap flow rate were measured in five laurel forest tree species (Laurus azorica (Seub.) Franco, Persea indica (L.) Spreng., Myrica faya Ait., Erica arborea L. and Ilex perado Ait. ssp. platyphylla (Webb & Berth.) Tutin) growing in an experimental plot at Agua García, Tenerife, Canary Islands. Measurements were performed around midday during warm and sunny days by the heat field deformation method. In all species, water content was almost constant (around 35% by volume) over the whole xylem cross-sectional area. There were no differences in wood color over the whole cross-sectional area of the stem in most species with the exception of E. arborea, whose wood became darker in the inner layers. Radial patterns of sap flow were highly variable and did not show clear relationships with tree diameter or species. Sap flow occurred over the whole xylem cross-sectional area in some species, whereas it was limited to the outer xylem layers in others. Sap flow rate was either similar along the xylem radius or exhibited a peak in the outer part of the xylem area. Low sap flow rates with little variation in radial pattern were typical for shaded suppressed trees, whereas dominant trees exhibited high sap flow rates with a peak in the radial pattern. Stem damage resulted in a significant decrease in sap flow rate in the outer xylem layers. The outer xylem is more important for whole tree water supply than the inner xylem because of its larger size. We conclude that measurement of radial flow pattern provides a reliable method of integrating sap flow from individual measuring points to the whole tree.