Hydraulic mechanism of limiting growth and maintaining survival of desert shrubs in arid habitats.

The growth and survival of woody plant species is mainly driven by evolutionary and environmental factors. However, little is known about the hydraulic mechanisms that respond to growth limitation and enable desert shrub survival in arid habitats. To shed light on these hydraulic mechanisms, 9-, 31-, and 56-year-old Caragana korshinskii plants that had been grown under different soil water conditions at the southeast edge of the Tengger Desert, Ningxia, China were used in this study. The growth of C. korshinskii was mainly limited by soil water rather than shrub age in non-watered habitats, which indicated the importance of maintaining shrub survival prior to growth under drought. Meanwhile, higher vessel density, narrower vessels and lower xylem hydraulic conductivity indicated that shrubs enhanced hydraulic safety and reduced their hydraulic efficiency in arid conditions. Importantly, xylem hydraulic conductivity mediated by variation in xylem hydraulic architecture regulated photosynthetic carbon assimilation and growth of C. korshinskii. Our study highlights that the synergistic variation in xylem hydraulic safety and hydraulic efficiency is the hydraulic mechanism limiting growth and maintaining survival of C. korshinskii under drought, providing insights into the strategies for growth and survival of desert shrubs in arid habitats.

An appreciation of apex-to-base variation in xylem traits will lead to more precise understanding of xylem phenotypic plasticity.

Xylem air embolism is the primary cause of drought-related tree mortality. Phenotypic plasticity of xylem traits is key for species acclimation to environmental variability and evolution. It is widely believed that plants increase xylem embolism resistance in response to drought. However, I argue that this hypothesis, based on extensive literature, relies on sampling methods that overlook predictable anatomical patterns, potentially biasing our understanding of acclimation and adaptation strategies.

Deep-water uptake under drought improved due to locally increased root conductivity in maize, but not in faba bean.

Moderate soil drying can cause a strong decrease in the soil-root system conductance. The resulting impact on root water uptake depends on the spatial distribution of the altered conductance relatively to remaining soil water resources, which is largely unknown. Here, we analyzed the vertical distribution of conductance across root systems using a novel, noninvasive sensor technology on pot-grown faba bean and maize plants. Withholding water for 4 days strongly enhanced the vertical gradient in soil water potential. Therefore, roots in upper and deeper soil layers were affected differently: In drier, upper layers, root conductance decreased by 66%-72%, causing an amplification of the drop in leaf water potential. In wetter, deeper layers, root conductance increased in maize but not in faba bean. The consequently facilitated deep-water uptake in maize contributed up to 21% of total water uptake at the end of the measurement. Analysis of root length distributions with MRI indicated that the locally increased conductance was mainly caused by an increased intrinsic conductivity and not by additional root growth. Our findings show that plants can partly compensate for a reduced root conductance in upper, drier soil layers by locally increasing root conductivity in wetter layers, thereby improving deep-water uptake.

Functional traits and water-transport strategies of woody species in an insular environment in a tropical forest.

PREMISE: Plants survive in habitats with limited resource availability and contrasting environments by responding to variation in environmental factors through morphophysiological traits related to species performance in different ecosystems. However, how different plant strategies influence the megadiversity of tropical species has remained a knowledge gap. METHODS: We analyzed variations in 27 morphophysiological traits of leaves and secondary xylem in Erythroxylum pulchrum and Tapirira guianensis, which have the highest absolute dominance in these physiognomies and occur together in areas of restinga and dense ombrophilous forest to infer water-transport strategies of Atlantic Forest woody plants. RESULTS: The two species presented different sets of morphophysiological traits, strategies to avoid embolism and ensure water transport, in different phytophysiognomies. Tapirira guianensis showed possible adaptations influenced by phytophysiognomy, while E. pulchrum showed less variation in the set of characteristics between different phytophysiognomies. CONCLUSIONS: Our results provide essential tools to understand how the environment can modulate morphofunctional traits and how each species adjusts differently to adapt to different phytophysiognomies. In this sense, the results for these species reveal new species-specific responses in the tropical forest. Such knowledge is a prerequisite to predict future development of the most vulnerable forests as climate changes.

Vessel dimorphism and wood traits in lianas and trees among three contrasting environments.

PREMISE: Determining how xylem vessel diameters vary among plants and across environments gives insights into different water-use strategies among species and ultimately their distributions. Here, we tested the vessel dimorphism hypothesis that the simultaneous occurrence of many narrow and a few wide vessels gives lianas an advantage over trees in seasonally dry environments. METHODS: We measured the diameters of 13,958 vessels from 15 liana species and 10,430 vessels from 16 tree species in a tropical seasonal rainforest, savanna, and subtropical evergreen broadleaved forest. We compared differences in mean and hydraulically weighted vessel diameter (MVD and Dh ), vessel density (VD), theoretical hydraulic conductivity (Kt ), vessel area fraction (VAF), and wood density (WD) between lianas and trees and among three sites. RESULTS: Nine liana species and four tree species had dimorphic vessels. From the tropical seasonal rainforest to the savanna, liana MVD, Dh and Kt decreased, and VD and WD increased, while only tree WD increased. From the tropical seasonal rainforest to the subtropical forest, six wood traits remained unchanged for lianas, while tree MVD, Dh and Kt decreased and VD increased. Trait space for lianas and trees were more similar in the savanna and more divergent in the subtropical forest compared to the tropical seasonal rainforest. CONCLUSIONS: These results suggest that lianas tend to possess greater vessel dimorphism, which may explain how lianas grow well during seasonal drought, influencing their unique distribution across tropical rainfall gradients.

Convergent tip-to-base widening of water-conducting conduits in the tallest bryophytes.

PREMISE: Tip-to-base conduit widening is considered a key mechanism that enables vascular plants to grow tall by decreasing the hydraulic resistance imposed by increasing height. Widening of hydraulic anatomy (larger conducting elements toward the base of the vascular system) minimizes gradients in leaf-specific hydraulic conductance with plant height, allowing uniform photosynthesis across the crown of trees. Tip-to-base conduit widening has also been associated with changes in conduit number. However, in bryophytes, despite having representatives with internal water-conducting tissue, conduit widening has been scarcely investigated. METHODS: Here, we examined the changes in hydroid diameter and number with distance from plant tip in Dawsonia superba and D. polytrichoides, two representatives of the genus containing the tallest extant bryophytes. RESULTS: The position of these moss species on the global scale of conduit size and plant size was consistent with a general scaling among plants with internal water transport. Within plants, patterns of conduit widening and number with distance from plant tip in endohydric mosses were similar to those observed in vascular plants. CONCLUSIONS: This study demonstrated that land plants growing upward in the atmosphere show analogous conduit widening of hydraulic structures, suggesting that efficient internal water transport is a convergent adaptation for photosynthesis on land.

Tip-to-base xylem conduit widening as an adaptation: causes, consequences, and empirical priorities.

In the stems of terrestrial vascular plants studied to date, the diameter of xylem water-conducting conduits D widens predictably with distance from the stem tip L approximating D âˆ Lb , with b ≈ 0.2. Because conduit diameter is central for conductance, it is essential to understand the cause of this remarkably pervasive pattern. We give reason to suspect that tip-to-base conduit widening is an adaptation, favored by natural selection because widening helps minimize the increase in hydraulic resistance that would otherwise occur as an individual stem grows longer and conductive path length increases. Evidence consistent with adaptation includes optimality models that predict the 0.2 exponent. The fact that this prediction can be made with a simple model of a single capillary, omitting much biological detail, itself makes numerous important predictions, e.g. that pit resistance must scale isometrically with conduit resistance. The idea that tip-to-base conduit widening has a nonadaptive cause, with temperature, drought, or turgor limiting the conduit diameters that plants are able to produce, is less consistent with the data than an adaptive explanation. We identify empirical priorities for testing the cause of tip-to-base conduit widening and underscore the need to study plant hydraulic systems leaf to root as integrated wholes.

The hydraulic architecture of an arborescent monocot: ontogeny-related adjustments in vessel size and leaf area compensate for increased resistance.

Bamboos are arborescent monocotyledons that have no secondary growth, but can continually produce conduits with diameters appropriate to the current size of the plant. Here, we studied bamboo hydraulic architecture to address the mechanisms involved in compensating for the increase in hydraulic resistance during ontogeny. We measured the hydraulic weighted vessel diameters (Dh ) at different distances from the apex along the stem of Bambusa textilis. The hydraulic resistance of different components and individuals of different heights were quantified using the high-pressure flowmeter method. The Dh showed tip-to-base widening with a scaling exponent in the range of those reported for trees. Although theoretical hydraulic conductivity decreased from base-to-tip, leaf-specific conductivity did not change. Leaves contributed the most to the whole-shoot hydraulic resistance, followed by the leaf-bearing branches. Roots contributed c. 13% to whole-plant resistance. Interestingly, taller individuals showed lower whole-shoot resistance owing to an increased number of resistances in parallel (side-branches), while leaf-specific resistance was independent of plant size. Tip-to-base vessel widening and height-independent constant leaf-specific conductance could be mechanisms for hydraulic optimization in B. textilis. Similar patterns have also been found in woody plants with secondary growth, but this bamboo exhibits them without secondary growth.

Quantifying vulnerability to embolism in tropical trees and lianas using five methods: can discrepancies be explained by xylem structural traits?

Vulnerability curves (VCs) describe the loss of hydraulic conductance against increasing xylem tension, providing valuable insights about the response of plant water transport to water stress. Techniques to construct VCs have been developed and modified continuously, but controversies continue. We compared VCs constructed using the bench-top dehydration (BD), air-injection-flow (AI), pneumatic-air-discharge (PAD), optical (OP) and X-ray-computed microtomography (MicroCT) methods for tropical trees and lianas with contrasting vessel lengths. The PAD method generated highly vulnerable VCs, the AI method intermediate VCs, whereas the BD, OP and MicroCT methods produced comparable and more resistant VCs. Vessel-length and diameter accounted for the overestimation ratio of vulnerability estimated using the AI but not the PAD method. Compared with directly measured midday embolism levels, the PAD and AI methods substantially overestimated embolism, whereas the BD, MicroCT and OP methods provided more reasonable estimations. Cut-open vessels, uncertainties in maximum air volume estimations, sample-length effects, tissue cracks and shrinkage together may impede the reliability of the PAD method. In conclusion, we validate the BD, OP and MicroCT methods for tropical plants, whereas the PAD and AI need further mechanistic testing. Therefore, applications of VCs in estimating plant responses to drought need to be cautious.

Interclonal variation, coordination, and trade-offs between hydraulic conductance and gas exchange in Pinus radiata: consequences on plant growth and wood density.

Stem growth reflects genetic and phenotypic differences within a tree species. The plant hydraulic system regulates the carbon economy, and therefore variations in growth and wood density. A whole-organism perspective, by partitioning the hydraulic system, is crucial for understanding the physical and physiological processes that coordinately mediate plant growth. The aim of this study was to determine whether the relationships and trade-offs between (i) hydraulic traits and their relative contribution to the whole-plant hydraulic system, (ii) plant water transport, (iii) CO2 assimilation, (iv) plant growth, and (v) wood density are revealed at the interclonal level within a variable population of 10 Pinus radiata (D. Don) clones for these characters. We demonstrated a strong coordination between several plant organs regarding their hydraulic efficiency. Hydraulic efficiency, gas exchange, and plant growth were intimately linked. Small reductions in stem wood density were related to a large increase in sapwood hydraulic efficiency, and thus to plant growth. However, stem growth rate was negatively related to wood density. We discuss insights explaining the relationships and trade-offs of the plant traits examined in this study. These insights provide a better understanding of the existing coordination, likely to be dependent on genetics, between the biophysical structure of wood, plant growth, hydraulic partitioning, and physiological plant functions in P. radiata.

Axial anatomy of the leaf midrib provides new insights into the hydraulic architecture and cavitation patterns of Acer pseudoplatanus leaves.

The structure of leaf veins is typically described by a hierarchical scheme (e.g. midrib, 1st order, 2nd order), which is used to predict variation in conduit diameter from one order to another whilst overlooking possible variation within the same order. We examined whether xylem conduit diameter changes within the same vein order, with resulting consequences for resistance to embolism. We measured the hydraulic diameter (Dh), and number of vessels (VN) along the midrib and petioles of leaves of Acer pseudoplatanus, and estimated the leaf area supplied (Aleaf-sup) at different points of the midrib and how variation in anatomical traits affected embolism resistance. We found that Dh scales with distance from the midrib tip (path length, L) with a power of 0.42, and that VN scales with Aleaf-sup with a power of 0.66. Total conductive area scales isometrically with Aleaf-sup. Embolism events along the midrib occurred first in the basipetal part and then at the leaf tip where vessels are narrower. The distance from the midrib tip is a good predictor of the variation in vessel diameter along the 1st order veins in A. pseudoplatanus leaves and this anatomical pattern seems to have an effect on hydraulic integrity since wider vessels at the leaf base embolize first.

Maximum-likelihood estimation of xylem vessel length distributions.

Vessel length is an important functional trait for plant hydraulics, because it determines the ratio of flow resistances posed by lumen and pit membranes and hence controls xylem hydraulic efficiency. The most commonly applied methods to estimate vessel lengths are based on the injection of silicon or paint into cut-off stem segments. The number of stained vessels in a series of cross-sections in increasing distance from the injection point is then counted. The resulting infusion profiles are used to estimate the vessel length distribution using one of several statistical algorithms. However, the basis of these algorithms has not been systematically analysed using probability theory. We derive a general mathematical expression for the expected shape of the infusion profile for a given vessel length distribution, provide analytic solutions for five candidate distributions (exponential, Erlang(2), gamma, Weibull, and log-normal), and present maximum likelihood estimators for the parameters of these distributions including implementations in R based on two potential sampling schemes (counting all injected vessels or counting the injected and empty vessels in a random subset of each cross-section). We then explore the performance of these estimators relative to other methods with Monte Carlo experiments. Our analysis demonstrates that most published methods estimate the conditional length distribution of vessels that cross an injection point, which is a size-biased version of the overall length distribution in the stem. We show the mathematical relationship between these distributions and provide methods to estimate either of them. According to our simulation experiments, vessel length distribution was best described by the more flexible models, especially the Weibull distribution. In simulations, the estimators were able to recover the parameters of the vessel length distribution if its functional form was known, achieving an overlap of 90% or more between the true and predicted length distribution when counting no more than 500 injected vessels in 10 cross-sections. This sample size nowadays can easily be reached with the help of automated image analysis.

Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept.

In this review, we address the relationship between stomatal behaviour, water potential regulation and hydraulic transport in plants, focusing on the implications for the iso/anisohydric classification of plant drought responses at seasonal timescales. We first revise the history of the isohydric concept and its possible definitions. Then, we use published data to answer two main questions: (1) is greater stomatal control in response to decreasing water availability associated with a tighter regulation of leaf water potential (ΨL ) across species? and (2) is there an association between tighter ΨL regulation (~isohydric behaviour) and lower leaf conductance over time during a drought event? These two questions are addressed at two levels: across species growing in different sites and comparing only species coexisting at a given site. Our analyses show that, across species, a tight regulation of ΨL is not necessarily associated with greater stomatal control or with more constrained assimilation during drought. Therefore, iso/anisohydry defined in terms of ΨL regulation cannot be used as an indicator of a specific mechanism of drought-induced mortality or as a proxy for overall plant vulnerability to drought.

Towards quantitative root hydraulic phenotyping: novel mathematical functions to calculate plant-scale hydraulic parameters from root system functional and structural traits.

Predicting root water uptake and plant transpiration is crucial for managing plant irrigation and developing drought-tolerant root system ideotypes (i.e. ideal root systems). Today, three-dimensional structural functional models exist, which allows solving the water flow equation in the soil and in the root systems under transient conditions and in heterogeneous soils. Yet, these models rely on the full representation of the three-dimensional distribution of the root hydraulic properties, which is not always easy to access. Recently, new models able to represent this complex system without the full knowledge of the plant 3D hydraulic architecture and with a limited number of parameters have been developed. However, the estimation of the macroscopic parameters a priori still requires a numerical model and the knowledge of the full three-dimensional hydraulic architecture. The objective of this study is to provide analytical mathematical models to estimate the values of these parameters as a function of local plant general features, like the distance between laterals, the number of primaries or the ratio of radial to axial root conductances. Such functions would allow one to characterize the behaviour of a root system (as characterized by its macroscopic parameters) directly from averaged plant root traits, thereby opening new possibilities for developing quantitative ideotypes, by linking plant scale parameters to mean functional or structural properties. With its simple form, the proposed model offers the chance to perform sensitivity and optimization analyses as presented in this study.

Vessel diameter and related hydraulic traits of 31 Eucalyptus species arrayed along a gradient of water availability.

We present two comprehensive data sets that describe xylem vessel diameters and related sapwood traits for species of Eucalyptus from arid and semi-arid woodlands and forests in Australia. Between 2009 and 2014, sapwood of mature trees was sampled in south-western, south-eastern and eastern Australia. One additional species was sampled from tropical north-western Australia. The first data set describes samples collected from the basal stem section (130 cm above ground) of three individuals of 31 species of which eight species were replicated at sites that differed in climatic conditions. The second data set describes vessel characteristics of three trees from each of 10 species that were sampled at 8 m below the tree apex. The sampled trees of these 10 species are also part of the first data set. In total, we report diameters (D) for over 25 100 vessels, from 494 digital images taken from 117 trees. We also report vessel frequencies, void-to-wood ratios, sapwood densities and hydraulically weighted vessel diameters (Dh). Supporting data of the first data set include tree diameter at breast height (130 cm above ground), tree height, sample locations, and summary climate data. In this data set, diameter of individual vessels ranges from 10 to over 300 µm, and vessel frequency from 360 to 9070 vessels cm-2 . Wood density ranges from 0.47 to 0.96 g cm-3 . Void-to-wood ratio ranges from 6% to 27% and Dh ranges from 46 to 236 µm. Mean annual rainfall (P) at sample sites ranges from 246 to 2274 mm and FAO56 reference evaporation (E) from 777 to 2110 mm. The aridity index (E/P) ranges from 0.15 to 2.93 (dimensionless). Tree diameters range from 9 to 90 cm and tree heights range from 6 to 70 m. D and Dh in the second data set range from 11 to 271 and 68 to 205 µm, respectively. These datasets will make a valuable contribution to future continental-scale and global-scale studies of the relationship between xylem hydraulic architecture and climate. The data sets are unique in the sense that they are phylogenetically constrained, allowing in-depth assessment of plasticity of hydraulic attributes within a single tree genus.

Isometric partitioning of hydraulic conductance between leaves and stems: balancing safety and efficiency in different growth forms and habitats.

Recent advances in modelling the architecture and function of the plant hydraulic network have led to improvements in predicting and interpreting the consequences of functional trait variation on CO2 uptake and water loss. We build upon one such model to make novel predictions for scaling of the total specific hydraulic conductance of leaves and shoots (kL and kSH , respectively) and variation in the partitioning of hydraulic conductance. Consistent with theory, we observed isometric (slope = 1) scaling between kL and kSH across several independently collected datasets and a lower ratio of kL and kSH , termed the leaf-to-shoot conductance ratio (CLSCR ), in arid environments and in woody species. Isometric scaling of kL and kSH supports the concept that hydraulic design is coordinated across the plant. We propose that CLSCR is an important adaptive trait that represents the trade-off between efficiency and safety at the scale of the whole plant.

Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates.

Angiosperm hydraulic performance is crucially affected by the diameters of vessels, the water conducting conduits in the wood. Hydraulic optimality models suggest that vessels should widen predictably from stem tip to base, buffering hydrodynamic resistance accruing as stems, and therefore conductive path, increase in length. Data from 257 species (609 samples) show that vessels widen as predicted with distance from the stem apex across angiosperm orders, habits and habitats. Standardising for stem length, vessels are only slightly wider in warm/moist climates and in lianas, showing that, rather than climate or habit, plant size is by far the main driver of global variation in mean vessel diameter. Terminal twig vessels become wider as plant height increases, while vessel density decreases slightly less than expected tip to base. These patterns lead to testable predictions regarding evolutionary strategies allowing plants to minimise carbon costs per unit leaf area even as height increases.

Deviation from symmetrically self-similar branching in trees predicts altered hydraulics, mechanics, light interception and metabolic scaling.

The West, Brown, Enquist (WBE) model derives symmetrically self-similar branching to predict metabolic scaling from hydraulic conductance, K, (a metabolism proxy) and tree mass (or volume, V). The original prediction was Kα V(0.75). We ask whether trees differ from WBE symmetry and if it matters for plant function and scaling. We measure tree branching and model how architecture influences K, V, mechanical stability, light interception and metabolic scaling. We quantified branching architecture by measuring the path fraction, Pf : mean/maximum trunk-to-twig pathlength. WBE symmetry produces the maximum, Pf = 1.0. We explored tree morphospace using a probability-based numerical model constrained only by biomechanical principles. Real tree Pf ranged from 0.930 (nearly symmetric) to 0.357 (very asymmetric). At each modeled tree size, a reduction in Pf led to: increased K; decreased V; increased mechanical stability; and decreased light absorption. When Pf was ontogenetically constant, strong asymmetry only slightly steepened metabolic scaling. The Pf ontogeny of real trees, however, was 'U' shaped, resulting in size-dependent metabolic scaling that exceeded 0.75 in small trees before falling below 0.65. Architectural diversity appears to matter considerably for whole-tree hydraulics, mechanics, photosynthesis and potentially metabolic scaling. Optimal architectures likely exist that maximize carbon gain per structural investment.