Radial-axial transport coordination enhances sugar translocation in the phloem vasculature of plants.

Understanding mass transport of photosynthates in the phloem of plants is necessary for predicting plant carbon allocation, productivity, and responses to water and thermal stress. Several hypotheses about optimization of phloem structure and function and limitations of phloem transport under drought have been proposed and tested with models and anatomical data. However, the true impact of radial water exchange of phloem conduits with their surroundings on mass transport of photosynthates has not been addressed. Here, the physics of the Munch mechanism of sugar transport is re-evaluated to include local variations in viscosity resulting from the radial water exchange in two dimensions (axial and radial) using transient flow simulations. Model results show an increase in radial water exchange due to a decrease in sap viscosity leading to increased sugar front speed and axial mass transport across a wide range of phloem conduit lengths. This increase is around 40% for active loaders (e.g. crops) and around 20% for passive loaders (e.g. trees). Thus, sugar transport operates more efficiently than predicted by previous models that ignore these two effects. A faster front speed leads to higher phloem resiliency under drought because more sugar can be transported with a smaller pressure gradient.

Evidence for distinct isotopic compositions of sap and tissue water in tree stems: consequences for plant water source identification.

The long-standing hypothesis that the isotopic composition of plant stem water reflects that of source water is being challenged by studies reporting bulk water from woody stems with an isotopic composition that cannot be attributed to any potential water source. The mechanism behind such source-stem water isotopic offsets is still poorly understood. Using a novel technique to extract selectively sap water from xylem conduits, we show that, in cut stems and potted plants, the isotopic composition of sap water reflects that of irrigation water, demonstrating unambiguously that no isotopic fractionation occurs during root water uptake or sap water extraction. By contrast, water in nonconductive xylem tissues is always depleted in deuterium compared with sap water, irrespective of wood anatomy. Previous studies have shown that isotopic heterogeneity also exists in soils at the pore scale in which water adsorbed onto soil particles is more depleted in deuterium than unbound water. Data collected at a riparian forest indicated that sap water matches best unbound soil water from depth below -70 cm, while bulk stem and soil water differ markedly. We conclude that source-stem isotopic offsets can be explained by micrometre-scale heterogeneity in the isotope ratios of water within woody stems and soil micro-pores.

Catastrophic hydraulic failure and tipping points in plants.

Water inside plants forms a continuous chain from water in soils to the water evaporating from leaf surfaces. Failures in this chain result in reduced transpiration and photosynthesis and are caused by soil drying and/or cavitation-induced xylem embolism. Xylem embolism and plant hydraulic failure share several analogies to 'catastrophe theory' in dynamical systems. These catastrophes are often represented in the physiological and ecological literature as tipping points when control variables exogenous (e.g., soil water potential) or endogenous (e.g., leaf water potential) to the plant are allowed to vary on time scales much longer than time scales associated with cavitation events. Here, plant hydraulics viewed from the perspective of catastrophes at multiple spatial scales is considered with attention to bubble expansion within a xylem conduit, organ-scale vulnerability to embolism, and whole-plant biomass as a proxy for transpiration and hydraulic function. The hydraulic safety-efficiency tradeoff, hydraulic segmentation and maximum plant transpiration are examined using this framework. Underlying mechanisms for hydraulic failure at fine scales such as pit membranes and cell-wall mechanics, intermediate scales such as xylem network properties and at larger scales such as soil-tree hydraulic pathways are discussed. Understudied areas in plant hydraulics are also flagged where progress is urgently needed.

The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants.

The coordination of plant leaf water potential (ΨL ) regulation and xylem vulnerability to embolism is fundamental for understanding the tradeoffs between carbon uptake and risk of hydraulic damage. There is a general consensus that trees with vulnerable xylem more conservatively regulate ΨL than plants with resistant xylem. We evaluated if this paradigm applied to three important eastern US temperate tree species, Quercus alba L., Acer saccharum Marsh. and Liriodendron tulipifera L., by synthesizing 1600 ΨL observations, 122 xylem embolism curves and xylem anatomical measurements across 10 forests spanning pronounced hydroclimatological gradients and ages. We found that, unexpectedly, the species with the most vulnerable xylem (Q. alba) regulated ΨL less strictly than the other species. This relationship was found across all sites, such that coordination among traits was largely unaffected by climate and stand age. Quercus species are perceived to be among the most drought tolerant temperate US forest species; however, our results suggest their relatively loose ΨL regulation in response to hydrologic stress occurs with a substantial hydraulic cost that may expose them to novel risks in a more drought-prone future.

Tallo: A global tree allometry and crown architecture database.

Data capturing multiple axes of tree size and shape, such as a tree's stem diameter, height and crown size, underpin a wide range of ecological research-from developing and testing theory on forest structure and dynamics, to estimating forest carbon stocks and their uncertainties, and integrating remote sensing imagery into forest monitoring programmes. However, these data can be surprisingly hard to come by, particularly for certain regions of the world and for specific taxonomic groups, posing a real barrier to progress in these fields. To overcome this challenge, we developed the Tallo database, a collection of 498,838 georeferenced and taxonomically standardized records of individual trees for which stem diameter, height and/or crown radius have been measured. These data were collected at 61,856 globally distributed sites, spanning all major forested and non-forested biomes. The majority of trees in the database are identified to species (88%), and collectively Tallo includes data for 5163 species distributed across 1453 genera and 187 plant families. The database is publicly archived under a CC-BY 4.0 licence and can be access from: https://doi.org/10.5281/zenodo.6637599. To demonstrate its value, here we present three case studies that highlight how the Tallo database can be used to address a range of theoretical and applied questions in ecology-from testing the predictions of metabolic scaling theory, to exploring the limits of tree allometric plasticity along environmental gradients and modelling global variation in maximum attainable tree height. In doing so, we provide a key resource for field ecologists, remote sensing researchers and the modelling community working together to better understand the role that trees play in regulating the terrestrial carbon cycle.

Beyond carbon flux partitioning: Carbon allocation and nonstructural carbon dynamics inferred from continuous fluxes.

Carbon (C) allocation and nonstructural carbon (NSC) dynamics play essential roles in plant growth and survival under stress and disturbance. However, quantitative understanding of these processes remains limited. Here we propose a framework where we connect commonly measured carbon cycle components (eddy covariance fluxes of canopy CO2 exchange, soil CO2 efflux, and allometry-based biomass and net primary production) by a simple mass balance model to derive ecosystem-level NSC dynamics (NSCi ), C translocation (dCi ), and the biomass production efficiency (BPEi ) in above- and belowground plant (i = agp and bgp) compartments. We applied this framework to two long-term monitored loblolly pine (Pinus taeda) plantations of different ages in North Carolina and characterized the variations of NSC and allocation in years under normal and drought conditions. The results indicated that the young stand did not have net NSC flux at the annual scale, whereas the mature stand stored a near-constant proportion of new assimilates as NSC every year under normal conditions, which was comparable in magnitude to new structural growth. Roots consumed NSC in drought and stored a significant amount of NSC post drought. The above- and belowground dCi and BPEi varied more from year to year in the young stand and approached a relatively stable pattern in the mature stand. The belowground BPEbgp differed the most between the young and mature stands and was most responsive to drought. With the internal C dynamics quantified, this framework may also improve biomass production estimation, which reveals the variations resulting from droughts. Overall, these quantified ecosystem-scale dynamics were consistent with existing evidence from tree-based manipulative experiments and measurements and demonstrated that combining the continuous fluxes as proposed here can provide additional information about plant internal C dynamics. Given that it is based on broadly available flux data, the proposed framework is promising to improve the allocation algorithms in ecosystem C cycle models and offers new insights into observed variability in soil-plant-climate interactions.

The roles of conduit redundancy and connectivity in xylem hydraulic functions.

Wood anatomical traits shape a xylem segment's hydraulic efficiency and resistance to embolism spread due to declining water potential. It has been known for decades that variations in conduit connectivity play a role in altering xylem hydraulics. However, evaluating the precise effect of conduit connectivity has been elusive. The objective here is to establish an analytical linkage between conduit connectivity and grouping and tissue-scale hydraulics. It is hypothesized that an increase in conduit connectivity brings improved resistance to embolism spread due to increased hydraulic pathway redundancy. However, an increase in conduit connectivity could also reduce resistance due to increased speed of embolism spread with respect to pressure. We elaborate on this trade-off using graph theory, percolation theory and computational modeling of xylem. The results are validated using anatomical measurements of Acer branch xylem. Considering only species with vessels, increases in connectivity improve resistance to embolism spread without negatively affecting hydraulic conductivity. The often measured grouping index fails to capture the totality of the effect of conduit connectivity on xylem hydraulics. Variations in xylem network characteristics, such as conduit connectivity, might explain why hypothesized trends among woody species, such as the 'safety-efficiency' trade-off hypothesis, are weaker than expected.

Persistent decay of fresh xylem hydraulic conductivity varies with pressure gradient and marks plant responses to injury.

Defining plant hydraulic traits is central to the quantification of ecohydrological processes ranging from land-atmosphere interactions, to tree mortality and water-carbon budgets. A key plant trait is the xylem specific hydraulic conductivity (Kx ), that describes the plant's vascular system capacity to transport water. While xylem's vessels and tracheids are dead upon maturity, the xylem is neither inert nor deadwood, various components of the sapwood and surrounding tissue remaining alive and functional. Moreover, the established definition of Kx assumes linear relations between water flux and pressure gradient by tacitly considering the xylem as a "passive conduit". Here, we re-examine this notion of an inert xylem by systematically characterizing xylem flow in several woody plants using Kx measurements under constant and cyclic pressure gradients. Results show a temporal and pressure gradient dependence of Kx . Additionally, microscopic features in "living branches" are irreversibly modified upon drying of the xylem, thus differentiating the macroscopic definition of Kx for living and dead xylem. The findings highlight the picture of the xylem as a complex and delicate conductive system whose hydraulic behaviour transcends a passive gradient-based flow. The study sheds new light on xylem conceptualization, conductivity measurement protocols, in situ long-distance water transport and ecosystem modelling.

Increased hydraulic constraints in Eucalyptus plantations fertilized with potassium.

Fertilization is commonly used to increase growth in forest plantations, but it may also affect tree water relations and responses to drought. Here, we measured changes in biomass, transpiration, sapwood-to-leaf area ratio (As :Al ) and sap flow driving force (ΔΨ) during the 6-year rotation of tropical plantations of Eucalyptus grandis under controlled conditions for throughfall and potassium (K) fertilization. K fertilization increased final tree height by 8 m. Throughfall exclusion scarcely affected tree functioning because of deep soil water uptake. Tree growth increased in K-supplied plots and remained stable in K-depleted plots as tree height increased, while growth per unit leaf area increased in all plots. Stand transpiration and hydraulic conductance standardized per leaf area increased with height in K-depleted plots, but remained stable or decreased in K-supplied plots. Greater Al in K-supplied plots increased the hydraulic constraints on water use. This involved a direct mechanism through halved As :Al in K-supplied plots relative to K-depleted plots, and an indirect mechanism through deteriorated water status in K-supplied plots, which prevented the increase in ΔΨ with tree height. K fertilization in tropical plantations reduces the hydraulic compensation to growth, which could increase the risk of drought-induced dieback under climate change.

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.

Aquaporins, and not changes in root structure, provide new insights into physiological responses to drought, flooding, and salinity.

The influence of aquaporin (AQP) activity on plant water movement remains unclear, especially in plants subject to unfavorable conditions. We applied a multitiered approach at a range of plant scales to (i) characterize the resistances controlling water transport under drought, flooding, and flooding plus salinity conditions; (ii) quantify the respective effects of AQP activity and xylem structure on root (Kroot), stem (Kstem), and leaf (Kleaf) conductances; and (iii) evaluate the impact of AQP-regulated transport capacity on gas exchange. We found that drought, flooding, and flooding plus salinity reduced Kroot and root AQP activity in Pinus taeda, whereas Kroot of the flood-tolerant Taxodium distichum did not decline under flooding. The extent of the AQP control of transport efficiency varied among organs and species, ranging from 35-55% in Kroot to 10-30% in Kstem and Kleaf. In response to treatments, AQP-mediated inhibition of Kroot rather than changes in xylem acclimation controlled the fluctuations in Kroot. The reduction in stomatal conductance and its sensitivity to vapor pressure deficit were direct responses to decreased whole-plant conductance triggered by lower Kroot and larger resistance belowground. Our results provide new mechanistic and functional insights on plant hydraulics that are essential to quantifying the influences of future stress on ecosystem function.

Anatomical changes with needle length are correlated with leaf structural and physiological traits across five Pinus species.

The genus Pinus has wide geographical range and includes species that are the most economically valued among forest trees worldwide. Pine needle length varies greatly among species, but the effects of needle length on anatomy, function, and coordination and trade-offs among traits are poorly understood. We examined variation in leaf morphological, anatomical, mechanical, chemical, and physiological characteristics among five southern pine species: Pinus echinata, Pinus elliottii, Pinus palustris, Pinus taeda, and Pinus virginiana. We found that increasing needle length contributed to a trade-off between the relative fractions of support versus photosynthetic tissue (mesophyll) across species. From the shortest (7 cm) to the longest (36 cm) needles, mechanical tissue fraction increased by 50%, whereas needle dry density decreased by 21%, revealing multiple adjustments to a greater need for mechanical support in longer needles. We also found a fourfold increase in leaf hydraulic conductance over the range of needle length across species, associated with weaker upward trends in stomatal conductance and photosynthetic capacity. Our results suggest that the leaf size strongly influences their anatomical traits, which, in turn, are reflected in leaf mechanical support and physiological capacity.

A dynamic yet vulnerable pipeline: Integration and coordination of hydraulic traits across whole plants.

The vast majority of measurements in the field of plant hydraulics have been on small-diameter branches from woody species. These measurements have provided considerable insight into plant functioning, but our understanding of plant physiology and ecology would benefit from a broader view, because branch hydraulic properties are influenced by many factors. Here, we discuss the influence that other components of the hydraulic network have on branch vulnerability to embolism propagation. We also modelled the impact of changes in the ratio of root-to-leaf areas and soil texture on vulnerability to hydraulic failure along the soil-to-leaf continuum and showed that hydraulic function is better maintained through changes in root vulnerability and root-to-leaf area ratio than in branch vulnerability. Differences among species in the stringency with which they regulate leaf water potential and in reliance on stored water to buffer changes in water potential also affect the need to construct embolism resistant branches. Many approaches, such as measurements on fine roots, small individuals, combining sap flow and psychrometry techniques, and modelling efforts, could vastly improve our understanding of whole-plant hydraulic functioning. A better understanding of how traits are coordinated across the whole plant will improve predictions for plant function under future climate conditions.

Mechanisms for minimizing height-related stomatal conductance declines in tall vines.

The ability to transport water through tall stems hydraulically limits stomatal conductance (gs ), thereby constraining photosynthesis and growth. However, some plants are able to minimize this height-related decrease in gs , regardless of path length. We hypothesized that kudzu (Pueraria lobata) prevents strong declines in gs with height through appreciable structural and hydraulic compensative alterations. We observed only a 12% decline in maximum gs along 15-m-long stems and were able to model this empirical trend. Increasing resistance with transport distance was not compensated by increasing sapwood-to-leaf-area ratio. Compensating for increasing leaf area by adjusting the driving force would require water potential reaching -1.9 MPa, far below the wilting point (-1.2 MPa). The negative effect of stem length was compensated for by decreasing petiole hydraulic resistance and by increasing stem sapwood area and water storage, with capacitive discharge representing 8-12% of the water flux. In addition, large lateral (petiole, leaves) relative to axial hydraulic resistance helped improve water flow distribution to top leaves. These results indicate that gs of distal leaves can be similar to that of basal leaves, provided that resistance is highest in petioles, and sufficient amounts of water storage can be used to subsidize the transpiration stream.

Aquaporin regulation in roots controls plant hydraulic conductance, stomatal conductance, and leaf water potential in Pinus radiata under water stress.

Stomatal regulation is crucial for forest species performance and survival on drought-prone sites. We investigated the regulation of root and shoot hydraulics in three Pinus radiata clones exposed to drought stress and its coordination with stomatal conductance (gs ) and leaf water potential (Ψleaf ). All clones experienced a substantial decrease in root-specific root hydraulic conductance (Kroot-r ) in response to the water stress, but leaf-specific shoot hydraulic conductance (Kshoot-l ) did not change in any of the clones. The reduction in Kroot-r caused a decrease in leaf-specific whole-plant hydraulic conductance (Kplant-l ). Among clones, the larger the decrease in Kplant-l , the more stomata closed in response to drought. Rewatering resulted in a quick recovery of Kroot-r and gs . Our results demonstrated that the reduction in Kplant-l , attributed to a down regulation of aquaporin activity in roots, was linked to the isohydric stomatal behaviour, resulting in a nearly constant Ψleaf as water stress started. We concluded that higher Kplant-l is associated with water stress resistance by sustaining a less negative Ψleaf and delaying stomatal closure.

Accounting for landscape heterogeneity improves spatial predictions of tree vulnerability to drought.

As climate change continues, forest vulnerability to droughts and heatwaves is increasing, but vulnerability varies regionally and locally through landscape position. Also, most models used in forecasting forest responses to heat and drought do not incorporate relevant spatial processes. In order to improve spatial predictions of tree vulnerability, we employed a nonlinear stochastic model of soil moisture dynamics accounting for landscape differences in aspect, topography and soils. Across a watershed in central Texas we modeled dynamic water stress for a dominant tree species, Juniperus ashei, and projected future dynamic water stress through the 21st century. Modeled dynamic water stress tracked spatial patterns of remotely sensed drought-induced canopy loss. Accuracy in predicting drought-impacted stands increased from 60%, accounting for spatially variable soil conditions, to 72% when also including lateral redistribution of water and radiation/temperature effects attributable to aspect. Our analysis also suggests that dynamic water stress will increase through the 21st century, with trees persisting at only selected microsites. Favorable microsites/refugia may exist across a landscape where trees can persist; however, if future droughts are too severe, the buffering capacity of an heterogeneous landscape could be overwhelmed. Incorporating spatial data will improve projections of future tree water stress and identification of potential resilient refugia.

A network model links wood anatomy to xylem tissue hydraulic behaviour and vulnerability to cavitation.

Plant xylem response to drought is routinely represented by a vulnerability curve (VC). Despite the significance of VCs, the connection between anatomy and tissue-level hydraulic response to drought remains a subject of inquiry. We present a numerical model of water flow in flowering plant xylem that combines current knowledge on diffuse-porous anatomy and embolism spread to explore this connection. The model produces xylem networks and uses different parameterizations of intervessel connection vulnerability to embolism spread: the Young-Laplace equation and pit membrane stretching. Its purpose is upscaling processes occurring on the microscopic length scales, such as embolism propagation through pit membranes, to obtain tissue-scale hydraulics. The terminal branch VC of Acer glabrum was successfully reproduced relying only on real observations of xylem tissue anatomy. A sensitivity analysis shows that hydraulic performance and VC shape and location along the water tension axis are heavily dependent on anatomy. The main result is that the linkage between pit-scale and vessel-scale anatomical characters, along with xylem network topology, affects VCs significantly. This work underscores the importance of stepping up research related to the three-dimensional network structure of xylem tissues. The proposed model's versatility makes it an important tool to explore similar future questions.

Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought.

From 2011 to 2013, Texas experienced its worst drought in recorded history. This event provided a unique natural experiment to assess species-specific responses to extreme drought and mortality of four co-occurring woody species: Quercus fusiformis, Diospyros texana, Prosopis glandulosa, and Juniperus ashei. We examined hypothesized mechanisms that could promote these species' diverse mortality patterns using postdrought measurements on surviving trees coupled to retrospective process modelling. The species exhibited a wide range of gas exchange responses, hydraulic strategies, and mortality rates. Multiple proposed indices of mortality mechanisms were inconsistent with the observed mortality patterns across species, including measures of the degree of iso/anisohydry, photosynthesis, carbohydrate depletion, and hydraulic safety margins. Large losses of spring and summer whole-tree conductance (driven by belowground losses of conductance) and shallower rooting depths were associated with species that exhibited greater mortality. Based on this retrospective analysis, we suggest that species more vulnerable to drought were more likely to have succumbed to hydraulic failure belowground.

Variability of sun-induced chlorophyll fluorescence according to stand age-related processes in a managed loblolly pine forest.

Leaf fluorescence can be used to track plant development and stress, and is considered the most direct measurement of photosynthetic activity available from remote sensing techniques. Red and far-red sun-induced chlorophyll fluorescence (SIF) maps were generated from high spatial resolution images collected with the HyPlant airborne spectrometer over even-aged loblolly pine plantations in North Carolina (United States). Canopy fluorescence yield (i.e., the fluorescence flux normalized by the light absorbed) in the red and far-red peaks was computed. This quantifies the fluorescence emission efficiencies that are more directly linked to canopy function compared to SIF radiances. Fluorescence fluxes and yields were investigated in relation to tree age to infer new insights on the potential of those measurements in better describing ecosystem processes. The results showed that red fluorescence yield varies with stand age. Young stands exhibited a nearly twofold higher red fluorescence yield than mature forest plantations, while the far-red fluorescence yield remained constant. We interpreted this finding in a context of photosynthetic stomatal limitation in aging loblolly pine stands. Current and future satellite missions provide global datasets of SIF at coarse spatial resolution, resulting in intrapixel mixture effects, which could be a confounding factor for fluorescence signal interpretation. To mitigate this effect, we propose a surrogate of the fluorescence yield, namely the Canopy Cover Fluorescence Index (CCFI) that accounts for the spatial variability in canopy structure by exploiting the vegetation fractional cover. It was found that spatial aggregation tended to mask the effective relationships, while the CCFI was still able to maintain this link. This study is a first attempt in interpreting the fluorescence variability in aging forest stands and it may open new perspectives in understanding long-term forest dynamics in response to future climatic conditions from remote sensing of SIF.

Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris.

Xylem vulnerability to embolism is emerging as a major factor in drought-induced tree mortality events across the globe. However, we lack understanding of how and to what extent climate has shaped vascular properties or functions. We investigated the evolution of xylem hydraulic function and diversification patterns in Australia's most successful gymnosperm clade, Callitris, the world's most drought-resistant conifers. For all 23 species in this group, we measured embolism resistance (P50 ), xylem specific hydraulic conductivity (Ks ), wood density, and tracheary element size from natural populations. We investigated whether hydraulic traits variation linked with climate and the diversification of this clade using a time-calibrated phylogeny. Embolism resistance varied widely across the Callitris clade (P50 : -3.8 to -18.8 MPa), and was significantly related to water scarcity, as was tracheid diameter. We found no evidence of a safety-efficiency tradeoff; Ks and wood density were not related to rainfall. Callitris diversification coincides with the onset of aridity in Australia since the early Oligocene. Our results highlight the evolutionary lability of xylem traits with climate, and the leading role of aridity in the diversification of conifers. The uncoupling of safety from other xylem functions allowed Callitris to evolve extreme embolism resistance and diversify into xeric environments.