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.

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.

Variations in leaf water status and drought tolerance of dominant tree species growing in multi-aged tropical forests in Thailand.

Large-scale abandoned agricultural areas in Southeast Asia resulted in patches of forests of multiple successions and characteristics, challenging the study of their responses to environmental changes, especially under climatic water stress. Here, we investigated seasonal variation in leaf water status and drought tolerance of dominant tree species in three multi-aged tropical forests, ranging from 5 to > 200 years old, with contrasting soil moisture in Thailand. Seasonal variation in leaf water status differed among the forests with trees in young and intermediate sites demonstrating larger differences between seasons than the old-growth forest. Although vulnerability to embolism curves revealed that trees in old-growth forest were potentially more sensitive to declining leaf water status than others, they were predicted to lose < 5% of their hydraulic capacity as opposed to 13% for the trees in the younger sites. Our results suggest that the responses to water stress of tree species in different forest ages greatly vary with a tendency of trees in younger sites to be more resilience than those in older sites. Such information would benefit the selection of tree species that could adapt well to specific environments, thus improving the strategies for managing forests of different ages under a warmer future.

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.

Spatial variability in tree-ring carbon isotope discrimination in response to local drought across the entire loblolly pine natural range.

Considering the temporal responses of carbon isotope discrimination (Δ13C) to local water availability in the spatial analysis of Δ13C is essential for evaluating the contribution of environmental and genetic facets of plant Δ13C. Using tree-ring Δ13C from years with contrasting water availability at 76 locations across the natural range of loblolly pine, we decomposed site-level Δ13C signals to maximum Δ13C in well-watered conditions (Δ13Cmax) and isotopic drought sensitivity (m) as a change in Δ13C per unit change of Palmer's Drought Severity Index (PDSI). Site water status, especially the tree lifetime average PDSI, was the primary factor affecting Δ13Cmax. The strong spatial correlation exhibited by m was related to both genetic and environmental factors. The long-term average water availability during the period relevant to trees as indicated by lifetime average PDSI correlated with Δ13Cmax, suggesting acclimation in tree gas-exchange traits, independent of incident water availability. The positive correlation between lifetime average PDSI and m indicated that loblolly pines were more sensitive to drought at mesic than xeric sites. The m was found to relate to a plant's stomatal control and may be employed as a genetic indicator of efficient water use strategies. Partitioning Δ13C to Δ13Cmax and m provided a new angle for understanding sources of variation in plant Δ13C, with several fundamental and applied implications.

Potassium supply modulates Eucalyptus leaf water-status under PEG-induced osmotic stress: integrating leaf gas exchange, carbon and nitrogen isotopic composition and plant growth.

The objective of this study was to quantify the effect of potassium (K) supply on osmotic adjustment and drought avoidance mechanisms of Eucalyptus seedlings growing under short-term water stress. The effects of K supply on plant growth, nutritional status, leaf gas exchange parameters, leaf water potential (Ψw), leaf area (LA), stomatal density (SD), leaf carbon (C) and nitrogen (N) isotopic compositions (δ13C and δ15N ‰) and leaf C/N ratio under polyethylene glycol (PEG)-induced water deficit were measured. Under both control (non-PEG) and osmotic stress (+PEG) conditions, K supply increased plant growth, boosting dry matter yield with decreased C/N leaf ratio and δ15N ‰ values. The +PEG significantly reduced LA, plant growth, dry matter yield, Ψw, number of stomata per plant and leaf gas exchange, relative to non-PEG condition. Potassium supply alleviated osmotic-induced alterations in Eucalyptus seedlings by better regulating leaf development as well as SD, thus improving the rate of leaf gas exchange parameters, mesophyll conductance to CO2 (lower δ13C ‰ values) and water use efficiency (WUE). Consequently, K-supplied plants under drought better acclimated to osmotic stress than K-deficient plants, which in turn induced lower CO2 assimilation and dry matter yield, as well as higher leaf δ13C ‰ and δ15N ‰ values. In conclusion, management practices should seek to optimize K-nutrition to improve WUE, photosynthesis-related parameters and plant growth under water deficit conditions.

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.

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.

Sap Flow Disruption in Grapevine Is the Early Signal Predicting the Structural, Functional, and Genetic Responses to Esca Disease.

Fungal species involved in Esca cause the formation of grapevine wood necroses. It results in the deterioration of vascular network transport capacity and the disturbance of the physiological processes, leading to gradual or sudden grapevine death. Herein, for two consecutive growing seasons, a detailed analysis of the structural (wood necrosis and leaf discoloration) and physiological parameters related to the water use of healthy and esca-symptomatic grapevines was conducted. Measurements were carried out on 17-year-old grapevines that expressed, or not, Esca-leaf symptoms in a vineyard of the Bordeaux region (France). Whole-plant transpiration was recorded continuously from pre-veraison to harvest, using noninvasive sap flow sensors. Whole-plant transpiration was systematically about 40-50% lower in Esca-diseased grapevines compared with controls, and this difference can be observed around 2 weeks before the first Esca-foliar symptoms appeared in the vineyard. Unlike grapevine sap flow disruption, structural (e.g., leaf discolorations), functional (e.g., stomatal conductance, photosynthetic activity, phenolic compounds), and genetic (e.g., expression of leaf-targeted genes) plant responses were only significantly impacted by Esca at the onset and during leaf symptoms development. We conclude that sap flow dynamic, which was related to a high level of a white-rot necrosis, provides a useful tool to predict plant disorders due to Esca-grapevine disease.

Extensive Variation in Drought-Induced Gene Expression Changes Between Loblolly Pine Genotypes.

Drought response is coordinated through expression changes in a large suite of genes. Interspecific variation in this response is common and associated with drought-tolerant and -sensitive genotypes. The extent to which different genetic networks orchestrate the adjustments to water deficit in tolerant and sensitive genotypes has not been fully elucidated, particularly in non-model or woody plants. Differential expression analysis via RNA-seq was evaluated in root tissue exposed to simulated drought conditions in two loblolly pine (Pinus taeda L.) clones with contrasting tolerance to drought. Loblolly pine is the prevalent conifer in southeastern U.S. and a major commercial forestry species worldwide. Significant changes in gene expression levels were found in more than 4,000 transcripts [drought-related transcripts (DRTs)]. Genotype by environment (GxE) interactions were prevalent, suggesting that different cohorts of genes are influenced by drought conditions in the tolerant vs. sensitive genotypes. Functional annotation categories and metabolic pathways associated with DRTs showed higher levels of overlap between clones, with the notable exception of GO categories in upregulated DRTs. Conversely, both differentially expressed transcription factors (TFs) and TF families were largely different between clones. Our results indicate that the response of a drought-tolerant loblolly pine genotype vs. a sensitive genotype to water limitation is remarkably different on a gene-by-gene level, although it involves similar genetic networks. Upregulated transcripts under drought conditions represent the most diverging component between genotypes, which might depend on the activation and repression of substantially different groups of TFs.

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.

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.

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.

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.

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.

Using δ13C and δ18O to analyze loblolly pine (Pinus taeda L.) response to experimental drought and fertilization.

Drought frequency and intensity are projected to increase throughout the southeastern USA, the natural range of loblolly pine (Pinus taeda L.), and are expected to have major ecological and economic implications. We analyzed the carbon and oxygen isotopic compositions in tree ring cellulose of loblolly pine in a factorial drought (~30% throughfall reduction) and fertilization experiment, supplemented with trunk sap flow, allometry and microclimate data. We then simulated leaf temperature and applied a multi-dimensional sensitivity analysis to interpret the changes in the oxygen isotope data. This analysis found that the observed changes in tree ring cellulose could only be accounted for by inferring a change in the isotopic composition of the source water, indicating that the drought treatment increased the uptake of stored moisture from earlier precipitation events. The drought treatment also increased intrinsic water-use efficiency, but had no effect on growth, indicating that photosynthesis remained relatively unaffected despite 19% decrease in canopy conductance. In contrast, fertilization increased growth, but had no effect on the isotopic composition of tree ring cellulose, indicating that the fertilizer gains in biomass were attributable to greater leaf area and not to changes in leaf-level gas exchange. The multi-dimensional sensitivity analysis explored model behavior under different scenarios, highlighting the importance of explicit consideration of leaf temperature in the oxygen isotope discrimination (Δ18Oc) simulation and is expected to expand the inference space of the Δ18Oc models for plant ecophysiological studies.

Ecophysiological impacts of Esca, a devastating grapevine trunk disease, on Vitis vinifera L.

Esca is a Grapevine Trunk Disease (GTD) caused by a broad range of taxonomically unrelated fungal pathogens. These attack grapevine wood tissues inducing necroses even in the conductive vascular tissues, thus affecting the vine physiology and potentially leading to plant death. However, the influence of Esca on leaf and whole-plant water transport disruption remains poorly understood. In this paper, a detailed analysis of xylem-related physiological parameters in grapevines that expressed Esca-foliar symptoms was carried out. The experiments were conducted in a vineyard in the Bordeaux region (France) on cv. Cabernet-Sauvignon (Vitis vinifera L.) grapevines, which were monitored for Esca-foliar symptoms over a two-year period. Heat dissipation sap-flow sensors were installed during the summer on grapevines having expressed or not Esca-foliar symptoms. Leaf water potential, stomatal conductance and leaf transpiration were also measured. Physiological monitoring showed that sap flow density and whole-plant transpiration of Esca-infected grapevines decreased significantly a week before the first foliar symptoms appeared. When atmospheric water demand (Vapour Pressure Deficit, VPD) was the highest, both parameters tended to be about twice as low in symptomatic grapevines as in asymptomatic ones. Sap flow density data at the maximum transpiration-time, was systematically 29-30% lower in Esca-infected grapevines compared to control plants before or after the appearance of Esca-foliar symptoms. This trend was observed whatever the temperatures and VPD values measured. In Esca-diseased plants, larger amounts of necrotic wood, mainly white rot, were found in the trunk and cordon of symptomatic grapevines compared to healthy ones, suggesting necroses have an influence in reducing the whole-plant hydraulic capacity. This study reveals that the use of physiological monitoring methods, together with the visual monitoring of foliar symptoms, could prove useful in providing accurate measurements of Esca disease severity.

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.