Plant hydraulics at the heart of plant, crops and ecosystem functions in the face of climate change.

Plant hydraulics is crucial for assessing the plants' capacity to extract and transport water from the soil up to their aerial organs. Along with their capacity to exchange water between plant compartments and regulate evaporation, hydraulic properties determine plant water relations, water status and susceptibility to pathogen attacks. Consequently, any variation in the hydraulic characteristics of plants is likely to significantly impact various mechanisms and processes related to plant growth, survival and production, as well as the risk of biotic attacks and forest fire behaviour. However, the integration of hydraulic traits into disciplines such as plant pathology, entomology, fire ecology or agriculture can be significantly improved. This review examines how plant hydraulics can provide new insights into our understanding of these processes, including modelling processes of vegetation dynamics, illuminating numerous perspectives for assessing the consequences of climate change on forest and agronomic systems, and addressing unanswered questions across multiple areas of knowledge.

Photosynthesis, leaf hydraulic conductance and embolism dynamics in the resurrection plant Barbacenia purpurea.

The main parameters determining photosynthesis are stomatal and mesophyll conductance and electron transport rate, and for hydraulic dynamics they are leaf hydraulic conductance and the spread of embolism. These parameters have scarcely been studied in desiccation-tolerant (resurrection) plants exposed to drought. Here, we characterized photosynthesis and hydraulics during desiccation and rehydration in a poikilochlorophyllous resurrection plant, Barbacenia purpurea (Velloziaceae). Gas exchange, chlorophyll fluorescence, and leaf water status were monitored along the whole dehydration-rehydration cycle. Simultaneously, embolism formation and hydraulic functioning recovery were measured at leaf level using micro-computed tomography imaging. Photosynthesis and leaf hydraulic conductance ceased at relatively high water potential (-1.28 and -1.54 MPa, respectively), whereas the onset of leaf embolism occurred after stomatal closure and photosynthesis cessation (<-1.61 MPa). This sequence of physiological processes during water stress may be associated with the need to delay dehydration, to prepare the molecular changes required in the desiccated state. Complete rehydration occurred rapidly in the mesophyll, whereas partial xylem refilling, and subsequent recovery of photosynthesis, occurred at later stages after rewatering. These results highlight the importance of stomata as safety valves to protect the vascular system from embolism, even in a plant able to fully recover after complete embolism.

Key hydraulic traits control the dynamics of plant dehydration in four contrasting tree species during drought.

Trees are at risk of mortality during extreme drought, yet our understanding of the traits that govern the timing of drought-induced hydraulic failure remains limited. To address this, we tested SurEau, a trait-based soil-plant-atmosphere model designed to predict the dynamics of plant dehydration as represented by the changes in water potential against those observed in potted trees of four contrasting species (Pinus halepensis Mill., Populus nigra L., Quercus ilex L. and Cedrus atlantica (Endl.) Manetti ex Carriére) exposed to drought. SurEau was parameterized with a range of plant hydraulic and allometric traits, soil and climatic variables. We found a close correspondence between the predicted and observed plant water potential (in MPa) dynamics during the early phase drought, leading to stomatal closure, as well as during the latter phase of drought, leading to hydraulic failure in all four species. A global model's sensitivity analysis revealed that, for a common plant size (leaf area) and soil volume, dehydration time from full hydration to stomatal closure (Tclose) was most strongly controlled by the leaf osmotic potential (Pi0) and its influence on stomatal closure, in all four species, while the maximum stomatal conductance (gsmax) also contributed to Tclose in Q. ilex and C. atlantica. Dehydration times from stomatal closure to hydraulic failure (Tcav) was most strongly controlled by Pi0, the branch residual conductance (gres) and Q10a sensitivity of gres in the three evergreen species, while xylem embolism resistance (P50) was most influential in the deciduous species P. nigra. Our findings point to SurEau as a highly useful model for predicting changes in plant water status during drought and suggest that adjustments made in key hydraulic traits are potentially beneficial to delaying the onset of drought-induced hydraulic failure in trees.

A bitter future for coffee production? Physiological traits associated with yield reveal high vulnerability to hydraulic failure in Coffea canephora.

The increase in frequency and intensity of drought events have hampered coffee production in the already threatened Amazon region, yet little is known about key aspects underlying the variability in yield potential across genotypes, nor to what extent higher productivity is linked to reduced drought tolerance. Here we explored how variations in morphoanatomical and physiological leaf traits can explain differences in yield and vulnerability to embolism in 11 Coffea canephora genotypes cultivated in the Western Amazon. The remarkable variation in coffee yield across genotypes was tightly related to differences in their carbon assimilation and water transport capacities, revealing a diffusive limitation to photosynthesis linked by hydraulic constraints. Although a clear trade-off between water transport efficiency and safety was not detected, all the studied genotypes operated in a narrow and/or negative hydraulic safety margin, suggesting a high vulnerability to leaf hydraulic failure (HF), especially on the most productive genotypes. Modelling exercises revealed that variations in HF across genotypes were mainly associated with differences in leaf water vapour leakage when stomata are closed, reflecting contrasting growth strategies. Overall, our results provide a new perspective on the challenges of sustaining coffee production in the Amazon region under a drier and warmer climate.

On the path from xylem hydraulic failure to downstream cell death.

Xylem hydraulic failure (HF) has been identified as a ubiquitous factor in triggering drought-induced tree mortality through the damage induced by the progressive dehydration of plant living cells. However, fundamental evidence of the mechanistic link connecting xylem HF to cell death has not been identified yet. The main aim of this study was to evaluate, at the leaf level, the relationship between loss of hydraulic function due to cavitation and cell death under drought conditions and discern how this relationship varied across species with contrasting resistances to cavitation. Drought was induced by withholding water from potted seedlings, and their leaves were sampled to measure their relative water content (RWC) and cell mortality. Vulnerability curves to cavitation at the leaf level were constructed for each species. An increment in cavitation events occurrence precedes the onset of cell mortality. A variation in cells tolerance to dehydration was observed along with the resistance to cavitation. Overall, our results indicate that the onset of cellular mortality occurs at lower RWC than the one for cavitation indicating the role of cavitation in triggering cellular death. They also evidenced a critical RWC for cellular death varying across species with different cavitation resistance.

Plant hydraulic modelling of leaf and canopy fuel moisture content reveals increasing vulnerability of a Mediterranean forest to wildfires under extreme drought.

Fuel moisture content (FMC) is a crucial driver of forest fires in many regions world-wide. Yet, the dynamics of FMC in forest canopies as well as their physiological and environmental determinants remain poorly understood, especially under extreme drought. We embedded a FMC module in the trait-based, plant-hydraulic SurEau-Ecos model to provide innovative process-based predictions of leaf live fuel moisture content (LFMC) and canopy fuel moisture content (CFMC) based on leaf water potential ( ψ Leaf ). SurEau-Ecos-FMC relies on pressure-volume (p-v) curves to simulate LFMC and vulnerability curves to cavitation to simulate foliage mortality. SurEau-Ecos-FMC accurately reproduced ψ Leaf and LFMC dynamics as well as the occurrence of foliage mortality in a Mediterranean Quercus ilex forest. Several traits related to water use (leaf area index, available soil water, and transpiration regulation), vulnerability to cavitation, and p-v curves (full turgor osmotic potential) had the greatest influence on LFMC and CFMC dynamics. As the climate gets drier, our results showed that drought-induced foliage mortality is expected to increase, thereby significantly decreasing CFMC. Our results represent an important advance in our capacity to understand and predict the sensitivity of forests to wildfires.

Leaf water potential measurements using the pressure chamber: Synthetic testing of assumptions towards best practices for precision and accuracy.

Leaf water potential (ψleaf ), typically measured using the pressure chamber, is the most important metric of plant water status, providing high theoretical value and information content for multiple applications in quantifying critical physiological processes including drought responses. Pressure chamber measurements of ψleaf (ψleafPC ) are most typical, yet, the practical complexity of the technique and of the underlying theory has led to ambiguous understanding of the conditions to optimize measurements. Consequently, specific techniques and precautions diversified across the global research community, raising questions of reliability and repeatability. Here, we surveyed specific methods of ψleafPC from multiple laboratories, and synthesized experiments testing common assumptions and practices in ψleafPC for diverse species: (i) the need for equilibration of previously transpiring leaves; (ii) leaf storage before measurement; (iii) the equilibration of ψleaf for leaves on bagged branches of a range of dehydration; (iv) the equilibration of ψleaf across the lamina for bagged leaves, and the accuracy of measuring leaves with artificially 'elongated petioles'; (v) the need in ψleaf measurements for bagging leaves and high humidity within the chamber; (vi) the need to avoid liquid water on leaf surfaces; (vii) the use of 'pulse' pressurization versus gradual pressurization; and (viii) variation among experimenters in ψleafPC determination. Based on our findings we provide a best practice protocol to maximise accuracy, and provide recommendations for ongoing species-specific tests of important assumptions in future studies.

Drought acclimation of Quercus ilex leaves improves tolerance to moderate drought but not resistance to severe water stress.

Increasing temperature and drought can result in leaf dehydration and defoliation even in drought-adapted tree species such as the Mediterranean evergreen Quercus ilex L. The stomatal regulation of leaf water potential plays a central role in avoiding this phenomenon and is constrained by a suite of leaf traits including hydraulic conductance and vulnerability, hydraulic capacitance, minimum conductance to water vapour, osmotic potential and cell wall elasticity. We investigated whether the plasticity in these traits may improve leaf tolerance to drought in two long-term rainfall exclusion experiments in Mediterranean forests. Osmotic adjustment was observed to lower the water potential at turgor loss in the rainfall-exclusion treatments, thus suggesting a stomatal closure at more negative water potentials and a more anisohydric behaviour in drier conditions. Conversely, leaf hydraulic conductance and vulnerability did not exhibit any plasticity between treatments so the hydraulic safety margins were narrower in the rainfall-exclusion treatments. The sequence of leaf responses to seasonal drought and dehydration was conserved among treatments and sites but trees were more likely to suffer losses of turgor and hydraulic functioning in the rainfall-exclusion treatments. We conclude that leaf plasticity might help the trees to tolerate moderate drought but not to resist severe water stress.

Conifer desiccation in the 2021 NW heatwave confirms the role of hydraulic damage.

The unprecedented heatwave which hit the Pacific northwest of North America in late June-early July 2021 impacted ecosystems and communities, yet evidence for and analysis of this impact are still missing. Here we bring a unique dataset quantifying the impact on conifer trees, which are keystone species of many northwest ecosystems. Moreover, we take advantage of this exceptional event as a broad, extreme, 'field experiment' to test a fundamental theory in plant physiology and prepare our forests for a harsher future. Overall, the data collected confirm the role of hydraulic vulnerability in drought-induced injury to trees.

Hydraulic failure and tree mortality: from correlation to causation.

Xylem hydraulic failure has been recognized as a pervasive factor in the triggering of drought-induced tree mortality. However, foundational evidence of the mechanistic link connecting hydraulic failure with living cell damage and tree death has not been identified yet, compromising our ability to predict mortality events. Meristematic cells are involved in the recovery of trees from drought, and focusing on their vitality and functionality after a drought event could provide novel information on the mechanistic link between hydraulic failure and drought-induced tree mortality. In this Opinion, we focus on the cell's critical hydration status for tree recovery from drought and how it links with the membrane integrity of the meristems.

Acclimation of hydraulic and morphological traits to water deficit delays hydraulic failure during simulated drought in poplar.

The capacity of trees to tolerate and survive increasing drought conditions in situ will depend in part on their ability to acclimate (via phenotypic plasticity) key hydraulic and morphological traits that increase drought tolerance and delay the onset of drought-induced hydraulic failure. However, the effect of water-deficit acclimation in key traits that determine time to hydraulic failure (THF) during extreme drought remains largely untested. We measured key hydraulic and morphological traits in saplings of a hybrid poplar grown under well-watered and water-limited conditions. The time for plants to dry-down to critical levels of water stress (90% loss of stem hydraulic conductance), as well as the relative contribution of drought acclimation in each trait to THF, was simulated using a soil-plant hydraulic model (SurEau). Compared with controls, water-limited plants exhibited significantly lower stem hydraulic vulnerability (P50stem), stomatal conductance and total canopy leaf area (LA). Taken together, adjustments in these and other traits resulted in longer modelled THF in water-limited (~160 h) compared with well-watered plants (~50 h), representing an increase of more than 200%. Sensitivity analysis revealed that adjustment in P50stem and LA contributed the most to longer THF in water-limited plants. We observed a high degree of trait plasticity in poplar saplings in response to water-deficit growth conditions, with decreases in stem hydraulic vulnerability and leaf area playing a key role in delaying the onset of hydraulic failure during a simulated drought event. These findings suggest that understanding the capacity of plants to acclimate to antecedent growth conditions will enable better predictions of plant survivorship during future drought.

Seasonal and long-term consequences of esca grapevine disease on stem xylem integrity.

Hydraulic failure has been extensively studied during drought-induced plant dieback, but its role in plant-pathogen interactions is under debate. During esca, a grapevine (Vitis vinifera) disease, symptomatic leaves are prone to irreversible hydraulic dysfunctions but little is known about the hydraulic integrity of perennial organs over the short- and long-term. We investigated the effects of esca on stem hydraulic integrity in naturally infected plants within a single season and across season(s). We coupled direct (ks) and indirect (kth) hydraulic conductivity measurements, and tylose and vascular pathogen detection with in vivo X-ray microtomography visualizations. Xylem occlusions (tyloses) and subsequent loss of stem hydraulic conductivity (ks) occurred in all shoots with severe symptoms (apoplexy) and in more than 60% of shoots with moderate symptoms (tiger-stripe), with no tyloses in asymptomatic shoots. In vivo stem observations demonstrated that tyloses occurred only when leaf symptoms appeared, and resulted in more than 50% loss of hydraulic conductance in 40% of symptomatic stems, unrelated to symptom age. The impact of esca on xylem integrity was only seasonal, with no long-term impact of disease history. Our study demonstrated how and to what extent a vascular disease such as esca, affecting xylem integrity, could amplify plant mortality through hydraulic failure.

The interplay of hydraulic failure and cell vitality explains tree capacity to recover from drought.

Global climatic models predict an increment in the frequency and intensity of drought events, which have important consequences on forest dieback. However, the mechanisms leading to tree mortality under drought conditions and the physiological thresholds for recovery are not totally understood yet. This study aimed to identify what are the key physiological traits that determine the tree capacity to recover from drought. Individuals of a conifer (Pseudotsuga menziesii M.) and an angiosperm (Prunus lusitanica L.) species were exposed to drought and their ability to recover after rehydration monitored. Results showed that the actual thresholds used for recovery from drought based on percentage loss of conductance (PLC) (i.e., 50% for conifers, 88% for angiosperms) do not provide accurate insights about the tree capacity for surviving extreme drought events. On the contrary, differences in stem relative water content (RWCStem ) and the level of electrolytes leakage (EL) were directly related to the capacity of the trees to recover from drought. This was the case for the conifer species, P. menziesii, for which higher RWCStem and lower EL values were related to the recovery capacity. Even if results showed a similar trend for the angiosperm P. lusitanica as for the conifers, differences between the two traits were much more subtle and did not allow an accurate differentiation between trees able to recover and those that were not. RWCStem and EL could work as indicators of tree capacity to recover from drought for conifers but more studies are required to confirm this observation for angiosperms.

Where do leaf water leaks come from? Trade-offs underlying the variability in minimum conductance across tropical savanna species with contrasting growth strategies.

Plants continue to lose water from their leaves even after complete stomatal closure. Although this minimum conductance (gleaf-res ) has substantial impacts on strategies of water use and conservation, little is known about the potential drivers underlying the variability of this trait across species. We thus untangled the relative contribution of water leaks from the cuticle and stomata in order to investigate how the variability in leaf morphological and anatomical traits is related to the variation in gleaf-res and carbon assimilation capacity across 30 diverse species from the Brazilian Cerrado. In addition to cuticle permeance, water leaks from stomata had a significant impact on gleaf-res . The differential pattern of stomata distribution in the epidermis was a key factor driving this variation, suggesting the existence of a trade-off between carbon assimilation and water loss through gleaf-res . For instance, higher gleaf-res , observed in fast-growing species, was associated with the investment in small and numerous stomata, which allowed higher carbon assimilation rates but also increased water leaks, with negative impacts on leaf survival under drought. Variation in cuticle structural properties was not linked to gleaf-res . Our results therefore suggest the existence of a trade-off between carbon assimilation efficiency and dehydration tolerance at foliar level.

How does contemporary selection shape oak phenotypes?

Most existing forests are subjected to natural and human-mediated selection pressures, which have increased due to climate change and the increasing needs of human societies for wood, fibre and fuel resources. It remains largely unknown how these pressures trigger evolutionary changes. We address this issue here for temperate European oaks (Quercus petraea and Q. robur), which grow in mixed stands, under even-aged management regimes. We screened numerous functional traits for univariate selection gradients and for expected and observed genetic changes over two successive generations. In both species, growth, leaf morphology and physiology, and defence-related traits displayed significant selection gradients and predicted shifts, whereas phenology, water metabolism, structure and resilience-related traits did not. However, the direction of the selection response and the potential for adaptive evolution differed between the two species. Quercus petraea had a much larger phenotypic and genetic variance of fitness than Q. robur. This difference raises concerns about the adaptive response of Q. robur to contemporary selection pressures. Our investigations suggest that Q. robur will probably decline steadily, particularly in mixed stands with Q. petraea, consistent with the contrasting demographic dynamics of the two species.

Importance of Physiological Traits Vulnerability in Determine Halophytes Tolerance to Salinity Excess: A Comparative Assessment in Atriplex halimus.

Many halophytic physiological traits related to the tolerance of plants to salinity excess have been extensively studied, with a focus on biomass and/or gas exchange parameters. To gain a more complete understanding of whether salinity excess affects the physiological performance of halophytes, an experiment was performed using the halophyte Atriplex halimus L. as a model. A. halimus plants were subjected to two salinity treatments (171 and 513 mM NaCl) over 60 days in a controlled environment. After this period, dry biomass, specific stem conductivity, water potential at turgor loss point, osmotic potential, gas exchange parameters, and the fluorescence of chlorophyll a derived parameters were assessed in order to obtain knowledge about the differences in vulnerability that these parameters can show when subjected to salinity stress. Our results showed a decrease in belowground and aboveground biomass. The decrement in biomass seen at 513 mM NaCl was related to photosynthetic limitations and specific stem conductivity. Turgor loss point did not vary significantly with the increment of salinity. Therefore, the parameter that showed less vulnerability to saline stress was the turgor loss point, with only a 5% decrease, and the more vulnerable trait was the stem conductivity, with a reduction of nearly 50%.

Drought-induced lacuna formation in the stem causes hydraulic conductance to decline before xylem embolism in Selaginella.

Lycophytes are the earliest diverging extant lineage of vascular plants, sister to all other vascular plants. Given that most species are adapted to ever-wet environments, it has been hypothesized that lycophytes, and by extension the common ancestor of all vascular plants, have few adaptations to drought. We investigated the responses to drought of key fitness-related traits such as stomatal regulation, shoot hydraulic conductance (Kshoot ) and stem xylem embolism resistance in Selaginella haematodes and S. pulcherrima, both native to tropical understory. During drought stomata in both species were found to close before declines in Kshoot , with a 50% loss of Kshoot occurring at -1.7 and -2.5 MPa in S. haematodes and S. pulcherrima, respectively. Direct observational methods revealed that the xylem of both species was resistant to embolism formation, with 50% of embolized xylem area occurring at -3.0 and -4.6 MPa in S. haematodes and S. pulcherrima, respectively. X-ray microcomputed tomography images of stems revealed that the decline in Kshoot occurred with the formation of an air-filled lacuna, disconnecting the central vascular cylinder from the cortex. We propose that embolism-resistant xylem and large capacitance, provided by collapsing inner cortical cells, is essential for Selaginella survival during water deficit.

In situ estimation of genetic variation of functional and ecological traits in Quercus petraea and Q.robur.

BACKGROUND: Predicting the evolutionary potential of natural tree populations requires the estimation of heritability and genetic correlations among traits on which selection acts, as differences in evolutionary success between species may rely on differences for these genetic parameters. In situ estimates are expected to be more accurate than measures done under controlled conditions which do not reflect the natural environmental variance. AIMS: The aim of the current study was to estimate three genetic parameters (i.e. heritability, evolvability and genetic correlations) in a natural mixed oak stand composed of Quercus petraea and Quercus robur about 100 years old, for 58 traits of ecological and functional relevance (growth, reproduction, phenology, physiology, resilience, structure, morphology and defence). METHODS: First we estimated genetic parameters directly in situ using realized genomic relatedness of adult trees and parentage relationships over two generations to estimate the traits additive variance. Secondly, we benefited from existing ex situ experiments (progeny tests and conservation collection) installed with the same populations, thus allowing comparisons of in situ heritability estimates with more traditional methods. RESULTS: Heritability and evolvability estimates obtained with different methods varied substantially and showed large confidence intervals, however we found that in situ were less precise than ex situ estimates, and assessments over two generations (with deeper relatedness) improved estimates of heritability while large sampling sizes are needed for accurate estimations. At the biological level, heritability values varied moderately across different ecological and functional categories of traits, and genetic correlations among traits were conserved over the two species. CONCLUSION: We identified limits for using realized genomic relatedness in natural stands to estimate the genetic variance, given the overall low variance of genetic relatedness and the rather low sampling sizes of currently used long term genetic plots in forestry. These limits can be overcome if larger sample sizes are considered, or if the approach is extended over the next generation.

The DroughtBox: A new tool for phenotyping residual branch conductance and its temperature dependence during drought.

Xylem hydraulic failure is a major driver of tree death during drought. However, to better understand mortality risk in trees, especially during hot-drought events, more information is required on both rates of residual water-loss from small branches (gres ) after stomatal closure, as well as the phase transition temperature (Tp ), beyond which gres significantly increases. Here, we describe and test a novel low-cost tool, the DroughtBox, for phenotyping gres and Tp across species. The system consists of a programmable climatically controlled chamber in which branches dehydrate and changes in the mass recorded. Test measurements show that the DroughtBox maintains stable temperature and relative humidity across a range of set points, a prerequisite for getting accurate gres and Tp values. Among a study group of four conifer and one angiosperm species, we observed a range of gres (0.44-1.64 mmol H2 O m-2 s-1 ) and Tp (39.4-43.8°C) values. Furthermore, the measured time to hydraulic failure varied between two conifers species and was shortened in both species following a heatwave event. The DroughtBox is a reliable and customizable tool for phenotyping gres and Tp , as well as for testing models of time to hydraulic failure that will improve our ability to assess climate change impacts on plants.