Unpacking the point of no return under drought in poplar: insight from stem diameter variation.

A specific, robust threshold for drought-induced tree mortality is needed to improve the prediction of forest dieback. Here, we tested the relevance of continuous measurements of stem diameter variations for identifying such a threshold, their relationship with hydraulic and cellular damage mechanisms, and the influence of growth conditions on these relationships. Poplar saplings were grown under well-watered, water-limited, or light-limited conditions and then submitted to a drought followed by rewatering. Stem diameter was continuously measured to investigate two parameters: the percentage loss of diameter (PLD) and the percentage of diameter recovery (DR) following rewatering. Water potentials, stomatal conductance, embolism, and electrolyte leakage were also measured, and light microscopy allowed investigating cell collapse induced by drought. The water release observed through loss of diameter occurred throughout the drought, regardless of growth conditions. Poplars did not recover from drought when PLD reached a threshold and this differed according to growth conditions but remained linked to cell resistance to damage and collapse. Our findings shed new light on the mechanisms of drought-induced tree mortality and indicate that PLD could be a relevant indicator of drought-induced tree mortality, regardless of the growth conditions.

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.

Mechanisms of grapevine resilience to a vascular disease: investigating stem radial growth, xylem development and physiological acclimation.

BACKGROUND AND AIMS: Plant vascular diseases significantly impact crop yield worldwide. Esca is a vascular disease of grapevine found globally in vineyards which causes a loss of hydraulic conductance due to the occlusion of xylem vessels by tyloses. However, the integrated response of plant radial growth and physiology in maintaining xylem integrity in grapevine expressing esca symptoms remains poorly understood. METHODS: We investigated the interplay between variation in stem diameter, xylem anatomy, plant physiological response and hydraulic traits in two widespread esca-susceptible cultivars, 'Sauvignon blanc' and 'Cabernet Sauvignon'. We used an original experimental design using naturally infected mature vines which were uprooted and transplanted into pots allowing for their study in a mini-lysimeter glasshouse phenotyping platform. KEY RESULTS: Esca significantly altered the timing and sequence of stem growth periods in both cultivars, particularly the shrinkage phase following radial expansion. Symptomatic plants had a significantly higher density of occluded vessels and lower leaf and whole-plant gas exchange. Esca-symptomatic vines showed compensation mechanisms, producing numerous small functional xylem vessels later in development suggesting a maintenance of stem vascular cambium activity. Stabilization or late recovery of whole-plant stomatal conductance coincided with new healthy shoots at the top of the plant after esca symptoms plateaued. CONCLUSIONS: Modified cropping practices, such as avoiding late-season topping, may enhance resilience in esca-symptomatic plants. These results highlight that integrating dendrometers, xylem anatomy and gas exchange provides insights into vascular pathogenesis and its effects on plant physiology.

Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks.

Quantitative knowledge of xylem physical tolerance limits to dehydration is essential to understanding plant drought tolerance but is lacking in many long-vessel angiosperms. We examine the hypothesis that a fundamental association between sustained xylem water transport and downstream tissue function should select for xylem that avoids embolism in long-vessel trees by quantifying xylem capacity to withstand air entry of western North American oaks (Quercus spp.). Optical visualization showed that 50% of embolism occurs at water potentials below -2.7 MPa in all 19 species, and -6.6 MPa in the most resistant species. By mapping the evolution of xylem vulnerability to embolism onto a fossil-dated phylogeny of the western North American oaks, we found large differences between clades (sections) while closely related species within each clade vary little in their capacity to withstand air entry. Phylogenetic conservatism in xylem physical tolerance, together with a significant correlation between species distributions along rainfall gradients and their dehydration tolerance, suggests that closely related species occupy similar climatic niches and that species' geographic ranges may have shifted along aridity gradients in accordance with their physical tolerance. Such trends, coupled with evolutionary associations between capacity to withstand xylem embolism and other hydraulic-related traits, yield wide margins of safety against embolism in oaks from diverse habitats. Evolved responses of the vascular system to aridity support the embolism avoidance hypothesis and reveal the importance of quantifying plant capacity to withstand xylem embolism for understanding function and biogeography of some of the Northern Hemisphere's most ecologically and economically important plants.

Is there tree senescence? The fecundity evidence.

Despite its importance for forest regeneration, food webs, and human economies, changes in tree fecundity with tree size and age remain largely unknown. The allometric increase with tree diameter assumed in ecological models would substantially overestimate seed contributions from large trees if fecundity eventually declines with size. Current estimates are dominated by overrepresentation of small trees in regression models. We combined global fecundity data, including a substantial representation of large trees. We compared size-fecundity relationships against traditional allometric scaling with diameter and two models based on crown architecture. All allometric models fail to describe the declining rate of increase in fecundity with diameter found for 80% of 597 species in our analysis. The strong evidence of declining fecundity, beyond what can be explained by crown architectural change, is consistent with physiological decline. A downward revision of projected fecundity of large trees can improve the next generation of forest dynamic models.

Antagonistic Effects of Assortative Mating on the Evolution of Phenotypic Plasticity along Environmental Gradients.

AbstractPrevious theory has shown that assortative mating for plastic traits can maintain genetic divergence across environmental gradients despite high gene flow. Yet these models did not examine how assortative mating affects the evolution of plasticity. We here describe patterns of genetic variation across elevation for plasticity in a trait under assortative mating, using multiple-year observations of budburst date in a common garden of sessile oaks. Despite high gene flow, we found significant spatial genetic divergence for the intercept, but not for the slope, of reaction norms to temperature. We then used individual-based simulations, where both the slope and the intercept of the reaction norm evolve, to examine how assortative mating affects the evolution of plasticity, varying the intensity and distance of gene flow. Our model predicts the evolution of either suboptimal plasticity (reaction norms with a slope shallower than optimal) or hyperplasticity (slopes steeper than optimal) in the presence of assortative mating when optimal plasticity would evolve under random mating. Furthermore, a cogradient pattern of genetic divergence for the intercept of the reaction norm (where plastic and genetic effects are in the same direction) always evolves in simulations with assortative mating, consistent with our observations in the studied oak populations.

Oak stands along an elevation gradient have different molecular strategies for regulating bud phenology.

BACKGROUND: Global warming raises serious concerns about the persistence of species and populations locally adapted to their environment, simply because of the shift it produces in their adaptive landscape. For instance, the phenological cycle of tree species may be strongly affected by higher winter temperatures and late frost in spring. Given the variety of ecosystem services they provide, the question of forest tree adaptation has received increasing attention in the scientific community and catalyzed research efforts in ecology, evolutionary biology and functional genomics to study their adaptive capacity to respond to such perturbations. RESULTS: In the present study, we used an elevation gradient in the Pyrenees Mountains to explore the gene expression network underlying dormancy regulation in natural populations of sessile oak stands sampled along an elevation cline and potentially adapted to different climatic conditions mainly driven by temperature. By performing analyses of gene expression in terminal buds we identified genes displaying significant dormancy, elevation or dormancy-by-elevation interaction effects. Our Results highlighted that low- and high-altitude populations have evolved different molecular strategies for minimizing late frost damage and maximizing the growth period, thereby increasing potentially their respective fitness in these contrasting environmental conditions. More particularly, population from high elevation overexpressed genes involved in the inhibition of cell elongation and delaying flowering time while genes involved in cell division and flowering, enabling buds to flush earlier were identified in population from low elevation. CONCLUSION: Our study made it possible to identify key dormancy-by-elevation responsive genes revealing that the stands analyzed in this study have evolved distinct molecular strategies to adapt their bud phenology in response to temperature.

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.

Microbial biomarkers of tree water status for next-generation biomonitoring of forest ecosystems.

Next-generation biomonitoring proposes to combine machine-learning algorithms with environmental DNA data to automate the monitoring of the Earth's major ecosystems. In the present study, we searched for molecular biomarkers of tree water status to develop next-generation biomonitoring of forest ecosystems. Because phyllosphere microbial communities respond to both tree physiology and climate change, we investigated whether environmental DNA data from tree phyllosphere could be used as molecular biomarkers of tree water status in forest ecosystems. Using an amplicon sequencing approach, we analysed phyllosphere microbial communities of four tree species (Quercus ilex, Quercus robur, Pinus pinaster and Betula pendula) in a forest experiment composed of irrigated and non-irrigated plots. We used these microbial community data to train a machine-learning algorithm (Random Forest) to classify irrigated and non-irrigated trees. The Random Forest algorithm detected tree water status from phyllosphere microbial community composition with more than 90% accuracy for oak species, and more than 75% for pine and birch. Phyllosphere fungal communities were more informative than phyllosphere bacterial communities in all tree species. Seven fungal amplicon sequence variants were identified as candidates for the development of molecular biomarkers of water status in oak trees. Altogether, our results show that microbial community data from tree phyllosphere provides information on tree water status in forest ecosystems and could be included in next-generation biomonitoring programmes that would use in situ, real-time sequencing of environmental DNA to help monitor the health of European temperate forest ecosystems.

Model-assisted ideotyping reveals trait syndromes to adapt viticulture to a drier climate.

Climate change is challenging the resilience of grapevine (Vitis), one of the most important crops worldwide. Adapting viticulture to a hotter and drier future will require a multifaceted approach including the breeding of more drought-tolerant genotypes. In this study, we focused on plant hydraulics as a multi-trait system that allows the plant to maintain hydraulic integrity and gas exchange rates longer under drought. We quantified a broad range of drought-related traits within and across Vitis species, created in silico libraries of trait combinations, and then identified drought tolerant trait syndromes. By modeling the maintenance of hydraulic integrity of current cultivars and the drought tolerant trait syndromes, we identified elite ideotypes that increased the amount of time they could experience drought without leaf hydraulic failure. Generally, elites exhibited a trait syndrome with lower stomatal conductance, earlier stomatal closure, and a larger hydraulic safety margin. We demonstrated that, when compared with current cultivars, elite ideotypes have the potential to decrease the risk of hydraulic failure across wine regions under future climate scenarios. This study reveals the syndrome of traits that can be leveraged to protect grapevine from experiencing hydraulic failure under drought and increase drought tolerance.

Drought survival in conifer species is related to the time required to cross the stomatal safety margin.

The regulation of water loss and the spread of xylem embolism have mostly been considered separately. The development of an integrated approach taking into account the temporal dynamics and relative contributions of these mechanisms to plant drought responses is urgently needed. Do conifer species native to mesic and xeric environments display different hydraulic strategies and temporal sequences under drought? A dry-down experiment was performed on seedlings of four conifer species differing in embolism resistance, from drought-sensitive to extremely drought-resistant species. A set of traits related to drought survival was measured, including turgor loss point, stomatal closure, minimum leaf conductance, and xylem embolism resistance. All species reached full stomatal closure before the onset of embolism, with all but the most drought-sensitive species presenting large stomatal safety margins, demonstrating that highly drought-resistant species do not keep their stomata open under drought conditions. Plant dry-down time to death was significantly influenced by the xylem embolism threshold, stomatal safety margin, and minimum leaf conductance, and was best explained by the newly introduced stomatal margin retention index (SMRIΨ50) which reflects the time required to cross the stomatal safety margin. The SMRIΨ50 may become a key tool for the characterization of interspecific drought survival variability in trees.

Drought response in Arabidopsis displays synergistic coordination between stems and leaves.

The synergy between drought-responsive traits across different organs is crucial in the whole-plant mechanism influencing drought resilience. These organ interactions, however, are poorly understood, limiting our understanding of drought response strategies at the whole-plant level. Therefore, we need more integrative studies, especially on herbaceous species that represent many important food crops but remain underexplored in their drought response. We investigated inflorescence stems and rosette leaves of six Arabidopsis thaliana genotypes with contrasting drought tolerance, and combined anatomical observations with hydraulic measurements and gene expression studies to assess differences in drought response. The soc1ful double mutant was the most drought-tolerant genotype based on its synergistic combination of low stomatal conductance, largest stomatal safety margin, more stable leaf water potential during non-watering, reduced transcript levels of drought stress marker genes, and reduced loss of chlorophyll content in leaves, in combination with stems showing the highest embolism resistance, most pronounced lignification, and thickest intervessel pit membranes. In contrast, the most sensitive Cvi ecotype shows the opposite extreme of the same set of traits. The remaining four genotypes show variations in this drought syndrome. Our results reveal that anatomical, ecophysiological, and molecular adaptations across organs are intertwined, and multiple (differentially combined) strategies can be applied to acquire a certain level of drought tolerance.

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.

Globally, tree fecundity exceeds productivity gradients.

Lack of tree fecundity data across climatic gradients precludes the analysis of how seed supply contributes to global variation in forest regeneration and biotic interactions responsible for biodiversity. A global synthesis of raw seedproduction data shows a 250-fold increase in seed abundance from cold-dry to warm-wet climates, driven primarily by a 100-fold increase in seed production for a given tree size. The modest (threefold) increase in forest productivity across the same climate gradient cannot explain the magnitudes of these trends. The increase in seeds per tree can arise from adaptive evolution driven by intense species interactions or from the direct effects of a warm, moist climate on tree fecundity. Either way, the massive differences in seed supply ramify through food webs potentially explaining a disproportionate role for species interactions in the wet tropics.

Functional xylem characteristics associated with drought-induced embolism in angiosperms.

Hydraulic failure resulting from drought-induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult to achieve at scale, leading to alternative metrics and correlations with more easily measured traits. These efforts have led to the longstanding and pervasive assumed mechanistic link between vessel diameter and vulnerability in angiosperms. However, there are at least two problems with this assumption that requires critical re-evaluation: (1) our current understanding of drought-induced embolism does not provide a mechanistic explanation why increased vessel width should lead to greater vulnerability, and (2) the most recent advancements in nanoscale embolism processes suggest that vessel diameter is not a direct driver. Here, we review data from physiological and comparative wood anatomy studies, highlighting the potential anatomical and physicochemical drivers of embolism formation and spread. We then put forward key knowledge gaps, emphasising what is known, unknown and speculation. A meaningful evaluation of the diameter-vulnerability link will require a better mechanistic understanding of the biophysical processes at the nanoscale level that determine embolism formation and spread, which will in turn lead to more accurate predictions of how water transport in plants is affected by drought.

Hurricanes increase tropical forest vulnerability to drought.

Rapid changes in climate and disturbance regimes, including droughts and hurricanes, are likely to influence tropical forests, but our understanding of the compound effects of disturbances on forest ecosystems is extremely limited. Filling this knowledge gap is necessary to elucidate the future of these ecosystems under a changing climate. We examined the relationship between hurricane response (damage, mortality, and resilience) and four hydraulic traits of 13 dominant woody species in a wet tropical forest subject to periodic hurricanes. Species with high resistance to embolisms (low P50 values) and higher safety margins ( SMP50 ) were more resistant to immediate hurricane mortality and breakage, whereas species with higher hurricane resilience (rapid post-hurricane growth) had high capacitance and P50 values and low SMP50 . During 26 yr of post-hurricane recovery, we found a decrease in community-weighted mean values for traits associated with greater drought resistance (leaf turgor loss point, P50 , SMP50 ) and an increase in capacitance, which has been linked with lower drought resistance. Hurricane damage favors slow-growing, drought-tolerant species, whereas post-hurricane high resource conditions favor acquisitive, fast-growing but drought-vulnerable species, increasing forest productivity at the expense of drought tolerance and leading to higher overall forest vulnerability to drought.

Physiological trait networks enhance understanding of crop growth and water use in contrasting environments.

Plant function arises from a complex network of structural and physiological traits. Explicit representation of these traits, as well as their connections with other biophysical processes, is required to advance our understanding of plant-soil-climate interactions. We used the Terrestrial Regional Ecosystem Exchange Simulator (TREES) to evaluate physiological trait networks in maize. Net primary productivity (NPP) and grain yield were simulated across five contrasting climate scenarios. Simulations achieving high NPP and grain yield in high precipitation environments featured trait networks conferring high water use strategies: deep roots, high stomatal conductance at low water potential ("risky" stomatal regulation), high xylem hydraulic conductivity and high maximal leaf area index. In contrast, high NPP and grain yield was achieved in dry environments with low late-season precipitation via water conserving trait networks: deep roots, high embolism resistance and low stomatal conductance at low leaf water potential ("conservative" stomatal regulation). We suggest that our approach, which allows for the simultaneous evaluation of physiological traits, soil characteristics and their interactions (i.e., networks), has potential to improve our understanding of crop performance in different environments. In contrast, evaluating single traits in isolation of other coordinated traits does not appear to be an effective strategy for predicting plant performance.

Pit and tracheid anatomy explain hydraulic safety but not hydraulic efficiency of 28 conifer species.

Conifers face increased drought mortality risks because of drought-induced embolism in their vascular system. Variation in embolism resistance may result from species differences in pit structure and function, as pits control the air seeding between water-transporting conduits. This study quantifies variation in embolism resistance and hydraulic conductivity for 28 conifer species grown in a 50-year-old common garden experiment and assesses the underlying mechanisms. Conifer species with a small pit aperture, high pit aperture resistance, and large valve effect were more resistant to embolism, as they all may reduce air seeding. Surprisingly, hydraulic conductivity was only negatively correlated with tracheid cell wall thickness. Embolism resistance and its underlying pit traits related to pit size and sealing were more strongly phylogenetically controlled than hydraulic conductivity and anatomical tracheid traits. Conifers differed in hydraulic safety and hydraulic efficiency, but there was no trade-off between safety and efficiency because they are driven by different xylem anatomical traits that are under different phylogenetic control.

Cross-validation of the high-capacity tensiometer and thermocouple psychrometer for continuous monitoring of xylem water potential in saplings.

The pressure chamber, the most popular method used to measure xylem water potential, is a discontinuous and destructive technique and is therefore not suitable for automated monitoring. Continuous non-destructive monitoring could until very recently be achieved only by use of the thermocouple psychrometer (TP). Here we present the high-capacity tensiometer (HCT) as an alternative method for continuous non-destructive monitoring. This provided us with a unique chance to cross-validate the two instruments by installing them simultaneously on the same sapling stem. The HCT and the TP showed excellent agreement for xylem water potential less than -0.5 MPa. Response to day/night cycles and watering was remarkably in phase, indicating excellent response time of both instruments despite substantially different working principles. For xylem water potential greater than -0.5 MPa, the discrepancies sometimes observed between the HCT and TP were mainly attributed to the kaolin paste used to establish contact between the xylem and the HCT, which becomes hydraulically poorly conductive in this range of water potential once dried beyond its air-entry value and subsequently re-wetted. Notwithstanding this limitation, which can be overcome by selecting a clay paste with higher air-entry value, the HCT has been shown to represent a valid alternative to the TP.