Régis Burlett

Summary: Plant ecological and evolutionary strategies are shaped by interactions between phylogenetic history and environmental constraints, resulting in leaf and stomatal traits. However, traditional trait-based and phylogenetic approaches often fail to fully explain biochemical mechanisms underlying ecological strategies, particularly for leaf and stomatal traits. Plant metabolomes integrate genetic, physiological, and environmental information and therefore represent a promising intermediate phenotype for investigating links between biochemical diversity, functional traits, and evolutionary patterns. We analysed metabolomic profiles from 74 plant species with various growth forms and ecological types. Using machine learning approaches, we explored whether metabolic variation could predict plant functional divisions, growth forms and phenological types, but also physiological traits related to drought resistance. Metabolomic data contained structured information associated with variation in plant functional traits, ecological strategies, and phylogenetic relationships. Machine learning models identified with high accuracy distinct metabolic signatures linked to differences among plant functional divisions, growth forms, phenology, and trait values. Our study demonstrates that predictive metabolomics provides a powerful and integrative framework to investigate plant ecological and evolutionary strategies. By linking biochemical diversity with plant phylogeny, and ecophysiological traits across multiple species, this approach offers new opportunities to explore the mechanistic basis of plant evolution.

Summary: Stomatal closure prevents significant water losses during drought events. Yet, leaves are not perfectly hermetic and dehydration ensues through residual water losses, known as minimum conductance ( g _min ), which is highly relevant since it informs on the water depletion dynamics under stress. We measured g _min on 101 species spanning phylogenetic and ecological diversities, from ferns to flowering plants. Sampling also included different growth forms and life cycles from annual herbs to longevous trees. We used stomatal measurements to estimate operational ( g _{th op} ) and maximum ( g _{th max} ) conductances. Minimum water conductance is highly variable across species, and g _min shows a weak phylogenetic signal across vascular plants. Annual herbaceous plants have greater water loss than woody plants, and deciduous species showed higher g _min rates than evergreen species. Relationships of g _min with g _{th op} and g _{th max} were weak, revealing the lack of a clear tradeoff between maximum potential conductance efficiency and water retention. We found reduced water expenses in species occupying hotter and more seasonal environments. This study integrates g _min in leaf economics, where long‐lived leaves show higher capabilities to retain water under stress. We provide important information in evolutionary physiology to understand the water loss dynamics under drought stress across clades of vascular plants.

Perennial plant dieback involves complex interactions between pathogens, plant morphology, ecophysiology, and environmental conditions. The factors driving intraspecific variation in dieback susceptibility remain unclear. Their identification could guide the selection of more resilient genotypes under global changes. We used a common garden containing 46 Vitis vinifera (grapevine) cultivars to test the hypothesis that differences in grapevine susceptibility to esca (a complex vascular disease leading to dieback) result from cultivar-specific interactions between leaf gas exchange, and the anatomical structure, metabolism and microbiome of stem wood. Cultivars with better water use and conservation strategies tended to be less susceptible to esca whereas xylem anatomy did not affect esca susceptibility. Symptomatic plants displayed decreases in leaf gas exchange, stem starch storage and theoretical hydraulic conductivity in response to esca, regardless of genotype, whereas microbial communities were unaffected. Symptomatic stems accumulated more secondary metabolites (mostly glycosylated flavonoids and terpenes) in highly susceptible than in weakly susceptible genotypes. Cultivar-specific physiological traits therefore shape esca susceptibility in grapevines and defence metabolites transported in the xylem may play a key role in the onset of leaf symptoms. Integrative studies unravelling plant-microorganism-environment interactions are crucial to improve our understanding of complex plant diseases.

In perennial plants, abiotic and biotic stresses may occur in combination and/or in sequence over many years, making understanding and predicting the combined effects of drought and pathogens on plant health and productivity a considerable challenge. In this study, we investigated the susceptibility of esca-symptomatic grapevines (Vitis vinifera L.) to drought. Esca is a grapevine vascular disease leading to decreased vineyard longevity worldwide. Using transplanted, naturally infected 20-yr-old “Sauvignon blanc” vines with known esca histories, we subjected esca-symptomatic and asymptomatic control vines to different drought periods. Whole-plant and leaf physiology, radial growth, anatomical traits, and long-term recovery were compared among treatments. Esca leaf symptoms were associated with stem xylem vessel occlusion, leaf drop, and decreased symptomatic leaf gas exchange, resulting in reduced canopy area and thus, lower whole canopy transpiration. When esca-symptomatic plants were subjected to drought, declines in water potential, CO2 assimilation and stomatal conductance measured on green leaves, as well as canopy maximum transpiration, were delayed. Water stress did not cause a significant increase in stem xylem occlusion. The esca-symptomatic stems showed greater radial stem diameter recovery that coincided with faster regrowth of healthy new shoots at the top of the plant associated with a recovery of whole plant gas exchange. Esca mitigates the effects of drought through reduced canopy area, confirming an antagonistic interaction between these stresses. These results demonstrate the importance of combining abiotic and biotic stresses and understanding their interactions when studying dieback in the climate change context.

Summary: Leaf water loss after stomatal closure is key to understanding the effects of prolonged drought on vegetation. It is therefore important to accurately quantify such water losses to improve physiology‐based models of drought‐induced plant mortality. We measured water loss of detached leaves continuously during dehydration in nine woody angiosperm species. We computed minimum leaf conductance (g_min) at different water potential thresholds along a sequence of physiological function losses, spanning from turgor loss point to hydraulic failure. A mechanistic model evaluated the impact of different g_min estimations on the time to hydraulic failure (THF). Residual conductance is not steady and decreases continuously at varying rates across species during the entire dehydration process, even after correcting for leaf shrinkage and vapor pressure deficit shifts. Different estimations of g_min had a significant impact on the THF predicted by the model, especially for drought‐resistant species. We demonstrate that residual conductance is variable during dehydration, and thus, it is important to use physiological or water status boundaries for its estimation in order to determine distinct g_min values of water loss. We describe an accurate, repeatable and open‐source methodology to estimate g_min. Such methodology could enhance models of plant mortality under drought.

Key message: The elapsed times to deplete starch concentrations and to reach a null hydraulic safety margin were related to tree seedling mortality under experimental drought. Starch concentration showed an accelerated decline across all species during the early stages of dehydration, while the concentrations of soluble sugars and total nonstructural carbohydrates remained stable. Concomitant carbohydrate depletion and hydraulic failure drive seedling mortality under drought. Context: Current upsurges of drought events are provoking impacts on tree physiology, resulting in forest mortality. Hydraulic dysfunction and nonstructural carbohydrate (NSC) depletion have been posited as the main mechanisms leading to plant mortality under drought. Aims: This study explores the dynamics of the two mortality-inducing processes during drought stress using an experimental approach with 12 evergreen tree species. Methods: Seedlings were subjected to drought until 100% mortality was observed. Midday (Ψ_MD) and predawn (Ψ_PD) water potentials, xylem pressure leading to a 50% loss of hydraulic conductivity (Ψ₅₀), along with NSC concentrations in different organs (leaves, stems, and roots) were measured regularly during drought. Results: Total NSC concentrations and soluble sugar pools did not decline during drought. However, starch pools showed strong reductions early during drought stress as Ψ_PD decreased, and the time leading to starch depletion emerged as a strong mortality predictor. Ψ₅₀ alone did not provide an accurate estimate of mortality, while the elapsed time to reach a null hydraulic safety margin (Ψ_MD—Ψ₅₀ = 0) was related to seedling mortality. Conclusion: Adopting a dynamic approach by estimating the times to consume both starch reserves and hydraulic safety margins is highly relevant to improve predictions of tree mortality under the current context of increasing global drought.

Measurements of resistance to embolism suggest that Cupressus sempervirens has a stem xylem that resists embolism at very negative water potentials, with 50% embolism (P₅₀) at water potentials of approximately −10 MPa. However, field observations in a semi‐arid region suggest tree mortality occurs before 10% embolism. To explore the interplay between embolism and plant mortality, we conducted a controlled drought experiment involving two types of CS seedlings: a local seed source (S‐type) and a drought‐resistant clone propagated from a semi‐arid forest (C‐type). We measured resistance to embolism, leaf relative water content (RWC), water potential, photosynthesis, electrolyte leakage (EL), plant water loss, leaf hydraulic conductivity, and leaf non‐structural carbohydrate (NSC) content during plant dehydration and before rewatering. All measured individuals were monitored for survival or mortality. While the S‐ and C‐types differed in P₅₀, transpiration, and mortality rates, both displayed seedling mortality corresponding to threshold values of 52–55% leaf RWC, 55% and 18.5% percent loss of conductivity (PLC) in the xylem, which corresponds to 48% and 37% average EL values for S and C types, respectively. Although C‐type C. sempervirens NSC content increased in response to drought, no differences were observed in NSC content between live and dead seedlings of both types. Our findings do not fully explain tree mortality in the field but they do indicate that loss of membrane integrity occurs before or at xylem water potential, leading to hydraulic failure.

Summary: 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.

Key message: The datasets describe bacterial and fungal communities of European beech (Fagus sylvatica) leaves collected along a vertical gradient in a gallery forest throughout the growing season. They also describe communities in the surrounding environment of beech trees. Dataset access is at https://doi.org/10.7910/DVN/FFHAQU, and associated metadata are available at https://metadata-afs.nancy.inra.fr/geonetwork/srv/fre/catalog.search#/metadata/f17fe848-fc3e-4297-be11-9871b35a1be4. Both can be used to uncover the dynamics and assembly processes of phyllosphere microbial communities in forest ecosystems.

Summary: 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.