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.

Grapevines under drought do not express esca leaf symptoms.

In the context of climate change, plant mortality is increasing worldwide in both natural and agroecosystems. However, our understanding of the underlying causes is limited by the complex interactions between abiotic and biotic factors and the technical challenges that limit investigations of these interactions. Here, we studied the interaction between two main drivers of mortality, drought and vascular disease (esca), in one of the world's most economically valuable fruit crops, grapevine. We found that drought totally inhibited esca leaf symptom expression. We disentangled the plant physiological response to the two stresses by quantifying whole-plant water relations (i.e., water potential and stomatal conductance) and carbon balance (i.e., CO2 assimilation, chlorophyll, and nonstructural carbohydrates). Our results highlight the distinct physiology behind these two stress responses, indicating that esca (and subsequent stomatal conductance decline) does not result from decreases in water potential and generates different gas exchange and nonstructural carbohydrate seasonal dynamics compared to drought.

Stomatal responses in grapevine become increasingly more tolerant to low water potentials throughout the growing season.

The leaf of a deciduous species completes its life cycle in a few months. During leaf maturation, osmolyte accumulation leads to a significant reduction of the turgor loss point (ΨTLP ), a known marker for stomatal closure. Here we exposed two grapevine cultivars to drought at three different times during the growing season to explore if the seasonal decrease in leaf ΨTLP influences the stomatal response to drought. The results showed a significant seasonal shift in the response of stomatal conductance to stem water potential (gs ~Ψstem ), demonstrating that grapevines become increasingly tolerant to low Ψstem as the season progresses in coordination with the decrease in ΨTLP . We also used the SurEau hydraulic model to demonstrate a direct link between osmotic adjustment and the plasticity of gs ~Ψstem . To understand the possible advantages of gs ~Ψstem plasticity, we incorporated a seasonally dynamic leaf osmotic potential into the model that simulated stomatal conductance under several water availabilities and climatic scenarios. The model demonstrated that a seasonally dynamic stomatal closure threshold results in trade-offs: it reduces the time to turgor loss under sustained long-term drought, but increases overall gas exchange particularly under seasonal shifts in temperature and stochastic water availability. A projected hotter future is expected to lower the increase in gas exchange that plants gain from the seasonal shift in gs ~Ψstem . These findings show that accounting for dynamic stomatal regulation is critical for understanding drought tolerance.

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.

Non-linear loss of suitable wine regions over Europe in response to increasing global warming.

Evaluating the potential climatic suitability for premium wine production is crucial for adaptation planning in Europe. While new wine regions may emerge out of the traditional boundaries, most of the present-day renowned winemaking regions may be threatened by climate change. Here, we analyse the future evolution of the geography of wine production over Europe, through the definition of a novel climatic suitability indicator, which is calculated over the projected grapevine phenological phases to account for their possible contractions under global warming. Our approach consists in coupling six different de-biased downscaled climate projections under two different scenarios of global warming with four phenological models for different grapevine varieties. The resulting suitability indicator is based on fuzzy logic and is calculated over three main components measuring (i) the timing of the fruit physiological maturity, (ii) the risk of water stress and (iii) the risk of pests and diseases. The results demonstrate that the level of global warming largely determines the distribution of future wine regions. For a global temperature increase limited to 2°C above the pre-industrial level, the suitable areas over the traditional regions are reduced by about 4%/°C rise, while for higher levels of global warming, the rate of this loss increases up to 17%/°C. This is compensated by a gradual emergence of new wine regions out of the traditional boundaries. Moreover, we show that reallocating better-suited grapevine varieties to warmer conditions may be a viable adaptation measure to cope with the projected suitability loss over the traditional regions. However, the effectiveness of this strategy appears to decrease as the level of global warming increases. Overall, these findings suggest the existence of a safe limit below 2°C of global warming for the European winemaking sector, while adaptation might become far more challenging beyond this threshold.

Chiral analysis of E-ε-viniferin enantiomers, towards a new chemotaxonomic marker of the vine.

BACKGROUND: The accurate characterization of grapevine cultivars (Vitis vinifera) is crucial for grape growers, winemakers, wine sellers, consumers and authorities, considering that mistakes could involve significant damage to the wine economic system. To avoid any misunderstanding, morphological, molecular and chemical tools are developed to positively identify grape varieties. RESULTS: E-ε-viniferin is a stilbene dimer mainly present in the woody part of grapevine and present as a mixture of two enantiomers: (7aR, 8aR)-(-)-E-ε-viniferin (1) and (7aS, 8aS)-(+)-E-ε-viniferin (2). In addition to phenotypic and genotypic approaches, a chemotaxonomic method using E-ε-viniferin enantiomers as chemical markers of grapevine cultivars was investigated. The isolation and purification of E-ε-viniferin enantiomers by preparative high-performance liquid chromatography (HPLC) and chiral HPLC from 14 red and eight white grapevine cane cultivars enabled us to determine the proportion of each enantiomer and therefore to calculate the enantiomeric excess for each variety. The relative abundance of each E-ε-viniferin enantiomer permitted us to distinguish grape varieties, as well as to establish cultivar relationships and patterns through statistical analysis. CONCLUSION: This pioneering work highlighting the enantiomeric excess of E-ε-viniferin as a chemical marker of grapevine paves the way for further studies to understand what mechanisms are involved in the production of these enantiomers in grapevine. © 2023 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Long-Term Esca Monitoring Reveals Disease Impacts on Fruit Yield and Wine Quality.

Esca is a widespread grapevine trunk disease, and a global increase in esca incidence has been observed in recent decades. Estimates attribute considerable economic losses to esca, and the disease is considered one of the major causes of vine mortality and vineyard dieback. However, accurate quantification of esca incidence is difficult due to symptom inconsistency, and there are very few studies precisely quantifying yield losses and impacts on fruit composition and wine quality. This study carried out an extensive esca surveying program; annually monitoring approximately 57,000 vines across 12 estates in the Bordeaux region for 9 years. In conjunction with this surveying program, we quantified the yield losses of vines with known esca symptom histories and assessed their fruit composition and resulting wine quality. The study revealed that, because of year-to-year variation in symptom expression, accurate rates of esca can only be obtained through monitoring over many years. We found that yield losses in individual vines exhibiting esca can reach up to 50% but they are rarely unproductive, and when scaled to the parcel scale yield losses are low, never exceeding 1 hl/ha. In addition, the quality of the grapes produced is similar to that obtained from vines without symptoms. Finally, the majority of mortality observed in vineyards was not due to esca, with only 40% of dead vines exhibiting an esca history. These results suggest that the impact of esca is likely overestimated and that it is necessary to more broadly investigate other factors contributing to vine mortality and vineyard dieback.[Formula: see text] Copyright © 2022 The Author(s). This is an open-access article distributed under the CC BY 4.0 International license.

Nighttime transpiration represents a negligible part of water loss and does not increase the risk of water stress in grapevine.

Nighttime transpiration has been previously reported as a significant source of water loss in many species; however, there is a need to determine if this trait plays a key role in the response to drought. This study aimed to determine the magnitude, regulation and relative contribution to whole plant water-use, of nighttime stomatal conductance (gnight ) and transpiration (Enight ) in grapevine (Vitis vinifera L.). Our results showed that nighttime water loss was relatively low compared to daytime transpiration, and that decreases in soil and plant water potentials were mainly explained by daytime stomatal conductance (gday ) and transpiration (Eday ). Contrary to Eday , Enight did not respond to VPD and possible effects of an innate circadian regulation were observed. Plants with higher gnight also exhibited higher daytime transpiration and carbon assimilation at midday, and total leaf area, suggesting that increased gnight may be linked with daytime behaviors that promote productivity. Modeling simulations indicated that gnight was not a significant factor in reaching critical hydraulic thresholds under scenarios of either extreme drought, or time to 20% of soil relative water content. Overall, this study suggests that gnight is not significant in exacerbating the risk of water stress and hydraulic failure in grapevine.

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.

Exploring the Hydraulic Failure Hypothesis of Esca Leaf Symptom Formation.

Vascular pathogens cause disease in a large spectrum of perennial plants, with leaf scorch being one of the most conspicuous symptoms. Esca in grapevine (Vitis vinifera) is a vascular disease with huge negative effects on grape yield and the wine industry. One prominent hypothesis suggests that vascular disease leaf scorch is caused by fungal pathogen-derived elicitors and toxins. Another hypothesis suggests that leaf scorch is caused by hydraulic failure due to air embolism, the pathogen itself, and/or plant-derived tyloses and gels. In this study, we transplanted mature, naturally infected esca symptomatic vines from the field into pots, allowing us to explore xylem integrity in leaves (i.e. leaf midveins and petioles) using synchrotron-based in vivo x-ray microcomputed tomography and light microscopy. Our results demonstrated that symptomatic leaves are not associated with air embolism. In contrast, symptomatic leaves presented significantly more nonfunctional vessels resulting from the presence of nongaseous embolisms (i.e. tyloses and gels) than control leaves, but there was no significant correlation with disease severity. Using quantitative PCR, we determined that two vascular pathogen species associated with esca necrosis in the trunk were not found in leaves where occlusions were observed. Together, these results demonstrate that symptom development is associated with the disruption of vessel integrity and suggest that symptoms are elicited at a distance from the trunk where fungal infections occur. These findings open new perspectives on esca symptom expression where the hydraulic failure and elicitor/toxin hypotheses are not necessarily mutually exclusive.

Behind the curtain of the compartmentalization process: Exploring how xylem vessel diameter impacts vascular pathogen resistance.

A key determinant of plant resistance to vascular infections lies in the ability of the host to successfully compartmentalize invaders at the xylem level. Growing evidence supports that the structural properties of the vascular system impact host vulnerability towards vascular pathogens. The aim of this study was to provide further insight into the impact of xylem vessel diameter on compartmentalization efficiency and thus vascular pathogen movement, using the interaction between Vitis and Phaeomoniella chlamydospora as a model system. We showed experimentally that an increased number of xylem vessels above 100 µm of diameter resulted in a higher mean infection level of host tissue. This benchmark was validated within and across Vitis genotypes. Although the ability of genotypes to restore vascular cambium integrity upon infection was highly variable, this trait did not correlate with their ability to impede pathogen movement at the xylem level. The distribution of infection severity of cuttings across the range of genotype's susceptibility suggests that a risk-based mechanism is involved. We used this experimental data to calibrate a mechanistic stochastic model of the pathogen spread and we provide evidence that the efficiency of the compartmentalization process within a given xylem vessel is a function of its diameter.

Over-accumulation of abscisic acid in transgenic tomato plants increases the risk of hydraulic failure.

Climate change threatens food security, and plant science researchers have investigated methods of sustaining crop yield under drought. One approach has been to overproduce abscisic acid (ABA) to enhance water use efficiency. However, the concomitant effects of ABA overproduction on plant vascular system functioning are critical as it influences vulnerability to xylem hydraulic failure. We investigated these effects by comparing physiological and hydraulic responses to water deficit between a tomato (Solanum lycopersicum) wild type control (WT) and a transgenic line overproducing ABA (sp12). Under well-watered conditions, the sp12 line displayed similar growth rate and greater water use efficiency by operating at lower maximum stomatal conductance. X-ray microtomography revealed that sp12 was significantly more vulnerable to xylem embolism, resulting in a reduced hydraulic safety margin. We also observed a significant ontogenic effect on vulnerability to xylem embolism for both WT and sp12. This study demonstrates that the greater water use efficiency in the tomato ABA overproducing line is associated with higher vulnerability of the vascular system to embolism and a higher risk of hydraulic failure. Integrating hydraulic traits into breeding programmes represents a critical step for effectively managing a crop's ability to maintain hydraulic conductivity and productivity under water deficit.

The physiology of drought stress in grapevine: towards an integrative definition of drought tolerance.

Water availability is arguably the most important environmental factor limiting crop growth and productivity. Erratic precipitation patterns and increased temperatures resulting from climate change will likely make drought events more frequent in many regions, increasing the demand on freshwater resources and creating major challenges for agriculture. Addressing these challenges through increased irrigation is not always a sustainable solution so there is a growing need to identify and/or breed drought-tolerant crop varieties in order to maintain sustainability in the context of climate change. Grapevine (Vitis vinifera), a major fruit crop of economic importance, has emerged as a model perennial fruit crop for the study of drought tolerance. This review synthesizes the most recent results on grapevine drought responses, the impact of water deficit on fruit yield and composition, and the identification of drought-tolerant varieties. Given the existing gaps in our knowledge of the mechanisms underlying grapevine drought responses, we aim to answer the following question: how can we move towards a more integrative definition of grapevine drought tolerance?

The sequence and thresholds of leaf hydraulic traits underlying grapevine varietal differences in drought tolerance.

Adapting agriculture to climate change is driving the need for the selection and breeding of drought-tolerant crops. The aim of this study was to identify key drought tolerance traits and determine the sequence of their water potential thresholds across three grapevine cultivars with contrasting water use behaviors, Grenache, Syrah, and Semillon. We quantified differences in water use between cultivars and combined this with the determination of other leaf-level traits (e.g. leaf turgor loss point, π TLP), leaf vulnerability to embolism (P50), and the hydraulic safety margin (HSM P50). Semillon exhibited the highest maximum transpiration (Emax), and lowest sensitivity of canopy stomatal conductance (Gc) to vapor pressure deficit (VPD), followed by Syrah and Grenache. Increasing Emax was correlated with more negative water potential at which stomata close (Pgs90), π TLP, and P50, suggesting that increasing water use is associated with hydraulic traits allowing gas exchange under more negative water potentials. Nevertheless, all the cultivars closed their stomata prior to leaf embolism formation. Modeling simulations demonstrated that despite a narrower HSM, Grenache takes longer to reach thresholds of hydraulic failure due to its conservative water use. This study demonstrates that the relationships between leaf hydraulic traits are complex and interactive, stressing the importance of integrating multiple traits in characterizing drought tolerance.

Drought stress modulates cuticular wax composition of the grape berry.

Drought events are a major challenge for many horticultural crops, including grapes, which are often cultivated in dry and warm climates. It is not understood how the cuticle contributes to the grape berry response to water deficit (WD); furthermore, the cuticular waxes and the related biosynthetic pathways are poorly characterized in this fruit. In this study, we identified candidate wax-related genes from the grapevine genome by phylogenetic and transcriptomic analyses. Developmental and stress response expression patterns of these candidates were characterized across pre-existing RNA sequencing data sets and confirmed a high responsiveness of the pathway to environmental stresses. We then characterized the developmental and WD-induced changes in berry cuticular wax composition, and quantified differences in berry transpiration. Cuticular aliphatic wax content was modulated during development and an increase was observed under WD, with wax esters being strongly up-regulated. These compositional changes were related to up-regulated candidate genes of the aliphatic wax biosynthetic pathway, including CER10, CER2, CER3, CER1, CER4, and WSD1. The effect of WD on berry transpiration was not significant. This study indicates that changes in cuticular wax amount and composition are part of the metabolic response of the grape berry to WD, but these changes do not reduce berry transpiration.

Merging genotypes: graft union formation and scion-rootstock interactions.

Grafting has been utilised for at least the past 7000 years. Historically, grafting has been developed by growers without particular interest beyond the agronomical and ornamental effects, and thus knowledge about grafting has remained largely empirical. Much of the commercial production of fruit, and increasingly vegetables, relies upon grafting with rootstocks to provide resistance to soil-borne pathogens and abiotic stresses as well as to influence scion growth and performance. Although there is considerable agronomic knowledge about the use and selection of rootstocks for many species, we know little of the molecular mechanisms underlying rootstock adaptation to different soil environments and rootstock-conferred modifications of scion phenotypes. Furthermore, the processes involved in the formation of the graft union and graft compatibility are poorly understood despite over a hundred years of scientific study. In this paper, we provide an overview of what is known about grafting and the mechanisms underlying rootstock-scion interactions. We highlight recent studies that have advanced our understanding of graft union formation and outline subjects that require further development.

Modelling grape growth in relation to whole-plant carbon and water fluxes.

The growth of fleshy fruits is still poorly understood as a result of the complex integration of water and solute fluxes, cell structural properties, and the regulation of whole plant source-sink relationships. To unravel the contribution of these processes to berry growth, a biophysical grape (Vitis vinifera L.) berry growth module was developed and integrated with a whole-plant functional-structural model, and was calibrated on two varieties, Cabernet Sauvignon and Sangiovese. The model captured well the variations in growth and sugar accumulation caused by environmental conditions, changes in leaf-to-fruit ratio, plant water status, and varietal differences, with obvious future application in predicting yield and maturity under a variety of production contexts and regional climates. Our analyses illustrated that grapevines strive to maintain proper ripening by partially compensating for a reduced source-sink ratio, and that under drought an enhanced berry sucrose uptake capacity can reverse berry shrinkage. Sensitivity analysis highlighted the importance of phloem hydraulic conductance, sugar uptake, and surface transpiration on growth, while suggesting that cell wall extensibility and the turgor threshold for cell expansion had minor effects. This study demonstrates that this integrated model is a useful tool in understanding the integration and relative importance of different processes in driving fleshy fruit growth.

The Xylella fastidosa RTX operons: evidence for the evolution of protein mosaics through novel genetic exchanges.

BACKGROUND: Xylella fastidiosa (Xf) is a gram negative bacterium inhabiting the plant vascular system. In most species this bacterium lives as a benign symbiote, but in several agriculturally important plants (e.g. coffee, citrus, grapevine) Xf is pathogenic. Xf has four loci encoding homologues to hemolysin RTX proteins, virulence factors involved in a wide range of plant pathogen interactions. RESULTS: We show that all four genes are expressed during pathogenesis in grapevine. The sequences from these four genes have a complex repetitive structure. At the C-termini, sequence diversity between strains is what would be expected from orthologous genes. However, within strains there is no N-terminal homology, indicating these loci encode RTXs of different functions and/or specificities. More striking is that many of the orthologous loci between strains share this extreme variation at the N-termini. Thus these RTX orthologues are most easily visualized as fusions between the orthologous C-termini and different N-termini. Further, the four genes are found in operons having a peculiar structure with an extensively duplicated module encoding a small protein with homology to the N-terminal region of the full length RTX. Surprisingly, some of these small peptides are most similar not to their corresponding full length RTX, but to the N-termini of RTXs from other Xf strains, and even other remotely related species. CONCLUSIONS: These results demonstrate that these genes are expressed in planta during pathogenesis. Their structure suggests extensive evolutionary restructuring through horizontal gene transfers and heterologous recombination mechanisms. The sum of the evidence suggests these repetitive modules are a novel kind of mobile genetic element.

Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine.

BACKGROUND: The major intrinsic protein (MIP) family is a family of proteins, including aquaporins, which facilitate water and small molecule transport across plasma membranes. In plants, MIPs function in a huge variety of processes including water transport, growth, stress response, and fruit development. In this study, we characterize the structure and transcriptional regulation of the MIP family in grapevine, describing the putative genome duplication events leading to the family structure and characterizing the family's tissue and developmental specific expression patterns across numerous preexisting microarray and RNAseq datasets. Gene co-expression network (GCN) analyses were carried out across these datasets and the promoters of each family member were analyzed for cis-regulatory element structure in order to provide insight into their transcriptional regulation. RESULTS: A total of 29 Vitis vinifera MIP family members (excluding putative pseudogenes) were identified of which all but two were mapped onto Vitis vinifera chromosomes. In this study, segmental duplication events were identified for five plasma membrane intrinsic protein (PIP) and four tonoplast intrinsic protein (TIP) genes, contributing to the expansion of PIPs and TIPs in grapevine. Grapevine MIP family members have distinct tissue and developmental expression patterns and hierarchical clustering revealed two primary groups regardless of the datasets analyzed. Composite microarray and RNA-seq gene co-expression networks (GCNs) highlighted the relationships between MIP genes and functional categories involved in cell wall modification and transport, as well as with other MIPs revealing a strong co-regulation within the family itself. Some duplicated MIP family members have undergone sub-functionalization and exhibit distinct expression patterns and GCNs. Cis-regulatory element (CRE) analyses of the MIP promoters and their associated GCN members revealed enrichment for numerous CREs including AP2/ERFs and NACs. CONCLUSIONS: Combining phylogenetic analyses, gene expression profiling, gene co-expression network analyses, and cis-regulatory element enrichment, this study provides a comprehensive overview of the structure and transcriptional regulation of the grapevine MIP family. The study highlights the duplication and sub-functionalization of the family, its strong coordinated expression with genes involved in growth and transport, and the putative classes of TFs responsible for its regulation.

A 3-D functional-structural grapevine model that couples the dynamics of water transport with leaf gas exchange.

Background and Aims: Predicting both plant water status and leaf gas exchange under various environmental conditions is essential for anticipating the effects of climate change on plant growth and productivity. This study developed a functional-structural grapevine model which combines a mechanistic understanding of stomatal function and photosynthesis at the leaf level (i.e. extended Farqhuhar-von Caemmerer-Berry model) and the dynamics of water transport from soil to individual leaves (i.e. Tardieu-Davies model). Methods: The model included novel features that account for the effects of xylem embolism (fPLC) on leaf hydraulic conductance and residual stomatal conductance (g0), variable root and leaf hydraulic conductance, and the microclimate of individual organs. The model was calibrated with detailed datasets of leaf photosynthesis, leaf water potential, xylem sap abscisic acid (ABA) concentration and hourly whole-plant transpiration observed within a soil drying period, and validated with independent datasets of whole-plant transpiration under both well-watered and water-stressed conditions. Key Results: The model well captured the effects of radiation, temperature, CO2 and vapour pressure deficit on leaf photosynthesis, transpiration, stomatal conductance and leaf water potential, and correctly reproduced the diurnal pattern and decline of water flux within the soil drying period. In silico analyses revealed that decreases in g0 with increasing fPLC were essential to avoid unrealistic drops in leaf water potential under severe water stress. Additionally, by varying the hydraulic conductance along the pathway (e.g. root and leaves) and changing the sensitivity of stomatal conductance to ABA and leaf water potential, the model can produce different water use behaviours (i.e. iso- and anisohydric). Conclusions: The robust performance of this model allows for modelling climate effects from individual plants to fields, and for modelling plants with complex, non-homogenous canopies. In addition, the model provides a basis for future modelling efforts aimed at describing the physiology and growth of individual organs in relation to water status.