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.

Seasonal weather impacts wine quality in Bordeaux.

Critics judge quality based upon subjective characteristics of wine. These judgments are converted by critics into quantitative scores, which allow for comparison of vintages. This paper uses high resolution discrete and continuous time-based weather estimates at both a local and regional level to determine the role of weather conditions on producing high quality Bordeaux vintages, as determined by critics scores. By using discrete-time weather variables across local AOCs, this study reveals climate-quality relationships across the whole year, including previously ignored season effects. By using continuous time weather variables, we reinforce the evidence for these local effects by finding higher quality wine is made in years with higher rainfall, warmer temperatures; and earlier, shorter seasons. We propose management impacts of our results and suggest that as the climate continues to change, the quality of Bordeaux wines may continue to improve.

GrapevineXL reliably predicts multi-annual dynamics of vine water status, berry growth, and sugar accumulation in vineyards.

Climate and water availability greatly affect each season's grape yield and quality. Using models to accurately predict environment impacts on fruit productivity and quality is a huge challenge. We calibrated and validated the functional-structural model, GrapevineXL, with a data set including grapevine seasonal midday stem water potential (Ψxylem), berry dry weight (DW), fresh weight (FW), and sugar concentration per volume ([Sugar]) for a wine grape cultivar (Vitis vinifera cv. Cabernet Franc) in field conditions over 13 years in Bordeaux, France. Our results showed that the model could make a fair prediction of seasonal Ψxylem and good-to-excellent predictions of berry DW, FW, [Sugar] and leaf gas exchange responses to predawn and midday leaf water potentials under diverse environmental conditions with 14 key parameters. By running virtual experiments to mimic climate change, an advanced veraison (i.e. the onset of ripening) of 14 and 28 days led to significant decreases of berry FW by 2.70% and 3.22%, clear increases of berry [Sugar] by 2.90% and 4.29%, and shortened ripening duration in 8 out of 13 simulated years, respectively. Moreover, the impact of the advanced veraison varied with seasonal patterns of climate and soil water availability. Overall, the results showed that the GrapevineXL model can predict plant water use and berry growth in field conditions and could serve as a valuable tool for designing sustainable vineyard management strategies to cope with climate change.

Quantifying the grapevine xylem embolism resistance spectrum to identify varieties and regions at risk in a future dry climate.

Maintaining wine production under global warming partly relies on optimizing the choice of plant material for a given viticultural region and developing drought-resistant cultivars. However, progress in these directions is hampered by the lack of understanding of differences in drought resistance among Vitis genotypes. We investigated patterns of xylem embolism vulnerability within and among 30 Vitis species and sub-species (varieties) from different locations and climates, and assessed the risk of drought vulnerability in 329 viticultural regions worldwide. Within a variety, vulnerability to embolism decreased during summer. Among varieties, we have found wide variations in drought resistance of the vascular system in grapevines. This is particularly the case within Vitis vinifera, with varieties distributed across four clusters of embolism vulnerability. Ugni blanc and Chardonnay featured among the most vulnerable, while Pinot noir, Merlot and Cabernet Sauvignon ranked among the most resistant. Regions possibly at greater risk of being vulnerable to drought, such as Poitou-Charentes, France and Marlborough, New Zealand, do not necessarily have arid climates, but rather bear a significant proportion of vulnerable varieties. We demonstrate that grapevine varieties may not respond equally to warmer and drier conditions, and highlight that hydraulic traits are key to improve viticulture suitability under climate change.

Esca grapevine disease involves leaf hydraulic failure and represents a unique premature senescence process.

Xylem anatomy may change in response to environmental or biotic stresses. Vascular occlusion, an anatomical modification of mature xylem, contributes to plant resistance and susceptibility to different stresses. In woody organs, xylem occlusions have been examined as part of the senescence process, but their presence and function in leaves remain obscure. In grapevine, many stresses are associated with premature leaf senescence inducing discolorations and scorched tissue in leaves. However, we still do not know whether the leaf senescence process follows the same sequence of physiological events and whether leaf xylem anatomy is affected in similar ways. In this study, we quantified vascular occlusions in midribs from leaves with symptoms of the grapevine disease esca, magnesium deficiency and autumn senescence. We found higher amounts of vascular occlusions in leaves with esca symptoms (in 27% of xylem vessels on average), whereas the leaves with other symptoms (as well as the asymptomatic controls) had far fewer occlusions (in 3% of vessels). Therefore, we assessed the relationship between xylem occlusions and esca leaf symptoms in four different countries (California in the USA, France, Italy and Spain) and eight different cultivars. We monitored the plants over the course of the growing season, confirming that vascular occlusions do not evolve with symptom age. Finally, we investigated the hydraulic integrity of leaf xylem vessels by optical visualization of embolism propagation during dehydration. We found that the occlusions lead to hydraulic dysfunction mainly in the peripheral veins compared with the midribs in esca symptomatic leaves. These results open new perspectives on the role of vascular occlusions during the leaf senescence process, highlighting the uniqueness of esca leaf symptoms and its consequence on leaf physiology.

Adapting wine grape production to climate change through canopy architecture manipulation and irrigation in warm climates.

Grape growing regions are facing constant warming of the growing season temperature as well as limitations on ground water pumping used for irrigating to overcome water deficits. Trellis systems are utilized to optimize grapevine production, physiology, and berry chemistry. This study aimed to compare 6 trellis systems with 3 levels of applied water amounts based on different replacements of crop evapotranspiration (ETc) in two consecutive seasons. The treatments included a vertical shoot position (VSP), two modified VSPs (VSP60 and VSP80), a single high wire (SH), a high quadrilateral (HQ), and a Guyot pruned VSP (GY) combined with 25%, 50%, and 100% ETc water replacement. The SH had greater yields, whereas HQ was slower to reach full production potential. At harvest in both years, the accumulation of anthocyanin derivatives was enhanced in SH, whereas VSPs decreased them. As crown porosity increased (mostly VSPs), berry flavonol concentration and likewise molar % of quercetin in berries increased. Conversely, as leaf area increased, total flavonol concentration and molar % of quercetin decreased, indicating a preferential arrangement of leaf area along the canopy for overexposure of grape berry with VSP types. The irrigation treatments revealed linear trends for components of yield, where greater applied water resulted in larger berry size and likewise greater yield. 25% ETc was able to increase berry anthocyanin and flavonol concentrations. Overall, this study evidenced the efficiency of trellis systems for optimizing production and berry composition in Californian climate, also, the feasibility of using flavonols as the indicator of canopy architecture.

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.

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.

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.

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.

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.

Linking root and stem hydraulic traits to leaf physiological parameters in Coffea canephora clones with contrasting drought tolerance.

Knowing the key hydraulic traits of different genotypes at early seedling stages can potentially provide crucial information and save time for breeding programs. In the current study we investigated: (1) how root, stem and whole plant conductivities are linked to xylem traits, and (2) how the integrated hydraulic system impacts leaf water potential, gas exchange, chlorophyll a fluorescence and the growth of three coffee cultivars (clones of Coffea canephora Pierre ex Froehner cv. Conilon) with known differences in drought tolerance. The Conilon clones CL 14, CL 5 V and CL 109A, classified as tolerant, moderately tolerant, and sensitive to drought respectively, were grown under non-limiting soil-water supply but high atmospheric demand (i.e., high VPDair). CL 14 and CL 5 V displayed higher root and stem hydraulic conductance and conductivity, and higher whole plant conductivity than CL 109A, and these differences were associated with higher root growth traits. In addition, CL 109A exhibited a non-significant trend towards wider vessels. Collectively, these responses likely contributed to reduce leaf water potential in CL 109A, and in turn, reduced leaf gas exchange, especially during elevated VPDair. Even when grown under well-watered conditions, the elevated VPDair observed during this study resulted in key differences in the hydraulic traits between the cultivars corresponding to differences in plant water status, gas exchange, and photochemical activity. Together these results suggest that coffee hydraulic traits, even when grown under non-water stress conditions, can be considered in breeding programs targeting more productive and efficient genotypes under drought and high atmospheric demand.

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.

Drought activates MYB41 orthologs and induces suberization of grapevine fine roots.

The permeability of roots to water and nutrients is controlled through a variety of mechanisms and one of the most conspicuous is the presence of the Casparian strips and suberin lamellae. Roots actively regulate the creation of these structures developmentally, along the length of the root, and in response to the environment, including drought. In the current study, we characterized the suberin composition along the length of grapevine fine roots during development and in response to water deficit, and in the same root systems we quantified changes in expression of suberin biosynthesis- and deposition-related gene families (via RNAseq) allowing the identification of drought-responsive suberin-related genes. Grapevine suberin composition did not differ between primary and lateral roots, and was similar to that of other species. Under water deficit there was a global upregulation of suberin biosynthesis which resulted in an increase of suberin specific monomers, but without changes in their relative abundances, and this upregulation took place across all the developmental stages of fine roots. These changes corresponded to the upregulation of numerous suberin biosynthesis- and export-related genes which included orthologs of the previously characterized AtMYB41 transcriptional factor. Functional validation of two grapevine MYB41 orthologs, VriMYB41 and VriMYB41-like, confirmed their ability to globally upregulate suberin biosynthesis, export, and deposition. This study provides a detailed characterization of the developmental and water deficit induced suberization of grapevine fine roots and identifies important orthologs responsible for suberin biosynthesis, export, and its regulation in grape.

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.

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.