Scion genotypes exert long distance control over rootstock transcriptome responses to low phosphate in grafted grapevine.

BACKGROUND: Grafting is widely used in horticulture and rootstocks are known to modify scion growth and adaptation to soil conditions. However, the role of scion genotype in regulating rootstock development and functioning has remained largely unexplored. In this study, reciprocal grafts of two grapevine genotypes were produced as well as the corresponding homo-graft controls. These plants were subjected to a low phosphate (LP) treatment and transcriptome profiling by RNA sequencing was done on root samples collected 27 h after the onset of the LP treatment. RESULTS: A set of transcripts responsive to the LP treatment in all scion/rootstock combinations was identified. Gene expression patterns associated with genetic variation in response to LP were identified by comparing the response of the two homo-grafts. In addition, the scion was shown to modify root transcriptome responses to LP in a rootstock dependent manner. A weighted gene co-expression network analysis identified modules of correlated genes; the analysis of the association of these modules with the phosphate treatment, and the scion and rootstock genotype identified potential hub genes. CONCLUSIONS: This study provides insights into the response of grafted grapevine to phosphate supply and identifies potential shoot-to-root signals that could vary between different grapevine genotypes.

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.

Potential contribution of strigolactones in regulating scion growth and branching in grafted grapevine in response to nitrogen availability.

In grafted plants, rootstocks assure the mineral nutrition of the scion and modify its development. In this study, we show that two grapevine rootstock genotypes have different shoot branching architectures when cultivated as cuttings and that this trait is transmitted to the scion when grafted. Shoot branching plasticity in response to nitrogen supply was also studied. As strigolactones are known to have a role in the regulation of shoot development in response to nutrient availability, their involvement in the control of scion architecture by the rootstock was investigated. Functional characterization of putative grapevine strigolactone biosynthetic genes in Arabidopsis mutants or grapevine cell suspensions showed similar functions to those of Arabidopsis. Both rootstocks produced strigolactone-like compounds; the quantity produced in response to nitrogen treatments differed between the two rootstock genotypes and correlated with the expression of putative strigolactone biosynthetic genes. Exudation of strigolactone-like compounds by both rootstocks was closely related to the developmental pattern of the scion in grafted plants. These results suggest that differential regulation of strigolactone biosynthesis in response to nitrogen availability may contribute to the control of scion development conferred by each rootstock genotype.

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.

Root transcriptomic responses of grafted grapevines to heterogeneous nitrogen availability depend on rootstock genotype.

In many fruit species, including grapevine, grafting is used to improve scion productivity and quality and to adapt the plant to environmental conditions. However, the mechanisms underlying the rootstock control of scion development are still poorly understood. The ability of rootstocks to regulate nitrogen uptake and assimilation may contribute to this control. A split-root system was used to grow heterografted grapevines and to investigate the molecular responses to changes in nitrate availability of two rootstocks known to affect scion growth differently. Transcriptome profiling by RNA sequencing was performed on root samples collected 3 and 24 h after nitrogen supply. The results demonstrated a common response involving nitrogen-related genes, as well as a more pronounced transcriptomic reprogramming in the genotype conferring the lower scion growth. A weighted gene co-expression network analysis allowed the identification of co-regulated gene modules, suggesting a role for nitrate transporter 2 family genes and some transcription factors as main actors controlling this genotype-dependent response to heterogeneous nitrogen supply. The relationship between nitrate, ethylene, and strigolactone hormonal pathways was found to differ between the two genotypes. These findings indicated that the genotypes responded differently to heterogeneous nitrogen availability, and this may contribute to their contrasting effect on scion growth.

Towards grapevine root architectural models to adapt viticulture to drought.

To sustainably adapt viticultural production to drought, the planting of rootstock genotypes adapted to a changing climate is a promising means. Rootstocks contribute to the regulation of scion vigor and water consumption, modulate scion phenological development and determine resource availability by root system architecture development. There is, however, a lack of knowledge on spatio-temporal root system development of rootstock genotypes and its interactions with environment and management that prevents efficient knowledge transfer into practice. Hence, winegrowers take only limited advantage of the large variability of existing rootstock genotypes. Models of vineyard water balance combined with root architectural models, using both static and dynamic representations of the root system, seem promising tools to match rootstock genotypes to frequently occurring future drought stress scenarios and address scientific knowledge gaps. In this perspective, we discuss how current developments in vineyard water balance modeling may provide the background for a better understanding of the interplay of rootstock genotypes, environment and management. We argue that root architecture traits are key drivers of this interplay, but our knowledge on rootstock architectures in the field remains limited both qualitatively and quantitatively. We propose phenotyping methods to help close current knowledge gaps and discuss approaches to integrate phenotyping data into different models to advance our understanding of rootstock x environment x management interactions and predict rootstock genotype performance in a changing climate. This could also provide a valuable basis for optimizing breeding efforts to develop new grapevine rootstock cultivars with optimal trait configurations for future growing conditions.

Soil composition and rootstock genotype drive the root associated microbial communities in young grapevines.

Soil microbiota plays a significant role in plant development and health and appears to be a major component of certain forms of grapevine decline. A greenhouse experiment was conducted to study the impact of the microbiological quality of the soil and grapevine rootstock genotype on the root microbial community and development of young plants. Two rootstocks heterografted with the same scion were grown in two vineyard soils differing in microbial composition and activities. After 4 months, culture-dependent approaches and amplicon sequencing of bacterial 16S rRNA gene and fungal ITS were performed on roots, rhizosphere and bulk soil samples. The root mycorrhizal colonization and number of cultivable microorganisms in the rhizosphere compartment of both genotypes were clearly influenced by the soil status. The fungal diversity and richness were dependent on the soil status and the rootstock, whereas bacterial richness was affected by the genotype only. Fungal genera associated with grapevine diseases were more abundant in declining soil and related root samples. The rootstock affected the compartmentalization of microbial communities, underscoring its influence on microorganism selection. Fluorescence in situ hybridization (FISH) confirmed the presence of predominant root-associated bacteria. These results emphasized the importance of rootstock genotype and soil composition in shaping the microbiome of young vines.

Pathogenicity Traits Correlate With the Susceptible Vitis vinifera Leaf Physiology Transition in the Biotroph Fungus Erysiphe necator: An Adaptation to Plant Ontogenic Resistance.

How and when the pathogen cycle is disrupted during plant development is crucial for harnessing ontogenic resistance in sustainable agriculture. Ontogenic resistance against powdery mildew (Erysiphe necator) was quantified on Vitis vinifera. Shoots were sampled in the vineyard at several dates during seasonal growth and processed in the laboratory under controlled conditions. Experiments were conducted on two susceptible Vitis vinifera Cabernet Sauvignon and Merlot. The process of leaf ontogenic resistance was investigated by measuring three quantitative traits of pathogenicity: the infection efficiency, sporulation and mycelium growth. Morphological and physiological plant indicators were used to identify leaf changes that resulted in ontogenic resistance and to predict pathogen variations that were linked to pathogenicity traits. The process of ontogenic resistance was established early in correspondence with the physiological transition of the leaf from sink to source status and was characterized by its increase in sugar content. The three traits of pathogenicity that we measured were affected, and their variation was strongly correlated with leaf age. Using leaf age, we were able to accurately predict the susceptibility of the leaf: a leaf aged, on average, 13.3 days had a very high probability (0.8) of being susceptible, while this probability decreased to 0.5 one week later. Sporulation was more closely correlated with variations in sugar and the infection efficiency in leaf water. The results for both cultivars were consistent. Ontogenic resistance on grapevine leaves is thus interpreted to be a strong, immutable physiological process that E. necator is able to circumvent by restricting its development to sink tissue. Future research should explore how this native plant resistance can be incorporated into grape management strategies to better control powdery mildew (PM) epidemics with reduced amounts of fungicides.

Phosphorus acquisition efficiency and phosphorus remobilization mediate genotype-specific differences in shoot phosphorus content in grapevine.

Crop productivity is limited by phosphorus (P) and this will probably increase in the future. Rootstocks offer a means to increase the sustainability and nutrient efficiency of agriculture. It is known that rootstocks alter petiole P concentrations in grapevine. The objective of this work was to determine which functional processes are involved in genotype-specific differences in scion P content by quantifying P uptake, P remobilization from the reserves in the cutting and P allocation within the plant in three grapevine genotypes. Cuttings of two American rootstocks and one European scion variety were grown in sand and irrigated with a nutrient solution containing either high P (0.6 mM) or low P (0 mM). The high P solution was labelled with 32P throughout the experiment. The grapevine genotypes studied show variation in the inhibition of shoot and root biomass in response to low P supply, and P supply also affected shoot, but not root, P concentrations. Genotype-specific differences in total P content were related to differences in P acquisition and utilization efficiencies (PAE and PUE, respectively). Phosphorus allocation within the plant was not affected by genotype or P supply. The rootstock genotype known to confer high petiole P content in the vineyard was associated with a high PAE under high P, and a high PUE under low P. This suggests that the petiole P concentrations in the vineyard are related to genotype-specific differences in PAE and PUE, and that these traits could be used for rootstock selection programmes in the future.

Dissecting the rootstock control of scion transpiration using model-assisted analyses in grapevine.

How rootstocks contribute to the control of scion transpiration under drought is poorly understood. We investigated the role of root characteristics, hydraulic conductance and chemical signals (abscisic acid, ABA) in the response of stomatal conductance (gs) and transpiration (E) to drought in Cabernet Sauvignon (Vitis vinifera) grafted onto drought-sensitive (Vitis riparia) and drought-tolerant (Vitis berlandieri × Vitis rupestris 110R) rootstocks. All combinations showed a concomitant reduction in gs and E, and an increase in xylem sap ABA concentration during the drought cycle. Cabernet Sauvignon grafted onto 110R exhibited higher gs and E under well-watered and moderate water deficit, but all combinations converged as water deficit increased. These results were integrated into three permutations of a whole-plant transpiration model that couples both chemical (i.e., ABA) and hydraulic signals in the modelling of stomatal control. Model comparisons revealed that both hydraulic and chemical signals were important for rootstock-specific stomatal regulation. Moreover, model parameter comparison and sensitivity analysis highlighted two major parameters differentiating the rootstocks: (i) ABA biosynthetic activity and (ii) the hydraulic conductance between the rhizosphere and soil-root interface determined by root system architecture. These differences in root architecture, specifically a higher root length area in 110R, likely explain its higher E and gs observed at low and moderate water deficit.

Model-based analysis of sugar accumulation in response to source-sink ratio and water supply in grape (Vitis vinifera) berries.

The dynamics of sugar (hexose) concentration in ripening grape berries (Vitis vinifera L.) were simulated with a refined mechanistic model. Changes in sugar concentration were reproduced by the sum of sugar import (S), sugar metabolism (M) and water budget (W). S and W were derived from model inputs of fresh and dry mass, and M was simulated with a relative metabolism rate describing the depletion of hexose. The relative metabolism rate was associated with the relative growth rate of dry mass with a coefficient (k) that was constant for a given cultivar under various growth conditions (temperature, water supply, and source-sink ratio) but varied with genotype. The k value was ~20% higher for cv. Merlot than for cv. Cabernet Sauvignon, indicating more imported sugars would be depleted by Merlot than Cabernet Sauvignon. The model correctly simulated the negative effect of lowered leaf-to-fruit ratio and the positive effect of water shortage on sugar concentration. Sensitivity analysis revealed that the present model was weakly sensitive to k because of sugar accumulation being predominantly controlled by S, with M relatively small (~20%) with respect to the increment of sugar concentration. Model simulation indicated that the decreasing leaf-to-fruit ratio reduced S more than M and W, causing a net decrease in sugar concentration. In contrast, the water shortage decreased S less than M and W, resulting in a net increase in sugar concentration.