Tomato genotype but not crop water deficit matters for tomato health benefits in diet-induced obesity of C57BL/6JRj male mice.

Several studies have linked the intake of lycopene and/or tomato products with improved metabolic health under obesogenic regime. The aim was to evaluate the differential impact of supplementations with several tomato genotypes differing in carotenoid content and subjected to different irrigation levels on obesity-associated disorders in mice. In this study, 80 male C57BL/6JRj mice were assigned into 8 groups to receive: control diet, high fat diet, high fat diet supplemented at 5 % w/w with 4 tomato powders originating from different tomato genotypes cultivated under control irrigation: H1311, M82, IL6-2, IL12-4. Among the 4 genotypes, 2 were also cultivated under deficit irrigation, reducing the irrigation water supply by 50 % from anthesis to fruit harvest. In controlled irrigation treatment, all genotypes significantly improved fasting glycemia and three of them significantly lowered liver lipids content after 12 weeks of supplementation. In addition, IL6-2 genotype, rich in ß-carotene, significantly limited animal adiposity, body weight gain and improved glucose homeostasis as highlighted in glucose and insulin tolerance tests. No consistent beneficial or detrimental impact of deficit irrigation to tomato promoting health benefits was found. These findings imply that the choice of tomato genotype can significantly alter the composition of fruit carotenoids and phytochemicals, thereby influencing the anti-obesogenic effects of the fruit. In contrast, deficit irrigation appears to have an overall insignificant impact on enhancing the health benefits of tomato powder in this context, particularly when compared to the genotype-related variations in carotenoid content.

Variety, growing conditions and processing method act on different structural and biochemical traits to modify viscosity in tomato puree.

The texture of tomato products can be modified by choice of variety, their growing conditions and/or processing method, but no clear explanation exists of the mechanisms that transform fruit tissue, how they act on texture, or whether genetics and processing impact the same physical parameters. We therefore conducted a study that processed 4 varieties produced under low/high nitrogen supply, into puree using both hot and cold break processes. No specific rheological signature allows discrimination between cultivar-induced or process-induced textural changes, but that they can be distinguished by sensory analysis. Growth conditions impacted but was not sensory distinguished. Both caused significant variations in 7 of 11 physico-chemical parameters, but the order of importance of these traits controlling texture varied, depending on whether the cause was genetic or process-related. Analysis of alcohol insoluble solids revealed a specific signature in pectin composition and conformation that could be linked to particle aggregation in the presence of lycopene-rich particles.

Effect of long-term deficit irrigation on tomato and goji berry quality: from fruit composition to in vitro bioaccessibility of carotenoids.

Drought is a persistent challenge for horticulture, affecting various aspects of fruit development and ultimately fruit quality, but the effect on nutritional value has been under-investigated. Here, fruit quality was studied on six tomato genotypes and one goji cultivar under deficit irrigation (DI), from fruit composition to in vitro bioaccessibility of carotenoids. For both species, DI concentrated most health-related metabolites in fresh fruit. On a dry mass basis, DI increased total phenolic and sugar concentration, but had a negative or insignificant impact on fruit ascorbic acid, organic acid, and alcohol-insoluble matter contents. DI also reduced total carotenoids content in tomato (-18.7% on average), especially ß-carotene (-32%), but not in goji berry DW (+15.5% and +19.6%, respectively). DI reduced the overall in vitro bioaccessibility of carotenoids to varying degrees depending on the compound and plant species. Consequently, mixed micelles produced by digestion of fruits subjected to DI contained either the same or lesser quantities of carotenoids, even though fresh fruits could contain similar or higher quantities. Thus, DI effects on fruit composition were species and genotype dependent, but an increase in the metabolite concentration did not necessarily translate into greater bioaccessibility potentially due to interactions with the fruit matrix.

Resource Translocation Modelling Highlights Density-Dependence Effects in Fruit Production at Various Levels of Organisation.

The size of fruit cells, seeds and fruits depends on their number. Could this density-dependence effect result from sugar resource sharing and, if so, does it involve phloem sugar flow or the intensity of sugar unloading to the sink? A density-dependence model (DDM) describing these processes was designed and parameterised for six species at five levels of organisation: cells and seeds within fruits, fruits within clusters, fruits within plants and plants within plots. Sugar flow was driven by phloem conductance, determined by parameters α, governing the shape of its relationship to population size, and κ, its value for a population size of one. Sugar unloading followed Michaelis-Menten kinetics with parameters Vm (maximal unloading rate) and Km (Michaelis constant). The DDM effectively reproduced the observed individual mass dynamics, the undercompensating density dependence observed in most species at all sub-plant levels and the undercompensating, exact and overcompensating density dependence observed at the plant level. Conductance (κ) was a scaling factor varying with the level of organisation. Vm was positively correlated with density dependence, and α was negatively correlated with density dependence only if the plant-within-plot level was not considered. Analysis of the model's behaviour indicates that density dependence of fruit growth could be a result of sugar sharing, and that both phloem sugar flow and sugar unloading contribute to these effects.

Pedicel anatomy and histology in tomato vary according to genotype and water-deficit environment, affecting fruit mass.

The growth and composition of fleshy fruits depend on resource acquisition and distribution in the plant. In tomato, the pedicel serves as the final connection between plant and fruit. However, very few quantitative data are available for the conducting tissues of the pedicel, nor is their genetic variability known. In the present study, a histological approach was combined with process-based modeling to evaluate the potential contribution made by the anatomy and histology of the pedicel to variations in fruit mass. Eleven genotypes were characterized and the impact of water deficit was studied for a single genotype using stress intensity and stage of application as variables. The results highlighted extensive variations in the relative proportions of the different pedicel tissues and in the absolute areas of xylem and phloem between genotypes. The model suggests that the variations in the area of the pedicel's vascular tissues induced by differences in genotype and water-deficit environments partly contributed to fruit mass variability. They therefore warrant phenotyping for use in the development of plant strains adapted to future environmental constraints. The results also demonstrated the need to develop non-invasive in vivo measurement methods to establish the number and size of active vessels and the flow rates in these vessels to improve prediction of water fluxes in plant architecture.

Effects of water deficit on leaves and fruit quality during the development period in tomato plant.

In nature, plants are often exposed to a multitude of environmental constraints that severely limit crop productivity. Water deficit is one of the factors that most affects agricultural production. The aim of this work is to evaluate the effect of water deficit on morphology, development, nutritional behavior, as well as chlorophyll fluorescence and certain important metabolic parameters (soluble sugars, organic acids, starch, carotenoid, and vitamin C) of the cultivated tomato (Solanum lycopersicum cv Plovdiv). In this study, the water supply was reduced by 60% compared to control conditions. The conditions of water deficit showed that the size of the different organs (leaves, fruits) was reduced. A reduction in the number, width, and length of the leaves, respectively, 9%, 36%, and 37%, then the leaf surface was also observed. Reduction of fluorescence (Fo, Fm, and Fv) and total index performance were among the other symptoms of plants with water deficiency. For fruit, we observed a significant decrease in diameter, fresh weight, and moisture content during the cell division period, the cell expansion period, and the fruit ripening period. In contrast, the composition of the Plovdiv fruit changed only during cell division and expansion phase. On the other hand, the water deficit induces an increase in the total carotenoid and vitamin C content of the fruits.. Besides, water deficit induced a reduction of fruit size, moisture content, and production dry matter during different phases of development. Decrease levels of soluble sugars and organic acid but increase in vitamin C and carotenoid content.

Insights into the Intraspecific Variability of the above and Belowground Emissions of Volatile Organic Compounds in Tomato.

The in-vivo monitoring of volatile organic compound (VOC) emissions is a potential non-invasive tool in plant protection, especially in greenhouse cultivation. We studied VOC production from above and belowground organs of the eight parents of the Multi-Parent Advanced Generation Intercross population (MAGIC) tomato population, which exhibits a high genetic variability, in order to obtain more insight into the variability of constitutive VOC emissions from tomato plants under stress-free conditions. Foliage emissions were composed of terpenes, the majority of which were also stored in the leaves. Foliage emissions were very low, partly light-dependent, and differed significantly among genotypes, both in quantity and quality. Soil with roots emitted VOCs at similar, though more variable, rates than foliage. Soil emissions were characterized by terpenes, oxygenated alkanes, and alkenes and phenolic compounds, only a few of which were found in root extracts at low concentrations. Correlation analyses revealed that several VOCs emitted from foliage or soil are jointly regulated and that above and belowground sources are partially interconnected. With respect to VOC monitoring in tomato crops, our results underline that genetic variability, light-dependent de-novo synthesis, and belowground sources are factors to be considered for successful use in crop monitoring.

Spatial and temporal evolution of quantitative magnetic resonance imaging parameters of peach and apple fruit - relationship with biophysical and metabolic traits.

Fruits are complex organs that are spatially regulated during development. Limited phenotyping capacity at cell and tissue levels is one of the main obstacles to our understanding of the coordinated regulation of the processes involved in fruit growth and quality. In this study, the spatial evolution of biophysical and metabolic traits of peach and apple fruit was investigated during fruit development. In parallel, the multi-exponential relaxation times and apparent microporosity were assessed by quantitative magnetic resonance imaging (MRI). The aim was to identify the possible relationships between MRI parameters and variations in the structure and composition of fruit tissues during development so that transverse relaxation could be proposed as a biomarker for the assessment of the structural and functional evolution of fruit tissues during growth. The study provides species-specific data on developmental and spatial variations in density, cell number and size distribution, insoluble and soluble compound accumulation and osmotic and water potential in the fruit mesocarp. Magnetic resonance imaging was able to capture tissue evolution and the development of pericarp heterogeneity by accessing information on cell expansion, water status and distribution at cell level, and microporosity. Changes in vacuole-related transverse relaxation rates were mostly explained by cell/vacuole size. The impact of cell solute composition, microporosity and membrane permeability on relaxation times is also discussed. The results demonstrate the usefulness of MRI as a tool to phenotype fruits and to access important physiological data during development, including information on spatial variability.

Decreased sink/source ratio enhances hexose transport in the fruits of greenhouse tomatoes: integration of gene expression and biochemical analyses.

To examine the physiological role of hexose transporters in determining the sink strength of individual fruits, the regulation of hexose transporters gene expression was studied when the sink/source ratio was artificially altered under the greenhouse condition; this was done in two cultivars of tomato, i.e. Grandella and Isabella. The sink/source ratio treatments included: saving one fruit per truss (1F), two fruits per truss (2F), three fruits per truss (3F) and no fruit pruning (control). The results showed that fruit thinning could increase starch, sucrose, and hexose contents in the fruits; it could also modulate the activity of the key enzymes and the expression of tomato hexose transporter genes (LeHTs). Based on the relative transcript levels, all examined LeHTs were unregulated at the end of cell division and the cell expansion stage of fruit development, but the strongest expression level observed at the onset of ripening was related to LeHT1 and LeHT2. Given the concomitancy of cell wall invertase (EC 3.2.1.26) activity and the LeHTs relative expression cell wall, invertase activity seemed to be involved in the expression level of LeHTs. The increased trends of the LeHTs expression with the decrease of the sink/source ratio confirmed the role of hexose transporters in determining the sink strength of the tomato fruits.

Fruit water content as an indication of sugar metabolism improves simulation of carbohydrate accumulation in tomato fruit.

Although fleshy fruit is mainly made up of water, little is known about the impact of its water status on sugar metabolism and its composition. In order to verify whether fruit water status is an important driver of carbohydrate composition in tomato fruit, an adaptation of the SUGAR model proposed previously by M. Génard and M. Souty was used. Two versions of the model, with or without integrating the influence of fruit water content on carbohydrate metabolism, were proposed and then assessed with the data sets from two genotypes, Levovil and Cervil, grown under different conditions. The results showed that, for both genotypes, soluble sugars and starch were better fitted by the model when the effects of water content on carbohydrate metabolism were taken into consideration. Water content might play a regulatory role in the carbon metabolism from sugars to compounds other than sugars and starch in Cervil fruit, and from sugars to starch in Levovil fruit. While water content influences tomato fruit carbohydrate concentrations by both metabolism and dilution/dehydration effects in the early developmental stage, it is mainly by dilution/dehydration effects in the late stage. The possible mechanisms underlying the effect of the fruit water content on carbohydrate metabolism are also discussed.

Leaf Production and Expansion: A Generalized Response to Drought Stresses from Cells to Whole Leaf Biomass-A Case Study in the Tomato Compound Leaf.

It is clearly established that there is not a unique response to soil water deficit but that there are as many responses as soil water deficit characteristics: Drought intensity, drought duration, and drought position during plant cycle. For a same soil water deficit, responses can also differ on plant genotype within a same species. In spite of this variability, at least for leaf production and expansion processes, robust tendencies can be extracted from the literature when similar watering regimes are compared. Here, we present response curves and multi-scale dynamics analyses established on tomato plants exposed to different soil water deficit treatments. Results reinforce the trends already observed for other species: Reduction in plant leaf biomass under water stress was due to reduction in individual leaf biomass and areas whereas leaf production and specific leaf area were not affected. The dynamics of leaf expansion was modified both at the leaf and cell scales. Cell division and expansion were reduced by drought treatments as well as the endoreduplication process. Combining response curves analyses together with dynamic analyses of tomato compound leaf growth at different scales not only corroborate results on simple leaf responses to drought but also increases our knowledge on the cellular mechanisms behind leaf growth plasticity.

Organ-wide and ploidy-dependent regulation both contribute to cell-size determination: evidence from a computational model of tomato fruit.

The development of a new organ is the result of coordinated events of cell division and expansion, in strong interaction with each other. This study presents a dynamic model of tomato fruit development that includes cell division, endoreduplication, and expansion processes. The model is used to investigate the potential interactions among these developmental processes within the context of the neo-cellular theory. In particular, different control schemes (either cell-autonomous or organ-controlled) are tested and compared to experimental data from two contrasting genotypes. The model shows that a pure cell-autonomous control fails to reproduce the observed cell-size distribution, and that an organ-wide control is required in order to get realistic cell-size variations. The model also supports the role of endoreduplication as an important determinant of the final cell size and suggests that a direct effect of endoreduplication on cell expansion is needed in order to obtain a significant correlation between size and ploidy, as observed in real data.

Coupling water fluxes with cell wall mechanics in a multicellular model of plant development.

The growth of plant organs is a complex process powered by osmosis that attracts water inside the cells; this influx induces simultaneously an elastic extension of the walls and pressure in the cells, called turgor pressure; above a threshold, the walls yield and the cells grow. Based on Lockhart's seminal work, various models of plant morphogenesis have been proposed, either for single cells, or focusing on the wall mechanical properties. However, the synergistic coupling of fluxes and wall mechanics has not yet been fully addressed in a multicellular model. This work lays the foundations of such a model, by simplifying as much as possible each process and putting emphasis on the coupling itself. Its emergent properties are rich and can help to understand plant morphogenesis. In particular, we show that the model can display a new type of lateral inhibitory mechanism that amplifies growth heterogeneities due e.g to cell wall loosening.

Are compound leaves more complex than simple ones? A multi-scale analysis.

Background and Aims: The question of which cellular mechanisms determine the variation in leaf size has been addressed mainly in plants with simple leaves. It is addressed here in tomato taking into consideration the expected complexity added by the several lateral appendages making up the compound leaf, the leaflets. Methods: Leaf and leaflet areas, epidermal cell number and areas, and endoreduplication (co-) variations were analysed in Solanum lycopersicum considering heteroblastic series in a wild type (Wva106) and an antisense mutant, the Pro35S:Slccs52AAS line, and upon drought treatments. All plants were grown in an automated phenotyping platform, PHENOPSIS, adapted to host plants grown in 7 L pots. Key Results: Leaf area, leaflet area and cell number increased with leaf rank until reaching a plateau. In contrast, cell area slightly decreased and endoreduplication did not follow any trend. In the transgenic line, leaf area, leaflet areas and cell number of basal leaves were lower than in the wild type, but higher in upper leaves. Reciprocally, cell area was higher in basal leaves and lower in upper leaves. When scaled up at the whole sympodial unit, all these traits did not differ significantly between the transgenic line and the wild type. In response to drought, leaf area was reduced, with a clear dose effect that was also reported for all size-related traits, including endoreduplication. Conclusions: These results provide evidence that all leaflets have the same cellular phenotypes as the leaf they belong to. Consistent with results reported for simple leaves, they show that cell number rather than cell size determines the final leaf areas and that endoreduplication can be uncoupled from leaf and cell sizes. Finally, they re-question a whole-plant control of cell division and expansion in leaves when the Wva106 and the Pro35S:Slccs52AAS lines are compared.

Putting primary metabolism into perspective to obtain better fruits.

Background: One of the key goals of fruit biology is to understand the factors that influence fruit growth and quality, ultimately with a view to manipulating them for improvement of fruit traits. Scope: Primary metabolism, which is not only essential for growth but is also a major component of fruit quality, is an obvious target for improvement. However, metabolism is a moving target that undergoes marked changes throughout fruit growth and ripening. Conclusions: Agricultural practice and breeding have successfully improved fruit metabolic traits, but both face the complexity of the interplay between development, metabolism and the environment. Thus, more fundamental knowledge is needed to identify further strategies for the manipulation of fruit metabolism. Nearly two decades of post-genomics approaches involving transcriptomics, proteomics and/or metabolomics have generated a lot of information about the behaviour of fruit metabolic networks. Today, the emergence of modelling tools is providing the opportunity to turn this information into a mechanistic understanding of fruits, and ultimately to design better fruits. Since high-quality data are a key requirement in modelling, a range of must-have parameters and variables is proposed.

Flip-flop method: A new T1-weighted flow-MRI for plants studies.

The climate warming implies an increase of stress of plants (drought and torrential rainfall). The understanding of plant behavior, in this context, takes a major importance and sap flow measurement in plants remains a key issue for plant understanding. Magnetic Resonance Imaging (MRI) which is well known to be a powerful tool to access water quantity can be used to measure moving water. We describe a novel flow-MRI method which takes advantage of inflow slice sensitivity. The method involves the slice selectivity in the context of multi slice spin echo sequence. Two sequences such as a given slice is consecutively inflow and outflow sensitive are performed, offering the possiblility to perform slow flow sensitive imaging in a quite straigthforward way. The method potential is demonstrated by imaging both a slow flow measurement on a test bench (as low as 10 µm.s-1) and the Poiseuille's profile of xylemian sap flow velocity in the xylematic tissues of a tomato plant stem.

Combined Effects of Irrigation Regime, Genotype, and Harvest Stage Determine Tomato Fruit Quality and Aptitude for Processing into Puree.

Industry tomatoes are produced under a range of climatic conditions and practices which significantly impact on main quality traits of harvested fruits. However, the quality of tomato intended for processing is currently addressed on delivery through color and Brix only, whereas other traits are overlooked. Very few works provided an integrated view of the management of tomato puree quality throughout the chain. To gain insights into pre- and post-harvest interactions, four genotypes, two water regimes, three maturity stages, and two processes were investigated. Field and glasshouse experiments were conducted near Avignon, France, from May to August 2016. Two irrigation regimes were applied: control plants were irrigated in order to match 100% of evapotranspiration (ETP); water deficit (WD) plants were irrigated as control plants until anthesis of the first flowers, then irrigation was reduced to 60 and 50% ETP in field, and glasshouse respectively. Fruits were collected at three stages during ripening. Their color, fresh weight, dry matter content, and metabolite contents were determined before processing. Pericarp cell size was evaluated in glasshouse only. Two laboratory-scaled processing methods were applied before structural and biochemical analyses of the purees. Results outlined interactive effects between crop and process management. WD hardly reduced yield, but increased dry matter content in the field, in contrast to the glasshouse. The puree viscosity strongly depended on the genotype and the maturity stage, but it was disconnected from fruit dry matter content or Brix. The process impact on puree viscosity strongly depended on water supply during fruit production. Moreover, the lycopene content of fresh fruit may influence puree viscosity. This work opens new perspectives for managing puree quality in the field showing that it was possible to reduce water supply without affecting yield and to improve puree quality.

Reduced susceptibility of tomato stem to the necrotrophic fungus Botrytis cinerea is associated with a specific adjustment of fructose content in the host sugar pool.

Background and aims: Plant soluble sugars, as main components of primary metabolism, are thought to be implicated in defence against pathogenic fungi. However, the function of sucrose and hexoses remains unclear. This study aimed to identify robust patterns in the dynamics of soluble sugars in sink tissues of tomato plants during the course of infection by the necrotrophic fungus Botrytis cinerea . Distinct roles for glucose and fructose in defence against B. cinerea were hypothesized. Methods: We examined sugar contents and defence hormonal markers in tomato stem tissues before and after infection by B. cinerea , in a range of abiotic environments created by various nitrogen and water supplies. Key Results: Limited nitrogen or water supplies increased tomato stem susceptibility to B. cinerea . Glucose and fructose contents of tissues surrounding infection sites evolved differently after inoculation. The fructose content never decreased after inoculation with B. cinerea , while that of glucose showed either positive or negative variation, depending on the abiotic environment. An increase in the relative fructose content (defined as the proportion of fructose in the soluble sugar pool) was observed in the absence of glucose accumulation and was associated with lower susceptibility. A lower expression of the salicylic acid marker PR1a , and a lower repression of a jasmonate marker COI1 were associated with reduced susceptibility. Accordingly, COI1 expression was positively correlated with the relative fructose contents 7 d after infection. Conclusions: Small variations of fructose content among the sugar pool are unlikely to affect intrinsic pathogen growth. Our results highlight distinct use of host glucose and fructose after infection by B. cinerea and suggest strongly that adjustment of the relative fructose content is required for enhanced plant defence.

Model-Assisted Estimation of the Genetic Variability in Physiological Parameters Related to Tomato Fruit Growth under Contrasted Water Conditions.

Drought stress is a major abiotic stress threatening plant and crop productivity. In case of fleshy fruits, understanding mechanisms governing water and carbon accumulations and identifying genes, QTLs and phenotypes, that will enable trade-offs between fruit growth and quality under Water Deficit (WD) condition is a crucial challenge for breeders and growers. In the present work, 117 recombinant inbred lines of a population of Solanum lycopersicum were phenotyped under control and WD conditions. Plant water status, fruit growth and composition were measured and data were used to calibrate a process-based model describing water and carbon fluxes in a growing fruit as a function of plant and environment. Eight genotype-dependent model parameters were estimated using a multiobjective evolutionary algorithm in order to minimize the prediction errors of fruit dry and fresh mass throughout fruit development. WD increased the fruit dry matter content (up to 85%) and decreased its fresh weight (up to 60%), big fruit size genotypes being the most sensitive. The mean normalized root mean squared errors of the predictions ranged between 16-18% in the population. Variability in model genotypic parameters allowed us to explore diverse genetic strategies in response to WD. An interesting group of genotypes could be discriminated in which (i) the low loss of fresh mass under WD was associated with high active uptake of sugars and low value of the maximum cell wall extensibility, and (ii) the high dry matter content in control treatment (C) was associated with a slow decrease of mass flow. Using 501 SNP markers genotyped across the genome, a QTL analysis of model parameters allowed to detect three main QTLs related to xylem and phloem conductivities, on chromosomes 2, 4, and 8. The model was then applied to design ideotypes with high dry matter content in C condition and low fresh mass loss in WD condition. The ideotypes outperformed the RILs especially for large and medium fruit-size genotypes, by combining high pedicel conductance and high active uptake of sugars. Interestingly, five small fruit-size RILs were close to the selected ideotypes, and likely bear interesting traits and alleles for adaptation to WD.