Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints.

Nitrogen (N) and water are crucial in crop production but increasingly scarce environmental resources. Reducing their inputs can affect the whole plant-arthropod community including biocontrol agents. In a multitrophic system, we studied the interaction of the bottom-up effects of moderately reduced N concentration and/or water supply as well as the top-down effects of pests of different feeding guilds on plant nutritional quality (N and carbon concentration), direct defense (alkaloids and phenolics), and indirect defense (plant volatile organic compounds); on herbivore performance and host quality (N and carbon) to parasitoids and the latter's performance. Studied organisms were tomato plants, the sap feeders Macrosiphum euphorbiae and Bemisia tabaci, the leaf chewers Tuta absoluta and Spodoptera littoralis, and the parasitic wasps Aphelinus abdominalis and Necremnus tutae. Resource limitation affected plant quality, triggering bottom-up effects on herbivore and parasitoid performance, except for T. absoluta and N. tutae. Feeding guild had a major influence: bottom-up effects were stronger on sap feeders; N effects were stronger on sap feeders while water effects were stronger with leaf chewers (S. littoralis). Top-down effects of leaf chewer herbivory partly attenuated bottom-up effects and partly suppressed plant defenses. Bottom-up effects weakened when cascading up trophic levels. In summary, the interaction between plants, pests, and beneficial insects was modulated by abiotic factors, affecting insect performance. Simultaneous abiotic and biotic impact shaped plant biochemistry depending on the feeding guild: the biotic top-down effect of leaf chewer herbivory attenuated the bottom-up effects of plant nutrition and hence dominated the plant biochemical profile whereas in sap feeder infested leaves, it corresponded to the abiotic impact. This study highlights the plant's finely tuned regulatory system facilitating response prioritization. It offers perspectives on how smart manipulation of plant nutrient solutions might save resources while maintaining efficient biocontrol in crop production.

Nitrogen nutrition of tomato plant alters leafminer dietary intake dynamics.

The leafminer Tuta absoluta (Meyrick) is a major pest of the tomato crop and its development rate is known to decline when nitrogen availability for crop growth is limited. Because N limitation reduces plant primary metabolism but enhances secondary metabolism, one can infer that the slow larval development arises from lower leaf nutritive value and/or higher plant defence. As an attempt to study the first alternative, we examined the tomato-T. absoluta interaction in terms of resource supply by leaves and intake by larvae. Tomato plants were raised under controlled conditions on N-sufficient vs. N-limited complete nutrient solutions. Plants were kept healthy or artificially inoculated with larvae for seven days. Serial harvests were taken and the N, C, dry mass and water contents were determined in roots, stems and leaves. Leaf and mine areas were also measured and the N, C, dry mass and water surface densities were calculated in order to characterize the diet of the larvae. The infestation of a specific leaf lessened its local biomass by 8-26%, but this effect was undetectable at the whole plant scale. Infestation markedly increased resource density per unit leaf area (water, dry mass, C and N) suggesting that the insect induced changes in leaf composition. Nitrogen limitation lessened whole plant growth (by 50%) and infested leaflet growth (by 32-44%). It produced opposite effects on specific resource density per unit area, increasing that of dry mass and C while decreasing water and N. These changes were ineffective on insect mining activity, but slowed down larval development. Under N limitation, T. absoluta consumed less water and N but more dry mass and C. The resulting consequences were a 50-70% increase of C:N stoichiometry in their diet and the doubling of faeces excretion. The observed limitation of larval development is therefore consistent with a trophic explanation caused by low N and/or water intakes.

Tomato response traits to pathogenic Pseudomonas species: Does nitrogen limitation matter?

Induced chemical defence is a cost-efficient protective strategy, whereby plants induce the biosynthesis of defence-related compounds only in the case of pest attack. Plant responses that are pathogen specific lower the cost of defence, compared to constitutive defence. As nitrogen availability (N) in the root zone is one of the levers mediating the concentration of defence-related compounds in plants, we investigated its influence on response traits of tomato to two pathogenic bacteria, growing plants hydroponically at low or high N supply. Using two sets of plants for each level of N supply, we inoculated one leaf of one set of plants with Pseudomonas syringae, and inoculated the stem of other set of plants with Pseudomonas corrugata. Tomato response traits (growth, metabolites) were investigated one and twelve days after inoculation. In infected areas, P. syringae decreased carbohydrate concentrations whereas they were increased by P. corrugata. P. syringae mediated a redistribution of carbon within the phenylpropanoid pathway, regardless of N supply: phenolamides, especially caffeoylputrescine, were stimulated, impairing defence-related compounds such as chlorogenic acid. Inoculation of P. syringae produced strong and sustainable systemic responses. By contrast, inoculation of P. corrugata induced local and transient responses. The effects of pathogens on plant growth and leaf gas exchanges appeared to be independant of N supply. This work shows that the same genus of plant pathogens with different infection strategies can mediate contrasted plant responses.

Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod.

Omnivorous arthropods make dietary choices according to the environment in which they forage, mainly availability/quality of plant and/or prey resources. Such decisions and their subsequent impacts on life-history traits may be affected by the availability of nutrients and water to plants, that is, through bottom-up forces. By setting up arenas for feeding behavior observation as well as glasshouse cages for plant preference assessment, we studied effects of the presence of prey (Lepidoptera eggs) and nitrogen/water availability to host tomato plants on the foraging behavior and life-history traits in the omnivorous predator Macrolophus pygmaeus (Heteroptera: Miridae). In the absence of prey, the predator fed equally on the plants treated with various levels of nitrogen and water. In the presence of prey, however, the feeding rate on plants decreased when the plant received low water input. The feeding rate on prey was positively correlated with feeding rate on plants; that is, prey feeding increased with plant feeding when the plants received high water input. Moreover, plants receiving high water input attracted more M. pygmaeus adults compared with those receiving low water input. For M. pygmaeus fitness, the presence of prey enhanced its fertility and longevity, but the longevity decreased when plants received low compared with high water input. In conclusion, the omnivorous predator may be obliged to feed on plants to obtain water, and plant water status may be a limiting factor for the foraging behavior and fitness of the omnivorous predator.

Phenolic characterization and variability in leaves, stems and roots of Micro-Tom and patio tomatoes, in response to nitrogen limitation.

Phenolics are implicated in the defence strategies of many plant species rendering their concentration increase of putative practical interest in the field of crop protection. Little attention has been given to the nature, concentration and distribution of phenolics within vegetative organs of tomato (Solanum lycopersicum. L) as compared to fruits. In this study, we extensively characterized the phenolics in leaves, stems and roots of nine tomato cultivars using high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry (LC-MS(n)) and assessed the impact of low nitrogen (LN) availability on their accumulation. Thirty-one phenolics from the four sub-classes, hydroxycinnamoyl esters, flavonoids, anthocyanins and phenolamides were identified, five of which had not previously been reported in these tomato organs. A higher diversity and concentration of phenolics was found in leaves than in stems and roots. The qualitative distribution of these compounds between plant organs was similar for the nine cultivars with the exception of Micro-Tom because of its significantly higher phenolic concentrations in leaves and stems as compared to roots. With few exceptions, the influence of the LN treatment on the three organs of all cultivars was to increase the concentrations of hydroxycinnamoyl esters, flavonoids and anthocyanins and to decrease those of phenolamides. This impact of LN was greater in roots than in leaves and stems. Nitrogen nutrition thus appears as a means of modulating the concentration and composition of organ phenolics and their distribution within the whole plant.

Is the C:N ratio a reliable indicator of C allocation to primary and defence-related metabolisms in tomato?

Plant growth and defence are both fuelled by compounds synthesized from a common pool of carbon and nitrogen, implying the existence of a competition for carbon and nitrogen allocation to both metabolisms. The ratio of carbon to nitrogen (C:N) of an organ is often regarded as a convenient indicator of growth and quality. The purpose of this work was to assess whether or not it is possible to extend its use to characterize the trade-off between growth and defence processes. Therefore, we calculated C:N ratios in the pool of resources and in the total plant, and correlated them to the concentrations of diverse compounds of the primary and secondary metabolisms in young tomatoes. Plants were grown hydroponically at N availabilities either limiting (0.1 mM) or not (7 mM) for growth in two glasshouses maintained either under ambient or enriched (700 vpm) air CO(2). These conditions yielded a large array of C:N in fully developed leaves, developing leaves, stem and roots, sampled 27, 35 and 47 days after sowing. Growth parameters and tissue concentrations of primary metabolites (carbohydrates, starch), defence-related compounds (polyphenols, glycoalkaloids), lignin, nitrate, ammonium, C and N were analyzed. Net CO(2) exchange rate was also measured at the last sampling date. Low N limited plant growth more than photosynthesis. The C:N in the resource pool was far higher than the total C:N. Starch was the most responsive compound, attaining high concentration under high C:N, whereas lignin remained stable. Chlorogenic acid, rutin, kaempferol-rutinoside and tomatine concentrations correlated positively to C:N. The same patterns were observed for most organs and molecules, except soluble carbohydrates in fully developed leaves whose concentration was not influenced. Among the organs, developing leaves showed the highest concentrations of secondary compounds and were the most responsive to C:N variations. Neither the biochemical nature of the compounds (C-based or N- containing metabolites) nor the calculation mode of C:N, influenced the patterns observed. Within the range of N availabilities considered (up to N limitation but not deficiency), the C:N can be considered as a good indicator of the secondary compounds concentrations in organs, especially for those involved in the chemical defence.

Totomatix: a novel automatic set-up to control diurnal, diel and long-term plant nitrate nutrition.

BACKGROUND: Stand-alone nutritional set-ups are useful tools to grow plants at defined nutrient availabilities and to measure nutrient uptake rates continuously, in particular that for nitrate. Their use is essential when the measurements are meant to cover long time periods. These complex systems have, however, important drawbacks, including poor long-term reliability and low precision at high nitrate concentration. This explains why the information dealing with diel dynamics of nitrate uptake rate is scarce and concerns mainly young plants grown at low nitrate concentration. SCOPE: The novel system detailed in this paper has been developed to allow versatile use in growth rooms, greenhouses or open fields at nitrate concentrations ranging from a few micro- to several millimoles per litres. The system controls, at set frequencies, the solution nitrate concentration, pH and volumes. Nitrate concentration is measured by spectral deconvolution of UV spectra. The main advantages of the set-up are its low maintenance (weekly basis), an ability to diagnose interference or erroneous analyses and high precision of nitrate concentration measurements (0·025 % at 3 mm). The paper details the precision of diurnal nitrate uptake rate measurements, which reveals sensitivity to solution volume at low nitrate concentration, whereas at high concentration, it is mostly sensitive to the precision of volume estimates. CONCLUSIONS: This novel set-up allows us to measure and characterize the dynamics of plant nitrate nutrition at high temporal resolution (minutes to hours) over long-term experiments (up to 1 year). It is reliable and also offers a novel method to regulate up to seven N treatments by adjusting the daily uptake of test plants relative to controls, in variable environments such as open fields and glasshouses.

The 'trade-off' between synthesis of primary and secondary compounds in young tomato leaves is altered by nitrate nutrition: experimental evidence and model consistency.

Plants allocate internal resources to fulfil essential, yet possibly conflicting, demands such as defence or growth, as hypothesized by the 'growth-differentiation balance theory' (GDB). This trade-off was examined in young tomato plants grown for 25 d using the nutrient film technique with seven nitrate concentrations ([NO(3)]). The modification of primary (growth-related: organic acids, carbohydrates) and secondary (defence-related: phenolics) metabolite concentrations in leaves was assessed. Then a simple model was devised to simulate the trade-off between growth and secondary metabolism in response to N nutrition. N affected growth and metabolite concentrations in the leaves. Dry biomass, leaf area, and concentrations of nitrate and organic acid (malic, citric) increased with rising [NO(3)], up to a threshold, above which they remained constant. Starch, sucrose, and organic N concentrations were invariant with [NO(3)]. Glucose, fructose, and phenolic (chlorogenic acid, rutin, and kaempferol-rutinoside) concentrations were highest at lowest [NO(3)]. They declined progressively with rising [NO(3)] until a threshold, above which they remained constant. Model predictions are in phase with experimental phenolic concentration data although the simulated metabolic rates differ from the GDBH proposals depicted in the literature. From the model output it is shown that a careful definition of the C reserve compounds is required.

Diel changes in nitrogen and carbon resource status and use for growth in young plants of tomato (Solanum lycopersicum).

BACKGROUND AND AIMS: Modellers often define growth as the development of plant structures from endogenous resources, thus making a distinction between structural (W(S)) and total (W) dry biomass, the latter being the sum of W(S) and the weight of storage compounds. In this study, short-term C and N reserves were characterized experimentally (forms, organ distribution, time changes) in relation to light and nutrition signals, and organ structural growth in response to reserve levels was evaluated. METHODS: Tomato plants (Solanum lycopersicum) were grown hydroponically in a growth room with a 12-h photoperiod and an adequate supply of NO(3)(-) (3 mol m(-3)). Three experiments were carried out 18 d after sowing: [NO(3)(-)] was either maintained at 3 mol m(-3), changed to 0.02 mol m(-3) or to 0 mol m(-3). Plants were sampled periodically throughout the light/dark cycles over 24-48 h. Organ W(S) was calculated from W together with the amount of different compounds that act as C and N resources, i.e. non-structural carbohydrates and carboxylates, nitrate and free amino acids. KEY RESULTS: With adequate nutrition, carbohydrates accumulated in leaves during light periods, when photosynthesis exceeded growth needs, but decreased at night when these sugars are the main source of C for growth. At the end of the night, carbohydrates were still high enough to fuel full-rate growth, as W(S) increased at a near constant rate throughout the light/dark cycle. When nitrate levels were restricted, C reserves increased, but [NO(3)(-)] decreased progressively in stems, which contain most of the plant N reserves, and rapidly in leaves and roots. This resulted in a rapid restriction of structural growth. CONCLUSIONS: Periodic darkness did not restrict growth because sufficient carbohydrate reserves accumulated during the light period. Structural growth, however, was very responsive to NO(3)(-) nutrition, because N reserves were mostly located in stems, which have limited nitrate reduction capacity.

Altering young tomato plant growth by nitrate and CO2 preserves the proportionate relation linking long-term organic-nitrogen accumulation to intercepted radiation.

* A previously published model of crop nitrogen (N) status based on intercepted photosynthetically active radiation (R(i), mol per plant) suggested that plant organic N accumulation is related to R(i) by a constant ratio, defined hereafter as the radiation use efficiency for N (NRUE). The aim of this paper was to compare the effects of N nutrition and CO2 enrichment on NRUE and RUE (radiation use efficiency for biomass accumulation). * In three unrelated glasshouse experiments, tomato plants (Solanum lycopersicum) grown in hydroponics were fed for 28 d (exponential growth) with full solutions containing constant NO3(-) concentrations ([NO3(-)]) ranging from 0.05 to 15 mol m(-3), both under ambient or CO2-enriched (1000 microl l(-1)) air. * Each experiment comprised five harvests. Low [NO3(-)] (< 0.3 mol m(-3)) limited growth via leaf area (LA) restriction and decreased light interception. CO2 enrichment enhanced dry weight and LA. RUE was not affected by [NO3(-)], but increased under CO2-enriched air. By contrast, NRUE was not affected by [NO3(-)] or CO2 enrichment. * It is suggested that the radiation efficiency for organic N acquisition (NRUE) did not depend on C or N nutrition for young plants grown under unstressed conditions.