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Journal of Food Quality
Volume 2019, Article ID 3598172, 15 pages
https://doi.org/10.1155/2019/3598172
Research Article

Effects of Root Cooling on Plant Growth and Fruit Quality of Cocktail Tomato during Two Consecutive Seasons

1Forschungszentrum Jülich, IBG-2: Plant Science, Wilhelm-Johnen-Straße, 52428 Jülich, Germany
2Forschungszentrum Jülich, IBG-3: Agrosphere, Wilhelm-Johnen-Straße, 52428 Jülich, Germany
3University of Bonn, Faculty of Agriculture, Campus Klein-Altendorf 1, 53359 Rheinbach, Germany
4Osnabrück University of Applied Sciences, Faculty of Agricultural Sciences and Landscape Architecture, Albrechtstr. 30, 49076 Osnabrück, Germany

Correspondence should be addressed to F. He; ed.hcileuj-zf@eh.f

Received 19 July 2019; Accepted 5 September 2019; Published 25 September 2019

Guest Editor: Urszula Złotek

Copyright © 2019 F. He et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Understanding the effects of root temperature on plant growth and key food components of horticultural crops under greenhouse conditions is important. Here, we assess the impact of root cooling on plant growth and fruit quality of two cocktail tomato cultivars (Lycopersicon esculentum cv “Amoroso” and cv “Delioso”) during the winter of 2017-2018 and the summer of 2018. Plants were grown hydroponically on rockwool under different root temperatures (16–27°C and 10°C) from the 2nd inflorescence to harvest inside the greenhouse. A root temperature of 10°C was controlled independently from air temperature (18–23°C in winter and 21–29°C in summer) by circulating cooling water. Reductions of marketable yield per plant (7.9–20.9%) in both cultivars were observed in response to root cooling in winter, but not significantly in summer. In most cases, root cooling had a positive effect on the functional quality (sugars, vitamin C, and carotenoids levels). In the case of “Delioso,” glucose concentration increased by 7.7–10.3%, vitamin C by 20–21%, and lycopene by 16.9–20.5% in both seasons. “Amoroso” exhibited only higher consistent values in glucose with increments between 6.9 and 7.8% in the two seasons. The levels of elements decreased by root cooling, with statistically significant reduction of N, P, S, and Fe by 12.1–15.7% in “Delioso” in winter and P and Zn by 9.1–22.2% in both cultivars in summer. Thus, manipulation of root temperature could be a feasible method to improve the overall fruit quality of cocktail tomato; however, this effect was also dependent on cultivars and other environmental factors.

1. Introduction

Tomato (Lycopersicon esculentum Mill.) is an important horticultural crop worldwide with increasing area of production, reaching 4.8 million hectares with an average of 37.6 tonnes/hectares and an overall production of more than 18 million tonnes, respectively, in 2017 [1]. Health promoting effects as well as potential risk of tomatoes and tomato-based product consumption for humans are well known and have been reviewed by Salehi et al. [2]. Hence, the protective action is typically assigned to significant levels of antioxidants such as vitamin C [3], lycopene [4], or carotenoids [5]. Cocktail tomatoes with an average weight of 20–50 g are perceived as tastier by consumers [6], and because of the suitable size they are getting more popular among consumers. Cocktail tomatoes are proven to contain higher levels of sugars, carotenoids, and other antioxidants than normal sized ones [7] because of its higher skin-to-volume ratio [8].

Among the environmental factors, temperature plays a crucial role in the growth of tomato plants and development of fruits. At suboptimal air temperature for the vegetative stage, tomato seedlings tend to produce larger cells to store more starch, indicating thicker leaves and relative lower growth rate [9]. Even short periods of low temperatures could induce blossom-end scarring of fruits, making them sensitive to bruising and serve as possible entrance for postharvest diseases [10]. During flower development stage, cooler air temperature induced an increase in the number of flowers, late ripeness, and eventually larger fruits [11, 12]. The optimal air temperature for fruit setting is 18–20°C, and a temperature higher than 30°C causes fruit cracking and blotchy ripening [13]. During fruit development stages, accumulation of carotenoids is promoted above 10°C, but inhibited above 30°C air temperature [14, 15].

Besides air temperature, root temperature has long been recognized as an important factor for the growth of the tomato plant. Originating from tropical regions, the cultivated tomato, Lycopersicon esculentum, is vulnerable to low root temperature [16, 17]. The mechanisms of root temperature on the growth of tomato plants are the results of both direct and indirect processes. Root growth, nutrient, and water uptake are directly influenced, whereas stomatal conductance, leaf expansion, photosynthesis, hormone synthesis, and distribution are indirectly related [1823]. Cooper [24] described the general response curve of all species to root temperature as a downward parabola, with optimal root temperature for tomato being between 25 and 30°C. Tomato plants at different growth stages have different root temperature preferences: 20–30°C for vegetative growth [25, 26], 25–30°C during flower differentiation, and 15–30°C during fruit development [26]. Root temperature also influences the distribution of carbohydrates between shoot and root by modifying the sink strength of root [2729]. The shoot-to-root ratio of tomato is positively correlated with root temperature [30].

The overall flavor of tomato is largely determined by the concentration of sugars and acids [31]. Many studies have proved that root temperature influenced the sugar concentrations of different plant organs. For example, lower root temperature induced higher concentration of sugars in the leaves of red leaf lettuce [32] and spinach [33]. Carotenoids of tomato are an important source for human nutrition due to high frequency in the diet [34]. A number of environmental factors, such as light intensity, CO2 levels, salinity, and temperature, are known to influence the levels of carotenoids in tomato [15, 34]. Lower root temperature was also demonstrated recently to enhance the accumulation of carotenoids, such as β-carotene, in hydroponically grown carrots [35]. Ascorbic acid (vitamin C) is another important antioxidant of tomato fruits. One-week application of 5°C root temperature to the root of spinach enriched the levels of ascorbic acids in the leaves [33]. Tomato fruits also supply essential elements for human health, such as K, Ca, P, and Mg [36]. Root temperature has been shown to alter the uptake and translocation of minerals to different parts of plant, such as K and P of maize [37]; Ca, Mg, P, K, Fe, and Mn of African snake tomato [38]; Fe of spinach [33]; K, N, P, Ca, and Mg of young tomato plants [22]. Thus, proper manipulation of root temperature could improve the taste and health components, leading to increased crop market value.

Maintaining the root temperature in the optimal range has been used an energy-efficient method to alleviate injury caused by suboptimal air temperature [39]. Trudel and Gosselin [40] and Gosselin and Trudel [41] reported that root temperatures lower than 16°C greatly reduced the yield of tomato, while warming the roots partially alleviate cool air temperature in the night by showing a rise in yield. Kawasaki et al. [22] also observed that root heating at low air temperature increased the root growth and total yield of tomato. Around 25°C root temperature increased photosynthesis, stomatal conductance, and shoot growth at high air temperatures (40°C day/23°C night) [42]. Furthermore, roots growth and nutrient uptake of young tomato plants were enhanced by root cooling at higher air temperatures by production of auxin [21]. However, little is known about the effect of excessive root cooling on plant growth and especially, fruit quality of tomato.

It has been shown that manipulation of water stress at the late stages of plant development improved the overall fruit quality without reducing yield [43, 44]. In line with the findings under water stress, application of root cooling after the 2nd anthesis only may, however, improve the fruit quality without decreasing the yield. We hypothesized that such conditions reduce root sink strength for photoassimilates and therefore favor the translocation of carbohydrates to the growing fruits. In addition, antioxidants, e.g., ascorbic acid and carotenoids, may be increased under suboptimal root temperature stress. Concentrations of ions are unaffected or enhanced after long-term adaptation to low root temperature by increasing the capacity for uptake and translocation [45]. To test this hypothesis in cocktail tomato, a soilless culture (rockwool) was carried out in the two seasons (2017-2018 winter and 2018 summer). At the start of the 2nd flowering, two root temperature treatments were applied: 10°C and control. Plant and fruit growth, the concentrations of carbohydrates (glucose, fructose, and sucrose), organic acids (malic acid, citric acid, and ascorbic acid), carotenoids (lycopene and β-carotene), and elements (macro and micro) were measured after harvest.

2. Materials and Methods

2.1. Plant Material and Growth Conditions

Cocktail tomato cv “Delioso” and cv “Amoroso” were provided from Rijk Zwaan breeding company (The Netherlands). Seeds were sown on 11th October 2017 and 10th April 2018 into rockwool plugs (25 × 25 × 40 mm with a 6/16 mm hole, Grodan Vital, Roermond, The Netherlands), which were previously submerged in distilled water for one hour. All the plugs with seeds were put in the tray and covered with a lid to prevent light, and the temperature was kept at 25°C. At 3-4 DAS (days after sowing), the seeds were germinated, and the lid was removed. After the 1st true leaf was developed (around 15 DAS), seedlings were transferred to rockwool cubes (100 × 100 × 65 mm, Grodan Vital, Roermond, The Netherlands) and fertilized with half-strength Hoagland solution (mg/L): N (105.0), Ca (100.2), K (117.3), Mg (24.6), S (32.0), P (15.5), Fe (0.5), Mn (0.55), Cu (0.064), Zn (0.065), B (0.54), and Mo (0.048) with EC 1.2 dS/m and pH 6.0. When the roots reached the bottom of the cubes (38–44 DAS), about 3 to 4 true leaves, the seedlings were placed on the top of the rockwool slabs (1000 × 200 × 75 mm; Grodan Vital, Roermond, The Netherlands). The composition of the nutrient solution was changed as follows (mg/L): N (120.6), Ca (108.3), K (180.6), Mg (28.8), S (70.5), P (23.8), Mn (0.27), Zn (0.16), B (0.04), Cu (0.025), Mo (0.023), and Fe (0.419) with pH around 5.8 and EC 2.8 dS/m. The nutrient solution was supplied automatically every hour from 6.00 until 19.00, and the total amount was 2–4 L per day per plant in order to keep 30–40% efflux and reduce salt accumulation [46]. Plants of both seasons were trained to one stem high-wire system. In both seasons, plants were grown at a density of 2.5 m2 (0.5 m between and 0.5 m within-row). Side shoots were pruned regularly, and leaves were removed once they were below the cluster that was picked. All the plants were topped, leaving two leaves above the 7th cluster. Flowers at anthesis were vibrated by electronic toothbrush to stimulate pollination. Six supplementary high pressure discharge lamps (720 μmol/s) (MGR-K400, DH LICHT, Germany) were open 16 h from 6.00 to 22.00 in the two seasons to compensate low daily PARs. Daily maximum air temperature and irradiation were continuously measured and recorded during both seasons by the climate sensor in the middle of the greenhouse.

2.2. Experimental Design and Root Temperature Management

In both seasons, two cultivars were randomly located on 14 slabs in two rows, with 2 plants in each slab. Considering the border effect, four plants in the corner of two rows were excluded from measurement. There were two treatments, control and roots treated at 10°C root temperature. Cooling mats (Clina Heiz und Kühlelemente GmbH, Germany) circulated with cooled distilled water from thermostat (Julabo, Germany) were placed on the top and bottom of slabs. Thermal insulation mats were wrapped outside the cooling mats to reduce heat transfer between rockwool and ambient air. The temperature of thermostat was set at 10°C and ten temperature loggers (developed by IBG-2, Forschungszentrum Jülich) were placed in the middle of slabs to record root-zone temperature, six in the cooling group and four in the control group. After the appearance of the 2nd inflorescences on 3rd January (84 DAS) and 6th June 2018 (62 DAS), 10°C root temperature was applied until the final harvest.

2.3. Harvest and Sample Preparation

Harvest of fruits was done between 28th February and 6th April and 20th July and 29th August 2018. After starting the treatment after the 2nd inflorescence, only the fruits from the 2nd to 5th cluster were harvested. Each cluster was separated into three parts, proximal, medium, and distal, based on the distance to the stem. Each part was harvested when the fruits of this part became red and ripe. Total yield per plant was the combination of the mass of all the fruits from the 2nd to 5th cluster per plant. Marketable yield was the combination of the mass of all healthy, red and ripe fruits above 20 g for “Amoroso,” while for “Delioso,” the minimum weight was 25 g. Mean fruit weight was approximated by dividing total yield by total number of fruits per plant. After the fruits of the 7th cluster were harvested, plant shoot length was also measured. Diameter at the base and internode between every two clusters was measured and averaged. After harvest, equatorial and longitudinal diameter (mm) and fresh weight (g) of the fruits were measured.

Two randomly selected red and ripe fruits from each part of two clusters (the 2nd and 3rd) were used for further biochemical analysis. Two fruits were quartered and the seeds and locular tissue were removed. Two quarters from each fruit were pooled and quickly frozen in liquid nitrogen. The other two diagonal quarters were also pooled and were dried at 65°C for 48 hrs until constant weight. The frozen samples were ground in a kitchen coffee bean grinder (Clatronic International GmbH, Germany) with liquid nitrogen and then stored at −80°C. The dried samples were ground in mixer mill (MM400, Retsch, Germany).

2.4. Sugar Quantification

Sugar concentrations were determined by enzymatic analysis according to Viola and Davies [47], with minor adjustments. To 50 mg of frozen samples 400 μl 80% (v/v) ethanol was added, incubated at 80°C for 15 min and centrifuged for 3 min. Supernatant was saved and 400 μl 50% (v/v) ethanol was added to the pellet and re-extracted using the same method. This was repeated again three times using 200 μl 80% (v/v) ethanol. All supernatants were pooled together, and ethanol was added to give 2 ml.

To determine the sugar concentrations, 20 μl aliquots were pipetted into 96-well plates and mixed with 160 μl enzyme mixture containing activated 1.12 units glucose-6-phosphate dehydrogenase (Roche diagnostics, Switzerland), 0.25 μmol NADP (Roche diagnostics, Switzerland), 0.5 μmol ATP (Merck, Germany), and 0.75 μmol Mg2+ and measured at 340 mm by using a microplate reader (Synergy™ 2 Multi-Mode, BioTek, USA) at room temperature. When the extinction curve reached the plateau, 3.6 units hexokinase (Roche diagnostics, Switzerland) was added. The same step was repeated until 1 unit phosphoglucose isomerase (Roche diagnostics, Switzerland) and 20 units invertase (Roche diagnostics, Switzerland) were successively added. Quantification of glucose, fructose, and sucrose were determined photometrically by calculating absorbance increase in each stage, which was proportional to the sugar content in each well. Each sample was extracted and analyzed in duplicate. Extract concentrations were converted into mg/g fresh weight and averaged.

2.5. Determination of Carotenoids

Carotenoids were consecutively extracted by using acetone and ethyl acetate and analyzed by high-performance liquid Chromatography (HPLC). Approximately 25 mg well-ground samples were weighed in 1.5 ml Eppendorf tubes and mixed with 1200 μl precooled acetone (VWR, USA). After centrifuging at 13,200 rpm for 15 min, the supernatant was carefully filtered through a 0.2 μm syringe filters (Sigma-Aldrich, USA). The filtered solvent was divided into two 1.5 ml Eppendorf tubes to which 500 μl water and 300 μl ethyl acetate were added. The mixture was then vortexed for 10 sec and centrifuged for 15 min at 13,200 rpm. Two ethyl acetate phases were combined and transferred to the amber vials for HPLC analysis.

Carotenoids were quantified by HPLC-PDA. Analyses were carried out on an Agilent 1220 Infinity II system (binary pump, autosampler, and column oven) coupled to an Agilent photodiode array (PDA) detector (Agilent Technologies, USA). 20 μl standard and sample extract, respectively, was injected in the HPLC system. The carotenoids were separated on a ProntoSIL 200-3-C30 column (250 × 4.6 mm; 3 μm particle size) and a corresponding guard column (10 × 4.0 mm; 3 μm particle size) from Bischoff (Leonberg, Germany). The mobile phase consisted of methanol/water (99.3 : 0.7, v/v) containing 1 mM ammonium acetate (A) and tert-butyl methyl ether (B). Samples were separated at room temperature and a flow rate of 500 μl/min using a gradient program as follows: 85% A, linear gradient to 70% A over 12 min, isocratic at 70% A for 6 min, linear gradient to 15% A over 5 min, and isocratic at 15% A for 5 min. Then the system was returned to its initial condition (85% A) within 5 min and was equilibrated for 5 min before the next run was started (total run time: 55 min). The PDA detector was operated at wavelengths of 475 nm and 450 nm for lycopene and β-carotene, respectively. Quantification was done by external calibration with corresponding standards (DHI, Denmark). The concentrations were converted into μg/g fresh weight and averaged.

2.6. Analysis of Organic Acid

Due to the similarity of structure and characteristics, three organic acids: citric acid, malic acid, and ascorbic acid (vitamin C) were extracted and analyzed simultaneously by liquid chromatography-mass spectrometry (LC-MS). Considering the matrix effect and high susceptibility of ascorbic acid to degrade, internal standard calibration 13C4 malic acid was chosen. 13C4 malic acid (Sigma-Aldrich, USA) was considered due to the similarity of chemical structure with other organic acids. 1200 μl extraction solvent containing 50 mg/l 1,4 dithiothreitol, and 50 mM ammonium acetate was added to approximately 20 mg sample along with internal standard 13C4 malic acid to determine extraction efficiency. The sample was then homogenized at 4°C for 15 min and centrifuged at 4°C for another 15 min at 13,200 rpm. The supernatant was then filtered through a 0.2 μm filter and diluted to the appropriate concentrations.

Quantification of organic acids was carried out using a Waters ACQUITY® UHPLC system (binary pump and autosampler) coupled to a Waters Xevo TQ-S® triple-quadrupole mass spectrometer (Waters Technologies Corp., MA, USA). Separation of three organic acids was achieved on a Nucleodur C18 Gravity-SB column (150 × 3 mm, 3 μm; Macherey-Nagel, Germany). The column was equipped with a precolumn (Macherey-Nagel, Germany). The mobile phase was water (A) and acetonitrile (B) each containing 0.1% formic acid, at a flow rate of 0.6 ml/min. The gradient program was as follows: 100% A isocratic for 4 min, to 97.5% A within 0.1 min, 97.5% A isocratic for 3.2 min, back to 100% A within 0.2 min and holding for 2.5 min. The electrospray ionization (ESI) interface of the mass spectrometer was driven in the negative mode. The capillary voltage was set to 2.5 kV. The desolvation temperature and source temperature was 600°C and 150°C, respectively. The desolvation gas flow was set to 1000 l/h, and the cone gas flow was set at 150 l/h using nitrogen in both cases. Mass spectrometric detection in the MRM mode was applied for quantification of the organic acids (Table 1). Nitrogen was used as the collision gas at a flow of 0.15 ml/min.

Table 1: MRM parameters for organic acids.

The concentration of each organic acid was determined by internal calibration using standard solutions composed of pure standard compounds (Sigma-Aldrich, USA). Each sample was extracted and analyzed in duplicate. Extract concentrations were converted into mg/g fresh weight and averaged.

2.7. Determination of Carbon, Nitrogen, Sulfur, and Other Elements

The ground dried sample was mixed with HNO3, H2O2, and HF, integrated by microwave. Then ICP-OES (inductively coupled plasma with optical emission spectroscopy, Elan 6000, PerkinElmer, Sciex; Agilent 7500ce, Planitz) was adopted to analyze P, K, Ca, Mg, and Fe in the diluted sample solution. C and S concentrations of the sample were determined by infrared absorption (Leco CS 600) based on the amount of CO2 and SO2 after conversion in flowing oxygen by radiofrequency heating. For the analysis of N, the samples were heated in flowing helium gas in a graphite crucible by means of resistance heating (Leco TCH 600).

2.8. Statistical Analysis

All statistical analyses were performed by R studio (version 1.2.1335). Each plant was regarded as one biological replicate, the data from the 2nd and 3rd clusters and three positions within one cluster were averaged. Quality analysis data from each season and each cultivar subjected to student’s t-test were used. Experimental results were expressed as the mean ± standard deviation.

3. Results and Discussion

3.1. Greenhouse Microenvironment Parameters

In the winter of 2017-2018, the daily PPFD (photosynthetic photon flux density) and maximum air temperature inside the greenhouse ranged from 21.49 to 97.08 μmol/m2s and from 19.84 to 29.17°C, respectively (Figure 1). The values were higher in the summer of 2018, indicating 53.21 to 125.75 μmol/m2s and 23.49 to 39.01°C. Since the climate sensor was installed in the middle of the greenhouse, the PPFD values were below the actual values at plant level. The optimal range for tomato growth is 20–30 mol/m2d [48], and the requirements of plants were met with supplementary lighting and extended length.

Figure 1: Moving average of daily maximum air temperature (Air_max), photosynthetic photon flux density (PPFD) recorded inside the greenhouse from 11 October 2017 to 20 August 2018. The two seasons were indicated by arrows at the top of the graph. Root temperature treatment in the two seasons were indicated as gray, and root temperature from control group (open circles) and cooling group (open triangles) were recorded in the middle of rockwool from 1 January to 6 April and 6 June to 20 August 2018.

In summer, the number of days exceeding daily maximum air temperature 30°C was 70, which covered half of the growth period and were mostly during fruit development. The optimal daily temperature for fruit production is 19–20°C [49]. Air temperature above 32°C during the day caused reduction of pollen formation and viability [50, 51]. From this, it could be assumed that plant growth was affected by extreme high air temperature during summer in our experiment. Root temperature in our control group was also higher in summer (19.78–26.47°C) than in winter (16.91–23.87°C).

3.2. Influence of Root Cooling on Plant Growth and Fruit Yield

As indicated in Table 2, total yield and marketable yield per plant (the 2nd to 5th cluster) in both cultivars were reduced significantly at 10°C root temperature in the winter of 2017, but number, size, and fresh weight of single fruit were not reduced significantly by root cooling. Besides, “Delioso” showed greater magnitudes of reduction by 17.9% in total yield and 20.9% in marketable yield. This is in contrast to an experiment by Fujimura et al. [52], where not only the total yield of tomato was reduced at 12°C root temperature but also fruit size and fruit number, regardless of the season. Many other studies further confirm the assumption that low root temperature leads to a reduced shoot growth and is mainly attributed to water stress [53, 54]. Reduction in water uptake leads to the stomata closure in order to maintain positive turgor pressure within the plant. The resultant CO2 uptake and net photosynthetic rate became reduced, with eventual restriction of carbon production [55]. By contrast, Fujimura et al. [52] observed that the photosynthesis rate and stomatal conductance of tomato plant were not significantly affected by root chilling at 12°C and suggested that the tomato plants showed acclimation within one week. Yan et al. [56] and Zhang et al. [57] suggested that loss of root cell viability and membrane lipid peroxidation inhibited plant growth. In our studies, the reduction of water content in the fruits (Table 2) confirmed that the plants suffered from water stress induced by root cooling. But water stress is not the only reason; otherwise, the yield should be reduced even more in summer. Other studies attributed restriction of shoot growth under low root temperature to the imbalance between growth promoters and inhibitors, such as cytokines, abscisic acid, and gibberellins [20, 58], which are primarily synthesized in root apical meristems [59]. Additionally, secondary metabolites, induced by abiotic and biotic stress, consumed more energy because carbon distribution was diverted to the production of secondary metabolites, and this resulted in the reduction of plant growth and development as well as the yield [60, 61].

Table 2: Effects of root cooling on yield and fruit and shoot growth parameters of cocktail tomato plants in the two seasons.

In summer, the yield was not affected by root cooling, and “Amoroso” even showed an increase in total and marketable yield with more fruits (Table 2), though not significantly. Most of the daily maximum air temperatures during the fruit development stage were above 30°C in the summer of 2018 (Figure 1). These results are similar to those reported by Adams et al. [50] and Domínguez et al. [51], which mentioned that air temperature above 32°C caused a reduction of pollen formation and viability. Thus, fruits of the 4th and 5th cluster only developed one fruit on some of the plants, leading to a reduction of overall yield and number of fruits in the control group (data not shown). Again, in the daytime, the root temperature in the control group was around 27°C, with maximum up to 30°C (Figure 1). Díaz-Pérez et al. [62] mentioned that high root temperature above 27°C resulted in reduction of plant growth and fruit yield. The increase in total and marketable yield under low root temperature (Table 2) indicated that root cooling to some extent relieved heat stress from aboveground for “Amoroso” in our experiment. Similarly, the fruit number and weight of cucumber were increased with root-zone cooling at high ambient temperature [63]. Furthermore, Mohammud et al. [64] as well as Kii and Araki [65] also proved that water chilling through the root zone of tomato during summer could improve the fruit yield by increasing the fruit number and average fruit weight. The response of root cooling in our two seasons, experiments, and other environmental factors, such as light and air temperature interacting with root temperature influenced the final yield. These results are in accordance with other studies on the interaction of root zone and air temperature and given lighting conditions as recently reviewed by Kawasaki and Yoneda [39].

In winter, both cultivars did not have significant differences in the shoot length and average diameter as a result of root cooling, as shown in Table 1. The effect of root cooling was also dependent on the period of treatment. Wan et al. [55] observed a sharp reduction of water uptake and stomatal conductance at 24 hrs after 5°C root temperature treatment. Fennell and Markhart [66] reported acclimation of stomatal conductance in spinach after three days’ 5°C root temperature treatment. In our studies, growth of shoot might also show acclimation after two-three months’ treatments, and hence, no statistically significant differences were observed. However, in 2018 summer, plant growth presented greater changes with longer and slender shoot as a result of treatment. Because in summer, the root cooling treatment started early (62 DAS) than in winter (84 DAS), it was assumed that the differences were caused mainly in the early stages of treatment, during which the shoot height was below 30 cm.

3.3. Influence of Root Cooling on Bioactive Compounds

Glucose and fructose are the major sugars present in both walls and locular of mature tomato fruits, accounts for nearly half of the total dry matter of tomato fruits, hence influencing tomato fruit quality largely [31]. The levels of glucose and fructose in control group ranged from 17.6 to 20.7 mg/g FW and 13.9 to 18.9 mg/g FW. These values were consistent with other studies, reporting ranges from 6.8 to 17.9 g/kg FW in tomato of different sizes [67, 68]. The levels of sucrose in control samples (ranging from 0.25 to 1.92 mg/g FW) were higher compared with previous report where sucrose is less than 0.05% of fresh weight [69]. The low levels of sucrose could be due to degradation of sucrose to glucose after transportation from the phloem [70]. In winter, glucose and fructose levels were strongly influenced by root temperature (Table 3). The treatment showed higher values in glucose and fructose with increments of 7.8% and 7.4%, respectively “Amoroso.” The rise of glucose (10.3%) and fructose (13.3%) concentrations in “Delioso” at low root temperature were even stronger. However, this effect was not significant for sucrose concentration in both cultivars. Similarly, in the summer of 2018, glucose levels increased by 6.9% and 7.7% in “Amoroso” and “Delioso,” respectively. The levels of fructose showed an increase by root cooling as well, however, not significant (Table 3). Soluble sugars are important signaling molecules to regulate carbohydrates metabolism when plants are exposed to abiotic stress [71]. When exposed to low-temperature stress, soluble sugars have multiple roles, such as function as nutrients, as osmoprotectants to keep the turgor pressure, interacting with lipid layer to protect cellular membranes, as primary messengers in signal transduction, or as scavengers for hydroxyl radicals to mention some of the reported roles [7274]. Another explanation is that, the reduction in sink strength of roots when exposed to suboptimal temperature without down-regulation of net photosynthesis [75]. Water stress caused by low root temperature could also explain the increase in sugar concentrations which accompany a reduction in water. However, Fujimura et al. [52] denied this cause and attributed it to an excess of photoassimilates lead by the imbalance of sink and source capacity to suboptimal temperature.

Table 3: Effects of root cooling on sugar, organic acid, and carotenoid concentrations of cocktail tomato fruits.

Citric acid and malic acid are the major nonvolatile organic acids, responsible for the sourness in tomato fruits [76]. And the total organic acids were generally positively related to total acidity [77]. In line with previous studies, the levels of citric acid in control samples (ranging from 3.4 to 6.0 mg/g FW) were 4 to 5 times higher than those of malic acid (0.22–1.21 mg/g FW) [77, 78]. In the two seasons and two cultivars, the concentration of citric acid and malic acid did not exhibit differences as a result of root cooling. These findings were similar to the results of Fujimura et al. [52]; the concentration of malic acid and citric acid was not influenced by root cooling regardless of the cultivar or the season. Shaw [79] also confirmed that total acidity was less controlled by environmental factors than genetic traits. Both cultivars showed higher levels of malic acid (0.88–1.21 mg/g FW) and citric acid (4.17–6.00 mg/g FW) in winter, especially for the values of malic acid. In contrary, strawberries planted in summer contained higher levels of titratable acidity than in winter [80]. Lobit et al. [81] modeled the vacuolar malic acid concentration of peach fruit versus air temperature and observed a reduction of about 50% with an increase in air temperature from 15 to 20°C. Wang and Camp [82] also proved that the concentrations of organic acids in strawberry grown at high temperature were lower, probably due to higher respiration rate. Higher air temperature in 2018 summer might have led to lower organic acid concentrations in the fruits of our tomatoes.

In this study, two cultivars showed similar ascorbic acid concentration compared with other studies, which reported values ranging from 1.6 to 6.4 mg/g FW of cherry tomatoes harvested at different times of the year [83]. The ascorbic acid concentrations of the treated samples were 20-21% higher than that of the control (no root controlling) in “Delioso” in winter and summer. On the other hand, ascorbic acid in “Amoroso” only exhibited higher (8.7%) value in summer. As expected, vitamin C changed as a result of the cooling treatment, and the increment was mainly due to the protection mechanism from low temperature-induced oxidative stress [33]. Nonetheless, both cultivars contained slightly higher concentrations in summer than those harvested in winter, which is in accordance with Massot et al. [84] and Roselló et al. [85]. Seasonal variations in ascorbate levels have been attributed to gene expression of biosynthesis and recycling, regulated by the interaction of temperature and light during the season [86, 87].

Amongst the carotenoids, only lycopene and β-carotene were measured in our studies. Lycopene predominates 60–74% of the carotenoids and is responsible for the red color [88]. The lycopene values reported in the present study (ranging from 71.3 to 108.9 μg/g FW) were similar to early studies (ranging from 15 to 160 μg/g FW) depending on different cultivars, ripeness, environmental factor, agricultural practices and postharvest storage conditions [8992]. In both seasons, low root temperature caused 16.9–20.5% accumulation of lycopene in “Delioso,” but had no impact on “Amoroso.” Fruit temperature plays an essential role in the synthesis of lycopene, below 12°C or above 30°C during fruit stage, synthesis of lycopene was inhibited [34, 85]. The concentration of lycopene has been reported to be lower in the summer months than other times due to high air temperatures and excessive sunlight [93, 94]. Krumbein et al. [34] observed that the optimal air temperature range for lycopene accumulation was 20–24°C. In winter, air temperature was in the optimal range, and the main stress for plants was from root cooling. Consequently, “Delioso” behaved more sensitively to root cooling by increasing the concentration of lycopene. As mentioned earlier, daily maximum air temperature during fruit development in summer was above 30°C. Seasonal changes in lycopene levels have been attributed to both heat stress aboveground and cold stress belowground. In summer, “Delioso” increased the concentration of lycopene under lower root temperature; probably root cooling partially alleviated the negative impacts of heat stress. However, the effects for “Amoroso” were not obvious. Therefore, biosynthesis of lycopene was a result of comprehensive effect of air temperature, root-zone temperature, solar irradiation, and other climatic factors.

β-carotene, a precursor of vitamin A, is associated with the orange color in tomatoes [88]. The levels of β-carotene in control samples (ranging from 7.0 to 11.5 μg/g FW) were lower than those reported by other authors in the range of 9.8–16.7 mg/kg FW [15]. In winter, the levels of β-carotene with root cooling were 10% higher than the control group in “Amoroso,” while no differences were observed in “Delioso.” In summer, the levels of β-carotene did not show differences in both cultivars when exposed to root cooling, but with higher levels than winter. β-carotene concentration was positively related to light intensity and less affected by high air temperature up to 38°C [95]. Therefore, higher light intensity accounted for the increase of β-carotene levels in summer. Lycopene and β-carotene indicated different sensitivities, and the response was dependent on the genotypes, which were consistent with Roselló et al. [85] and Gautier et al. [90].

Low air temperature was known to cause stress for plants, which lead to down-regulation of Calvin cycle and accumulation of reactive oxygen species (ROS), such as 1O2, O2, H2O2, and ⋅OH [96, 97]. To counteract the deleterious oxidative damage of ROS, plants have to produce antioxidant enzymes and antioxidants [17], such as ascorbate and carotenoids, as defense systems. With the application of low air temperature, levels of sugars and antioxidants were increased in the spinach [98]; the concentration of vitamin C increased in strawberry [82]. Likewise, extreme root temperature stress also leads to the increased production of various metabolites in plants. In red romaine lettuce and red leaf lettuce, 10°C root temperature accelerated the accumulation of anthocyanin, phenols, and sugars than other temperatures [32, 99]. Cucumber seedlings had higher sugar concentrations at 12°C than 20°C root temperature [56]. In two medicinal plants, Catharanthus roseus and Nicotiana tabacum, the biosynthesis and accumulation of alkaloid were increased by altering root temperature during 48h root temperature treatment [100]. In agreement with previous studies, higher concentrations of glucose, fructose, ascorbic acid, lycopene, and β-carotene were observed as a function of root cooling in our experiments. The response of cultivar to root temperature was different, depending on the sensitivity to cooling and other environmental factors.

3.4. Influence of Root Cooling on Concentrations of Elements

Already Pollock and Eagles [101] reported that the effect of low temperature on carbon fixation and translocation is relatively mild, which was true in our case (Table 4). Concentration of carbon did not vary significantly with treatment in both seasons, except for “Amoroso” in the summer of 2018 with a reduction of 0.8%. It is commonly believed that carbon is accumulated in leaves in response to low root temperature. And this accumulation is attributed to reduced translocation rates and decreased sink demand by cold roots [102, 103]. By contrast, Wilson [104] and Hamblin et al. [105] observed an increased fraction of carbon to root under low temperature for the maintenance of construction and respiration; however, these changes seem to depend on species and types of cultivars. Carbon concentration in the fruit is the result of the balance between carbon partitioning and respiration. Carbon portioning between sink and source is also influenced by other environmental factors. The higher air temperature in summer complicated the carbon accumulation in fruits and may explain the inconsistent results of two seasons for “Amoroso.”

Table 4: Effects of root cooling on concentrations of elements of cocktail tomato fruits in two seasons.

The results indicated a large number of elements with reduced concentration in “Delioso” during winter, especially N, P, S, and Fe with varying reductions of 12.1%, 15.7%, 13.3%, and 15.4%, respectively (Table 4). However, all the nutrients were not affected by root temperature in “Amoroso” at the same time. In summer, both the levels of macro and micro elements in “Amoroso” showed a general reduction as a function of root cooling, but only P levels decreased by 15.0% and Zn values decreased by 22.2% significantly. In response to root cooling, “Delioso” showed statistical similarities in P and Zn concentrations by reduction of 9.1% and 13.7%, respectively, but Mg values increased by 11.1% in “Delioso.” Cooper [24] described tomato as one representative species in which the mineral concentrations increase with root temperature, achieve the highest at one point, and afterwards, concentrations decline. And this optimal point is around 25°C based on the different cultivars and light conditions [106]. Concentrations of ions in the fruits were influenced by root uptake, transport from root to shoot, and dilution effect caused by growth as well [107]. Considering the reduction in fresh biomass of fruits in our studies, the dilution effects by growth could be excluded.

In short-term, uptake of ions was severely affected by suboptimal root temperature which has been further proved in other species: grapevine [108], African snake tomato [38], spring barley [109], rice [110], and lettuce [111]. Altered root morphology under low root temperature was one reason [28, 102]. The mobility of cellular membrane phospholipids was lost induced by low root temperature below the phase transition point [112]. Thus, ion carrier proteins and enzymes function were hampered [113, 114]. Another factor was related to limited energy available for ion uptake caused by reduced root respiration with root chilling [32], which also, in turn, inhibited ion carriers’ function. Reduced root hydraulic conductivity, which regulates water and nutrient uptake, was another reason suggested by George et al. [115] and Lee et al. [116]. However, tomato plants of our studies were exposed to low root temperature for extended periods. White et al. [45] and Engels et al. [117] indicated that roots increased the capacity of ion uptake after long exposure to low root temperature. This acclimation is currently attributed to the adaptation of previously mentioned alterations caused by low root temperature, e.g., increased ion transporters in the plasma membrane, insensitive flux of ions into the xylem (reviewed by [118]), enhanced hydraulic conductivity [119], and increased shoot demand with growth. But, this adaption to low root temperature was not detected if the shoot base temperature was within the cooling zone [117]. In our setup, the isolation Matt covered and wrapped the shoot base; consequently, the base temperature was reduced as well. The uptake of N, P, K, S, Fe, and Zn did not demonstrate acclimation. On the contrary, the increased level of Mg in “Delioso” could be explained by the long-term adaption to root cooling.

The concentrations of nutrients in the fruits were also dependent on the translocation of minerals from root to shoot through xylem. The translocation rate was determined by complex processes: uptake rate of nutrients, retention of nutrients in root or for root growth, and transpiration rate [107]. Ca, P, and K in the leaf of snake gourd (Trichosanthes cucumerina L.) at suboptimal root temperature preferred to retain in the root than relocation to the shoot. Adebooye et al. [38] found that the partitioning of Fe and Mn was not influenced by root temperature. In the present study, the reduction of N, P, S, Fe, and Zn concentrations of fruits could also be explained by the lower translocation rate to fruits at low root temperature.

Other hypotheses also exist for the altered concentrations of minerals in shoots as a function of low root temperatures. Iron levels were observed to be higher in the leaf of spinach and rice at low root temperature, and the increment was attributed to the enhanced biosynthesis of isozymes such as Fe-SOD, Zn-SOD, and Mn-SOD [120, 121]. In our tomato fruits, the concentrations of Fe, Zn, and Mn were either decreased or unaffected. It was assumed that the increased amount caused by the isozymes may not compensate for the reduced amount by uptake or translocation.

4. Conclusions

In conclusion, our results confirmed that it is possible to improve the fruit quality of cocktail tomato by modifying root temperature in winter and summer. Cooling root had a beneficial effect on the accumulation of sugars, especially glucose, in both cultivars and both seasons, despite a reduction of yield in winter. Though root temperature differences between control and cooling treated group increased in summer, no reduction of yield was observed. Other than root temperature, the main differences between two seasons were the climatic conditions inside the greenhouse, which could explain the different impacts. Besides, the two cultivars behaved differently to root cooling. Root cooling improved the accumulation of vitamin C and lycopene in “Delioso” in both seasons, while only higher values of β-carotene in winter and vitamin C in summer were observed in “Amoroso.” Therefore, fruit quality can be improved as a result of application of root cooling during fruit growth and development, but the effects are also dependent on other climatic factors and cultivars.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

Many thanks go to Beate Uhlig, Katharina Wolter-Heinen, Thorsten Brehm, Esther Breuer, and Andrea Neuwohner for their generous support and excellent advice on technical in the greenhouse and lab work. The authors also gratefully appreciate the help of Felix Frimpong in revising and checking the grammar and languages.

References

  1. FAO, Global Tomato Production in 2017, FAO, Rome, Italy, 2019.
  2. B. Salehi, R. Sharifi-Rad, F. Sharopov et al., “Beneficial effects and potential risks of tomato consumption for human health: an overview,” Nutrition, vol. 62, pp. 201–208, 2019. View at Publisher · View at Google Scholar · View at Scopus
  3. R. G. Borguini and E. A. Ferraz da Silva Torres, “Tomatoes and tomato products as dietary sources of antioxidants,” Food Reviews International, vol. 25, no. 4, pp. 313–325, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. E. N. Story, R. E. Kopec, S. J. Schwartz, and G. K. Harris, “An update on the health effects of tomato lycopene,” Annual Review of Food Science and Technology, vol. 1, no. 1, pp. 189–210, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. C. O. Perera and G. M. Yen, “Functional properties of carotenoids in human health,” International Journal of Food Properties, vol. 10, no. 2, pp. 201–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Casals, A. Rivera, J. Sabaté, R. R. del Castillo, and J. Simó, “Cherry and fresh market tomatoes: differences in chemical, morphological, and sensory traits and their implications for consumer acceptance,” Agronomy, vol. 9, no. 1, 2019. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Leonardi, P. Ambrosino, F. Esposito, and V. Fogliano, “Antioxidative activity and carotenoid and tomatine contents in different typologies of fresh consumption tomatoes,” Journal of Agricultural and Food Chemistry, vol. 48, no. 10, pp. 4723–4727, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. A. J. Stewart, S. Bozonnet, W. Mullen, G. I. Jenkins, M. E. J. Lean, and A. Crozier, “Occurrence of flavonols in tomatoes and tomato-based products,” Journal of Agricultural and Food Chemistry, vol. 48, no. 7, pp. 2663–2669, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. J. H. Venema, B. E. Dijk, J. M. Bax, P. R. van Hasselt, and J. T. M. Elzenga, “Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habrochaites improves suboptimal-temperature tolerance,” Environmental and Experimental Botany, vol. 63, no. 1–3, pp. 359–367, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. H. M. Barten, J. W. Scott, N. Kedar, and Y. Elkind, “Low temperatures induce rough blossom-end scarring of tomato fruit during early flower development,” Journal of the American Society for Horticultural Science, vol. 117, no. 2, pp. 298–303, 1992. View at Publisher · View at Google Scholar
  11. I. Rylski, “Fruit set and development of seeded and seedless tomato fruits under diverse regimes of temperature and pollination,” Journal of American Society for Horticultural Science, vol. 104, no. 6, pp. 835–838, 1979. View at Google Scholar
  12. V. K. Sawhney and P. L. Polowick, “Fruit development in tomato: the role of temperature,” Canadian Journal of Botany, vol. 63, no. 6, pp. 1031–1034, 1985. View at Publisher · View at Google Scholar · View at Scopus
  13. A. N. M. de Koning, “Development and dry matter distribution in glasshouse tomato: a quantitative approach,” Wageningen Agricultural University, Wageningen, Netherlands, 1994, Ph.D. thesis. View at Google Scholar
  14. Y. Dumas, M. Dadomo, G. Di Lucca, and P. Grolier, “Effects of environmental factors and agricultural techniques on antioxidantcontent of tomatoes,” Journal of the Science of Food and Agriculture, vol. 83, no. 5, pp. 369–382, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Gautier, V. Diakou-Verdin, C. Bénard et al., “How does tomato quality (sugar, acid, and nutritional quality) vary with ripening stage, temperature, and irradiance?” Journal of Agricultural and Food Chemistry, vol. 56, no. 4, pp. 1241–1250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. A. J. Caris-Veyrat, M. A. Zwieniecki, J. B. Passioura, L. B. Randall, N. M. Holbrook, and D. A. S. Clair, “Water relations under root chilling in a sensitive and tolerant tomato species,” Plant, Cell and Environment, vol. 27, no. 8, pp. 971–979, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. He, J. Yang, B. Zhu, and Z.-J. Zhu, “Low root zone temperature exacerbates the ion imbalance and photosynthesis inhibition and induces antioxidant responses in tomato plants under salinity,” Journal of Integrative Agriculture, vol. 13, no. 1, pp. 89–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. S. V. Veselova, R. G. Farhutdinov, S. Y. Veselov, G. R. Kudoyarova, D. S. Veselov, and W. Hartung, “The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.),” Journal of Plant Physiology, vol. 162, no. 1, pp. 21–26, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Malcolm, P. Holford, B. McGlasson, and I. Barchia, “Leaf development, net assimilation and leaf nitrogen concentrations of five Prunus rootstocks in response to root temperature,” Scientia Horticulturae, vol. 115, no. 3, pp. 285–291, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Ntatsi, D. Savvas, U. Druege, and D. Schwarz, “Contribution of phytohormones in alleviating the impact of sub-optimal temperature stress on grafted tomato,” Scientia Horticulturae, vol. 149, pp. 28–38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Kawasaki, S. Matsuo, K. Suzuki, Y. Kanayama, and K. Kanahama, “Root-zone cooling at high air temperatures enhances physiological activities and internal structures of roots in young tomato plants,” Journal of the Japanese Society for Horticultural Science, vol. 82, no. 4, pp. 322–327, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Kawasaki, S. Matsuo, Y. Kanayama, and K. Kanahama, “Effect of root-zone heating on root growth and activity, nutrient uptake, and fruit yield of tomato at low air temperatures,” Journal of the Japanese Society for Horticultural Science, vol. 83, no. 4, pp. 295–301, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. J. A. Gonzalez-Fuentes, K. Shackel, J. Heinrich Lieth, F. Albornoz, A. Benavides-Mendoza, and R. Y. Evans, “Diurnal root zone temperature variations affect strawberry water relations, growth, and fruit quality,” Scientia Horticulturae, vol. 203, pp. 169–177, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. A. J. Cooper, Root Temperature and Plant Growth, Commonwealth Agricutural Bureaux, Farnham Royal, England, 1973.
  25. N. Fujishige and T. Sugiyama, “Effect of soil temperature on growth of seedlings of a few fruit vegetables (a preliminary report),” Engei Gakkai Zasshi, vol. 37, no. 3, pp. 221–226, 1968. View at Publisher · View at Google Scholar
  26. N. Fujishige, T. Sugiyama, and R. Ogata, “Effect of root temperature on the flower formation and fruit yield of tomatoes,” Engei Gakkai Zasshi, vol. 60, no. 1, pp. 97–103, 1991. View at Publisher · View at Google Scholar
  27. J. Hurewitz and H. W. Janes, “Effect of altering the root-zone temperature on growth, translocation, carbon exchange rate, and leaf starch accumulation in the tomato,” Plant Physiology, vol. 73, no. 1, pp. 46–50, 1983. View at Publisher · View at Google Scholar
  28. J. He, L. P. Tan, and S. K. Lee, “Root-zone temperature effects on photosynthesis, 14C-photoassimilate partitioning and growth of temperate lettuce (Lactuca sativa cv. ‘Panama') in the tropics,” Photosynthetica, vol. 47, no. 1, pp. 95–103, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. M. T. Islam, “Effect of temperature on photosynthesis, yield attributes and yield of tomato genotypes,” Journal of Experimental Agriculture International, vol. 2, no. 1, pp. 8–11, 2011. View at Google Scholar
  30. A. Gosselin and M. J. Trudel, “Influence de La temperature du substrat sur La croissance, le developpement et le contenu en elements mineraux de plants de tomate (cv. Vendor),” Canadian Journal of Plant Science, vol. 62, no. 3, pp. 751–757, 1982. View at Publisher · View at Google Scholar
  31. A. A. Kader, “Flavor quality of fruits and vegetables,” Journal of the Science of Food and Agriculture, vol. 88, no. 11, pp. 1863–1868, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Sakamoto and T. Suzuki, “Effect of root-zone temperature on growth and quality of hydroponically grown red leaf lettuce (Lactuca sativa L. cv. Red Wave),” American Journal of Plant Sciences, vol. 6, no. 14, pp. 2350–2360, 2015. View at Publisher · View at Google Scholar
  33. K. Hidaka, D. Yasutake, M. Kitano et al., “Production of high quality vegetable by applying low temperature stress to roots,” Acta Horticulturae, vol. 801, pp. 1431–1436, 2007. View at Google Scholar
  34. A. Krumbein, D. Schwarz, and H. P. Kläring, “Effects of environmental factors on carotenoid content in tomato (Lycopersicon esculentum (L.) Mill.) grown in a greenhouse,” Journal of Applied Botany and Food Quality, vol. 80, no. 2, pp. 160–164, 2006. View at Google Scholar
  35. M. Sakamoto and T. Suzuki, “Elevated root-zone temperature modulates growth and quality of hydroponically grown carrots,” Agricultural Sciences, vol. 6, no. 8, pp. 749–757, 2015. View at Publisher · View at Google Scholar
  36. A. R. Vicente, G. A. Manganaris, G. O. Sozzi, and C. H. Crisosto, “Nutritional quality of fruits and vegetables,” in Postharvest Handling, pp. 57–106, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Engels, “Differences between maize and wheat in growth-related nutrient demand and uptake of potassium and phosphorus at suboptimal root zone temperatures,” Plant and Soil, vol. 150, no. 1, pp. 129–138, 1993. View at Publisher · View at Google Scholar · View at Scopus
  38. O. C. Adebooye, M. Schmitz-Eiberger, C. Lankes, and G. J. Noga, “Inhibitory effects of sub-optimal root zone temperature on leaf bioactive components, photosystem II (PS II) and minerals uptake in Trichosanthes cucumerina L. Cucurbitaceae,” Acta Physiologiae Plantarum, vol. 32, no. 1, pp. 67–73, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Kawasaki and Y. Yoneda, “Local temperature control in greenhouse vegetable production,” The Horticulture Journal, vol. 88, no. 3, pp. 305–314, 2019. View at Publisher · View at Google Scholar
  40. M. J. Trudel and A. Gosselin, “Influence of soil temperature in greenhouse tomato production,” HortScience, vol. 17, no. 6, pp. 928-929, 1982. View at Google Scholar
  41. A. Gosselin and M. J. Trudel, “Effect of soil heating on plant productivity and energy conservation in Northern greenhouses,” in Proceedings of the III International Symposium on Energy in Protected Cultivation, vol. 148, pp. 853–858, Columbus, OH, USA, August 1983.
  42. G. O. Nkansah and T. Ito, “Effect of air and root-zone temperatures on physiological characteristics and yield of heat-tolerant and non heat-tolerant tomato cultivars,” Engei Gakkai Zasshi, vol. 64, no. 2, pp. 315–320, 1995. View at Publisher · View at Google Scholar
  43. J. Ripoll, L. Urban, M. Staudt, F. Lopez-Lauri, L. P. R. Bidel, and N. Bertin, “Water shortage and quality of fleshy fruits-making the most of the unavoidable,” Journal of Experimental Botany, vol. 65, no. 15, pp. 4097–4117, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Ripoll, L. Urban, B. Brunel, and N. Bertin, “Water deficit effects on tomato quality depend on fruit developmental stage and genotype,” Journal of Plant Physiology, vol. 190, pp. 26–35, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. P. J. White, D. T. Clarkson, and M. J. Earnshaw, “Acclimation of potassium influx in rye (Secale cereale) to low root temperatures,” Planta, vol. 171, no. 3, pp. 377–385, 1987. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Wu and C. Kubota, “Effects of high electrical conductivity of nutrient solution and its application timing on lycopene, chlorophyll and sugar concentrations of hydroponic tomatoes during ripening,” Scientia Horticulturae, vol. 116, no. 2, pp. 122–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Viola and H. V. Davies, “A microplate reader assay for rapid enzymatic quantification of sugars in potato tubers,” Potato Research, vol. 35, no. 1, pp. 55–58, 1992. View at Publisher · View at Google Scholar · View at Scopus
  48. J. B. Jones Jr., “Plant characteristics and physiology,” in Tomato Plant Culture: In the Field, Greenhouse, and Home Garden, pp. 55–78, CRC Press, Boca Raton, FL, USA, 2007. View at Google Scholar
  49. D. Van Ploeg and E. Heuvelink, “Influence of sub-optimal temperature on tomato growth and yield: a review,” The Journal of Horticultural Science and Biotechnology, vol. 80, no. 6, pp. 652–659, 2005. View at Publisher · View at Google Scholar
  50. S. R. Adams, K. E. Cockshull, and C. R. J. Cave, “Effect of temperature on the growth and development of tomato fruits,” Annals of Botany, vol. 88, no. 5, pp. 869–877, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Domínguez, J. Cuartero, and R. Fernández-Muñoz, “Breeding tomato for pollen tolerance to low temperatures by gametophytic selection,” Euphytica, vol. 142, no. 3, pp. 253–263, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Fujimura, K. Suzuki, M. Nagao, and M. Okada, “Acclimation to root chilling increases sugar concentrations in tomato (Solanum lycopersicum L.) fruits,” Scientia Horticulturae, vol. 147, pp. 34–41, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. X. Wan, J. J. Zwiazek, V. J. Lieffers, and S. M. Landhäusser, “Hydraulic conductance in aspen (Populus tremuloides) seedlings exposed to low root temperatures,” Tree Physiology, vol. 21, no. 10, pp. 691–696, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Murai-Hatano, T. Kuwagata, J. Sakurai et al., “Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins,” Plant and Cell Physiology, vol. 49, no. 9, pp. 1294–1305, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. X. Wan, S. M. Landhäusser, J. J. Zwiazek, and V. J. Lieffers, “Root water flow and growth of aspen (Populus tremuloides) at low root temperatures,” Tree Physiology, vol. 19, no. 13, pp. 879–884, 1999. View at Publisher · View at Google Scholar · View at Scopus
  56. Q.-Y. Yan, Z.-Q. Duan, J.-D. Mao, X. Li, and F. Dong, “Low root zone temperature limits nutrient effects on cucumber seedling growth and induces adversity physiological response,” Journal of Integrative Agriculture, vol. 12, no. 8, pp. 1450–1460, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. P. Zhang, F. F. Jia, X. M. Zhang et al., “Temperature effects on the reactive oxygen species formation and antioxidant defence in roots of two cucurbit species with contrasting root zone temperature optima,” Acta Physiologiae Plantarum, vol. 34, no. 2, pp. 713–720, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Bugbee and J. W. White, “Tomato growth as affected by root-zone temperature and the addition of gibberellic acid and kinetin to nutrient solutions,” Journal of the American Society for Horticultural Science, American Society for Horticultural Science, vol. 109, no. 1, pp. 121–125, 1984. View at Google Scholar
  59. L. Taiz and E. Zeiger, Plant Physiology, Springer-Verlag, Berlin, Germany, 4th edition, 2007.
  60. R. W. Hofmann and M. Z. Z. Jahufer, “Tradeoff between biomass and flavonoid accumulation in white clover reflects contrasting plant strategies,” PLoS One, vol. 6, no. 4, Article ID e18949, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. B. Huot, J. Yao, B. L. Montgomery, and S. Y. He, “Growth-defense tradeoffs in plants: a balancing act to optimize fitness,” Molecular Plant, vol. 7, no. 8, pp. 1267–1287, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. J. C. Díaz-Pérez, R. Gitaitis, and B. Mandal, “Effects of plastic mulches on root zone temperature and on the manifestation of tomato spotted wilt symptoms and yield of tomato,” Scientia Horticulturae, vol. 114, no. 2, pp. 90–95, 2007. View at Google Scholar
  63. J. H. Moon, Y. K. Kang, and H. D. Suh, “Effect of root-zone cooling on the growth and yield of cucumber at supraoptimal air temperature,” Acta Horticulturae, vol. 761, pp. 271–274, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. C. H. Mohammud, M. K. Illias, O. Zaulia, S. S. Ahmad Syafk, and M. Y. Angelina Ho, “Effect of rhizosphere cooling on tomato crop performance under controlled environment structure,” Journal of Tropical Agriculture and Food Science, vol. 44, no. 1, pp. 19–27, 2016. View at Google Scholar
  65. S. Kii and H. Araki, “Root-zone cooling improves fruit production in high sugar content tomato,” in Proceedings of the II Asian Horticultural Congress 1208, pp. 291–296, Chengdu City, China, September 2016.
  66. A. Fennell and A. H. Markhart, “Rapid acclimation of root hydraulic conductivity to low temperature,” Journal of Experimental Botany, vol. 49, no. 322, pp. 879–884, 1998. View at Publisher · View at Google Scholar · View at Scopus
  67. N. J. Atkinson, T. P. Dew, C. Orfila, and P. E. Urwin, “Influence of combined biotic and abiotic stress on nutritional quality parameters in tomato (Solanum lycopersicum),” Journal of Agricultural and Food Chemistry, vol. 59, no. 17, pp. 9673–9682, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. M. R. Figàs, J. Prohens, M. D. Raigón et al., “Characterization of composition traits related to organoleptic and functional quality for the differentiation, selection and enhancement of local varieties of tomato from different cultivar groups,” Food Chemistry, vol. 187, pp. 517–524, 2015. View at Publisher · View at Google Scholar · View at Scopus
  69. S. W. Lu, T. L. Li, and J. Jiang, “Effects of tomato fruit under Na+-salt and Cl-salt stresses on sucrose metabolism,” African Journal of Agricultural Research, vol. 5, no. 16, pp. 2227–2231, 2010. View at Google Scholar
  70. K. Koch, “Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development,” Current Opinion in Plant Biology, vol. 7, no. 3, pp. 235–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. W. J. Patrick, C. Botha, F., and R. G. Birch, “Metabolic engineering of sugars and simple sugar derivatives in plants,” Plant Biotechnology Journal, vol. 11, no. 2, pp. 142–156, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Zhang, Y. Zhang, Y. Zhou, and J. Yu, “Adaptation of cucurbit species to changes in substrate temperature: root growth, antioxidants, and peroxidation,” Journal of Plant Biology, vol. 50, no. 5, pp. 527–532, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Ma, Y. Z. Zhang, Y. Lu, and H. Shao, “Roles of plant soluble sugars and their responses to plant cold stress,” African Journal of Biotechnology, vol. 8, no. 10, pp. 2004–2010, 2009. View at Google Scholar
  74. F. Sami, M. Yusuf, M. Faizan, A. Faraz, and S. Hayat, “Role of sugars under abiotic stress,” Plant Physiology and Biochemistry, vol. 109, pp. 54–61, 2016. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Ntatsi, D. Savvas, G. Ntatsi, H.-P. Kläring, and D. Schwarz, “Growth, yield, and metabolic responses of temperature-stressed tomato to grafting onto rootstocks differing in cold tolerance,” Journal of the American Society for Horticultural Science, vol. 139, no. 2, pp. 230–243, 2014. View at Publisher · View at Google Scholar
  76. O. Schwarz, S. Floridi, and L. Montanari, “Organic acids profile in tomato juice by HPLC with UV detection,” Journal of Food Quality, vol. 30, no. 2, pp. 253–266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. G. E. Anthon, M. LeStrange, and D. M. Barrett, “Changes in pH, acids, sugars and other quality parameters during extended vine holding of ripe processing tomatoes,” Journal of the Science of Food and Agriculture, vol. 91, no. 7, pp. 1175–1181, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Hernández Suárez, E. Rodríguez Rodríguez, and C. Díaz Romero, “Analysis of organic acid content in cultivars of tomato harvested in Tenerife,” European Food Research and Technology, vol. 226, no. 3, pp. 423–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. D. V. Shaw, “Response to selection and associated changes in genetic variance for soluble solids and titratable acids contents in strawberries,” Journal of the American Society for Horticultural Science, vol. 115, no. 5, pp. 839–843, 1990. View at Publisher · View at Google Scholar
  80. A. A. Kader, “Quality and its maintenance in relation to the postharvest physiology of strawberry,” The Strawberry Into the 21st Century, Chapter 29, Timber Press, portland, Oregon, 1991. View at Google Scholar
  81. P. Lobit, M. Genard, P. Soing, and R. Habib, “Modelling malic acid accumulation in fruits: relationships with organic acids, potassium, and temperature,” Journal of Experimental Botany, vol. 57, no. 6, pp. 1471–1483, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Y. Wang and M. J. Camp, “Temperatures after bloom affect plant growth and fruit quality of strawberry,” Scientia Horticulturae, vol. 85, no. 3, pp. 183–199, 2000. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Raffo, M. Salucci, E. AzzinI et al., “Nutritional characteristics of greenhouse cherry tomatoes,” Acta Horticulturae, vol. 614, pp. 681–686, 2002. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Massot, M. Génard, R. Stevens, and H. Gautier, “Fluctuations in sugar content are not determinant in explaining variations in vitamin C in tomato fruit,” Plant Physiology and Biochemistry, vol. 48, no. 9, pp. 751–757, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Roselló, A. M. Adalid, J. Cebolla-Cornejo, and F. Nuez, “Evaluation of the genotype, environment and their interaction on carotenoid and ascorbic acid accumulation in tomato germplasm,” Journal of the Science of Food and Agriculture, vol. 91, no. 6, pp. 1014–1021, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Johkan, M. Ishii, T. Maruo et al., “Improved light conditions at the fruit truss accelerate harvest time and enhance ascorbic acid concentration in a low-truss, high-density tomato production system,” Journal of the Japanese Society for Horticultural Science, vol. 82, no. 4, pp. 317–321, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. C. Massot, D. Bancel, F. Lopez Lauri et al., “High temperature inhibits ascorbate recycling and light stimulation of the ascorbate pool in tomato despite increased expression of biosynthesis genes,” PLoS One, vol. 8, no. 12, Article ID e84474, 2013. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Langi, S. Kiokias, T. Varzakas, and C. Proestos, “Carotenoids: from plants to food and feed industries,” in Microbial Carotenoids, pp. 57–71, Humana Press, New York, NY, 2018. View at Google Scholar
  89. I. Martínez-Valverde, M. J. Periago, G. Provan, and A. Chesson, “Phenolic compounds, lycopene and antioxidant activity in commercial varieties of tomato (Lycopersicum esculentum),” Journal of the Science of Food and Agriculture, vol. 82, no. 3, pp. 323–330, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. H. l. n. Gautier, A. Rocci, M. Buret, D. Grasselly, and M. Causse, “Fruit load or fruit position alters response to temperature and subsequently cherry tomato quality,” Journal of the Science of Food and Agriculture, vol. 85, no. 6, pp. 1009–1016, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. K. A. Thompson, M. R. Marshall, C. A. Sims, C. I. Wei, S. A. Sargent, and J. W. Scott, “Cultivar, maturity, and heat treatment on lycopene content in tomatoes,” Journal of Food Science, vol. 65, no. 5, pp. 791–795, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Zanfini, G. G. Franchi, P. Massarelli, G. Corbini, and E. Dreassi, “Phenolic compounds, carotenoids and antioxidant activity in five tomato (Lycopesicon esculentum Mill.) cultivars,” Italian Journal of Food Science, vol. 29, no. 1, 2016. View at Google Scholar
  93. R. K. Toor, G. P. Savage, and C. E. Lister, “Seasonal variations in the antioxidant composition of greenhouse grown tomatoes,” Journal of Food Composition and Analysis, vol. 19, no. 1, pp. 1–10, 2006. View at Publisher · View at Google Scholar · View at Scopus
  94. M. A. Rosales, J. M. Ruiz, J. Hernández, T. Soriano, N. Castilla, and L. Romero, “Antioxidant content and ascorbate metabolism in cherry tomato exocarp in relation to temperature and solar radiation,” Journal of the Science of Food and Agriculture, vol. 86, no. 10, pp. 1545–1551, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Brandt, A. Lugasi, Éa Barna, J. Hóvári, Z. Pék, and L. Helyes, “Effects of the growing methods and conditions on the lycopene content of tomato fruits,” Acta Alimentaria, vol. 32, no. 3, pp. 269–278, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. L.-J. Wang, W.-D. Huang, J.-Y. Li, Y.-F. Liu, and Y.-L. Shi, “Peroxidation of membrane lipid and Ca2+ homeostasis in grape mesophyll cells during the process of cross-adaptation to temperature stresses,” Plant Science, vol. 167, no. 1, pp. 71–77, 2004. View at Publisher · View at Google Scholar
  97. I. Ensminger, F. Busch, and N. P. A. Huner, “Photostasis and cold acclimation: sensing low temperature through photosynthesis,” Physiologia Plantarum, vol. 126, no. 1, pp. 28–44, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. T. Kato, K. Aoki, and H. Yamanishi, “Effects of low temperatures on the vitamin C, beta-carotene, tocopherol and oxalate contents of spinach grown in the vinyl house,” Japanese Journal of Soil Science and Plant Nutrition (Japan), vol. 66, no. 5, pp. 563–566, 1995. View at Google Scholar
  99. M. Islam, Y.-T. Lee, M. Mele, I.-L. Choi, and H.-M. Kang, “The effect of phosphorus and root zone temperature on anthocyanin of red romaine lettuce,” Agronomy, vol. 9, no. 2, p. 47, 2019. View at Publisher · View at Google Scholar
  100. S. Malik, S. A. L. Andrade, A. C. H. F. Sawaya, A. Bottcher, and P. Mazzafera, “Root-zone temperature alters alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum,” Industrial Crops and Products, vol. 49, pp. 318–325, 2013. View at Publisher · View at Google Scholar · View at Scopus
  101. C. J. Pollock and C. F. Eagles, “Low temperature and the growth of plants,” Symposia of the Society for Experimental Biology, vol. 42, pp. 157–180, 1988. View at Google Scholar
  102. K. A. Nagel, B. Kastenholz, S. Jahnke et al., “Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping,” Functional Plant Biology, vol. 36, no. 11, pp. 947–959, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Poiré, H. Schneider, M. R. Thorpe, A. J. Kuhn, U. Schurr, and A. Walter, “Root cooling strongly affects diel leaf growth dynamics, water and carbohydrate relations inRicinus communis,” Plant, Cell and Environment, vol. 33, no. 3, pp. 408–417, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. J. B. Wilson, “A review of evidence on the control of shoot: root ratio, in relation to models,” Annals of Botany, vol. 61, no. 4, pp. 433–449, 1988. View at Publisher · View at Google Scholar
  105. A. Hamblin, D. Tennant, and M. W. Perry, “The cost of stress: dry matter partitioning changes with seasonal supply of water and nitrogen to dryland wheat,” Plant and Soil, vol. 122, no. 1, pp. 47–58, 1990. View at Publisher · View at Google Scholar · View at Scopus
  106. J. A. Tindall, H. A. Mills, and D. E. Radcliffe, “The effect of root zone temperature on nutrient uptake of tomato,” Journal of Plant Nutrition, vol. 13, no. 8, pp. 939–956, 1990. View at Publisher · View at Google Scholar · View at Scopus
  107. Q. F. Quadir, T. Watanabe, Z. Chen, M. Osaki, and T. Shinano, “Ionomic response of Lotus japonicusto different root-zone temperatures,” Soil Science and Plant Nutrition, vol. 57, no. 2, pp. 221–232, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. S. J. Clarke, K. J. Lamont, H. Y. Pan, L. A. Barry, A. Hall, and S. Y. Rogiers, “Spring root-zone temperature regulates root growth, nutrient uptake and shoot growth dynamics in grapevines,” Australian Journal of Grape and Wine Research, vol. 21, no. 3, pp. 479–489, 2015. View at Publisher · View at Google Scholar · View at Scopus
  109. K. Füllner, “The influence of spatially heterogeneous soil temperatures on plant structure and functions,” Heinrich-Heine Universität Düsseldorf, Düsseldorf, Germany, 2007, Ph. D. thesis. View at Google Scholar
  110. Y. Jia, J. Wang, Z. Qu et al., “Effects of low water temperature during reproductive growth on photosynthetic production and nitrogen accumulation in rice,” Field Crops Research, vol. 242, p. 107587, 2019. View at Publisher · View at Google Scholar
  111. L. P. Tan, J. He, and S. K. Lee, “Effects of root-zone temperature on the root development and nutrient uptake oflactuca satival. “Panama” grown in an aeroponic system in the tropics,” Journal of Plant Nutrition, vol. 25, no. 2, pp. 297–314, 2002. View at Publisher · View at Google Scholar · View at Scopus
  112. C. Badea and S. K. Basu, “The effect of low temperature on metabolism of membrane lipids in plants and associated gene expression,” Plant Omics, vol. 2, no. 2, p. 78, 2009. View at Google Scholar
  113. S.-J. Ahn, Y.-J. Im, G.-C. Chung, K.-Y. Seong, and B.-H. Cho, “Sensitivity of plasma membrane H + -ATPase of cucumber root system in response to low root temperature,” Plant Cell Reports, vol. 19, no. 8, pp. 831–835, 2000. View at Publisher · View at Google Scholar · View at Scopus
  114. H. Feng, M. Yan, X. Fan et al., “Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status,” Journal of Experimental Botany, vol. 62, no. 7, pp. 2319–2332, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. H. L. George, F. S. Davies, J. H. Crane, and B. Schaffer, “Root temperature effects on ‘Arkin’ carambola (Averrhoa carambola L.) trees,” Scientia Horticulturae, vol. 96, no. 1–4, pp. 53–65, 2002. View at Publisher · View at Google Scholar · View at Scopus
  116. S. H. Lee, A. P. Singh, G. C. Chung, S. J. Ahn, E. K. Noh, and E. Steudle, “Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport of nutrients,” Physiologia Plantarum, vol. 120, no. 3, pp. 413–420, 2004. View at Publisher · View at Google Scholar · View at Scopus
  117. C. Engels, L. Munkle, and H. Marschner, “Effect of root zone temperature and shoot demand on uptake and xylem transport of macronutrients in maize (Zea maysL.),” Journal of Experimental Botany, vol. 43, no. 4, pp. 537–547, 1992. View at Publisher · View at Google Scholar · View at Scopus
  118. A. Janská, P. Maršík, S. Zelenková, and J. Ovesná, “Cold stress and acclimation - what is important for metabolic adjustment?” Plant Biology, vol. 12, no. 3, pp. 395–405, 2010. View at Publisher · View at Google Scholar · View at Scopus
  119. A. Ahamed, M. Murai-Hatano, J. Ishikawa-Sakurai, H. Hayashi, Y. Kawamura, and M. Uemura, “Cold stress-induced acclimation in rice is mediated by root-specific aquaporins,” Plant and Cell Physiology, vol. 53, no. 8, pp. 1445–1456, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Kitano, K. Hidaka, K. Zushi, and T. Araki, “Production of value-added vegetables by applying environmental stresses to roots in soil-less culture,” Shokubutsu Kankyo Kogaku, vol. 20, no. 4, pp. 210–218, 2008. View at Publisher · View at Google Scholar
  121. Y. Chadirin, K. Hidaka, Y. Sago, T. Wajima, and M. Kitano, “Application of temperature stress to root zone of spinach II. Effect of the high temperature pre-treatment on quality,” Environment Control in Biology, vol. 49, no. 4, pp. 157–164, 2011. View at Publisher · View at Google Scholar · View at Scopus