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ASHS 2024 Annual Conference

 

Physiological and Growth Characteristics of Tomato Seedlings in Response to Low Root-zone Temperature

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Han Zhang College of Water Resources and Civil Engineering, China Agriculture University, Beijing, 100083, China

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Xuguang Sun College of Water Resources and Civil Engineering, China Agriculture University, Beijing, 100083, China

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Weitang Song Key Laboratory of Agricultural Engineering in Structure and Environment, Ministry of Agriculture and Rural Affairs, College of Water Resources and Civil Engineering, China Agriculture University, Beijing, 100083, China

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Abstract

Root-zone temperature (RZT) is an indispensable environmental factor for the proper growth and development of plants. Low RZT is one of the major limitations for agricultural production during cold seasons. In this study, the physiological responses of tomato seedlings to low RZT stress (10 °C) and its recovery were investigated with hydroponic cultivation in an artificial climate-controlled chamber. The stress reaction of tomato seedlings was evaluated by combining various indexes, including photosynthesis, chlorophyll fluorescence, root activity, hydrogen peroxide, and antioxidants. The results showed that low RZT adversely affected root activity, and in response to the limited root-source water and mineral elements, supply for shoot metabolism, leaf photosynthesis, and chlorophyll fluorescence were negatively influenced, which led to inhibited leaf area development and biomass accumulation. Hydrogen peroxide (H2O2), malondialdehyde (MDA), and proline accumulated with the time of low RZT stress. When restored to normal temperature (∼20 °C), the physiological parameters recovered to a certain degree, although most parameters were not at a similar level with the control. In crop production during cold seasons, it is necessary to improve the RZT to achieve high quality and yield production.

Temperature, as one of the most important environmental factors, vitally influences various growth and developmental processes of plants. In both natural and artificial crop production condition, plant shoots and roots are regularly exposed to different ambient temperature conditions due to their growing media (air/soil or substrate). Air temperature critically influences plant developmental and physiological characteristics (Liu et al. 2012; Makino et al. 1994; Stasik and Jones 2007). Therefore, RZT unavoidably influences root growth and development (Franco et al. 2011), which makes it more restrictive in regulating plant growth of a variety of important crops (Arai-Sanoh et al. 2010; Göbel et al. 2019; He et al. 2016; Shimono et al. 2002).

The root growth rate of maize reduced from 1.2 mm⋅h−1 to 0.02 mm⋅h−1 when temperature dropped from 20 °C to 5 °C (Pritchard et al. 1990). Low RZT induces decrease of the root meristem size and cell number by suppressing related gene expression and auxin accumulation (Zhu et al. 2015). Plant root system functions in uptake and transportation of water and mineral nutrients, which are also sensitive to the temperature condition (Calatayud et al. 2008; Domisch et al. 2001; Posmyk et al. 2005). The differentiation of root morphogenesis and alteration of water/minerals delivery under suboptimal temperature potentially influence functioning of both the root and shoot, although the air temperature might be within adequate range (Gonzalez-Fuentes et al. 2016; Stoltzfus et al. 1998).

On the view of whole plant, impacts of RZT on root development induce pronounced responses of shoot development and crop productivity; this has been reported on many plants, such as lettuce (Luo et al. 2012; Sun et al. 2016), bent grass (Xu and Huang 2000), and rice (Kuwagata et al. 2012). Photosynthesis is one of the most important physiological processes that determine plant growth, and it is sensitive to temperature condition (Berry and Bjorkman 1980). When day temperature was reduced, the photosynthetic rate of wild Lycopersicon species was also decreased (Xiao et al. 2018). Low RZT reduces root water permeability and thereby decreases plant water absorption (McWilliam et al. 1982). Decrease in the root hydraulic conductance results in leaf water deficit and stomatal closure under low substrate temperature (Santos et al. 2011). As a result of stomatal limitation, photosynthetic activity is negatively affected by low RZT (Farquhar and Sharkey 1982), along with decline of leaf stomatal conductance (gS) as reported in cucumber (Ahn et al. 1999), tomato (He et al. 2014), and grapevine (Rogiers and Clarke 2013). Plants generate defensive responses to low RZT condition, as a detrimental abiotic stress, low RZT stimulates the synthesis of proteins that associate with oxidoreductase activity of apple seedlings (Li et al. 2018). Impairment in the photosynthetic electron consumption under low-temperature stress might cause the accumulation of reactive oxygen species, and therefore the scavenging enzyme activity is increased as a defensive mechanism (Chawla et al. 2013; Janmohammadi et al. 2015; Mirza et al. 2020; Sales et al. 2013).

During cold seasons in the high latitude greenhouse producing areas, the air inside greenhouses could warm rapidly after sunrise. However, increase of soil temperature is largely lagged because of its relative high heat capacity, thus resulting in roots being exposed to low RZT stress during the important growing periods (Li et al. 2018). The impairment of root and shoot thermal condition is therefore an unavoidable limitation on the plant yield and product quality. Exposure to low RZT of different species and growth stages may result in different capacity to recover or even irreversible damage to the root system and subsequent growth when restored to normal temperature (Meena et al. 2017; Posmyk et al. 2005; Reyes and Jennings 1994).

Tomato (Lycopersicon esculentum) is one of the most important vegetables that is cultivated worldwide. Attributed to its origin, tomato is cold sensitive during vegetative and productive growth (Foolad and Lin 2000; Lyons 1973). Especially, the seedling stage is the most susceptible stage for the cultivation of horticultural crops for year-round production in greenhouses. Tomato normally grows at 15 to 33 °C, when the external temperature is lower than 10 °C, the growth rate slows down, and the growth stops when the external temperature decreases to below 5 °C. Therefore, low-temperature injury is one of the main natural stress factors affecting the growth of tomato (Chen et al. 2015). Low temperature results in inactivation of PSII reaction center in tomato leaves, but activation of electron transport chain on the PSI side (Zushi et al. 2012). In addition, low temperature inhibited the photosynthetic efficiency and chlorophyll biosynthesis, and reduced the accumulation of dry matter, and ultimately led to the decline of quality and yield of tomato (Brüggemann et al. 1994). Consequently, it is of great significance to study the effects of low RZT on the physiological characteristics and plant development of tomato seedlings to control their later growth and substantial fruit yield.

There are many studies on optimizing RZT by root warming or cooling to improve plant productivity in field experiments (Kawasaki et al. 2013; Sun et al. 2016; Wang et al. 2016); however, limited understanding has been gained on the negative impacts of unfavorable low RZT on the shoot activities, and the underlying physiological mechanism remains unclear. In the present study, under a controlled condition, we applied low RZT treatment by manipulating the nutrient solution temperature with hydroponic cultivation. The leaf photosynthesis, chlorophyll fluorescence induction, and oxidant state under both low RZT and recovered root condition were investigated. Accordingly, the objective of this study was to investigate the adaptability and physiological responses of plant root under low RZT stress and the possibility to recover when subject to rewarming condition.

Materials and Methods

Plant material and growth condition.

Tomato (L. esculentum, cv. Zhongshu No. 4) seedlings were soaked for 3 h after being disinfected with warm soup, and buds were accelerated for 36 h in an incubator at 30 °C until the roots were stretched. Then the seedlings were sown in plug trays and allowed to grow to four leaves and one center (∼40 d). About 30 uniform seedlings were selected and transplanted into the RZT controlled hydroponic system in a growth chamber 1 week before treatment. Plants were cultivated with half-strength Hoagland’s nutrient solution (pH = 6.5 ± 0.2, electrical conductivity = 1.0 mS·cm−1) that aerated with an aeration pump. RZT was controlled by cooling/warming of the nutrient solution with a semiconductor refrigerator (AL36G-160; AL-Electron Inc., Shenzhen, China) and electrothermal bar. Air temperature of the climate-controlled chamber was maintained at 25 °C during the day and 18 °C at night, the relative humidity was set at 70%. Plants received irradiation with light intensity of 200 μmol⋅m−2⋅s−1 (12 h/12 h day/night) on the canopy level with fluorescent lamps.

Experimental setup.

Two experimental stages were set in this study, and each stage was 5 d. At the initial stage, two groups of the seedlings were subjected to low RZT treatment at 10 °C (10 °C-RZT), and control RZT at 20 °C (control, 20 °C) for 5 d. After that, on the following stage, half of the plants of either the low treatment (10 °C-RZT) or control group were transferred to the other root temperature condition (either control temperature at 20 °C or cold temperature at 10 °C), thereby resulting in four treatment groups, which were two treatments with changed root temperature (20 °C–10 °C and 10 °C–20 °C), and two controls (20 °C–20 °C and 10 °C–10 °C), respectively. Two treatment groups (20 °C–10 °C and 10 °C–20 °C) were set up to study the effects of two intense transition periods of light and temperature change on physiological characteristics and photosynthesis of tomato on the first day of low-temperature treatment and the first day of recovery. Measurement and sampling for biochemical assay were conducted at day 5 and day 10 at the end of each experimental stage. All measurements were performed in four replications per treatment.

Phytochemicals content.

The malonaldehyde (MDA) content was determined following the method described by Hodges et al. (1999). Homogenized leaf sample was extracted with 10% trichloroacetic acid (TCA) solution for the MDA content determination; 2 mL of the obtained supernatant was mixed with 2 mL 0.6% thiobarbituric acid (TBA) in 10% TCA, and then subjected to boiled water bath for 30 min until the reaction was ended with an ice bath. The absorbance of the supernatant at 532 nm, 600 nm, and 450 nm was determined with a spectrophotometer, and MDA content was calculated as μg⋅g−1 fresh weight.

The proline content was determined following the method described by Bates et al. (1973), homogenized leaf sample was extracted with 3% sulfosalicylic acid. The extracted supernatant (1 mL) was mixed with ninhydrine acid (1 mL) and acetic acid (1 mL) and boil water bathed for 1 h, and the reaction was stopped with an ice bath. The absorbance at 520 nm of the formed chromophore that extracted with cold toluene was measured with a spectrophotometer. Proline concentration was calculated as µmol proline per gram fresh weight.

For the determination of H2O2 content, leaf tissue (0.2 g) was homogenized and extracted with acetone at 0 °C. H2O2 content was estimated by measuring the absorbance of the titanium-hydroperoxide complex, and the concentration of H2O2 was calculated from a standard curve of H2O2 reagent following the description of Sairam and Srivastava (2002).

Homogenized leaf sample was extracted with 2 mL 6% metaphosphoric acid (containing 2 mm EDTA) for ascorbic acid content determination. The extraction was then centrifuged and its supernatants were used for the determination of ascorbate (AsA), and DHA (dehydroascorbate) determined according to Kampfenkel et al. (1995).

Measurement of gas exchange parameters and chlorophyll a fluorescence.

Leaf gas exchange parameters were measured with a portable photosynthesis system (Li-6400XT; LI-COR Inc., Lincoln, Nebraska, USA) on the third fully expanded and functioning leaves. For the photosynthetic parameter measurement, light intensity of the leaf chamber was set to 200 μmol⋅m−2⋅s−1, temperature at 25 °C, CO2 concentration at 400 μmol⋅m−2, and relative humidity at 70%. Net photosynthetic rate (PN), gS, intercellular CO2 concentration (Ci), and transpiration rate (Tr) were recorded until a steady state of photosynthetic rate reached.

Chlorophyll a fluorescence induction was conducted with a plant efficiency analyzer (Handy PEA; Hansatech Instruments, Norfolk, UK). Leaves were dark-adapted for 30 min before subjected to the induction of fast chlorophyll fluorescence induction (OJIP) curves with red light (peak 660 nm) at ∼3000 µmol⋅m−2⋅s−1. Based on the fluorescence intensity values obtained from the induction steps, the biophysical parameters derived from the OJIP transient were calculated according to Strasser et al. (2004).

Measurement of root activity.

Fresh root sample (0.5 g) was mixed thoroughly with 0.1% 2,3,5-triphenyltetrazolium chloride (5 mL) and potassium phosphate buffer (5 mL, pH = 7.0), and then subjected to incubate at 37 °C for 2 h until the reaction was ended with 2 mL H2SO4 (1 mol⋅L−1). Then the roots were rinsed with deionized water and ground in 10 mL acetone until the root turned white. The absorbance at 490 nm of the obtained supernatant was measured with a spectrophotometer. Root activities were calculated as follows: root activity (mg⋅g−1⋅h−1) = A490 × V/WT, where V is the total volume of extract (mL), W is the fresh weight (g) of the sample, and T is the reaction time (h).

Measurement of plant growth.

At day 5 and day 10 (end of each stage), plants were collected for the biomass measurement. Sample was oven dried at 80 °C until a constant weight was reached to obtain its dry weight. Plant height was measured with a ruler, and stem diameter was measured with clipper. The leaves of each sample plant were scanned with a digital scanner and the leaf area per plant was determined with ImageJ software (National Institutes of Health, Bethesda, MD, USA). Leaf chlorophyll content was measured as soil-plant analysis development (SPAD) value with a chlorophyll meter (SPAD-502; Minolta Inc., Tokyo, Japan).

Data analysis method.

Data are presented as mean with standard error. All statistical analyses were performed with SPSS 22.0 (SPSS software, Chicago, IL, USA). Tukey’s highly significant difference test was performed for one-way analysis of variance to separate significant differences between groups at P = 0.05. Independent samples t tests (two-tailed) were used to test statistically significant differences between the control and low RZT treatment (P = 0.05).

Results

Plant growth parameters.

During the first treatment stage, RZT significantly influenced the growth of the tomato seedlings (Fig. 1). Dry weight, and total leaf area were significantly lower for the 10 °C treatment compared with the control (20 °C). No significant difference was noted for the stem diameter, whereas the plant under low RZT was numerically shorter than the control (P = 0.051).

Fig. 1.
Fig. 1.

Effect of temperature at 10 °C, 20 °C (stage 1), and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on the plant height (A), stem diameter (B), dry weight (DM, C), and total leaf area (D) in the leaves of tomato plants. Data are presented as mean values ± SE (n = 4). Different letters indicate significant differences between values (P < 0.05) according to Tukey’s highly significant difference test. *P < 0.05; ***P < 0.001; ns, not significant according to independent sample t test.

Citation: HortScience 58, 4; 10.21273/HORTSCI16924-22

At the second treatment stage, the tomato seedlings under further root low RZT treatment (10 °C–10 °C) resulted in the lowest dry weight, as well as the smallest total leaf area. Recovered RZT of the 10 °C–20 °C treatment resulted in greater biomass accumulation and leaf area, though they were still significantly lower than the control of 20 °C–20 °C. No significant influence was recorded for the plant height and stem diameter after the two treatment stages.

Root activity.

Root activity of the tomato seedlings was significantly influenced by RZT (Table 1). Low RZT (10 °C, 10 °C–10 °C, and 20 °C–10 °C treatments) induced significant inhibition on the root activity at both stages. When subjected to rewarming, the recovered RZT treatment (10 °C–20 °C) resulted in increased root activity, although it was still significantly lower than the 20 °C–20 °C control group. Shift of RZT from control to low RZT (20 °C–10 °C) led to a significant reduction of root activity.

Table 1.

Effect of temperature at 10 °C, 20 °C (stage 1), and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on soil-plant analysis development (SPAD) value and root activity of tomato seedlings.

Table 1.

Chlorophyll accumulation.

Low RZT inhibited the accumulation of chlorophyll in the leaves, which was indicated by the decrease of SPAD values (Table 1). Prolonged low RZT treatment (10 °C–10 °C) resulted in the lowest SPAD value, whereas return to control temperature (10 °C–20 °C) resulted in a re-accumulation of chlorophyll, although it was still significantly lower than the control group (20 °C–20 °C).

Gas exchange parameters.

RZT influenced the gas exchange parameter of tomato seedling leaves (Fig. 2). After the first stage, low RZT significantly reduced the leaf photosynthetic rate, gS, intercellular CO2 concentration, and transpiration rate compared with control (20 °C). At the second stage, 10 °C–10 °C resulted in further inhibited photosynthetic rate (P < 0.001), gS (P < 0.001), Ci (P = 0.015), and Tr (P = 0.004) compared with 10 °C of stage 1. At the second stage, PN, gS, Ci, and Tr decreased significantly when shifted to lower root temperature (20 °C–10 °C) compared with the control (20 °C–20 °C), whereas PN of the low RZT groups (10 °C) alleviated in a certain degree when they were moved to normal RZT (10 °C–20 °C), and PN, gS, Ci, and Tr resulted in the lowest value for the 10 °C–10 °C treatment.

Fig. 2.
Fig. 2.

Effect of temperature at 10 °C, 20 °C (stage 1). and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on net photosynthetic rate (PN, A), stomatal conductance (gS, B), intercellular CO2 concentration (Ci, C), and transpiration rate (Tr, D) in the leaves of tomato plants. Data are presented as mean values ± SE (n = 4). Different letters indicate significant differences between values (P < 0.05) according to Tukey’s highly significant difference test. **P < 0.01; ***P < 0.001 according to independent sample t test.

Citation: HortScience 58, 4; 10.21273/HORTSCI16924-22

Chlorophyll a fluorescence induction.

Table 2 gives the chlorophyll fluorescence parameters derived from the OJIP test. Cold RZT induced inhibition in all the parameters. The Fv/Fm values of tomato plants exposed to 10 °C root temperature at stage 1 decreased significantly in relation to the values of control plants (20 °C), indicating an inhibition of the photosynthesis efficiency (Krause and Weis 1991). However, the Fv/Fm value fell to below 0.56 with the continued cold stress for plants exposed to 10 °C–10 °C treatment, indicating severe photoinhibition of PSII. Fv/Fm alleviated to 0.73 when rewarmed to normal root temperature for the 10 °C–20 °C group. After stage 1, the energy absorbed per excited cross section (ABS/CSm), trapped energy flux per CSm (TRo/CSm), electron transport flux per CSm (ETo/CSm), and PSI acceptor per CSm (REo/CSm) were significantly decreased for low root treatment (10 °C) than that of control (20 °C), whereas non-photochemical quenching per CSm (DIo/CSm) significantly increased. After stage 2, ABS/CSm, TRo/CSm, ETo/CSm, and REo/CSm were the lowest for 10 °C–10 °C treatment, and significantly alleviated by shifting to control RZT (10 °C–20 °C), as TRo/CSm and REo/CSm of this group recovered to a similar level with the 20 °C–20 °C control, although ABS/CSm and ETo/CSm were still significantly lower than that of the control. ABS/CSm, ETo/CSm, and REo/CSm were significantly decreased by shifting from control to low RZT (20 °C–10 °C), whereas TRo/CSm was unaffected. DIo/CSm was the lowest for 20 °C–20 °C treatment and significantly increased for 10 °C–20 °C treatment, and the greatest for 10 °C–10 °C treatment.

Table 2.

Effect of temperature at 10 °C, 20 °C (stage 1) and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on chlorophyll fluorescence of tomato seedlings.

Table 2.

Ascorbate and hydrogen peroxide.

Low RZT induced a significant decrease of the ascorbate (AsA and DHA) concentration in tomato leaves compared with that of the control at stage 1 (Table 3). After stage 2, the greatest content of ascorbates was found under 20 °C–20 °C, whereas 20 °C–10 °C also resulted in a reduction in total ascorbate content, and 10 °C–20 °C resulted in an increase of total content compared with 10 °C–10 °C treatment. Under low RZT condition, H2O2 accumulated to a significantly greater level compared with their respective control group of both stages. H2O2 accumulation of 10 °C–20 °C treatment was alleviated at recovered temperature, whereas when subjected to low RZT (20 °C–10 °C) induced synthesis of H2O2.

Table 3.

Effect of temperature at 10 °C, 20 °C (stage 1) and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on metabolite of tomato seedlings.

Table 3.

Lipid peroxidation and proline accumulation.

Lipid peroxidation (expressed in terms of MDA content) and proline accumulation were significantly increased under low RZT condition at stage 1, whereas after stage 2, 10 °C–10 °C treatment further increased the MDA and proline content compared with 10 °C treatments (P < 0.001 and P < 0.001, respectively), and resulted in the greatest amount of MDA and proline content. MDA content was the lowest for 20 °C–20 °C treatment, and the greatest for 10 °C–10 °C, whereas the 10 °C–20 °C and 20 °C–10 °C treatments were significant increased compared with control. Proline content was the lowest for 20 °C–20 °C and 10 °C–20 °C, and significantly greater in the 20 °C–10 °C and 10 °C–10 °C treatments.

Discussion

Air and soil temperatures are frequently below optimal levels for horticultural crop production in temperate regions during the cold seasons, and thereby leading to various injury to the plants. Particularly, being exposed to cold RZT environment, plants experience unfavorable conditions for the water and mineral nutrient supply, resulting in alteration of physiology and crop productivity. Due to the biochemical limitations, plants that suffer low RZT result in an even greater reduction in photosynthetic assimilation compared with low air temperature (Santos et al. 2011). Our results confirmed that photosynthetic capability and antioxidant status were markedly affected by the RZT, which is consistent with many previous investigations, including Artemisia tridentate (BassiriRad et al. 1993), citrus plants (Santos et al. 2011), and cucumber (Ahn et al. 1999).

Indicated by root activity, our results certainly demonstrated the importance of ambient temperature on root system functioning, and low RZT condition (either the 10 °C or the 20 °C–10 °C and 10 °C–10 °C treatments at both stages) led to a marked reduction in root activity of the tomato seedlings (Table 1). Root activity is considered as the physiological index reflecting the ability of root functioning and certain phytochemical biosynthesis (Luo et al. 2016), and it is significantly correlated with root respiration (Kawasaki et al. 2013). Limited root respiration under low temperature inhibits many root physiological functions, such as active uptake and transport of nutrients, and hydraulic conductance (Anwar et al. 2019; BassiriRad et al. 1991; Lee et al. 2004). Reduction of water and nutrient elements source supply further limits the photosynthetic assimilation of the shoot. In the present study, the average Fv/Fm (maximum quantum efficiency of PSII) values of tomato plants decreased when exposed to 10 °C RZT, indicating an inhibition of the photosynthesis efficiency (Krause and Weis 1991). The value of Fv/Fm indicates the energy conversion efficiency of PSII reaction centers. Such reduction in PSII limited the photosynthetic rate. We found a positive correlation of root activity and photosynthetic rate in our result (r = 0.946, P = 0.004), which is consistent with previous investigations (Gai et al. 2017; Luo et al. 2016). A well functioning root system allows adequate water and mineral supply to the leaves, thus increasing sources supply for photosynthetic activity (Al-Khafaf et al. 1989). Furthermore, cold RZT condition substantially decreases the root hydraulic conductivity (Murai-Hatano et al. 2008) and aquaporin activity (Maurel et al. 2008). Limitation of the water supply to leaf transpiration and evaporation activity lead to concomitant reduction in gS (Wan et al. 2004), which was also observed in our study. Intercellular CO2 concentration reduced simultaneously as a consequence of stomata closure, and results in stomatal limitation of photosynthesis (Pinheiro and Chaves 2011). However, upon release from the cold RZT condition, root activity and photosynthetic performance are alleviated at the rewarming environment of the second stage (10 °C–20 °C treatment), indicating a certain ability of the tomato plants to recover from cold RZT stress and synthesize metabolites for growth and development.

Chlorophyll fluorescence parameters reflect the energy flux in photosynthetic biomembrane of the photosystems (Strasser et al. 2004). ABS/CSm, TRo/CSm, and ETo/CSm decreased with low RZT, while the amounts of energy dissipated as heat from PSII (DIo/CSm) increased, indicating inhibition or injury on the reaction center, as well as reduced light capture and utilization efficiency by alteration of the light-harvesting antenna. Simultaneously, under low RZT, tomato leaves increased the energy dissipation by heat, which implies that a defensive mechanism was activated to prevent photosynthetic apparatus from photoinhibition of excessive light energy (Zheng et al. 2020). Those parameters increase upon rewarming of the root zone, although may still lower compared with the 20 °C–20 °C group, which indicated a certain damage to the light harvesting system of the tomato leaves caused by the imbalanced supply sink.

Photosynthetic carbon fixation is a physiological basis in plant yield (Raines 2011). We report considerable decrease of photosynthetic capacity under low RZT, which leads to reduced dry weight of the low RZT treatments compared with their respective control (Fig. 1). This is consistent with many previous investigations, such as on rice (Kuwagata et al. 2012), cucumber (Yan et al. 2012), and prunus (Malcolm et al. 2008), of which their photosynthetic ability was markedly suppressed under low RZT stress. In agreement with the investigation on Ricinus communis (Poiré et al. 2010), limitation of root-sourced water and nutrient elements supply under low RZT strongly restrict the leaf area expansion in the current study and are accompanied by a limited photosynthetic ability (Wang et al. 2016). Associated with the decreased SPAD value, low RZT leads to a negative influence on the overall CO2 assimilation capability of the whole plant.

Our data showed that antioxidative status of the leaves under normal air temperature condition was also modified by the RZT condition. Impairment between the light energy absorption and the metabolic sink caused by various abiotic stress would lead to over-reduction and/or block the electron transport chain, and further induces accumulation of reactive oxygen species (ROS) (Demmig-Adams and Adams 2006). Accumulation of ROS under low RZT caused dysfunction of photosystem II and accelerated photoinhibition of the tomato seedling leaves in this study (Szarka et al. 2012). Excessive ROS would cause oxidative injury to the plasma membrane and eventually lead to increase of MDA level (Ozfidan et al. 2012). We found that the leaf H2O2 content was significantly increased when subject to low RZT condition and it was even enhanced with the continuation of treatment. MDA content estimates the lipid peroxidation level, and increase of MDA accumulation coupled with the genesis of hydrogen peroxide on exposure to lowered RZT in our study. Long-term low RZT (10 °C–10 °C) resulted in reduced AsA/DHA ratio, indicating stress-induced inactivation of the redox capacity. Plants use stress protective machinery with enzymes and antioxidants in scavenging ROS to protect plants against oxidative damage (Gill and Tuteja 2010; Sales et al. 2013). Ascorbates eliminate hydrogen peroxide and other ROS by catalysis of enzymes (Mastropasqua et al. 2012). As observed by Yan et al. (2013) in the study of cucumber seedlings, the secondary metabolism including antioxidants of cucumber leaves was altered by low RZT stress. Metabolism of proline is closely related to ROS generation under adverse environmental conditions (Ben Rejeb et al. 2014). Accumulation of proline functions in mediating scavenging of ROS (Chen and Dickman 2005; Hare and Cress 1997), as well as increases the activity of antioxidant enzymes relating to free radical scavenging (Hoque et al. 2007).

Conclusion

This research investigated the effects of low RZT on the physiology and metabolism of hydroponic tomato seedlings. Our results showed that the root activity was inhibited under low RZT and led to the injurious dysfunction of the shoot under normal temperature condition. Imbalanced source supply to the shoot resulted in a decrease in photosynthetic assimilation and the electron transport chain, as well as reduction/accumulation of stress-related metabolites. Therefore, because of the importance of a well-functioning root system for crop productivity, it would be an effective manner by improving the RZT management for crop production during cold seasons to maximize crop potential. However, in the actual production, different growing environments and environmental factors play an important role in the growth and development stages of crops. This study provides a theoretical basis for the regulation of the actual production environment in the future, and different experimental studies are needed in different situations.

References Cited

  • Ahn, SJ, Im, YJ, Chung, GC, Cho, BH & Suh, SR. 1999 Physiological responses of grafted-cucumber leaves and rootstock roots affected by low root temperature Scientia Hort. 81 4 397 408 https://doi.org/10.1016/S0304-4238(99)00042-4

    • Search Google Scholar
    • Export Citation
  • Al-Khafaf, S, Aziz, FG, Salih, HM & Jack, FJ. 1989 Shoot and root growth and nutrients uptake of wheat as affected by soil layers Plant Soil. 117 59 66 https://doi.org/10.1007/BF02206257

    • Search Google Scholar
    • Export Citation
  • Anwar, A, Li, YS, He, CX & Yu, XC. 2019 24-Epibrassinolide promotes NO3 and NH4 + ion flux rate and NRT1 gene expression in cucumber under suboptimal root zone temperature BMC Plant Biol. 19 225 https://doi.org/10.1186/s12870-019-1838-3

    • Search Google Scholar
    • Export Citation
  • Arai-Sanoh, Y, Ishimaru, T, Ohsumi, A & Kondo, M. 2010 Effects of Soil Temperature on Growth and Root Function in Rice Plant Prod Sci. 13 235 242 https://doi.org/10.1626/pps.13.235

    • Search Google Scholar
    • Export Citation
  • BassiriRad, H, Caldwell, MM & Mott, KA. 1993 Effect of root cooling on photosynthesis of Artemisia tridentata seedlings under different light levels Bot Acta. 106 223 227 https://doi.org/10.1111/j.1438-8677.1993.tb00744.x

    • Search Google Scholar
    • Export Citation
  • BassiriRad, H, Radin, JW & Matsuda, K. 1991 Temperature-dependent water and ion transport properties of barley and sorghum roots - I. Relationship to leaf growth Plant Physiol. 97 426 432 https://doi.org/10.1104/pp.97.1.426

    • Search Google Scholar
    • Export Citation
  • Bates, LS, Waldren, RP & Teare, ID. 1973 Rapid determination of free proline for water-stress studies Plant Soil. 39 205 207 https://doi.org/10.1007/bf00018060

    • Search Google Scholar
    • Export Citation
  • Ben Rejeb, K, Abdelly, C & Savouré, A. 2014 How reactive oxygen species and proline face stress together Plant Physiol Biochem. 80 278 284 https://doi.org/10.1016/j.plaphy.2014.04.007

    • Search Google Scholar
    • Export Citation
  • Berry, J & Bjorkman, O. 1980 Photosynthetic response and adaptation to temperature in higher plants Annu Rev Plant Physiol. 31 491 543 https://doi.org/10.1146/annurev.pp.31.060180.002423

    • Search Google Scholar
    • Export Citation
  • Brüggemann, W, Klaucke, S & Maas-Kantel, K. 1994 Long-term chilling of young tomato plants under low light—V. Kinetic and molecular properties of two key enzymes of the Calvin cycle in Lycopersicon esculentum Mill. and L. peruvianum Mill Planta. 194 160 168 https://doi.org/10.2307/23383000

    • Search Google Scholar
    • Export Citation
  • Calatayud, Á, Gorbe, E, Roca, D & Martínezet, PF. 2008 Effect of two nutrient solution temperatures on nitrate uptake, nitrate reductase activity, NH4 + concentration and chlorophyll a fluorescence in rose plants Environ Exp Bot. 64 65 74 https://doi.org/10.1016/j.envexpbot.2008.02.003

    • Search Google Scholar
    • Export Citation
  • Chawla, S, Jain, S & Jain, V. 2013 Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.) J Plant Biochem Biotechnol. 22 27 34 https://doi.org/10.1007/s13562-012-0107-4

    • Search Google Scholar
    • Export Citation
  • Chen, C & Dickman, MB. 2005 Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii Proc Natl Acad Sci USA. 102 3459 3464 https://doi.org/10.1073/pnas.0407960102

    • Search Google Scholar
    • Export Citation
  • Chen, HY, Chen, XL, Chen, D, Li, JF, Zhang, Y & Wang, AX. 2015 A comparison of the low temperature transcriptomes of two tomato genotypes that differ in freezing tolerance: Solanum lycopersicum and Solanum habrochaites BMC Plant Biol. 15 1 16 https://doi.org/10.1186/s12870-015-0521-6

    • Search Google Scholar
    • Export Citation
  • Demmig-Adams, B & Adams, WW. 2006 Photoprotection in an ecological context: The remarkable complexity of thermal energy dissipation New Phytol. 172 11 21 https://doi.org/10.111/j.1469-8137.2006.01835.x

    • Search Google Scholar
    • Export Citation
  • Domisch, T, Finér, L & Lehto, T. 2001 Effects of soil temperature on biomass and carbohydrate allocation in Scots pine (Pinus sylvestris) seedlings at the beginning of the growing season Tree Physiol. 21 465 472 https://doi.org/10.1093/treephys/21.7.465

    • Search Google Scholar
    • Export Citation
  • Xiao, F, Yang, ZQ & Zhua, LY. 2018 Low temperature and weak light affect greenhouse tomato growth and fruit quality J Plant Sci. 6 16 24 https://doi.org/10.11648/J.JPS.20180601.14

    • Search Google Scholar
    • Export Citation
  • Farquhar, GD & Sharkey, TD. 1982 Stomatal conductance and photosynthesis Annu Rev Plant Physiol. 33 317 345 https://doi.org/10.1146/annurev.pp.33.060182.001533

    • Search Google Scholar
    • Export Citation
  • Foolad, MR & Lin, GY. 2000 Relationship between cold tolerance during seed germination and vegetative growth in tomato: Germplasm evaluation J Amer Soc Hort Sci. 125 679 683 https://doi.org/10.1023/A:1008766707266

    • Search Google Scholar
    • Export Citation
  • Franco, JA, Bañón, S, Vicente, MJ, Miralles, J & Martínez-Sánchez, JJ. 2011 Root development in horticultural plants grown under abiotic stress conditions—A review J Hortic Sci Biotechnol. 86 543 556 https://doi.org/10.1080/14620316.2011.11512802

    • Search Google Scholar
    • Export Citation
  • Gai, ZJ, Zhang, JT & Li, CF. 2017 Effects of starter nitrogen fertilizer on soybean root activity, leaf photosynthesis and grain yield PLoS One. 12 1 15 https://doi.org/10.2991/ifeesm-17.2018.165

    • Search Google Scholar
    • Export Citation
  • Gill, SS & Tuteja, N. 2010 Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants Plant Physiol Biochem. 48 909 930 https://doi.org/10.1016/j.plaphy.2010.08.016

    • Search Google Scholar
    • Export Citation
  • Göbel, L, Coners, H, Hertel, D, Willinghfer, S & Leuschner, S. 2019 The role of low soil temperature for photosynthesis and stomatal conductance of three graminoids from different elevations Front. Plant Sci. 10 330 https://doi.org/10.3389/fpls.2019.00330

    • Search Google Scholar
    • Export Citation
  • Gonzalez-Fuentes, JA, Shackel, K, Heinrich Lieth, J, Albornoz, F, Benavides-Mendoza, A & Evans, R. 2016 Diurnal root zone temperature variations affect strawberry water relations, growth, and fruit quality Scientia Hort. 203 169 177 https://doi.org/10.1016/j.scienta.2016.03.039

    • Search Google Scholar
    • Export Citation
  • Hare, PD & Cress, WA. 1997 Metabolic implications of stress-induced proline accumulation in plants Plant Growth Regulat. 21 79 102 https://doi.org/1023/A:1005703923347

    • Search Google Scholar
    • Export Citation
  • He, J, Xin, ES, Lin, Q & Choong, TW. 2016 Effects of root-zone temperature on photosynthesis, productivity and nutritional quality of aeroponically grown salad rocket (Eruca sativa) vegetable Am J Plant Sci. 07 1993 2005 https://doi.org/10.4236/ajps.2016.714181

    • Search Google Scholar
    • Export Citation
  • He, Y, Yang, J, Zhu, B & Zhu, ZJ. 2014 Low root zone temperature exacerbates the ion imbalance and photosynthesis inhibition and induces antioxidant responses in tomato plants under salinity J Integr Agr. 13 89 99 https://doi.org/10.1016/S2095-3119(13)60586-9

    • Search Google Scholar
    • Export Citation
  • Hodges, DM, DeLong, JM, Forney, CF & Prange, RK. 1999 Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds Planta. 207 604 611 http://link.springer.com/article/10.1007/s004250050524

    • Search Google Scholar
    • Export Citation
  • Hoque, A, Nasrin, M, Banu, A, Okuma, E, Amako, K, Makamura, Y, Shimoishi, Y & Murata, Y. 2007 Exogenous proline and glycinebetaine increase NaCl-induced ascorbate–glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells J Plant Physiol. 164 11 1457 1468 https://doi.org/10.1016/j.jplph.2006.10.004

    • Search Google Scholar
    • Export Citation
  • Janmohammadi, M, Zolla, L & Rinalducci, S. 2015 Low temperature tolerance in plants: Changes at the protein level Phytochemistry. 117 76 89 https://doi.org/10.1016/j.phytochem.2015.06.003

    • Search Google Scholar
    • Export Citation
  • Kampfenkel, K, Vanmontagu, M & Inzé, D. 1995 Extraction and determination of ascorbate and dehydroascorbate from plant tissue Anal Biochem. 225 165 167 https://doi.org/10.1006/abio.1995.1127

    • Search Google Scholar
    • Export Citation
  • Kawasaki, Y, Matsuo, S, Suzuki, K, Kanayama, Y & Kanahama, K. 2013 Root-zone cooling at high air temperatures enhances physiological activities and internal structures of roots in young tomato plants J Jpn Soc Hortic Sci. 82 322 327 https://doi.org/10.2503/jjshs1.82.322

    • Search Google Scholar
    • Export Citation
  • Krause, GH & Weis, E. 1991 Chlorophyll fluorescence and photosynthesis: The basics Annu Rev Plant Physiol Plant Mol Biol. 42 313 349 https://doi.org/10.1146/annurev.pp.42.060191.001525

    • Search Google Scholar
    • Export Citation
  • Kuwagata, T, Ishikawa-Sakurai, J, Hayashi, H, Nagasuga, K, Fukushi, K, Ahamed, A, Takasugi, K, Katsuhara, M & Murai-Hatano, M. 2012 Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants Plant Cell Physiol. 53 1418 1431 https://doi.org/10.1093/pcp/pcs087

    • Search Google Scholar
    • Export Citation
  • Lee, SH, Singh, AP, Chung, GC, Ahn, SJ, Noh, EK & Steudle, E. 2004 Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport of nutrients Physiol Plant. 120 413 420 https://doi.org/10.1111/j.0031-9317.2004.00248.x

    • Search Google Scholar
    • Export Citation
  • Li, LJ, Lu, XC, Ma, HY & Lyu, DG. 2018 Comparative proteomic analysis reveals the roots response to low root-zone temperature in Malus baccata J Plant Res. 131 5 865 878 https://doi.org/10.1007/s10265-018-1045-6

    • Search Google Scholar
    • Export Citation
  • Liu, YF, Qi, MF & Li, TL. 2012 Photosynthesis, photoinhibition, and antioxidant system in tomato leaves stressed by low night temperature and their subsequent recovery Plant Sci. 196 8 17 https://doi.org/10.1016/j.plantsci.2012.07.005

    • Search Google Scholar
    • Export Citation
  • Luo, HH, Zhang, YL & Zhang, WF. 2016 Effects of water stress and rewatering on photosynthesis, root activity, and yield of cotton with drip irrigation under mulch Photosynthetica. 54 65 73 https://doi.org/10.1007/s11099-015-0165-7

    • Search Google Scholar
    • Export Citation
  • Luo, HYJ, He, J & Lee, SK. 2012 Interaction between potassium concentration and root-zone temperature on growth and photosynthesis of temperate lettuce grown in the tropics J Plant Nutr. 35 1004 1021 https://doi.org/10.1080/01904167.2012.671404

    • Search Google Scholar
    • Export Citation
  • Lyons, JM. 1973 Chilling injury in plants Annu Rev Plant Physiol. 24 445 466 https://doi.org/10.1146/annurev.pp.24.060173.002305

  • Makino, A, Nakano, H & Mae, T. 1994 Effects of growth temperature on the responses of ribulose-1,5-biphosphate carboxylase, electron transport components, and sucrose synthesis enzymes to leaf nitrogen in rice, and their relationships to photosynthesis Plant Physiol. 105 1231 1238 https://doi.org/10.1104/pp.105.4.1209

    • Search Google Scholar
    • Export Citation
  • Malcolm, P, Holford, P, McGlasson, B & Barchia, I. 2008 Leaf development, net assimilation and leaf nitrogen concentrations of five Prunus rootstocks in response to root temperature Scientia Hort. 115 285 291 https://doi.org/10.1016/j.scienta.2007.10.010

    • Search Google Scholar
    • Export Citation
  • Mastropasqua, L, Borraccino, G, Bianco, L & Paciolla, C. 2012 Light qualities and dose influence ascorbate pool size in detached oat leaves Plant Sci. 183 57 64 https://doi.org/10.1016/j.plantsci.2011.11.009

    • Search Google Scholar
    • Export Citation
  • Maurel, C, Verdoucq, L & Luu, D. 2008 Plant aquaporins: Membrane channels with multiple integrated functions Annu. Rev. Plant Biol. 59 595 624 https://doi.org/10.1146/annurev.arplant.59.032607.092734

    • Search Google Scholar
    • Export Citation
  • McWilliam, JR, Kramer, PJ & Musser, RL. 1982 Temperature-induced water stress in chilling-sensitive plants Aust J Plant Physiol. 9 343 352 https://doi.org/10.1071/PP9820343

    • Search Google Scholar
    • Export Citation
  • Meena, YK, Khurana, DS, Kaur, N & Singh, K. 2017 Phenolic compounds enhanced low temperature stress tolerance in tomato (Solanum lycopersicum L.) Br J Appl Sci Technol. 20 3 1 9 https://doi.org/10.9734/BJAST/2017/32889

    • Search Google Scholar
    • Export Citation
  • Mirza, H, Borhannuddin Bhuyan, MHM, Zulfiqar, F, Ali, R, Mohammad Mohsin, S, Al Mahmud, J, Masayuki, F & Fotopoulos, V. 2020 Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator Antioxidants (Basel). 9 8 681 https://doi.org/10.3390/antiox9080681

    • Search Google Scholar
    • Export Citation
  • Murai-Hatano, M, Kuwagata, T, Sakurai, J, Nonami, H, Ahamed, A, Nagasuga, K, Matsunam, T, Fukushi, K, Maeshima, M & Okada, M. 2008 Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins Plant Cell Physiol. 49 1294 1305 https://doi.org/10.1093/pcp/pcn104

    • Search Google Scholar
    • Export Citation
  • Ozfidan, C, Turkan, I, Sekmen, AH & Seckin, B. 2012 Abscisic acid-regulated responses of aba2-1 under osmotic stress: The abscisic acid-inducible antioxidant defence system and reactive oxygen species production Plant Biol. 14 337 346 https://doi.org/10.1111/j.1438-8677.2011.00496.x

    • Search Google Scholar
    • Export Citation
  • Pinheiro, C & Chaves, MM. 2011 Photosynthesis and drought: Can we make metabolic connections from available data? J Expt Bot. 62 869 882 https://doi.org/10.1093/aob/mcs29810.1093/jxb/erq340

    • Search Google Scholar
    • Export Citation
  • Poiré, R, Schneider, H, Thorpe, MR, Kuhn, AJ, Schurr, U & Walter, A. 2010 Root cooling strongly affects diel leaf growth dynamics, water and carbohydrate relations in Ricinus communis Plant Cell Environ. 33 408 417 https://doi.org/10.1093/aob/mcs29810.1111/j.1365-3040.2009.02090.x

    • Search Google Scholar
    • Export Citation
  • Posmyk, MM, Bailly, C, Szafrańska, K, Janas, KM & Corbineau, F. 2005 Antioxidant enzymes and isoflavonoids in chilled soybean [Glycine max (L.) Merr.] seedlings J Plant Physiol. 162 403 412 https://doi.org/10.1016/j.jplph.2004.08.004

    • Search Google Scholar
    • Export Citation
  • Pritchard, J, Barlow, PW, Adam, JS & Tomos, AD. 1990 Biophysics of the inhibition of the growth of maize roots by lowered temperature Plant Physiol. 93 222 230 https://doi.org/10.1093/aob/mcs29810.1104/pp.93.1.222

    • Search Google Scholar
    • Export Citation
  • Raines, CA. 2011 Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: Current and future strategies Plant Physiol. 155 36 42 https://doi.org/10.1093/aob/mcs29810.1104/PP.110.168559

    • Search Google Scholar
    • Export Citation
  • Reyes, E & Jennings, PH. 1994 Response of cucumber (Cucumis sativus L.) and squash (Cucurbita pepo L. var. melopepo) roots to chilling stress during early stages of seedling development J Amer Soc Hort Sci. 119 964 970 https://doi.org/10.1007/BF01876243

    • Search Google Scholar
    • Export Citation
  • Rogiers, SY & Clarke, SJ. 2013 Nocturnal and daytime stomatal conductance respond to root-zone temperature in ‘Shiraz’ grapevines Ann Bot. 111 433 444 https://doi.org/10.1093/aob/mcs298

    • Search Google Scholar
    • Export Citation
  • Sairam, RK & Srivastava, GC. 2002 Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress Plant Sci. 162 897 904 https://doi.org/10.1016/S0168-9452(02)00037-7

    • Search Google Scholar
    • Export Citation
  • Sales, CRG, Ribeiro, RV, Silveira, JAG, Machado, C, Martins, MO & Lagôa, AMMA. 2013 Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature Plant Physiol Biochem. 73 326 336 https://doi.org/10.1016/j.plaphy.2013.10.012

    • Search Google Scholar
    • Export Citation
  • Santos, CMA, Ribeiro, RV, Magalhães Filho, JR, Machado, DFSP & Machado, EC. 2011 Low substrate temperature imposes higher limitation to photosynthesis of orange plants as compared to atmospheric chilling Photosynthetica. 49 546 554 https://doi.org/10.1007/s11099-0071-6

    • Search Google Scholar
    • Export Citation
  • Shimono, H, Hasegawa, T & Iwama, K. 2002 Response of growth and grain yield in paddy rice to cool water at different growth stages F. Crop. Res. 73 67 79 https://doi.org/10.1016/S0378-4290(01)00184-8

    • Search Google Scholar
    • Export Citation
  • Stasik, O & Jones, HG. 2007 Response of photosynthetic apparatus to moderate high temperature in contrasting wheat cultivars at different oxygen concentrations J Expt Bot. 58 2133 2143 https://doi.org/10.1093/jxb/erm067

    • Search Google Scholar
    • Export Citation
  • Stoltzfus, RMB, Taber, HG & Aiello, AS. 1998 Effect of increasing root-zone temperature on growth and nutrient uptake by ‘Gold Star’ muskmelon plants 1 J Plant Nutr. 21 321 328 https://doi.org/10.1080/01904169809365406

    • Search Google Scholar
    • Export Citation
  • Strasser, RJ, Tsimilli-Michael, M & Srivastava, A. 2004 Analysis of the chlorophyll a fluorescence transient. Chlorophyll a Fluoresc 321 362 Papageorgiou, GC & Govindjee Chlorophyll a fluorescence. advances in photosynthesis and respiration vol 19 Springer Dordrecht https://doi.org/10.1007/978-1-4020-3218-9_12

    • Search Google Scholar
    • Export Citation
  • Sun, J, Lu, N, Xu, HJ, Maruo, T & Guo, SR. 2016 Root zone cooling and exogenous spermidine root-pretreatment promoting Lactuca sativa L. Growth and photosynthesis in the high-temperature season Front. Plant Sci. 7 1 14 https://doi.org/10.3389/fpls.2016.00368

    • Search Google Scholar
    • Export Citation
  • Szarka, A, Tomasskovics, B & Bánhegyi, G. 2012 The ascorbate-glutathione-α-tocopherol triad in abiotic stress response Int J Mol Sci. 13 4458 4483 https://doi.org/10.3390/ijms13044458

    • Search Google Scholar
    • Export Citation
  • Wan, X, Landhäusser, SM, Zwiazek, JJ & Lieffers, V. 2004 Stomatal conductance and xylem sap properties of aspen (Populus tremuloides) in response to low soil temperature Physiol Plant. 122 79 85 https://doi.org/10.1111/j.1399-3054.2004.00385.x

    • Search Google Scholar
    • Export Citation
  • Wang, XZ, Zhang, WH, Miao, YX & Gao, LH. 2016 Root-zone warming differently benefits mature and newly unfolded leaves of Cucumis sativus L. seedlings under sub-optimal temperature stress PLoS One. 11 1 20 https://doi.org/10.1371/journal.pone.0155298

    • Search Google Scholar
    • Export Citation
  • Xu, Q & Huang, BR. 2000 Effects of differential air and soil temperature on carbohydrate metabolism in creeping bentgrass Crop Sci. 40 1368 1374 https://doi.org/10.2135/cropsci2000.4051368x

    • Search Google Scholar
    • Export Citation
  • Yan, QY, Duan, ZQ, Mao, JD, Li, X & Dong, F. 2012 Effects of root-zone temperature and N, P, and K supplies on nutrient uptake of cucumber (Cucumis sativus L.) seedlings in hydroponics Soil Sci Plant Nutr. 58 707 717 https://doi.org/10.1080/00380768.2012.733925

    • Search Google Scholar
    • Export Citation
  • Yan, QY, Duan, ZQ, Mao, JD, Li, X & Dong, F. 2013 Low root zone temperature limits nutrient effects on cucumber seedling growth and induces adversity physiological response J Integr Agric. 12 1450 1460 https://doi.org/10.1016/S2095-3119(13)60549-3

    • Search Google Scholar
    • Export Citation
  • Zheng, L, Steppe, K & Van Labeke, MC. 2020 Spectral quality of monochromatic LED affects photosynthetic acclimation to high-intensity sunlight of Chrysanthemum and Spathiphyllum Physiol Plant. 169 10 26 https://doi.org/10.1111/ppl.13067

    • Search Google Scholar
    • Export Citation
  • Zhu, J, Zhang, KX, Wang, WS, Gong, W, Liu, WC, Chen, HG, Xu, HH & Lu, YT. 2015 Low temperature inhibits root growth by reducing auxin accumulation via ARR1/12 Plant Cell Physiol. 56 727 736 https://doi.org/10.1093/pcp/pcu217

    • Search Google Scholar
    • Export Citation
  • Zushi, K, Kajiwara, S & Matsuzoe, N. 2012 Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit Scientia Hort. 148 39 46 https://doi.org/10.1016/j.scienta.2012.09.022

    • Search Google Scholar
    • Export Citation
  • Fig. 1.

    Effect of temperature at 10 °C, 20 °C (stage 1), and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on the plant height (A), stem diameter (B), dry weight (DM, C), and total leaf area (D) in the leaves of tomato plants. Data are presented as mean values ± SE (n = 4). Different letters indicate significant differences between values (P < 0.05) according to Tukey’s highly significant difference test. *P < 0.05; ***P < 0.001; ns, not significant according to independent sample t test.

  • Fig. 2.

    Effect of temperature at 10 °C, 20 °C (stage 1). and 10–10 °C, 10–20 °C, 20–10 °C, 20–20 °C (stage 2) on net photosynthetic rate (PN, A), stomatal conductance (gS, B), intercellular CO2 concentration (Ci, C), and transpiration rate (Tr, D) in the leaves of tomato plants. Data are presented as mean values ± SE (n = 4). Different letters indicate significant differences between values (P < 0.05) according to Tukey’s highly significant difference test. **P < 0.01; ***P < 0.001 according to independent sample t test.

  • Ahn, SJ, Im, YJ, Chung, GC, Cho, BH & Suh, SR. 1999 Physiological responses of grafted-cucumber leaves and rootstock roots affected by low root temperature Scientia Hort. 81 4 397 408 https://doi.org/10.1016/S0304-4238(99)00042-4

    • Search Google Scholar
    • Export Citation
  • Al-Khafaf, S, Aziz, FG, Salih, HM & Jack, FJ. 1989 Shoot and root growth and nutrients uptake of wheat as affected by soil layers Plant Soil. 117 59 66 https://doi.org/10.1007/BF02206257

    • Search Google Scholar
    • Export Citation
  • Anwar, A, Li, YS, He, CX & Yu, XC. 2019 24-Epibrassinolide promotes NO3 and NH4 + ion flux rate and NRT1 gene expression in cucumber under suboptimal root zone temperature BMC Plant Biol. 19 225 https://doi.org/10.1186/s12870-019-1838-3

    • Search Google Scholar
    • Export Citation
  • Arai-Sanoh, Y, Ishimaru, T, Ohsumi, A & Kondo, M. 2010 Effects of Soil Temperature on Growth and Root Function in Rice Plant Prod Sci. 13 235 242 https://doi.org/10.1626/pps.13.235

    • Search Google Scholar
    • Export Citation
  • BassiriRad, H, Caldwell, MM & Mott, KA. 1993 Effect of root cooling on photosynthesis of Artemisia tridentata seedlings under different light levels Bot Acta. 106 223 227 https://doi.org/10.1111/j.1438-8677.1993.tb00744.x

    • Search Google Scholar
    • Export Citation
  • BassiriRad, H, Radin, JW & Matsuda, K. 1991 Temperature-dependent water and ion transport properties of barley and sorghum roots - I. Relationship to leaf growth Plant Physiol. 97 426 432 https://doi.org/10.1104/pp.97.1.426

    • Search Google Scholar
    • Export Citation
  • Bates, LS, Waldren, RP & Teare, ID. 1973 Rapid determination of free proline for water-stress studies Plant Soil. 39 205 207 https://doi.org/10.1007/bf00018060

    • Search Google Scholar
    • Export Citation
  • Ben Rejeb, K, Abdelly, C & Savouré, A. 2014 How reactive oxygen species and proline face stress together Plant Physiol Biochem. 80 278 284 https://doi.org/10.1016/j.plaphy.2014.04.007

    • Search Google Scholar
    • Export Citation
  • Berry, J & Bjorkman, O. 1980 Photosynthetic response and adaptation to temperature in higher plants Annu Rev Plant Physiol. 31 491 543 https://doi.org/10.1146/annurev.pp.31.060180.002423

    • Search Google Scholar
    • Export Citation
  • Brüggemann, W, Klaucke, S & Maas-Kantel, K. 1994 Long-term chilling of young tomato plants under low light—V. Kinetic and molecular properties of two key enzymes of the Calvin cycle in Lycopersicon esculentum Mill. and L. peruvianum Mill Planta. 194 160 168 https://doi.org/10.2307/23383000

    • Search Google Scholar
    • Export Citation
  • Calatayud, Á, Gorbe, E, Roca, D & Martínezet, PF. 2008 Effect of two nutrient solution temperatures on nitrate uptake, nitrate reductase activity, NH4 + concentration and chlorophyll a fluorescence in rose plants Environ Exp Bot. 64 65 74 https://doi.org/10.1016/j.envexpbot.2008.02.003

    • Search Google Scholar
    • Export Citation
  • Chawla, S, Jain, S & Jain, V. 2013 Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.) J Plant Biochem Biotechnol. 22 27 34 https://doi.org/10.1007/s13562-012-0107-4

    • Search Google Scholar
    • Export Citation
  • Chen, C & Dickman, MB. 2005 Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii Proc Natl Acad Sci USA. 102 3459 3464 https://doi.org/10.1073/pnas.0407960102

    • Search Google Scholar
    • Export Citation
  • Chen, HY, Chen, XL, Chen, D, Li, JF, Zhang, Y & Wang, AX. 2015 A comparison of the low temperature transcriptomes of two tomato genotypes that differ in freezing tolerance: Solanum lycopersicum and Solanum habrochaites BMC Plant Biol. 15 1 16 https://doi.org/10.1186/s12870-015-0521-6

    • Search Google Scholar
    • Export Citation
  • Demmig-Adams, B & Adams, WW. 2006 Photoprotection in an ecological context: The remarkable complexity of thermal energy dissipation New Phytol. 172 11 21 https://doi.org/10.111/j.1469-8137.2006.01835.x

    • Search Google Scholar
    • Export Citation
  • Domisch, T, Finér, L & Lehto, T. 2001 Effects of soil temperature on biomass and carbohydrate allocation in Scots pine (Pinus sylvestris) seedlings at the beginning of the growing season Tree Physiol. 21 465 472 https://doi.org/10.1093/treephys/21.7.465

    • Search Google Scholar
    • Export Citation
  • Xiao, F, Yang, ZQ & Zhua, LY. 2018 Low temperature and weak light affect greenhouse tomato growth and fruit quality J Plant Sci. 6 16 24 https://doi.org/10.11648/J.JPS.20180601.14

    • Search Google Scholar
    • Export Citation
  • Farquhar, GD & Sharkey, TD. 1982 Stomatal conductance and photosynthesis Annu Rev Plant Physiol. 33 317 345 https://doi.org/10.1146/annurev.pp.33.060182.001533

    • Search Google Scholar
    • Export Citation
  • Foolad, MR & Lin, GY. 2000 Relationship between cold tolerance during seed germination and vegetative growth in tomato: Germplasm evaluation J Amer Soc Hort Sci. 125 679 683 https://doi.org/10.1023/A:1008766707266

    • Search Google Scholar
    • Export Citation
  • Franco, JA, Bañón, S, Vicente, MJ, Miralles, J & Martínez-Sánchez, JJ. 2011 Root development in horticultural plants grown under abiotic stress conditions—A review J Hortic Sci Biotechnol. 86 543 556 https://doi.org/10.1080/14620316.2011.11512802

    • Search Google Scholar
    • Export Citation
  • Gai, ZJ, Zhang, JT & Li, CF. 2017 Effects of starter nitrogen fertilizer on soybean root activity, leaf photosynthesis and grain yield PLoS One. 12 1 15 https://doi.org/10.2991/ifeesm-17.2018.165

    • Search Google Scholar
    • Export Citation
  • Gill, SS & Tuteja, N. 2010 Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants Plant Physiol Biochem. 48 909 930 https://doi.org/10.1016/j.plaphy.2010.08.016

    • Search Google Scholar
    • Export Citation
  • Göbel, L, Coners, H, Hertel, D, Willinghfer, S & Leuschner, S. 2019 The role of low soil temperature for photosynthesis and stomatal conductance of three graminoids from different elevations Front. Plant Sci. 10 330 https://doi.org/10.3389/fpls.2019.00330

    • Search Google Scholar
    • Export Citation
  • Gonzalez-Fuentes, JA, Shackel, K, Heinrich Lieth, J, Albornoz, F, Benavides-Mendoza, A & Evans, R. 2016 Diurnal root zone temperature variations affect strawberry water relations, growth, and fruit quality Scientia Hort. 203 169 177 https://doi.org/10.1016/j.scienta.2016.03.039

    • Search Google Scholar
    • Export Citation
  • Hare, PD & Cress, WA. 1997 Metabolic implications of stress-induced proline accumulation in plants Plant Growth Regulat. 21 79 102 https://doi.org/1023/A:1005703923347

    • Search Google Scholar
    • Export Citation
  • He, J, Xin, ES, Lin, Q & Choong, TW. 2016 Effects of root-zone temperature on photosynthesis, productivity and nutritional quality of aeroponically grown salad rocket (Eruca sativa) vegetable Am J Plant Sci. 07 1993 2005 https://doi.org/10.4236/ajps.2016.714181

    • Search Google Scholar
    • Export Citation
  • He, Y, Yang, J, Zhu, B & Zhu, ZJ. 2014 Low root zone temperature exacerbates the ion imbalance and photosynthesis inhibition and induces antioxidant responses in tomato plants under salinity J Integr Agr. 13 89 99 https://doi.org/10.1016/S2095-3119(13)60586-9

    • Search Google Scholar
    • Export Citation
  • Hodges, DM, DeLong, JM, Forney, CF & Prange, RK. 1999 Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds Planta. 207 604 611 http://link.springer.com/article/10.1007/s004250050524

    • Search Google Scholar
    • Export Citation
  • Hoque, A, Nasrin, M, Banu, A, Okuma, E, Amako, K, Makamura, Y, Shimoishi, Y & Murata, Y. 2007 Exogenous proline and glycinebetaine increase NaCl-induced ascorbate–glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells J Plant Physiol. 164 11 1457 1468 https://doi.org/10.1016/j.jplph.2006.10.004

    • Search Google Scholar
    • Export Citation
  • Janmohammadi, M, Zolla, L & Rinalducci, S. 2015 Low temperature tolerance in plants: Changes at the protein level Phytochemistry. 117 76 89 https://doi.org/10.1016/j.phytochem.2015.06.003

    • Search Google Scholar
    • Export Citation
  • Kampfenkel, K, Vanmontagu, M & Inzé, D. 1995 Extraction and determination of ascorbate and dehydroascorbate from plant tissue Anal Biochem. 225 165 167 https://doi.org/10.1006/abio.1995.1127

    • Search Google Scholar
    • Export Citation
  • Kawasaki, Y, Matsuo, S, Suzuki, K, Kanayama, Y & Kanahama, K. 2013 Root-zone cooling at high air temperatures enhances physiological activities and internal structures of roots in young tomato plants J Jpn Soc Hortic Sci. 82 322 327 https://doi.org/10.2503/jjshs1.82.322

    • Search Google Scholar
    • Export Citation
  • Krause, GH & Weis, E. 1991 Chlorophyll fluorescence and photosynthesis: The basics Annu Rev Plant Physiol Plant Mol Biol. 42 313 349 https://doi.org/10.1146/annurev.pp.42.060191.001525

    • Search Google Scholar
    • Export Citation
  • Kuwagata, T, Ishikawa-Sakurai, J, Hayashi, H, Nagasuga, K, Fukushi, K, Ahamed, A, Takasugi, K, Katsuhara, M & Murai-Hatano, M. 2012 Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants Plant Cell Physiol. 53 1418 1431 https://doi.org/10.1093/pcp/pcs087

    • Search Google Scholar
    • Export Citation
  • Lee, SH, Singh, AP, Chung, GC, Ahn, SJ, Noh, EK & Steudle, E. 2004 Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport of nutrients Physiol Plant. 120 413 420 https://doi.org/10.1111/j.0031-9317.2004.00248.x

    • Search Google Scholar
    • Export Citation
  • Li, LJ, Lu, XC, Ma, HY & Lyu, DG. 2018 Comparative proteomic analysis reveals the roots response to low root-zone temperature in Malus baccata J Plant Res. 131 5 865 878 https://doi.org/10.1007/s10265-018-1045-6

    • Search Google Scholar
    • Export Citation
  • Liu, YF, Qi, MF & Li, TL. 2012 Photosynthesis, photoinhibition, and antioxidant system in tomato leaves stressed by low night temperature and their subsequent recovery Plant Sci. 196 8 17 https://doi.org/10.1016/j.plantsci.2012.07.005

    • Search Google Scholar
    • Export Citation
  • Luo, HH, Zhang, YL & Zhang, WF. 2016 Effects of water stress and rewatering on photosynthesis, root activity, and yield of cotton with drip irrigation under mulch Photosynthetica. 54 65 73 https://doi.org/10.1007/s11099-015-0165-7

    • Search Google Scholar
    • Export Citation
  • Luo, HYJ, He, J & Lee, SK. 2012 Interaction between potassium concentration and root-zone temperature on growth and photosynthesis of temperate lettuce grown in the tropics J Plant Nutr. 35 1004 1021 https://doi.org/10.1080/01904167.2012.671404

    • Search Google Scholar
    • Export Citation
  • Lyons, JM. 1973 Chilling injury in plants Annu Rev Plant Physiol. 24 445 466 https://doi.org/10.1146/annurev.pp.24.060173.002305

  • Makino, A, Nakano, H & Mae, T. 1994 Effects of growth temperature on the responses of ribulose-1,5-biphosphate carboxylase, electron transport components, and sucrose synthesis enzymes to leaf nitrogen in rice, and their relationships to photosynthesis Plant Physiol. 105 1231 1238 https://doi.org/10.1104/pp.105.4.1209

    • Search Google Scholar
    • Export Citation
  • Malcolm, P, Holford, P, McGlasson, B & Barchia, I. 2008 Leaf development, net assimilation and leaf nitrogen concentrations of five Prunus rootstocks in response to root temperature Scientia Hort. 115 285 291 https://doi.org/10.1016/j.scienta.2007.10.010

    • Search Google Scholar
    • Export Citation
  • Mastropasqua, L, Borraccino, G, Bianco, L & Paciolla, C. 2012 Light qualities and dose influence ascorbate pool size in detached oat leaves Plant Sci. 183 57 64 https://doi.org/10.1016/j.plantsci.2011.11.009

    • Search Google Scholar
    • Export Citation
  • Maurel, C, Verdoucq, L & Luu, D. 2008 Plant aquaporins: Membrane channels with multiple integrated functions Annu. Rev. Plant Biol. 59 595 624 https://doi.org/10.1146/annurev.arplant.59.032607.092734

    • Search Google Scholar
    • Export Citation
  • McWilliam, JR, Kramer, PJ & Musser, RL. 1982 Temperature-induced water stress in chilling-sensitive plants Aust J Plant Physiol. 9 343 352 https://doi.org/10.1071/PP9820343

    • Search Google Scholar
    • Export Citation
  • Meena, YK, Khurana, DS, Kaur, N & Singh, K. 2017 Phenolic compounds enhanced low temperature stress tolerance in tomato (Solanum lycopersicum L.) Br J Appl Sci Technol. 20 3 1 9 https://doi.org/10.9734/BJAST/2017/32889

    • Search Google Scholar
    • Export Citation
  • Mirza, H, Borhannuddin Bhuyan, MHM, Zulfiqar, F, Ali, R, Mohammad Mohsin, S, Al Mahmud, J, Masayuki, F & Fotopoulos, V. 2020 Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator Antioxidants (Basel). 9 8 681 https://doi.org/10.3390/antiox9080681

    • Search Google Scholar
    • Export Citation
  • Murai-Hatano, M, Kuwagata, T, Sakurai, J, Nonami, H, Ahamed, A, Nagasuga, K, Matsunam, T, Fukushi, K, Maeshima, M & Okada, M. 2008 Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins Plant Cell Physiol. 49 1294 1305 https://doi.org/10.1093/pcp/pcn104

    • Search Google Scholar
    • Export Citation
  • Ozfidan, C, Turkan, I, Sekmen, AH & Seckin, B. 2012 Abscisic acid-regulated responses of aba2-1 under osmotic stress: The abscisic acid-inducible antioxidant defence system and reactive oxygen species production Plant Biol. 14 337 346 https://doi.org/10.1111/j.1438-8677.2011.00496.x

    • Search Google Scholar
    • Export Citation
  • Pinheiro, C & Chaves, MM. 2011 Photosynthesis and drought: Can we make metabolic connections from available data? J Expt Bot. 62 869 882 https://doi.org/10.1093/aob/mcs29810.1093/jxb/erq340

    • Search Google Scholar
    • Export Citation
  • Poiré, R, Schneider, H, Thorpe, MR, Kuhn, AJ, Schurr, U & Walter, A. 2010 Root cooling strongly affects diel leaf growth dynamics, water and carbohydrate relations in Ricinus communis Plant Cell Environ. 33 408 417 https://doi.org/10.1093/aob/mcs29810.1111/j.1365-3040.2009.02090.x

    • Search Google Scholar
    • Export Citation
  • Posmyk, MM, Bailly, C, Szafrańska, K, Janas, KM & Corbineau, F. 2005 Antioxidant enzymes and isoflavonoids in chilled soybean [Glycine max (L.) Merr.] seedlings J Plant Physiol. 162 403 412 https://doi.org/10.1016/j.jplph.2004.08.004

    • Search Google Scholar
    • Export Citation
  • Pritchard, J, Barlow, PW, Adam, JS & Tomos, AD. 1990 Biophysics of the inhibition of the growth of maize roots by lowered temperature Plant Physiol. 93 222 230 https://doi.org/10.1093/aob/mcs29810.1104/pp.93.1.222

    • Search Google Scholar
    • Export Citation
  • Raines, CA. 2011 Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: Current and future strategies Plant Physiol. 155 36 42 https://doi.org/10.1093/aob/mcs29810.1104/PP.110.168559

    • Search Google Scholar
    • Export Citation
  • Reyes, E & Jennings, PH. 1994 Response of cucumber (Cucumis sativus L.) and squash (Cucurbita pepo L. var. melopepo) roots to chilling stress during early stages of seedling development J Amer Soc Hort Sci. 119 964 970 https://doi.org/10.1007/BF01876243

    • Search Google Scholar
    • Export Citation
  • Rogiers, SY & Clarke, SJ. 2013 Nocturnal and daytime stomatal conductance respond to root-zone temperature in ‘Shiraz’ grapevines Ann Bot. 111 433 444 https://doi.org/10.1093/aob/mcs298

    • Search Google Scholar
    • Export Citation
  • Sairam, RK & Srivastava, GC. 2002 Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress Plant Sci. 162 897 904 https://doi.org/10.1016/S0168-9452(02)00037-7

    • Search Google Scholar
    • Export Citation
  • Sales, CRG, Ribeiro, RV, Silveira, JAG, Machado, C, Martins, MO & Lagôa, AMMA. 2013 Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature Plant Physiol Biochem. 73 326 336 https://doi.org/10.1016/j.plaphy.2013.10.012

    • Search Google Scholar
    • Export Citation
  • Santos, CMA, Ribeiro, RV, Magalhães Filho, JR, Machado, DFSP & Machado, EC. 2011 Low substrate temperature imposes higher limitation to photosynthesis of orange plants as compared to atmospheric chilling Photosynthetica. 49 546 554 https://doi.org/10.1007/s11099-0071-6

    • Search Google Scholar
    • Export Citation
  • Shimono, H, Hasegawa, T & Iwama, K. 2002 Response of growth and grain yield in paddy rice to cool water at different growth stages F. Crop. Res. 73 67 79 https://doi.org/10.1016/S0378-4290(01)00184-8

    • Search Google Scholar
    • Export Citation
  • Stasik, O & Jones, HG. 2007 Response of photosynthetic apparatus to moderate high temperature in contrasting wheat cultivars at different oxygen concentrations J Expt Bot. 58 2133 2143 https://doi.org/10.1093/jxb/erm067

    • Search Google Scholar
    • Export Citation
  • Stoltzfus, RMB, Taber, HG & Aiello, AS. 1998 Effect of increasing root-zone temperature on growth and nutrient uptake by ‘Gold Star’ muskmelon plants 1 J Plant Nutr. 21 321 328 https://doi.org/10.1080/01904169809365406

    • Search Google Scholar
    • Export Citation
  • Strasser, RJ, Tsimilli-Michael, M & Srivastava, A. 2004 Analysis of the chlorophyll a fluorescence transient. Chlorophyll a Fluoresc 321 362 Papageorgiou, GC & Govindjee Chlorophyll a fluorescence. advances in photosynthesis and respiration vol 19 Springer Dordrecht https://doi.org/10.1007/978-1-4020-3218-9_12

    • Search Google Scholar
    • Export Citation
  • Sun, J, Lu, N, Xu, HJ, Maruo, T & Guo, SR. 2016 Root zone cooling and exogenous spermidine root-pretreatment promoting Lactuca sativa L. Growth and photosynthesis in the high-temperature season Front. Plant Sci. 7 1 14 https://doi.org/10.3389/fpls.2016.00368

    • Search Google Scholar
    • Export Citation
  • Szarka, A, Tomasskovics, B & Bánhegyi, G. 2012 The ascorbate-glutathione-α-tocopherol triad in abiotic stress response Int J Mol Sci. 13 4458 4483 https://doi.org/10.3390/ijms13044458

    • Search Google Scholar
    • Export Citation
  • Wan, X, Landhäusser, SM, Zwiazek, JJ & Lieffers, V. 2004 Stomatal conductance and xylem sap properties of aspen (Populus tremuloides) in response to low soil temperature Physiol Plant. 122 79 85 https://doi.org/10.1111/j.1399-3054.2004.00385.x

    • Search Google Scholar
    • Export Citation
  • Wang, XZ, Zhang, WH, Miao, YX & Gao, LH. 2016 Root-zone warming differently benefits mature and newly unfolded leaves of Cucumis sativus L. seedlings under sub-optimal temperature stress PLoS One. 11 1 20 https://doi.org/10.1371/journal.pone.0155298

    • Search Google Scholar
    • Export Citation
  • Xu, Q & Huang, BR. 2000 Effects of differential air and soil temperature on carbohydrate metabolism in creeping bentgrass Crop Sci. 40 1368 1374 https://doi.org/10.2135/cropsci2000.4051368x

    • Search Google Scholar
    • Export Citation
  • Yan, QY, Duan, ZQ, Mao, JD, Li, X & Dong, F. 2012 Effects of root-zone temperature and N, P, and K supplies on nutrient uptake of cucumber (Cucumis sativus L.) seedlings in hydroponics Soil Sci Plant Nutr. 58 707 717 https://doi.org/10.1080/00380768.2012.733925

    • Search Google Scholar
    • Export Citation
  • Yan, QY, Duan, ZQ, Mao, JD, Li, X & Dong, F. 2013 Low root zone temperature limits nutrient effects on cucumber seedling growth and induces adversity physiological response J Integr Agric. 12 1450 1460 https://doi.org/10.1016/S2095-3119(13)60549-3

    • Search Google Scholar
    • Export Citation
  • Zheng, L, Steppe, K & Van Labeke, MC. 2020 Spectral quality of monochromatic LED affects photosynthetic acclimation to high-intensity sunlight of Chrysanthemum and Spathiphyllum Physiol Plant. 169 10 26 https://doi.org/10.1111/ppl.13067

    • Search Google Scholar
    • Export Citation
  • Zhu, J, Zhang, KX, Wang, WS, Gong, W, Liu, WC, Chen, HG, Xu, HH & Lu, YT. 2015 Low temperature inhibits root growth by reducing auxin accumulation via ARR1/12 Plant Cell Physiol. 56 727 736 https://doi.org/10.1093/pcp/pcu217

    • Search Google Scholar
    • Export Citation
  • Zushi, K, Kajiwara, S & Matsuzoe, N. 2012 Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit Scientia Hort. 148 39 46 https://doi.org/10.1016/j.scienta.2012.09.022

    • Search Google Scholar
    • Export Citation
Han Zhang College of Water Resources and Civil Engineering, China Agriculture University, Beijing, 100083, China

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Xuguang Sun College of Water Resources and Civil Engineering, China Agriculture University, Beijing, 100083, China

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Weitang Song Key Laboratory of Agricultural Engineering in Structure and Environment, Ministry of Agriculture and Rural Affairs, College of Water Resources and Civil Engineering, China Agriculture University, Beijing, 100083, China

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Contributor Notes

W.S. is the corresponding author. E-mail: songchali@cau.edu.cn.

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