Interaction of Supplementary Light and CO2 Enrichment Improves Growth, Photosynthesis, Yield, and Quality of Tomato in Autumn through Spring Greenhouse Production

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  • 1 Key Laboratory of Protected Horticultural Engineering in Northwest, Ministry of Agriculture, Northwest Agriculture and Forest University, Yangling 712100, China; and Research Center of Protected Horticultural Engineering and Technology, College of Horticulture, Northwest Agriculture and Forest University, Yangling 712100, China

During the autumn/spring “off” season, yield and quality of tomatoes are often affected by insufficient CO2 and low light in greenhouse production. Although tomato is one of the most widely cultivated vegetables, few studies have investigated the interactive effects of supplementary light and CO2 enrichment on its growth, photosynthesis, yield, and fruit quality in greenhouse production. This study investigates the effects of supplementary light (200 ± 20 μmol·m–2·s–1) and CO2 enrichment (increases to about 800 μmol·mol–1), independently and in combination, on these parameters in autumn through spring tomato production. Compared with tomatoes grown under ambient CO2 concentrations and no supplementary light (CaLn), supplementary light (CaLs) and supplementary light and CO2 enrichment (CeLs) significantly promoted growth and dry weight accumulation. Meanwhile, CO2 enrichment (CeLn) and CaLs significantly improved photosynthetic pigment contents and net photosynthetic (Pn) rates, whereas CeLs further improved these and also increased water use efficiency (WUE). CeLn, CaLs, and CeLs significantly increased single fruit weight by 16.2%, 28.9%, and 36.6%, and yield per plant by 19.0%, 35.6%, and 60.8%, respectively. The effect of supplementary light on these parameters was superior to that of CO2 enrichment. In addition, CaLs and CeLs improved nutritional quality significantly. Taken together, CeLs promoted the greatest yield, WUE, and fruit quality, suggesting it may be a worthwhile practice for off-season tomato cultivation.

Abstract

During the autumn/spring “off” season, yield and quality of tomatoes are often affected by insufficient CO2 and low light in greenhouse production. Although tomato is one of the most widely cultivated vegetables, few studies have investigated the interactive effects of supplementary light and CO2 enrichment on its growth, photosynthesis, yield, and fruit quality in greenhouse production. This study investigates the effects of supplementary light (200 ± 20 μmol·m–2·s–1) and CO2 enrichment (increases to about 800 μmol·mol–1), independently and in combination, on these parameters in autumn through spring tomato production. Compared with tomatoes grown under ambient CO2 concentrations and no supplementary light (CaLn), supplementary light (CaLs) and supplementary light and CO2 enrichment (CeLs) significantly promoted growth and dry weight accumulation. Meanwhile, CO2 enrichment (CeLn) and CaLs significantly improved photosynthetic pigment contents and net photosynthetic (Pn) rates, whereas CeLs further improved these and also increased water use efficiency (WUE). CeLn, CaLs, and CeLs significantly increased single fruit weight by 16.2%, 28.9%, and 36.6%, and yield per plant by 19.0%, 35.6%, and 60.8%, respectively. The effect of supplementary light on these parameters was superior to that of CO2 enrichment. In addition, CaLs and CeLs improved nutritional quality significantly. Taken together, CeLs promoted the greatest yield, WUE, and fruit quality, suggesting it may be a worthwhile practice for off-season tomato cultivation.

Tomato (Solanum lycopersicum Mill.) is one of the most widely cultivated food plants in the world. It enjoys a wide range of uses in the kitchen and contains an abundance of dietary nutrients, including antioxidants (Mamatha et al., 2014). Tomato fruit yield and quality are affected by a large number of environment factors, including the levels of CO2 and light (Mamatha et al., 2014; Tewolde et al., 2016). How these two factors can be regulated to maximize fruit yield and quality has been the subject of considerable research. This work should help us meet the increasing food demands of a growing world population.

Atmospheric CO2 concentration has increased considerably since the beginning of the Industrial Revolution (in 1825, 285 μmol·mol–1). By the middle of the past century, it had risen by about 15% (in 1950, 320 μmol·mol–1); by the beginning of this century, it had risen by 30% (in 2000, 375 μmol·mol–1), and it is now rising faster than ever. The CO2 level is about 400 μmol·mol–1, and this value is projected to double by the end of 21st century (Urban et al., 2014).

However, in a closed greenhouse, as plants absorb CO2 for photosynthesis, CO2 levels may fall to as low as 150 μmol·mol–1 in bright sunlight (Kläring et al., 2007). Because CO2 is the key substrate for photosynthesis, CO2 fertilization is widely accepted as a key technique for enhancing photosynthesis, thus increasing yield and commercial revenue (Chalabi et al., 2002; Kläring et al., 2007). Numerous studies have shown that CO2 enrichment can increase growth, affect physiology, and increase both yield and quality in tomatoes (Mamatha et al., 2014; Nilsen et al., 1983; Yelle et al., 1990). Atmospheric CO2 enrichment can also increase the numbers of branches and leaves, the average leaf area, and the rate of dry matter accumulation in tomatoes (Fierro et al., 1994; Mamatha et al., 2014). Moreover, it may increase photosynthetic rate, while also reducing transpiration, hence significantly increasing WUE (Bencze et al., 2011; Mamatha et al., 2014; Pazzagli et al., 2016; Wei et al., 2018a, 2018b).

However, photosynthetic acclimation may also occur after prolonged periods of CO2 enrichment (Yelle et al., 1990). Also, although elevated CO2 levels can promote fruit yield and have positive effects on fruit quality, it can also have negative effects (Mamatha et al., 2014; Zhang et al., 2014). Because regulation of the CO2 environment in a greenhouse is technically demanding and expensive, the use of CO2 fertilization is rather limited in China. Therefore, studies on how and to what extent CO2 enrichment can improve yield of tomatoes in greenhouses seems well worth investigating.

Light is the primary energy source for photosynthesis, so light intensity is one of the key environmental factors driving plant growth (Fukuda et al., 2008). Many studies have reported on the effects of light intensity on the growth of tomatoes (Fan et al., 2013; Hao et al., 2017; O’Carrigan et al., 2014). In general, increasing light intensity increases dry weight gain and stem diameter, but decreases height (Fan et al., 2013). Meanwhile, within certain limits, increases in light intensity result in increases in photosynthesis (Fan et al., 2013), although excessive light intensities cause photoinhibition (Carvalho and Amâncio, 2002; O’Carrigan et al., 2014). Because growth and yield of plants is so strongly affected by photosynthetic rate (Yamori, 2013, 2016; Yamori and Shikanai, 2016; Yamori et al., 2016), in greenhouse horticulture, the provision of supplementary lighting significantly increases growth and yield by increasing photosynthesis (Jiang et al., 2017). However, Tewolde et al. (2016) showed that supplementary daytime lighting with light-emitting diodes significantly increased photosynthesis and yield of tomato during winter but not in summer. In winter and early spring, sunlight intensity is low in the early morning and late afternoon. Under these conditions, supplementary lighting significantly enhances growth and yield in tomato.

Previous research has focused largely on the effects of individual factors of supplementary light or supplementary CO2 on plant growth, yield, and quality (Hikosaka et al., 2013; Mamatha et al., 2014; Yelle et al., 1990; Zou et al., 2016). Urban et al. (2014) reported that the enhancement of photosynthesis under CO2 enrichment is strongly affected by light intensity. Kaiser et al. (2017) reported that CO2 enrichment can stimulate photosynthesis under conditions of fluctuating irradiance. Bencze et al. (2011) reported that CO2 enrichment can enhance photosynthesis in tomatoes and peppers even under low-light conditions. Interestingly, combinations of CO2 enrichment and supplementary lighting can result in greater positive effects on plant growth and yield than enhancement of either factor on its own (Labeke and Dambre, 1998; Naing et al., 2016). To the best of our knowledge, the effects of the combination of supplementary lighting and CO2 enrichment in winter and spring on the growth of tomatoes have not been thoroughly investigated. The aims of this study were 1) to investigate the effects of supplementary lighting and CO2 enrichment on tomato yield and quality under the irradiance conditions in northwest China and 2) to seek a practicable method for providing supplemental lighting and CO2 enrichment for local greenhouse tomato growers, particularly for use in winter and springtime. We also sought to test the hypothesis that there is a positive interaction between supplementary lighting and CO2 enrichment on the growth and yield of tomatoes.

Materials and Methods

Location and plant materials.

The experiment was conducted from 1 Nov. 2016 to 30 Mar. 2017 at the North Experimental Station of Northwest Agriculture and Forestry University, Yangling, China (lat. 34°20'N, long. 108°24'E; altitude, 443.6 m). The region enjoys an average temperature of 12.9 °C, 211 frost-free days, an average annual photoperiod of 2163.8 h, annual solar radiation of 4810 MJ·m–2, and annual precipitation of 635.1 mm. We used tomato Lycopersicum esculentum Mill., cv. Jinpeng No.1. Uniform seedlings with four leaves were cultivated in polyethylene bags filled with a commercial peat-based compost (Yufeng Seed Industry Co., Ltd., Yangling, China) with two seedlings per bag. The plastic bags were 45 × 60 cm, 24 L in volume, and white internally and gray externally.

Experimental design.

There were four treatments: 1) ambient CO2 and no supplementary light (CaLn), 2) elevated CO2 (about 800 mol·mol–1) and no supplementary light (CeLn), 3) ambient CO2 and supplementary light of 200 ± 20 μmol·m–2·s–1 (CaLs), and 4) elevated CO2 and supplementary light (CeLs). Four identical and adjacent 4 × 4 × 2.5-m open-top chambers were established with an aluminum frame and 0.25-mm-thick polythene (ultraviolet proof) in a greenhouse. Each chamber had side and top windows of 0.8 × 1.5 m and contained 60 tomato seedlings. The apical growth was stopped 115 d after transplanting (DAT). CO2 enrichment was from steel cylinders containing liquid CO2 (Qinhong gas Co. Ltd., Xianyang, China) and was controlled by a CO2 infrared (IR) gas analyzer (JSA5-Gas; Shenzhen, China). Supplementary light was provided by high-pressure sodium lamps (HPS1000; Zhuhai Meiguangyuan, Co. Ltd., Zhushai, China) (see Supplemental Fig. 1 for spectral distribution). These were all controlled by a central control system during the two daily periods 0800 to 1000 hr and 1600 to 1800 hr from 1 Nov. 2016 to 1 Mar. 2017. Irrigation was by dripper, and this and other management occurred according to local commercial practice.

Indices measurement and methods.

Environmental data in the chambers were recorded every 30 min from the beginning of the experiment to the end of the treatments. CO2 concentrations were recorded by a CO2 analyzer (TPJ-26-I; Zhejiang, China). Photosynthetically active radiation (PAR) at a height of 1.5 m was recorded by a quantum sensor (MQ-100; Apogee, Logan, UT), and temperature and humidity were recorded by a dual external sensor (PDEI-2-2X; Heilongjiang, China).

Before treatment, four plants were selected from the same position in each chamber and marked. At 110 DAT, we measured plant height, stem diameter, and leaf number per plant. The leaf area was determined using a leaf area meter (Li-3000; LI-COR, Lincoln, NE). The plants were then each divided into leaves, stem, and roots, and these fractions were oven-dried to a constant weight (80 °C, 72 h) and weighed.

The gas exchange parameters, including Pn, stomatal conductance (gS), and transpiration rate (Tr) were measured from 1030–1200 hr on two consecutive sunny days at four stages: seedling, flowering, initial fruiting, and fruiting at 15, 45, 75, and 105 DAT, respectively. Measurements were made with a portable IR photosynthesis analyzer (Li-6400, LI-COR) (n = 6). The light density was set at 800 μmol·m–2·s–1, with the block temperature, flow rate, relative humidity, and CO2 concentration set at 25 ± 1 °C, 500 μmol·s–1, 50% to 65%, and 400 μmol·mol–1, respectively. WUE was calculated as WUE = Pn/Tr (Rasineni et al., 2011).

Leaf pigments were assayed according to Jia et al. (2010), with some modifications (n = 6). Briefly, leaf samples (0.05 g) were ground and placed into 10-mL centrifuge tubes along with 95% ethyl alcohol, then incubated in darkness for 24 h, during which the tubes were shaken up and down gently by hand three times for 30 s each time. The chlorophyll a (Chla) content, chlorophyll b (Chlb) content, and carotenoid content were assayed using a ultraviolet spectrophotometer (ultraviolet-1800; Shimadzu, Kyoto, Japan) at A665, A649, and A470 and calculated according to Lichtenthaler and Wellburn (1983).

Ten plants were selected for uniformity from the middle and sides of each treatment and were tagged before harvest to determine yield characteristics. Ripe fruits were harvested every 5 d during harvest, and fruit number per plant, single fruit weight, and yield per plant were measured. Yield was calculated as tons per hectare.

At harvest, five ripe fruit were selected randomly from each treatment to determine quality index. Soluble sugar content was measured as follows: Fruit samples (2 g) were homogenized with 5 mL 80% ethyl alcohol, incubated for 30 min in an 80 °C water bath. and centrifuged at 3500 rpm for 10 min. Then, the supernatant was transferred to a 25-mL volumetric flask and the sediment was homogenized and extracted twice. Next, all the supernatants were combined and volumed to 25-mL with extract solution. Then, 2 mL of the solution was transferred to a 10-mL centrifuge tube and dried. After this, 10 mL of distilled water was added and centrifuged at 3500 rpm for 10 min before being diluted 20 times. Last, the mixture, which contained 5 mL of anthrone sulfuric acid and 2 mL of the dilute solution, was boiled for 10 min and measured at A620 using a spectrophotometer (ultraviolet-1800, Shimadzu).

The lycopene content was determined using the method of Marković et al. (2006). Briefly, fruit samples (5 g) were homogenized and placed in 200-mL flasks wrapped with aluminum foil. They were then agitated for 10 min after addition of a 100-mL mixture of hexane/acetone/ethanol (2/1/1, v/v/v). After this, 15 mL of distilled water was added to each flask and agitated for another 5 min. The contents were then divided into distinct polar and nonpolar layers. Last, the nonpolar layer containing lycopene was filtered through 0.2-mm filter paper before the filtrate was diluted with the hexane/acetone/ethanol mixture and measured at an absorbance of 470 nm.

Ascorbic acid content was measured according to Kampfenkel et al. (1995). Briefly, fruit samples (0.15 g) were homogenized with 5% (w/v) aqueous trichloroacetic acid and centrifuged for 10 min at 4 °C. The mixtures containing 0.05 mL of the supernatant, 0.1 mL 0.2 M phosphate buffer (pH 7.4), and 6 mm DL-dithiothreitol (DTT) were held in a water bath at 42 °C for 15 min. The excess DTT was then removed by the addition of 0.05 mL 0.5% (w/v) aqueous N-ethylmaleimide for 2 min at room temperature. Last, the mixtures containing 1 mL 10% (w/v) trichloroacetic acid (TCA), 0.8 mL of 42% (v/v) o-phosphoric acid, 0.8 mL of 4% (w/v) a,a′-dipyridyl, and 0.1 mL of 3% (w/v) FeC13 were incubated at 42 °C for 40 min and measured at A525.

The soluble solids content and organic acid content were measured using a digital refractometer (DG-NXT; ARKO India Ltd., India). Before each measurement, the refractometer was zeroed with distilled water and wiped with mirror paper. Data were recorded as percent Brix and percent organic acid content, respectively.

Data analysis.

Data except environmental factors were measured in triplicate and are presented as means ± se. SPSS 20.0 (IBM Corp., Armonk, NY) was used to examine significant differences among treatments (P < 0.05). GraphPad Prism 6 (GraphPad Software Inc., La Jolla, CA) was used to draw graphs.

Results

Environmental factors.

The environmental factors during the experimental period are shown in Fig. 1 in terms of the daytime course of CO2 concentration (Fig. 1A), daytime course of light intensity on sunny days and cloudy days (Fig. 1B), average daytime and nighttime temperatures (Fig. 1C), and air relative humidity and average daily light intensity (Fig. 1D). Under no CO2 enrichment (treatments CaLn and CaLs), the CO2 concentration ranged from 382 to 530 μmol·mol–1 during 0800 to 1000 hr and 1600 to 1800 hr each day, whereas under CO2 enrichment (treatments CeLn and CeLs) CO2 concentrations were increased significantly to about 800 μmol·mol–1 (Fig. 1A). Meanwhile, the PAR intensity on sunny and cloudy days during the period was low, with maximum light intensities of about 200 μmol·m–2·s–1 on sunny days (Fig. 1B). Average daytime (≈18 °C) and nighttime (≈12 °C) temperatures fluctuated first down and then up, then bottomed at the end of Jan. 2017 (Fig. 1C). Average daily light intensity followed the same general pattern as temperature, whereas air relative humidity showed an inverse trend (Fig. 1D).

Fig. 1.
Fig. 1.

Values of CO2 concentration, light intensity, temperature, and air relative humidity in the greenhouse during the experimental period. (A) Daytime course of CO2 concentration from 0800 to 1800 hr. The solid line, dotted solid line, dotted line, and circle dotted line represent the four treatments of ambient CO2 and no supplementary light (CaLn), CO2 enrichment and no supplementary light (CeLn), ambient CO2 and supplementary light (CaLs), and CO2 enrichment and supplementary light (CeLs), respectively. (B) Daytime course of light intensity during a typical sunny day (dotted line) and cloudy day (solid line). (C) Temporal changes in average daytime (solid line) and nighttime (dotted line) temperatures. (D) Temporal changes in air relative humidity (solid line) and average daily light intensity (dotted line). PAR = photosynthetically active radiation; DAT = days after transplanting.

Citation: HortScience horts 54, 2; 10.21273/HORTSCI13709-18

Effects of CO2 enrichment and supplementary light on growth and dry weight.

All growth parameters, except stem diameter, were significantly increased by CaLs and CeLs, but not significantly by CeLn (Fig. 2). Compared with CaLn, CaLs and CeLs significantly increased plant height by 12.7% and 14.3%, respectively (Fig. 2A); leaf area was increased by 19.0% and 21.2%, respectively (Fig. 2C); and leaf number by 12.8% and 17.7%, respectively (Fig. 2D). CeLs had the most significant effects on plant height, leaf area, and leaf number, whereas CaLs was ranked second, indicating that CO2 enrichment enhanced the effects of supplementary light on growth.

Fig. 2.
Fig. 2.

Effects of CO2 enrichment and supplementary lighting on (A) plant height, (B) stem diameter, (C) leaf area, and (D) leaf number of tomato plants grown in a greenhouse. Values represent the means ± se (n = 4). Different letters indicate significant differences at P < 0.05 according to Duncan’s multiple range test. CaLn = ambient CO2 and no supplementary light; CeLn = CO2 enrichment and no supplementary light; CaLs = ambient CO2 and supplementary light; CeLs = CO2 enrichment and supplementary light.

Citation: HortScience horts 54, 2; 10.21273/HORTSCI13709-18

Compared with CaLn, CeLn and CaLs significantly increased the dry weight of leaves, roots, and shoots, whereas CeLs increased them further (Table 1). CeLs significantly increased the dry weight of leaves, stems, and roots by 40.0%, 102.1%, and 98.4%, respectively. Hence, it also increased the shoot dry weight and the ratio of root dry weight to shoot dry weight by 57.6% and 26.7%, respectively. Overall, CO2 enrichment and supplementary light promoted accumulation of dry weight during the vegetative period, and the interaction between CO2 enrichment and supplementary light was positive.

Table 1.

Effects of CO2 enrichment and supplementary light on dry weight distribution of greenhouse-grown tomato plants.

Table 1.

Effects of CO2 enrichment and supplementary light on gas exchange and photosynthetic pigment content.

Leaf gas exchange parameters including Pn, gS, and Tr changed significantly with time—first increasing, then decreasing, and finally increasing. Meanwhile, WUE showed a gradual downward trend (Fig. 3). At the seedling, flowering, and initial fruiting stages, compared with CaLn, CeLn and CaLs increased Pn by 9.2% to 26.8% and by 20.5% to 38.9%, respectively, whereas CeLs increased Pn by 28.1% to 49.5% (Fig. 3A). The value of gS in CeLn was significantly less than in CaLn, and was less in CeLs than in CaLs, indicating CO2 enrichment decreased gS (Fig. 3B). A similar response was observed for Tr, with CaLs having the greatest effect, followed in descending order by CeLs, CaLn, and CeLn (Fig. 3C). On average, in comparison with CaLn, CeLs enhanced WUE by 22.7% to 52.6% before fruiting stage, whereas CeLn and CaLs improved WUE by 16.9% to 49.4% and 9.0% to 24.8%, respectively. However, at fruiting stage, treatment effects were reduced, with CeLn having the greatest WUE (Fig. 3D).

Fig. 3.
Fig. 3.

Effects of CO2 enrichment and supplementary light on (A) net photosynthetic rate (Pn), (B) stomatal conductance (gS), (C) transpiration rate (Tr), and (D) water use efficiency (WUE; calculated as Pn/Tr) of tomato plants grown in a greenhouse, with values shown representing means ± se (n = 6). DAT = days after transplanting; CaLn = ambient CO2 and no supplementary light; CeLn = CO2 enrichment and no supplementary light; CaLs = ambient CO2 and supplementary light; CeLs = both CO2 enrichment and supplementary light.

Citation: HortScience horts 54, 2; 10.21273/HORTSCI13709-18

Photosynthetic pigment contents were increased by supplemental light and by CO2 enrichment to different degrees (Table 2). The content of Chla was greatest under CaLs, followed in descending order by CeLs, CeLn, and CaLn, with significant differences between CaLs, CeLs, CeLn, and CaLn. The content of Chl a+b was most affected by CaLs, followed in descending order by CeLn, CeLs, and CaLn. Overall, CaLs had the most significant positive effect on all photosynthetic pigments, promoting Chla, Chlb, and Chla+b contents by 42.28%, 40.50% and 40.84%, respectively. Next for overall photosynthetic pigment content was CeLs.

Table 2.

Effects of CO2 enrichment and supplementary light on photosynthetic pigment content in tomato leaves.

Table 2.

Effects of CO2 enrichment and supplementary light on yield characteristics and fruit quality of tomatoes.

Single fruit weight, yield per plant, and yield per hectare were significantly increased by CeLn, followed in increasing order by CaLs and CeLs; fruit number per plant, compared with CaLn, was significantly enhanced only by CeLs (Table 3). Compared with CaLn, single fruit weight was significantly increased in CeLn, CaLs, and CeLs by 16.2%, 28.9%, and 36.6%, respectively. Yield per plant (the same as yield per hectare) was also increased in CeLn, CaLs, and CeLs by 19.0%, 35.6%, and 60.8%, respectively. Summarizing, among all treatments, CeLs had the greatest fruit number per plant and greatest single fruit weight, combining to create the greatest fruit yield per plant and total yield. The results indicate CO2 enrichment and supplementary light can each significantly improve single fruit weight and yield of tomato, whereas supplementary light was more effective than CO2 enrichment. Moreover, this result indicates there is a positive interactive effect between these treatments on yield characteristics.

Table 3.

Effects of CO2 enrichment and supplementary light on tomato fruit yield characteristics.

Table 3.

Nutritional qualities were promoted by CaLs and CeLs, but were slightly reduced by CeLn (Table 4). Compared with CaLn, CaLs affected nutrient contents the most, with increases in soluble sugars, lycopene, ascorbic acid, soluble solids, and sugar-to-acid ratio by 42.4%, 17.3%, 38.7%, 7.3%, and 13.1%, respectively. In addition, CeLs markedly increased the contents of soluble sugar, lycopene, and ascorbic acid. There were no significant differences between CeLn and CeLs for lycopene or organic acid. CeLn significantly decreased soluble sugar and lycopene by 25.5% and 21.6%, respectively, but increased ascorbic acid and organic acid by 11.8% and 9.1%, respectively. There were no significant differences in organic acid content among CaLn, CaLs, and CeLs.

Table 4.

Effects of CO2 enrichment and supplementary light on tomato fruit quality.

Table 4.

Discussion

Previous studies in this area are few (Fierro et al., 1994; Hikosaka et al., 2013; Nilsen et al., 1983). Here we investigate the effects of CO2 enrichment and supplementary light on photosynthesis, growth, yield, and quality of tomatoes.

Light is the primary source of energy, the intensity and spectral composition (light quality) of which play crucial roles in plant growth, morphological establishment, and physiology (Fukuda et al., 2008; Hernández et al., 2016; Li and Kubota, 2009; Zou et al., 2016). Enhanced light intensity can promote the previously mentioned parameters by optimizing stomatal morphology, enhancing enzyme activity (e.g., Rubisco and 1,6-diphosphate fructose phosphatase) (Li et al., 2017), and affecting the distribution of dry weight (Fan et al., 2013). Appropriate spectral composition may promote the growth and yield of plants (Tsujita and Dutton, 1983). A composite spectrum could enhance photosynthesis compared with red–blue light (Bergstrand et al., 2016). The spectral composition of the high-pressure sodium lamps used in this study was different from that used by others (Hikosaka et al., 2013; Jiang et al., 2017), so it is possible some results will also be different. Because CO2 is the key substrate for photosynthesis, a high CO2 concentration may significantly enhance photosynthesis of tomato and pepper (Bencze et al., 2011). However, the effects of CO2 enrichment are usually modulated by light conditions (Bencze et al., 2011; Kaiser et al., 2017; Urban et al., 2014). Hence, supplementary light should be combined with CO2 enrichment (Bergstrand et al., 2016), and our research supports this (Fig. 3; Table 3).

In this research, CeLn and CaLs significantly enhanced plant height, leaf area, and leaf number whereas CeLs further enhanced them, suggesting CO2 enrichment and supplementary lighting exert positive interactive effects on plant growth (Fig. 2). This result agrees with previous studies (Madhana et al., 2014; Naing et al., 2016). Compared with CaLn, dry weight components (leaf, stem, and roots) were significantly affected by CeLn and CaLs, but the greatest affect was with CeLs (Table 1). We found CeLn, CeLn, and CeLs increased dry weight accumulation in shoots and roots, which agrees with the result of Fierro et al. (1994), but they also shifted dry weight to the roots, resulting in a higher root-to-shoot ratio compared with CaLn. This result is consistent with the effects of CO2 enrichment in grape (Wu and Lin, 2013) and in Rhodes grass (Ksiksi and Youssef, 2010), indicating supplementary light and CO2 enrichment may promote the uptake of nutrients from culture substrate by altering the distribution of dry weight and thus increasing yields.

We found both photosynthetic pigments (Table 2) and gas exchange parameters (Fig. 3) were increased significantly by CeLn, CaLs and CeLs, which may be the result of enhanced photosynthesis-related enzyme activity (Nilsen et al., 1983; Yu and Wang, 2010). The gas exchange parameters fluctuated with time, which may be the result of the combined influences of growth status and fluctuating temperature and humidity (Fig. 1). Transpiration of tomato increases with decreasing humidity (Jolliet et al., 1993), which is consistent with our study. gS and Tr were inhibited by CO2 enrichment, which may be a result of increased resistance to gas diffusion in mesophyll cells, hence reducing transpiration and increasing WUE. This was consistent with previous studies (Jin et al., 2014; Nabity et al., 2012). In our study, CeLs had the greatest WUE, indicating it can balance water use and carbon assimilation of plants (Wang and Feng, 2012). However, WUE decreased with time, which may be the result of decreasing water uptake and use as a result of decreased temperatures. This mechanism deserves further investigation.

Fruit yield and quality parameters are the primary focus of farmers. Therefore, all kinds of methods have been investigated to achieve them, ranging from agricultural management to gene manipulation (Ho, 2003; Simkin et al., 2015). In the current study, CO2 enrichment and supplementary light, and the hypothesis of a positive interaction between them on yield is confirmed (Table 3). This is consistent with previous studies (Ma et al., 2015; Yelle et al., 1990). Nutritional quality is one of the most important factors affecting consumer choice, with lycopene and ascorbic acid being antioxidants that are particularly beneficial for human health (Hooper and Cassidy, 2006). In addition, the soluble solid content, organic acid content, and sugar-to-acid ratio are also important nutritional indexes that affect flavor (Li et al., 2017; Mamatha et al., 2014). CaLs and CeLs improved all these quality parameters except for soluble solid content, whereas CeLn slightly decreased some quality parameters (Table 4). This too is consistent with previous studies (Helyes et al., 2015; Li et al., 2017). This result may be because supplementary light increases the primary and secondary metabolites of photosynthesis, thus enhancing quality, whereas a greater CO2 concentration may result in greater fruit water content, hence diluting the quality-determining contents (Di, 1999; Li et al., 2017; Mamatha et al., 2014). In this study, it is clear that supplementary light had a greater effect than CO2 enrichment on growth, yield, and quality. This could be explained by heating effects and should be investigated further. Also, because different CO2 concentrations and/or different light intensities may exert varying effects on tomato growth and yield, much work should be conducted in the future to explore the optimal combination of CO2 concentration and light intensity to obtain the greatest yield and quality of tomatoes.

Conclusions

Supplementary light and CO2 enrichment during winter and spring each enhanced significantly shoot dry weight growth, photosynthesis, and fruit yield of tomatoes grown under greenhouse conditions. The effect of supplementary light on these parameters was superior to that of CO2 enrichment. The combination of CO2 enrichment and supplementary light further increased the growth, photosynthesis, yield, and quality of tomatoes. The practice proposed to increase the yield and quality of greenhouse-grown tomatoes in northwest China in winter and spring (November to March) is simultaneous CO2 enrichment (to 800 μmol·mol–1) and supplementary lighting (to 200 ± 20 μmol·m–2·s–1) during the mornings (0800–1000 hr) and afternoons (1600–1800 hr).

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  • Hao, X., Guo, X.B., Chen, X.J., Zheng, L. & Kholsa, C.S. 2017 Dynamic temperature integration with temperature drop improved the response of greenhouse tomato to long photoperiod of supplemental lighting Acta Hort. 1170 995 1002

    • Search Google Scholar
    • Export Citation
  • Helyes, L., Lugasi, A., Peli, E. & Pek, Z. 2015 Effect of elevated CO2 on lycopene content of tomato (Lycopersicon lycopersicum L. karsten) fruits Acta Aliment. Hung. 40 80 86

    • Search Google Scholar
    • Export Citation
  • Hernández, R., Eguchi, T., Deveci, M. & Kubota, C. 2016 Tomato seedling physiological responses under different percentages of blue and red photon flux ratios using LEDs and cool white fluorescent lamps Scientia Hort. 213 270 280

    • Search Google Scholar
    • Export Citation
  • Hikosaka, S., Iyoki, S., Hayakumo, M. & Goto, E. 2013 Effects of light intensity and amount of supplemental LED lighting on photosynthesis and fruit growth of tomato plants under artificial conditions J. Agr. Meteorol. 69 93 100

    • Search Google Scholar
    • Export Citation
  • Ho, L.C. 2003 Genetic and cultivation manipulation for improving tomato fruit quality Acta Hort. 613 21 31

  • Hooper, L. & Cassidy, A. 2006 A review of the health care potential of bioactive compounds J. Sci. Food Agr. 86 1805 1813

  • Jia, Y., Tang, S., Wang, R., Ju, X., Ding, Y., Tu, S. & Smith, D.L. 2010 Effects of elevated CO2 on growth, photosynthesis, elemental composition, antioxidant level, and phytochelatin concentration in Lolium mutiforum and Lolium perenne under Cd stress J. Hazard. Mater. 180 384 394

    • Search Google Scholar
    • Export Citation
  • Jiang, C., Johkan, M., Hohjo, M., Tsukagoshi, S., Ebihara, M., Nakaminami, A. & Maruo, T. 2017 Photosynthesis, plant growth, and fruit production of single-truss tomato improves with supplemental lighting provided from underneath or within the inner canopy Scientia Hort. 222 221 229

    • Search Google Scholar
    • Export Citation
  • Jin, J., Lauricella, D., Armstrong, R., Sale, P. & Tang, C. 2014 Phosphorus application and elevated CO2 enhance drought tolerance in field pea grown in a phosphorus-deficient vertisol Ann. Bot. 116 975 985

    • Search Google Scholar
    • Export Citation
  • Jolliet, O., Bailey, B.J., Hand, D.J. & Cockshull, K. 1993 Tomato yield in greenhouses related to humidity and transpiration Acta Hort. 328 115 124

  • Kaiser, E., Zhou, D.F., Heuvelink, E., Harbinson, J., Morales, A. & Marcelis, L.F.M. 2017 Elevated CO2 increases photosynthesis in fluctuating irradiance regardless of photosynthetic induction state J. Expt. Bot. 68 5629 5640

    • Search Google Scholar
    • Export Citation
  • Kampfenkel, K., Montagu, M.V. & Inzé, D. 1995 Effects of iron excess on Nicotiana plumbaginifolia plants: Implications to oxidative stress Plant Physiol. 107 725 735

    • Search Google Scholar
    • Export Citation
  • Kläring, H.P., Hauschild, C., Heißner, A. & Baryosef, B. 2007 Model-based control of CO2 concentration in greenhouses at ambient levels increases cucumber yield Agr. For. Meteorol. 143 208 216

    • Search Google Scholar
    • Export Citation
  • Ksiksi, T. & Youssef, T. 2010 Effects of CO2 enrichment on growth partitioning of Chloris gayana in the arid environment of the UAE Grassl. Sci. 56 183 187

    • Search Google Scholar
    • Export Citation
  • Labeke, M.C.V. & Dambre, P. 1998 Effect of supplementary lighting and CO2 enrichment on yield and flower stem quality of Alstroemeria cultivars Scientia Hort. 74 269 278

    • Search Google Scholar
    • Export Citation
  • Lichtenthaler, H. & Wellburn, A. 1983 Determination of total carotenoids and chlorophylls a and b of leaf in different solvents Biochem. Soc. Trans. 11 591 592

    • Search Google Scholar
    • Export Citation
  • Li, X.J., Kang, S.Z., Li, F.S., Zhang, X.T., Huo, Z.L., Ding, R.S., Tong, L., Du, T.S. & Li, S.E. 2017 Light supplement and carbon dioxide enrichment affect yield and quality of off-season pepper Agron. J. 109 2107 2118

    • Search Google Scholar
    • Export Citation
  • Li, Q. & Kubota, C. 2009 Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce J. Environ. Exp. Bot. 67 59 64

  • Ma, X., Liu, S., Li, Y. & Gao, Q. 2015 Effectiveness of gaseous CO2 fertilizer application in China’s greenhouses between 1982 and 2010 J. CO2 Util. 11 63 66

    • Search Google Scholar
    • Export Citation
  • Madhana, S.K., Rachapudi, V.S., Mudalkar, S. & Reddy, A.R. 2014 Persistent stimulation of photosynthesis in short rotation coppice mulberry under elevated CO2 atmosphere J. Photochem. Photobiol. B 137 21 30

    • Search Google Scholar
    • Export Citation
  • Mamatha, H., Srinivasarao, N.K., Laxman, R.H., Shivashankara, K.S., Bhatt, R.M. & Pavithra, K.C. 2014 Impact of elevated CO2 on growth, physiology, yield, and quality of tomato (Lycopersicon esculentum Mill) cv. Arka Ashish Photosynthetica 52 519 528

    • Search Google Scholar
    • Export Citation
  • Marković, K., Hruškar, M. & Vahčić, N. 2006 Lycopene content of tomato products and their contribution to the lycopene intake of Croatians Nutr. Res. 26 556 560

    • Search Google Scholar
    • Export Citation
  • Nabity, P.D., Hillstrom, M.L., Lindroth, R.L. & Delucia, E.H. 2012 Elevated CO2 interacts with herbivory to alter chlorophyll fluorescence and leaf temperature in Betula papyrifera and Populus tremuloides Oecologia 169 905 913

    • Search Google Scholar
    • Export Citation
  • Naing, A.H., Jeon, S.M., Park, J.S. & Kim, C.K. 2016 Combined effects of supplementary light and CO2 on rose growth and the production of good quality cut flowers Can. J. Plant Sci. 96 503 510

    • Search Google Scholar
    • Export Citation
  • Nilsen, S., Hovland, K., Dons, C. & Sletten, S.P. 1983 Effect of CO2 enrichment on photosynthesis, growth and yield of tomato Scientia Hort. 20 1 14

  • O’Carrigan, A., Hinde, E., Lu, N., Xu, X.Q., Duan, H.L., Huang, G.M., Mak, M., Bellotti, B. & Chen, Z.H. 2014 Effects of light irradiance on stomatal regulation and growth of tomato Environ. Exp. Bot. 98 65 73

    • Search Google Scholar
    • Export Citation
  • Pazzagli, P.T., Weiner, J. & Liu, F.L. 2016 Effects of CO2 elevation and irrigation regimes on leaf gas exchange, plant water relations, and water use efficiency of two tomato cultivars Agr. Water Mgt 169 26 33

    • Search Google Scholar
    • Export Citation
  • Rasineni, G.K., Guha, A. & Reddy, A.R. 2011 Responses of Gmelina arborea, a tropical deciduous tree species, to elevated atmospheric CO2: Growth, biomass productivity and carbon sequestration efficacy Plant Sci. 181 428 438

    • Search Google Scholar
    • Export Citation
  • Simkin, A.J., Mcausland, L., Headland, L.R., Lawson, T. & Raines, C.A. 2015 Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco J. Expt. Bot. 66 1 16

    • Search Google Scholar
    • Export Citation
  • Tewolde, F.T., Na, L., Shiina, K., Maruo, T., Takagaki, M., Kozai, T. & Yamori, W. 2016 Nighttime supplemental LED inter-lighting improves growth and yield of single-truss tomatoes by enhancing photosynthesis in both winter and summer Front. Plant Sci. 7 1 10

    • Search Google Scholar
    • Export Citation
  • Tsujita, M.J. & Dutton, R.G. 1983 Root zone temperature effects on greenhouse roses in relation to supplementary lighting at reduced air temperature HortScience 18 874 876

    • Search Google Scholar
    • Export Citation
  • Urban, O., Klem, K., Holisová, P., Sigut, L., Sprtová, M., Teslová-Navrátilová, P., Zitová, M., Spunda, V., Marek, M.V. & Grace, J. 2014 Impact of elevated CO2 concentration on dynamics of leaf photosynthesis in Fagus sylvatica is modulated by sky conditions Environ. Pollut. 185 271 280

    • Search Google Scholar
    • Export Citation
  • Wang, G. & Feng, X. 2012 Response of plants’ water use efficiency to increasing atmospheric CO2 concentration Environ. Sci. Technol. 46 8610 8620

    • Search Google Scholar
    • Export Citation
  • Wei, Z.H., Du, T.C., Li, X.N., Fang, L. & Liu, F.L. 2018a Interactive effects of CO2 concentration elevation and nitrogen fertilization on water and nitrogen use efficiency of tomato grown under reduced irrigation regimes Agr. Water Mgt. 202 174 182

    • Search Google Scholar
    • Export Citation
  • Wei, Z.H., Du, T.C., Li, X.N., Fang, L. & Liu, F.L. 2018b Simulation of stomatal conductance and water use efficiency of tomato leaves exposed to different irrigation regimes and air CO2 concentrations by a modified “ball-berry” model Front. Plant Sci. 9 1 13

    • Search Google Scholar
    • Export Citation
  • Wu, H.C. & Lin, C.C. 2013 Carbon dioxide enrichment during photoautotrophic micropropagation of Protea cynaroides L. plantlets improves in vitro growth, net photosynthetic rate, and acclimatization HortScience 48 1293 1297

    • Search Google Scholar
    • Export Citation
  • Yamori, W. 2013 Improving photosynthesis to increase food and fuel production by biotechnological strategies in crops J. Plant Biochem. Physiol. 1 1 3

    • Search Google Scholar
    • Export Citation
  • Yamori, W. 2016 Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress J. Plant Res. 129 379 395

    • Search Google Scholar
    • Export Citation
  • Yamori, W., Kondo, E., Sugiura, D., Terashima, I., Suzuki, Y. & Makino, A. 2016 Enhanced leaf photosynthesis as a target to increase grain yield: Insights from transgenic rice lines with variable Rieske FeS protein content in the cytochrome b6/f complex Plant Cell Environ. 39 80 87

    • Search Google Scholar
    • Export Citation
  • Yamori, W. & Shikanai, T. 2016 Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth Annu. Rev. Plant Biol. 67 1 26

    • Search Google Scholar
    • Export Citation
  • Yelle, S., Beeson, R.C.J., Trudel, M.J. & Gosselin, A. 1990 Duration of CO2 enrichment influences growth, yield, and gas exchange of two tomato species J. Amer. Soc. Hort. Sci. 115 52 57

    • Search Google Scholar
    • Export Citation
  • Yu, G.R. & Wang, Q.F. 2010 Ecophysiology of plant photosynthesis, transpiration, and water use. Science Press, Beijing, China

  • Zhang, Z.M., Liu, L.H., Zhang, M., Zhang, Y.S. & Wang, Q.M. 2014 Effect of carbon dioxide enrichment on health-promoting compounds and organoleptic properties of tomato fruits grown in greenhouse Food Chem. 153 157 163

    • Search Google Scholar
    • Export Citation
  • Zou, Q.Y., Ji, J.W. & Li, Z.M. 2016 Effect of supplemental light with different spectral LEDs on the growth of tomato seedlings in north greenhouse, p. 377–380. In: H. Wang and X. Jia (eds.). 2nd International Forum on Electrical Engineering and Automation. Atlantis Press, Amsterdam/Paris

Supplemental Fig. 1.
Supplemental Fig. 1.

The spectral distribution of high pressure sodium lamps.

Citation: HortScience horts 54, 2; 10.21273/HORTSCI13709-18

Contributor Notes

This work was funded by Structure Optimization and Supporting Technology Development Study for Energy-saving Solar Greenhouse (2017ZDXM-NY-057) and also by the Fundamental Research Funds for the Central Universities (Z109021609).

We thank the editors and anonymous reviewers for their constructive suggestions and comments. We also thank the undergraduates who helped to complete the experiment.

These authors contributed equally to this work and are first coauthors.

Corresponding authors. E-mail: yyzhj@nwsuaf.edu.cn or zouzhirong2005@hotmail.com.

  • View in gallery

    Values of CO2 concentration, light intensity, temperature, and air relative humidity in the greenhouse during the experimental period. (A) Daytime course of CO2 concentration from 0800 to 1800 hr. The solid line, dotted solid line, dotted line, and circle dotted line represent the four treatments of ambient CO2 and no supplementary light (CaLn), CO2 enrichment and no supplementary light (CeLn), ambient CO2 and supplementary light (CaLs), and CO2 enrichment and supplementary light (CeLs), respectively. (B) Daytime course of light intensity during a typical sunny day (dotted line) and cloudy day (solid line). (C) Temporal changes in average daytime (solid line) and nighttime (dotted line) temperatures. (D) Temporal changes in air relative humidity (solid line) and average daily light intensity (dotted line). PAR = photosynthetically active radiation; DAT = days after transplanting.

  • View in gallery

    Effects of CO2 enrichment and supplementary lighting on (A) plant height, (B) stem diameter, (C) leaf area, and (D) leaf number of tomato plants grown in a greenhouse. Values represent the means ± se (n = 4). Different letters indicate significant differences at P < 0.05 according to Duncan’s multiple range test. CaLn = ambient CO2 and no supplementary light; CeLn = CO2 enrichment and no supplementary light; CaLs = ambient CO2 and supplementary light; CeLs = CO2 enrichment and supplementary light.

  • View in gallery

    Effects of CO2 enrichment and supplementary light on (A) net photosynthetic rate (Pn), (B) stomatal conductance (gS), (C) transpiration rate (Tr), and (D) water use efficiency (WUE; calculated as Pn/Tr) of tomato plants grown in a greenhouse, with values shown representing means ± se (n = 6). DAT = days after transplanting; CaLn = ambient CO2 and no supplementary light; CeLn = CO2 enrichment and no supplementary light; CaLs = ambient CO2 and supplementary light; CeLs = both CO2 enrichment and supplementary light.

  • View in gallery

    The spectral distribution of high pressure sodium lamps.

  • Bencze, S., Keresztényi, I., Varga, B., Kőszegi, B., Balla, K., Gémesné-Juhász, A. & Veisz, O. 2011 Effect of CO2 enrichment on canopy photosynthesis, water use efficiency and early development of tomato and pepper hybrids Acta Agron. Hung. 59 275 284

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  • Bergstrand, K.J., Suthaparan, A., Mortensen, L.M. & Gisleröd, H.R. 2016 Photosynthesis in horticultural plants in relation to light quality and CO2 concentration Eur. J. Hort. Sci. 81 237 242

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  • Carvalho, L.C. & Amâncio, S. 2002 Antioxidant defence system in plantlets transferred from in vitro to ex vitro: Effects of increasing light intensity and CO2 concentration Plant Sci. 162 33 40

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  • Chalabi, Z.S., Biro, A., Bailey, B.J., Aikman, D.P. & Cockshull, K.E. 2002 SE-structures and environment: Optimal control strategies for carbon dioxide enrichment in greenhouse tomato crops. Part 1: Using pure carbon dioxide Biosyst. Eng. 81 421 431

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  • Di, Y. 1999 Fundamental studies on the effect of light intensity on quality and capsaicin degradation metabolism in hot pepper (Capsicun annuum L.) fruits. China Agric. Univ., Master’s thesis

  • Fan, X.X., Xu, Z.G., Liu, X.Y., Tang, C.M., Wang, L.W. & Han, X.L. 2013 Effects of light intensity on the growth and leaf development of young tomato plants grown under a combination of red and blue light Scientia Hort. 153 50 55

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  • Fierro, A., Tremblay, N. & Gosselin, A. 1994 Supplemental carbon dioxide and light improved tomato and pepper seedling growth and yield HortScience 29 152 154

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  • Fukuda, N., Fjita, M., Ohta, Y., Sase, S., Nishimura, S. & Ezura, H. 2008 Directional blue light irradiation triggers epidermal cell elongation of abaxial side resulting in inhibition of leaf epinasty in geranium under red light condition Scientia Hort. 115 176 182

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  • Hao, X., Guo, X.B., Chen, X.J., Zheng, L. & Kholsa, C.S. 2017 Dynamic temperature integration with temperature drop improved the response of greenhouse tomato to long photoperiod of supplemental lighting Acta Hort. 1170 995 1002

    • Search Google Scholar
    • Export Citation
  • Helyes, L., Lugasi, A., Peli, E. & Pek, Z. 2015 Effect of elevated CO2 on lycopene content of tomato (Lycopersicon lycopersicum L. karsten) fruits Acta Aliment. Hung. 40 80 86

    • Search Google Scholar
    • Export Citation
  • Hernández, R., Eguchi, T., Deveci, M. & Kubota, C. 2016 Tomato seedling physiological responses under different percentages of blue and red photon flux ratios using LEDs and cool white fluorescent lamps Scientia Hort. 213 270 280

    • Search Google Scholar
    • Export Citation
  • Hikosaka, S., Iyoki, S., Hayakumo, M. & Goto, E. 2013 Effects of light intensity and amount of supplemental LED lighting on photosynthesis and fruit growth of tomato plants under artificial conditions J. Agr. Meteorol. 69 93 100

    • Search Google Scholar
    • Export Citation
  • Ho, L.C. 2003 Genetic and cultivation manipulation for improving tomato fruit quality Acta Hort. 613 21 31

  • Hooper, L. & Cassidy, A. 2006 A review of the health care potential of bioactive compounds J. Sci. Food Agr. 86 1805 1813

  • Jia, Y., Tang, S., Wang, R., Ju, X., Ding, Y., Tu, S. & Smith, D.L. 2010 Effects of elevated CO2 on growth, photosynthesis, elemental composition, antioxidant level, and phytochelatin concentration in Lolium mutiforum and Lolium perenne under Cd stress J. Hazard. Mater. 180 384 394

    • Search Google Scholar
    • Export Citation
  • Jiang, C., Johkan, M., Hohjo, M., Tsukagoshi, S., Ebihara, M., Nakaminami, A. & Maruo, T. 2017 Photosynthesis, plant growth, and fruit production of single-truss tomato improves with supplemental lighting provided from underneath or within the inner canopy Scientia Hort. 222 221 229

    • Search Google Scholar
    • Export Citation
  • Jin, J., Lauricella, D., Armstrong, R., Sale, P. & Tang, C. 2014 Phosphorus application and elevated CO2 enhance drought tolerance in field pea grown in a phosphorus-deficient vertisol Ann. Bot. 116 975 985

    • Search Google Scholar
    • Export Citation
  • Jolliet, O., Bailey, B.J., Hand, D.J. & Cockshull, K. 1993 Tomato yield in greenhouses related to humidity and transpiration Acta Hort. 328 115 124

  • Kaiser, E., Zhou, D.F., Heuvelink, E., Harbinson, J., Morales, A. & Marcelis, L.F.M. 2017 Elevated CO2 increases photosynthesis in fluctuating irradiance regardless of photosynthetic induction state J. Expt. Bot. 68 5629 5640

    • Search Google Scholar
    • Export Citation
  • Kampfenkel, K., Montagu, M.V. & Inzé, D. 1995 Effects of iron excess on Nicotiana plumbaginifolia plants: Implications to oxidative stress Plant Physiol. 107 725 735

    • Search Google Scholar
    • Export Citation
  • Kläring, H.P., Hauschild, C., Heißner, A. & Baryosef, B. 2007 Model-based control of CO2 concentration in greenhouses at ambient levels increases cucumber yield Agr. For. Meteorol. 143 208 216

    • Search Google Scholar
    • Export Citation
  • Ksiksi, T. & Youssef, T. 2010 Effects of CO2 enrichment on growth partitioning of Chloris gayana in the arid environment of the UAE Grassl. Sci. 56 183 187

    • Search Google Scholar
    • Export Citation
  • Labeke, M.C.V. & Dambre, P. 1998 Effect of supplementary lighting and CO2 enrichment on yield and flower stem quality of Alstroemeria cultivars Scientia Hort. 74 269 278

    • Search Google Scholar
    • Export Citation
  • Lichtenthaler, H. & Wellburn, A. 1983 Determination of total carotenoids and chlorophylls a and b of leaf in different solvents Biochem. Soc. Trans. 11 591 592

    • Search Google Scholar
    • Export Citation
  • Li, X.J., Kang, S.Z., Li, F.S., Zhang, X.T., Huo, Z.L., Ding, R.S., Tong, L., Du, T.S. & Li, S.E. 2017 Light supplement and carbon dioxide enrichment affect yield and quality of off-season pepper Agron. J. 109 2107 2118

    • Search Google Scholar
    • Export Citation
  • Li, Q. & Kubota, C. 2009 Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce J. Environ. Exp. Bot. 67 59 64

  • Ma, X., Liu, S., Li, Y. & Gao, Q. 2015 Effectiveness of gaseous CO2 fertilizer application in China’s greenhouses between 1982 and 2010 J. CO2 Util. 11 63 66

    • Search Google Scholar
    • Export Citation
  • Madhana, S.K., Rachapudi, V.S., Mudalkar, S. & Reddy, A.R. 2014 Persistent stimulation of photosynthesis in short rotation coppice mulberry under elevated CO2 atmosphere J. Photochem. Photobiol. B 137 21 30

    • Search Google Scholar
    • Export Citation
  • Mamatha, H., Srinivasarao, N.K., Laxman, R.H., Shivashankara, K.S., Bhatt, R.M. & Pavithra, K.C. 2014 Impact of elevated CO2 on growth, physiology, yield, and quality of tomato (Lycopersicon esculentum Mill) cv. Arka Ashish Photosynthetica 52 519 528

    • Search Google Scholar
    • Export Citation
  • Marković, K., Hruškar, M. & Vahčić, N. 2006 Lycopene content of tomato products and their contribution to the lycopene intake of Croatians Nutr. Res. 26 556 560

    • Search Google Scholar
    • Export Citation
  • Nabity, P.D., Hillstrom, M.L., Lindroth, R.L. & Delucia, E.H. 2012 Elevated CO2 interacts with herbivory to alter chlorophyll fluorescence and leaf temperature in Betula papyrifera and Populus tremuloides Oecologia 169 905 913

    • Search Google Scholar
    • Export Citation
  • Naing, A.H., Jeon, S.M., Park, J.S. & Kim, C.K. 2016 Combined effects of supplementary light and CO2 on rose growth and the production of good quality cut flowers Can. J. Plant Sci. 96 503 510

    • Search Google Scholar
    • Export Citation
  • Nilsen, S., Hovland, K., Dons, C. & Sletten, S.P. 1983 Effect of CO2 enrichment on photosynthesis, growth and yield of tomato Scientia Hort. 20 1 14

  • O’Carrigan, A., Hinde, E., Lu, N., Xu, X.Q., Duan, H.L., Huang, G.M., Mak, M., Bellotti, B. & Chen, Z.H. 2014 Effects of light irradiance on stomatal regulation and growth of tomato Environ. Exp. Bot. 98 65 73

    • Search Google Scholar
    • Export Citation
  • Pazzagli, P.T., Weiner, J. & Liu, F.L. 2016 Effects of CO2 elevation and irrigation regimes on leaf gas exchange, plant water relations, and water use efficiency of two tomato cultivars Agr. Water Mgt 169 26 33

    • Search Google Scholar
    • Export Citation
  • Rasineni, G.K., Guha, A. & Reddy, A.R. 2011 Responses of Gmelina arborea, a tropical deciduous tree species, to elevated atmospheric CO2: Growth, biomass productivity and carbon sequestration efficacy Plant Sci. 181 428 438

    • Search Google Scholar
    • Export Citation
  • Simkin, A.J., Mcausland, L., Headland, L.R., Lawson, T. & Raines, C.A. 2015 Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco J. Expt. Bot. 66 1 16

    • Search Google Scholar
    • Export Citation
  • Tewolde, F.T., Na, L., Shiina, K., Maruo, T., Takagaki, M., Kozai, T. & Yamori, W. 2016 Nighttime supplemental LED inter-lighting improves growth and yield of single-truss tomatoes by enhancing photosynthesis in both winter and summer Front. Plant Sci. 7 1 10

    • Search Google Scholar
    • Export Citation
  • Tsujita, M.J. & Dutton, R.G. 1983 Root zone temperature effects on greenhouse roses in relation to supplementary lighting at reduced air temperature HortScience 18 874 876

    • Search Google Scholar
    • Export Citation
  • Urban, O., Klem, K., Holisová, P., Sigut, L., Sprtová, M., Teslová-Navrátilová, P., Zitová, M., Spunda, V., Marek, M.V. & Grace, J. 2014 Impact of elevated CO2 concentration on dynamics of leaf photosynthesis in Fagus sylvatica is modulated by sky conditions Environ. Pollut. 185 271 280

    • Search Google Scholar
    • Export Citation
  • Wang, G. & Feng, X. 2012 Response of plants’ water use efficiency to increasing atmospheric CO2 concentration Environ. Sci. Technol. 46 8610 8620

    • Search Google Scholar
    • Export Citation
  • Wei, Z.H., Du, T.C., Li, X.N., Fang, L. & Liu, F.L. 2018a Interactive effects of CO2 concentration elevation and nitrogen fertilization on water and nitrogen use efficiency of tomato grown under reduced irrigation regimes Agr. Water Mgt. 202 174 182

    • Search Google Scholar
    • Export Citation
  • Wei, Z.H., Du, T.C., Li, X.N., Fang, L. & Liu, F.L. 2018b Simulation of stomatal conductance and water use efficiency of tomato leaves exposed to different irrigation regimes and air CO2 concentrations by a modified “ball-berry” model Front. Plant Sci. 9 1 13

    • Search Google Scholar
    • Export Citation
  • Wu, H.C. & Lin, C.C. 2013 Carbon dioxide enrichment during photoautotrophic micropropagation of Protea cynaroides L. plantlets improves in vitro growth, net photosynthetic rate, and acclimatization HortScience 48 1293 1297

    • Search Google Scholar
    • Export Citation
  • Yamori, W. 2013 Improving photosynthesis to increase food and fuel production by biotechnological strategies in crops J. Plant Biochem. Physiol. 1 1 3

    • Search Google Scholar
    • Export Citation
  • Yamori, W. 2016 Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress J. Plant Res. 129 379 395

    • Search Google Scholar
    • Export Citation
  • Yamori, W., Kondo, E., Sugiura, D., Terashima, I., Suzuki, Y. & Makino, A. 2016 Enhanced leaf photosynthesis as a target to increase grain yield: Insights from transgenic rice lines with variable Rieske FeS protein content in the cytochrome b6/f complex Plant Cell Environ. 39 80 87

    • Search Google Scholar
    • Export Citation
  • Yamori, W. & Shikanai, T. 2016 Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth Annu. Rev. Plant Biol. 67 1 26

    • Search Google Scholar
    • Export Citation
  • Yelle, S., Beeson, R.C.J., Trudel, M.J. & Gosselin, A. 1990 Duration of CO2 enrichment influences growth, yield, and gas exchange of two tomato species J. Amer. Soc. Hort. Sci. 115 52 57

    • Search Google Scholar
    • Export Citation
  • Yu, G.R. & Wang, Q.F. 2010 Ecophysiology of plant photosynthesis, transpiration, and water use. Science Press, Beijing, China

  • Zhang, Z.M., Liu, L.H., Zhang, M., Zhang, Y.S. & Wang, Q.M. 2014 Effect of carbon dioxide enrichment on health-promoting compounds and organoleptic properties of tomato fruits grown in greenhouse Food Chem. 153 157 163

    • Search Google Scholar
    • Export Citation
  • Zou, Q.Y., Ji, J.W. & Li, Z.M. 2016 Effect of supplemental light with different spectral LEDs on the growth of tomato seedlings in north greenhouse, p. 377–380. In: H. Wang and X. Jia (eds.). 2nd International Forum on Electrical Engineering and Automation. Atlantis Press, Amsterdam/Paris

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