Leaf Shape, Growth, and Antioxidant Phenolic Compounds of Two Lettuce Cultivars Grown under Various Combinations of Blue and Red Light-emitting Diodes

in HortScience

Light-emitting diodes (LEDs) of short wavelength ranges are being developed as light sources in closed-type plant production systems. Among the various wavelengths, red and blue lights are known to be effective for enhancing plant photosynthesis. In this study, we determined the effects of blue and red LED ratios on leaf shape, plant growth, and the accumulation of antioxidant phenolic compounds of a red leaf lettuce (Lactuca sativa L. ‘Sunmang’) and a green leaf lettuce (Lactuca sativa L. ‘Grand Rapid TBR’). Lettuce seedlings grown under normal growth conditions (20 °C, fluorescent lamp + high-pressure sodium lamp 177 ± 5 μmol·m−2·s−1, 12-hour photoperiod) for 18 days were transferred into growth chambers that were set at 20 °C and equipped with various combinations of blue (456 nm) and red (655 nm) LEDs [blue:red = 0:100 (0 B), 13:87 (13 B), 26:74 (26 B), 35:65 (35 B), 47:53 (47 B) or 59:41 (59 B)] under the same light intensity and photoperiod (171 ± 7 μmol·m−2·s−1, 12-hour photoperiod). Leaf width, leaf length, leaf area, fresh and dry weights of shoots and roots, chlorophyll content (SPAD value), total phenolic concentration, total flavonoid concentration, and antioxidant capacity were measured at 2 and 4 weeks after the onset of LED treatment. The leaf shape indices (leaf length/leaf width) of the two lettuce cultivars subjected to blue LEDs treatment were similar to the control, regardless of the blue-to-red ratio during the entire growth stage. However, 0 B (100% red LED) induced a significantly higher leaf shape index, which represents elongated leaf shape, compared with the other treatments. Increasing blue LED levels negatively affected lettuce growth. Most growth characteristics (such as the fresh and dry weights of shoots and leaf area) were highest under 0 B for both cultivars compared with all other LED treatments. For red and green leaf lettuce cultivar plants, shoot fresh weight under 0 B was 4.3 and 4.1 times higher compared with that under 59 B after 4 weeks of LED treatment, respectively. In contrast, the accumulation of chlorophyll, phenolics (including flavonoids), and antioxidants in both red and green leaf lettuce showed an opposite trend compared with that observed for growth. The SPAD value (chlorophyll content), total phenolic concentration, total flavonoid concentration, and antioxidant capacity of lettuces grown under high ratios of blue LED (such as 59 B, 47 B, and 35 B) were significantly higher compared with 0 B or control conditions. Thus, this study indicates that the ratio of blue to red LEDs is important for the morphology, growth, and phenolic compounds with antioxidant properties in the two lettuce cultivars tested.

Abstract

Light-emitting diodes (LEDs) of short wavelength ranges are being developed as light sources in closed-type plant production systems. Among the various wavelengths, red and blue lights are known to be effective for enhancing plant photosynthesis. In this study, we determined the effects of blue and red LED ratios on leaf shape, plant growth, and the accumulation of antioxidant phenolic compounds of a red leaf lettuce (Lactuca sativa L. ‘Sunmang’) and a green leaf lettuce (Lactuca sativa L. ‘Grand Rapid TBR’). Lettuce seedlings grown under normal growth conditions (20 °C, fluorescent lamp + high-pressure sodium lamp 177 ± 5 μmol·m−2·s−1, 12-hour photoperiod) for 18 days were transferred into growth chambers that were set at 20 °C and equipped with various combinations of blue (456 nm) and red (655 nm) LEDs [blue:red = 0:100 (0 B), 13:87 (13 B), 26:74 (26 B), 35:65 (35 B), 47:53 (47 B) or 59:41 (59 B)] under the same light intensity and photoperiod (171 ± 7 μmol·m−2·s−1, 12-hour photoperiod). Leaf width, leaf length, leaf area, fresh and dry weights of shoots and roots, chlorophyll content (SPAD value), total phenolic concentration, total flavonoid concentration, and antioxidant capacity were measured at 2 and 4 weeks after the onset of LED treatment. The leaf shape indices (leaf length/leaf width) of the two lettuce cultivars subjected to blue LEDs treatment were similar to the control, regardless of the blue-to-red ratio during the entire growth stage. However, 0 B (100% red LED) induced a significantly higher leaf shape index, which represents elongated leaf shape, compared with the other treatments. Increasing blue LED levels negatively affected lettuce growth. Most growth characteristics (such as the fresh and dry weights of shoots and leaf area) were highest under 0 B for both cultivars compared with all other LED treatments. For red and green leaf lettuce cultivar plants, shoot fresh weight under 0 B was 4.3 and 4.1 times higher compared with that under 59 B after 4 weeks of LED treatment, respectively. In contrast, the accumulation of chlorophyll, phenolics (including flavonoids), and antioxidants in both red and green leaf lettuce showed an opposite trend compared with that observed for growth. The SPAD value (chlorophyll content), total phenolic concentration, total flavonoid concentration, and antioxidant capacity of lettuces grown under high ratios of blue LED (such as 59 B, 47 B, and 35 B) were significantly higher compared with 0 B or control conditions. Thus, this study indicates that the ratio of blue to red LEDs is important for the morphology, growth, and phenolic compounds with antioxidant properties in the two lettuce cultivars tested.

The consumption of plant-based foods represents one of the essential components for the nutrition of humans. In this aspect, increasing crop yield is the most fundamental and important issue for farmers and agronomists and will continue to be in the future. The importance of the fruits and vegetables that we ingest daily has been rediscovered, because horticultural crops contain various types of health-promoting phytochemicals, including antioxidant, anticancer, and anti-inflammatory substances (Brandt et al., 2004; Pennington and Fisher, 2009). In particular, phenolic compounds, which are one of the most widely occurring groups of phytochemicals, exhibit various types of physiological properties, including antioxidant activity (Balasundram et al., 2006). Many epidemiological studies have shown that the intake of fruits and vegetables maintains and improves human health (Hooper and Cassidy, 2006). Thus, improving the quality of fruits and vegetables is a matter of interest for both consumers and producers.

Among several environmental factors affecting crop yield and quality, light is a crucial factor. Basically, light is an energy source for photosynthesis. In addition, various components contribute to light serving as a signal stimulus to plants, including light intensity, light quality, and daylength. Plants perceive light signals through photoreceptors such as phytochromes, cryptochromes, and phototropins. Consequently, most developmental processes that occur throughout the life cycle of plants are dependent on light, including seed germination, phototropism, gravitropism, chloroplast movement, shade avoidance, circadian rhythms, and flower induction (Carvalho et al., 2011; Jiao et al., 2007). In the case of growing a crop under different light sources, each cultural practice must be differentiated, because each light source has a unique light quality that directly affects plant growth and development.

Recently, LEDs have been used as sources of artificial lighting in closed-type plant production systems, where environmental conditions are controlled, allowing crops to be produced throughout the year regardless of external weather conditions. In comparison with other conventional artificial lighting sources used in plant cultivation, LEDs have the advantages of high light-conversion efficiency with low radiant heat output, semipermanence, and small mass; hence, plants may be irradiated close to the plants. In addition, LEDs are available in a variety of narrow wavebands; hence, it is possible to optimize light quality to improve both crop yield and quality (Morrow, 2008; Yeh and Chung, 2009).

Blue and red LEDs are usually used for plant growth because chlorophyll a and b efficiently absorb wavelengths in the blue (maximum absorption at 430 and 453 nm) and red (maximum absorption at 663 and 642 nm) ranges (Hopkins and Huner, 2004). Previous studies assessing the effects of red and blue wavelengths on plants indicated that red LED generally induces plant growth by increasing fresh and dry plant weight, plant height, and leaf area (Heo et al., 2012; Johkan et al., 2010; Wang et al., 2009; Wu et al., 2007). In comparison, blue LED influences photosynthetic function, chlorophyll formation, and chloroplast development rather than having a direct effect on biomass accumulation (Johkan et al., 2010; Savvides et al., 2012; Wang et al., 2009). The synergetic effect was observed when mixtures of blue and red LEDs were used to irradiate plants. Mixed light conditions enhance the growth of various vegetables, including lettuce, more compared with red LEDs alone (Hogewoning et al., 2010; Matsuda et al., 2007; Savvides et al., 2012; Stutte et al., 2009; Yorio et al., 2001). However, other studies have reported the opposite results (Heo et al., 2012; Johkan et al., 2010). It is difficult to understand how plants respond to changes in blue and red light ratios because most existing LED-related studies simply compare plant growth for specific ratios of blue and red LEDs, leading to inconsistent results.

Thus, this study aimed at determining the effect of different blue and red LED ratios on the morphological changes, growth characteristics, and the accumulation of antioxidant phenolic compounds of two lettuce cultivars. The results obtained from this study are expected to provide baseline information toward designing artificial lighting sources in closed-type plant production systems.

Materials and Methods

Plant growth conditions and light spectrum.

Seeds of red leaf lettuce (Lactuca sativa L. ‘Sunmang’; Nongwoo Bio Co., Suwon, Korea) and green leaf lettuce (Lactuca sativa L. ‘Grand Rapid TBR’; Asia Seed Co., Seoul, Korea) were sown in a 105-plug tray (32 mL/cell, two seeds per cell) containing a growing medium (Myung-Moon; Dongbu Hannong Co., Seoul, Korea). One of two seedlings per cell was thinned 1 week after sowing. The plants were then grown within a growth chamber (DS-96S; Dasol Scientific Co., Hwaseong, Korea) with normal growing conditions [20 °C, fluorescent lamp + high-pressure sodium lamp, photosynthetic photon flux (PPF) 177 ± 5 μmol·m−2·s−1, 12-h photoperiod] for 18 d. Fifteen seedling plugs per treatment were transferred to a growth chamber (VS-1203P1; Vision Scientific Co., Daejeon, Korea) equipped with six different blue and red LED ratios and a growth chamber (DS-96S; Dasol Scientific Co., Hwaseong, Korea) to serve as the control. The six lighting sources using LEDs, which were plate type (48 × 48 cm, length × width), were manufactured to generate a combination of blue (456 nm; Itswell Co., Incheon, Korea) and red (655 nm; Bright LED Electronics Co., Seoul, Korea) LEDs. The spectral distribution was initially measured at 25 cm from LED lighting sources to top of the pots and at five points (center and four edges of a tray including pots) using a spectroradiometer (LI-1800; LI-COR, Lincoln, NE), which presented as relative spectral distribution (Fig. 1). All plants were grown at 20 °C, PPF of 171 ± 7 μmol·m−2·s−1, and a 12-h photoperiod for 4 weeks. The PPF of each LED treatment, which was measured at the top of lettuce plants, was maintained at a similar level by adjusting currents of LED lighting systems. To minimize light distribution being disproportionate within each treatment, the pots were systematically rearranged everyday. For the first 18 d after sowing, distilled water (2 L) was subirrigated to pots in a tray at intervals of 2 to 3 d, and a nutrient solution for lettuce (17.3N–4.0P–8.0K) was subirrigated to the lettuce plants once a week for the rest of the cultivation period. The pH and electrical conductivity of the nutrient solution were 5.5 and 1.16 dS·m−1, respectively.

Fig. 1.
Fig. 1.

Relative spectral distribution of various combinations of blue and red light-emitting diodes (LEDs) used in this study. (A) blue:red = 0:100, (B) blue:red = 13:87, (C) blue:red = 26:74, (D) blue:red = 35:65, (E) blue:red = 47:53, (F) blue:red = 59:41, and (G) control (fluorescent lamp + high-pressure sodium lamp). Total photosynthetic photon flux (PPF) was 171 ± 7 μmol·m−2·s−1 in each treatment. Spectral scans were measured at 25 cm from LED lighting sources and at five points (a center and four edges of each tray of pots).

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

Growth characteristics.

Growth characteristics such as the fresh and dry weights of shoots and roots, shoot/root ratio (S/R ratio), total leaf area, and chlorophyll content (SPAD value) were measured at 4 weeks after the onset of LED treatment. The shoots and roots were dried at 70 °C in a drying oven (FS-420; Advantec Co., Tokyo, Japan) for 3 d and were weighed to determine dry weight using a scale (Si-234; Denver Instrument, New York, NY). The S/R ratio was calculated from the fresh weight of shoots and roots. Total leaf area and SPAD value were measured using a leaf area meter (LI-3000A; LI-COR) and a portable chlorophyll meter (SPAD-502; Minolta, Osaka, Japan), respectively. The most fully expanded leaf was used for leaf shape indices, which were determined as the leaf length divided by the leaf width at 0, 2, and 4 weeks after the onset of LED treatment.

Chlorophyll fluorescence.

Chlorophyll fluorescence [maximum variable fluorescence (Fv)/maximum fluorescence (Fm)] was measured to evaluate the maximal photochemical efficiency of photosystem II in ‘Grand Rapid TBR’ green leaf lettuce plants grown under various combinations of blue and red LEDs and under the control treatment. Measurements of Fv/Fm were recorded at 0, 2, and 4 weeks after the onset of LED treatment using a chlorophyll fluorescence meter (PAM 2000; Walz, Effeltrich, Germany). Fully expanded leaves were kept in the dark for ≈30 min, and then Fm and minimum fluorescence (Fo) were obtained by applying 1100 μmol·m−2·s−1 PPF saturating light pulse (20 kHz). The maximum PS II quantum yield (Fv/Fm) was calculated using the equation Fv/Fm = (Fm – Fo)/Fm.

Total phenolic concentration.

To analyze the total phenolic concentration of leaves, the third leaf from the top was collected at 4 weeks after the onset of LED treatment and stored in a deep freezer at –70 °C (DF8524; IlShinBioBase Co., Dongducheon, Korea) until use. The total phenolic concentration of lettuce was determined using the modified Folin-Ciocalteu reagent method (Ainsworth and Gillespie, 2007). Approximately 0.2 g of each sample was macerated in a mortar and pestle with liquid nitrogen and extracted with 3 mL of 80% (v/v) acetone for a phenolic substance. Approximately 1 mL of extract was placed in a microtube and incubated in darkness at 4 °C overnight. Subsequently, the extract was centrifuged at 905 gn for 2 min, and the supernatant was used to measure the total phenolic concentration. A mixture of 135 μL distilled water, 750 μL 1/10 dilution Folin-Ciocalteau reagent (Sigma-Aldrich, St. Louis, MO), and 600 μL 7.5% (w/v) Na2CO3 was added to 50 μL of the extract and vortexed for 10 s. The mixture was incubated at 45 °C in a water bath (MSB-2011D; Mono Tech Co., Siheung, Korea) for 15 min and allowed to cool down to room temperature. The absorbance of samples was read at 765 nm with a blank [50 μL of 80% (v/v) acetone] using a spectrophotometer (ultraviolet-1800; Shimadzu Co., Kyoto, Japan). A standard curve was prepared from a freshly made 1 mg·mL−1 gallic acid [Acros Organics, Geel, Belgium in 80% (v/v) acetone)] stock solution. The total phenolic concentration of lettuce was expressed as milligrams gallic acid equivalent (GAE) per gram of fresh weight of lettuce leaves.

Antioxidant capacity.

The collection method for antioxidant capacity was the same as that for total phenolic concentration. The antioxidant capacity of lettuce leaves was determined using the modified 2,2′-azino-bis (3-ethylbenzthiazoline-6-sulfonic acid) (ABTS) method (Miller and Rice-Evans, 1996; Pennycooke et al., 2005). Lettuce samples were extracted with 3 mL of 80% (v/v) acetone, and the extract was incubated overnight in darkness at –20 °C. Subsequently, the extract was centrifuged at 905 gn for 2 min, and the supernatant was used to measure the antioxidant capacity. ABTS [(2.5 mm) Sigma-Aldrich] solution was mixed with ≈0.4 g of MnO2 (Sigma-Aldrich) to generate ABTS radical cation (ABTS*) for 30 min at room temperature. ABTS* solution was filtered using a 0.22-μM syringe filter (NS25-N02; Noble Bio Co., Suwon, Korea) and was incubated in a water bath at 30 °C. To obtain an ABTS* solution with an absorbance of 0.7 (± 0.02) at 730 nm, 5 mm phosphate-buffered saline solution [pH 7.4, ionic strength (150 mm NaCl)] was used for dilution. A 100 μL of the extract was added to 1 mL of ABTS* solution and vortexed for 10 s and then the mixture was measured at 730 nm in a spectrophotometer after 1 min of reaction period. Trolox [(6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxyl acid) (Sigma-Aldrich)] standard curve was prepared using the 0.5-mm stock solution. The antioxidant capacity of lettuce was expressed as millimoles Trolox equivalent antioxidant capacity (TEAC) per gram of fresh weight of lettuce leaves.

Total flavonoid concentration.

Total flavonoid concentration was determined according to the method of Dewanto et al. (2002). Approximately 0.2 g of the fourth leaf from the top, which were collected at 4 weeks after the onset of LED treatment, were extracted with 3 mL of 70% (v/v) ethanol (pH 3.2, using formic acid) and placed in the dark at 4 °C for 12 h. Subsequently, the extract was centrifuged at 905 gn for 2 min, and the supernatant was used to measure the total flavonoid concentration. A mixture of 1.25 mL distilled water and 75 μL of 5% NaNO2 was added to 250 μL of the extract. After 6 and 5 min, the mixture was sequentially added to 150 μL of 10% AlCl3 and 500 μL of 1 M NaOH with 275 μL of distilled water, respectively. A blank (control) was prepared using 250 μL of 70% ethanol (pH 3.2, using formic acid) instead of the extract. The absorbance of the mixture was measured at 510 nm. The total flavonoid concentration of lettuce was expressed as milligrams of (+)-catechin hydrate equivalents per gram of fresh weight of lettuce leaves.

Statistical analysis.

Four plants per treatment were used to determine all growth and antioxidant phenolic compounds, except for leaf shape index and SPAD value, which has eight samples per treatment. Chlorophyll fluorescence was determined by using three plants per treatment. The experiment was repeated twice to verify reproducibility. The statistical analysis was performed using the statistical analysis system (SAS 9.2; SAS Institute Inc., Cary, NC) program. Analysis of variance was performed and Duncan’s multiple range test was used to compare the means.

Results

Growth characteristics and leaf shape.

Both lettuce cultivars grown under various ratios of blue to red LEDs showed significant differences in growth characteristics such as the fresh and dry weights of shoots and roots, leaf area, and S/R ratio (Table 1). For the red leaf lettuce ‘Sunmang’, the fresh and dry weights of shoots and leaf area increased with an increasing proportion of red LEDs. The fresh weight of 0 B (100% red LED) was ≈2.8 times higher than that of control. In addition, 13 B and 26 B significantly induced a higher fresh weight of shoots compared with the control, although these treatments were less effective than 0 B. In comparison, an increase in blue LED ratio had a negative effect on shoot growth. Treatments of 35 B, 47 B, and 59 B showed no significant difference in the fresh and dry weights of shoots and leaf area compared with the control. As the ratio of red LED increased, the lettuce also showed more vigorous root growth, which was a similar trend as that observed for shoot growth. The S/R ratio was highest for lettuce plants grown under 0 B, whereas blue LEDs induced a significant decrease in this ratio. Some of the results obtained for the green leaf lettuce ‘Grand Rapid TBR’ differed from those obtained for ‘Sunmang’, although overall trend was similar for both cultivars. For ‘Grand Rapid TBR’, the fresh weight of shoots was significantly higher under 0 B and 13 B compared with the control, whereas root growth was unaffected by blue and red LED ratios. ‘Grand Rapid TBR’ showed a significant difference between 0 B and the other treatments including control for the S/R ratio. The S/R ratio under 0 B was ≈2.6 to 3.4 times higher than the ratio for plants grown under blue LED-contained treatments.

Table 1.

Growth characteristics of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment (n = 4).

Table 1.

Fv/Fm varied with different blue and red LED ratios in ‘Grand Rapid TBR’ (Table 2). Fv/Fm gradually decreased as the ratio of blue LEDs was reduced after 2 weeks of LED treatment. The value under 0 B declined to 0.75, which was a significant decrease compared with the other treatments. At harvest, there was also a significant decrease in Fv/Fm under 0 B; however, significant differences between treatments having both blue and red LEDs were not observed. Control lettuce plants showed normal Fv/Fm values (≈0.815 to 0.825) after both 2 and 4 weeks of LED treatment.

Table 2.

Chlorophyll fluorescence (Fv/Fm) of green leaf lettuce (‘Grand Rapid TBR’) grown under various combinations of blue and red light-emitting diodes (LEDs) at 0, 2, and 4 weeks after the onset of LED treatment (n = 3).

Table 2.

The blue and red LED ratio also affected the chlorophyll content in the leaves of the two leafy lettuce cultivars (Fig. 2). The SPAD value of the two lettuce cultivars grown under 0 B without blue LEDs was significantly lower compared with the other blue LED treatments and the control. For ‘Sunmang’, the SPAD value increased as the proportion of blue LEDs increased, showing the highest value under 47 B. Although the change in SPAD values for ‘Grand Rapid TBR’ was not as clear as for ‘Sunmang’, treatments containing more than 26% of blue light induced high SPAD values. The SPAD values of the ‘Sunmang’ and ‘Grand Rapid TBR’ controls were similar for plants grown under 35 B and 26 B, respectively.

Fig. 2.
Fig. 2.

SPAD value (chlorophyll content) of two lettuce cultivars grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 8). Significant at P = 0.001.

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

The ratio of blue to red LEDs directly affected leaf shape for both cultivars with 2 weeks of LED treatment (Fig. 3). The leaf shape index of treatments containing blue LEDs was similar to that of the control, regardless of the blue LED ratio. In contrast, only the red LED treatment (0 B) induced a significantly higher leaf shape index compared with the other treatments.

Fig. 3.
Fig. 3.

Leaf shape index at 2 and 4 weeks after the onset of light-emitting diode (LED) treatment (left) and lettuce plants grown under various combinations of blue and red LEDs at 4 weeks after the onset of LED treatment (right) in both ‘Sunmang’ (A) and ‘Grand Rapid TBR’ (B). Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 8). Significant at P = 0.001.

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

Antioxidant phenolic compounds.

The blue and red LED ratio significantly altered the total phenolic concentration in both cultivars (Fig. 4). In contrast to the results obtained for growth characteristics, increased blue LED ratios stimulated the accumulation of total phenolics. ‘Sunmang’ lettuce plants grown under 47 B had 1.4 and 2.4 times significantly higher total phenolic concentration compared with those grown under the control and 0 B, respectively, at 4 weeks after the onset of LED treatment. The total phenolic concentrations under 26 B to 59 B for ‘Grand Rapid TBR’ were 2.2 to 2.7 times significantly higher compared with the control. The lettuce plants grown under 0 B and 13 B had similar total phenolic concentrations as the control.

Fig. 4.
Fig. 4.

Total phenolic concentrations of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 4). Significant at P = 0.001.

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

Antioxidant capacity also showed a similar trend to total phenolic concentration at 4 weeks after the onset of LED treatment (Fig. 5). For ‘Sunmang’, as the proportion of blue LEDs increased, the production of antioxidants was promoted with the highest value being obtained under 47 B. Although ‘Grand Rapid TBR’ also showed high antioxidant capacity in blue LED-rich treatments, there were no significant difference between treatments with blue LEDs above 26%. When comparing the two lettuce cultivars, the red leaf lettuce ‘Sunmang’ had more antioxidants than the green leaf lettuce ‘Grand Rapid TBR’ under all tested light conditions.

Fig. 5.
Fig. 5.

Antioxidant capacity of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 4). Significant at P = 0.01.

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

Most changes in total flavonoid concentrations with differences in blue and red LED ratio were similar to those recorded for total phenolic concentration and antioxidant capacity in both cultivars, except under 0 B for ‘Sunmang’ (Fig. 6). Flavonoid concentration of 0 B for ‘Sunmang’ was similar to that of 35 B and 47 B. The 59 B treatment induced the highest total flavonoid concentrations for ‘Grand Rapid TBR’.

Fig. 6.
Fig. 6.

Total flavonoid concentration of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 4). Significant at P = 0.01.

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

Discussion

In this study, varied ratios of blue to red LEDs were applied to identify the relationship of the two wavelengths in terms of lettuce growth and intracellular phenolic compounds with antioxidant properties. This aspect distinguishes the current study from previous LED-related studies, in which limited specific ratios of blue to red LEDs were applied to plants. The growth characteristic results for the two lettuce cultivars grown under various ratios of blue to red LEDs confirmed that red LED serves as a major light source that improves lettuce growth rates. As the PPF of red LEDs increased, the fresh and dry weights of the shoots and roots and the leaf area increased. In addition, the S/R ratio increased with increasing red LED ratio, because the growth rate of shoots was relatively higher than that of the roots. The positive effects of red light on plant growth have been reported for various crops such as perilla, chrysanthemum, tomato, poinsettia, and herbs as well as lettuce (Heo et al., 2012; Johkan et al., 2010; Lee et al., 2010; Mortensen and Strømme, 1987; Nishimura et al., 2007, 2009). Moreover, our previous study using several monochromatic LEDs indicated that red LED was the most effective at increasing the biomass of lettuce plants (Son et al., 2012). Red light is perceived by phytochrome, which is one of several photoreceptors that are known to play a major role in the growth and development of plants. Red light converts phytochrome from an inactive state to an active phytochrome with this receptor being involved in plastid development and the gene expression of chloroplasts and the nucleus (Folta and Childers, 2008). Red light also plays a crucial role in photosynthesis, because it induces CO2 absorption into the intercellular spaces of the mesophyll as a result of guard cells being stimulated and produces the energy required to open the stomata by inducing photophosphorylation in guard cells (Olsen et al., 2002; Tominaga et al., 2001). Finally, red light is effective at improving photosynthetic ability, which directly leads to the promotion of growth (Kim et al., 2005).

However, it is also of interest that one specific ratio of blue to red LEDs, i.e., the 47 B/53 R treatment, slightly increased lettuce weight and leaf area. These results were obtained for both lettuce cultivars, particularly the green leaf lettuce. This result probably implies that this specific blue and red LED ratio is quite effective for enhancing lettuce growth; however, further research is required to explore this finding. Stutte et al. (2009) and Yorio et al. (2001) reported that the biomass of lettuce plants grown under mixed blue and red LED lights was higher compared with plants grown under monochromatic red LEDs. When red light is used as the exclusive lighting source, the photosynthetic rate and chlorophyll fluorescence (Fv/Fm) were recorded as declining for a variety of crops (Goins et al., 1997; Hogewoning et al., 2010; Matsuda et al., 2004; Savvides et al., 2012). Healthy plants typically had 0.83 of Fv/Fm and a low level of Fv/Fm represents the stress level of plants from the external environment or photochemical efficiency of photosystem II (Maxwell and Johnson, 2000). The current study also showed that 100% red LED treatment (0 B) had lower Fv/Fm compared with other treatments, indicating that the photosynthetic machinery may not be functioning properly, although the low value directly did not reflect reduced biomass accumulation on lettuce leaves. In comparison, net photosynthesis, stomatal conductance, CO2 fixation, and the efficiency of photosystem II was promoted by the combination of mixed blue and red LEDs, rather than monochromic red LEDs, in cucumber leaves (Hogewoning et al., 2010; Savvides et al., 2012). Typically, blue and red wavelengths are more efficiently absorbed by plant leaves compared with other visible wavelength ranges such as green and yellow, indicating that both blue and red light represent the essential wavelength ranges for plant growth and development (Lichtenthaler et al., 1980; McCree, 1972). In the current study, 0 B, 13 B, and 26 B treatments for ‘Sunmang’ and 0 B and 13 B treatments for ‘Grand Rapid TBR’ induced significantly higher shoot fresh weight compared with the control and other LED treatments. The blue to red wavelength of control, which consisted of fluorescent lamps and high-pressure sodium lamps, was 61:39 (data not shown) so that the low proportion of red light may contribute to shoot fresh weight inferior to several LED treatments having a high proportion of red light. This result indicates that the use of LEDs better stimulates plant growth compared with conventional lamps in addition to saving energy.

Typically, there is a highly correlation between chlorophyll content and plant growth rate (Brougham, 1960). However, in this study, the SPAD value, which indirectly represents chlorophyll content in leaves, showed the opposite trend for the growth characteristics results, indicating chlorophyll content is not the only indicator for plant growth. Thus, it might be inferred that blue light, rather than red light, is closely associated with chlorophyll content. The primary effect of blue light on chlorophyll biosynthesis has been reported in previous studies using lettuce, cucumber, and spinach (Hogewoning et al., 2010; Lee et al., 2010; Matsuda et al., 2007). These studies reported that blue light had a qualitative effect, rather than a quantitative effect, on the chlorophyll biosynthesis of plants. This finding was supported by the results of the current study, whereby all LED treatments containing more than 13% blue light led to a significantly higher accumulation of chlorophyll compared with the 0 B treatment (i.e., without blue LEDs). In addition, our previous study comparing the various effects of monochromatic LEDs on lettuce plants demonstrated that blue LEDs improved chlorophyll content (Son et al., 2012). When comparing both lettuce cultivars, the SPAD value of ‘Sunmang’ gradually increased with increasing blue LED ratios; however, there was no significant difference in the chlorophyll content of ‘Grand Rapid TBR’ grown under treatments with more than 26% blue light. This finding indicates that different cultivars respond differently to light quality. In general, chlorophyll content is positively associated with photosynthetic ability (Buttery and Buzzell, 1977; Emerson, 1929); however, abundant chlorophyll produced by blue light did not promote plant growth in this study. This result might be because both blue and red wavelengths are required for promoting the whole photosynthetic process but the role of each wavelength somewhat differs. Indeed, it has been reported that blue light plays a major role toward generating and moving chlorophyll in plant leaves (Banaś et al., 2012; Briggs and Christie, 2002).

In the current study, clear differences were observed in the presence and absence of blue light for the leaf shape index (leaf length/leaf width), which represents the morphological characteristics of the leaf. The leaf shape index under the 0 B (100% red LED) treatment was significantly higher compared with the control and the other blue LED treatments throughout the entire growth stage. This result was consistent with previous studies, which showed that red LEDs induced lettuce leaf elongation, whereas irradiation with additional blue LEDs inhibited the expansion and elongation of leaves (Hoenecke et al., 1992; Lee et al., 2010; Stutte et al., 2009).

Recently, there has been increased research interest in the phenolic compounds contained in vegetables, including lettuce. In particular, the antioxidant activity of several thousands of phenolics is an important property, because antioxidants remove harmful reactive oxygen species that cause aging and chronic diseases in humans (Rajashekar et al., 2009). Flavonoids represent one group of phenolics that affect the color, flavor, and fragrance of plants (Hichri et al., 2011). Flavonoid content is an important factor that influences the nutritional quality of plant-based foods such as vegetables, because flavonoids have strong antioxidant activity (Ebisawa et al., 2008). The phytochemical quality of crops grown in closed-type plant production systems using LEDs as an artificial light source might be lower compared with crops grown under sunlight. However, there is limited information about how LEDs affect phytochemicals in crops with most LED-based studies primarily focusing on growth characteristics and crop yield. Thus, our study presents an interesting and useful trial, as we determined the effect of blue and red LED ratios on phenolic compounds and antioxidants in lettuce plants.

In this study, total phenolic concentration and antioxidant capacity increased with increasing blue LED ratios for two lettuce cultivars. Johkan et al. (2010) and Stutte et al. (2009) also reported that the additional irradiation of blue LEDs in combination with red LED irradiation induced the accumulation of phenolic compounds and antioxidants in lettuce plants. This phenomenon might be explained by a reduction in the growth of lettuce plants grown under LED treatments, including blue LEDs, because total phenolic concentration and antioxidant capacity are expressed through fresh weight. Indeed, there was an inverse correlation between shoot fresh weight and total phenolic concentration in the current study (Fig. 7). However, the activity of phenylalanine ammonia-lyase (PAL), which is a key enzyme in the phenylpropanoid pathway, was stimulated by the irradiation of blue LED in a previous study (Heo et al., 2012). Moreover, PAL gene expression was activated more by monochromatic blue LED than other monochromatic LEDs used on lettuce plants (Son et al., 2012). Thus, blue light might be involved in the activation of the biosynthetic pathway for secondary metabolites. In comparison, Wu et al. (2007) reported that red LEDs cause the accumulation of antioxidants in pea seedlings. Ultimately, the ability of light quality to cause the accumulation of plant secondary metabolites is probably dependent on plant species or variety (cultivar). In the current study, the two lettuce cultivars showed a difference in the accumulation of phenolic compounds and antioxidants. Although changes in the total phenolic concentration of the two lettuce cultivars grown under various blue and red LED ratios were similar, polyphenolic compounds and antioxidants were more abundant in the red leaf lettuce compared with the green leaf lettuce. This result was consistent with previous studies that compared the phytochemical content of different lettuce cultivars (Bunning et al., 2010; Liu et al., 2007). Because LED treatments caused the total phenolic concentration to change in a similar manner to that of antioxidant capacity, this study demonstrated that most phenolic compounds, including flavonoids, contribute to antioxidant capacity (Oh et al., 2009).

Fig. 7.
Fig. 7.

Correlation of total phenolic concentration and shoot fresh weight for ‘Sunmang’ red leaf lettuce (A) and ‘Grand Rapid TBR’ green leaf lettuce (B) grown under various combinations of blue and red light-emitting diodes (LEDs) for 4 weeks after the onset of LED treatment. The data indicate the means (n = 4).

Citation: HortScience horts 48, 8; 10.21273/HORTSCI.48.8.988

Finally, it may be concluded that blue and red LEDs have a positive effect on the accumulation of antioxidant phenolic compounds and lettuce growth, respectively. Red light irradiation in the absence of blue light was effective at stimulating the biomass accumulation of lettuce plants; however, this lighting alone induced abnormal leaf shape and had a negative effect on polyphenolics and antioxidant levels. Thus, based on the study results, we recommend that a mixture of blue and red LEDs is a critical lighting condition to enhance both crop quality and crop yield in closed-type plant production systems.

Literature Cited

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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
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    • Search Google Scholar
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    • Search Google Scholar
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    • Search Google Scholar
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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
  • LeeJ.G.OhS.S.ChaS.H.JangY.A.KimS.Y.UmY.C.CheongS.R.2010Effects of red/blue light ratio and short-term light quality conversion on growth and anthocyanin contents of baby leaf lettuceJ. Bio-Environ. Control19351359

    • Search Google Scholar
    • Export Citation
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  • LiuX.ArdoS.BunningM.ParryJ.ZhouK.StushnoffC.StonikerF.YuL.KendallP.2007Total phenolic content and DPPH˙ radical scavenging activity of lettuce (Lactuca sativa L.) grown in ColoradoSwiss Soc. Food Sci. Technol.40552557

    • Search Google Scholar
    • Export Citation
  • MatsudaR.Ohashi-kanekoK.FujiwaraK.GotoE.KurataK.2004Photosynthetic characteristics of rice leaves grown under red light with or without supplemental blue lightPlant Cell Physiol.4518701874

    • Search Google Scholar
    • Export Citation
  • MatsudaR.Ohashi-kanekoK.FujiwaraK.KurataK.2007Analysis of the relationship between blue-light photon flux density and the photosynthetic properties of spinach (Spinacia oleracea L.) leaves with regard to the acclimation of photosynthesis to growth irradianceSoil Sci. Plant Nutr.53459465

    • Search Google Scholar
    • Export Citation
  • MaxwellK.JohnsonG.N.2000Chlorophyll fluorescence—A practical guideJ. Expt. Bot.51659668

  • McCreeK.J.1972Action spectrum, absorptance and quantum yield of photosynthesis in crop plantsAgr. Meteorol.9191216

  • MillerN.J.Rice-EvansC.A.1996Spectrophotometric determination of antioxidant activityRedox Rpt.2161171

  • MorrowR.C.2008LED lighting in horticultureHortScience4319471950

  • MortensenL.M.StrømmeE.1987Effects of light quality on some greenhouse cropsSci. Hort.332736

  • NishimuraT.OhyamaK.GotoE.IangakiN.2009Concentration of perillaldehyde, limonene, and anthocyanin of Perilla plants as affected by light quality under controlled environmentsSci. Hort.122134137

    • Search Google Scholar
    • Export Citation
  • NishimuraT.ZobayedS.M.A.KozaiT.GotoE.2007Medicinally important secondary metabolites and growth of Hypericum perforatum L. plants as affected by light quality and intensityEnvrion. Control Biol.45113120

    • Search Google Scholar
    • Export Citation
  • OhM.-M.CareyE.E.RajashekarC.B.2009Environmental stresses induce health-promoting phytochemicals in lettucePlant Physiol. Biochem.47578583

    • Search Google Scholar
    • Export Citation
  • OlsenR.L.PrattR.B.GumpP.KemperA.TallmanG.2002Red light activates a chloroplast-dependent ion uptake mechanism for stomatal opening under reduced CO2 concentrations in Vicia sppNew Phytol.153497508

    • Search Google Scholar
    • Export Citation
  • PenningtonJ.A.T.FisherR.A.2009Classification of fruits and vegetablesJ. Food Compost. Anal.222331

  • PennycookeJ.C.CoxS.StushnoffC.2005Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia × hybrida)Environ. Exp. Bot.53225232

    • Search Google Scholar
    • Export Citation
  • RajashekarC.B.CareyE.E.ZhaoX.OhM.-M.2009Health-promoting phytochemicals in fruits and vegetables: Impact of abiotic stresses and crop production practicesFunctional Plant Sci. Biotechnol.33038

    • Search Google Scholar
    • Export Citation
  • SavvidesA.FanourakisD.van IeperenW.2012Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leavesJ. Expt. Bot.6311351143

    • Search Google Scholar
    • Export Citation
  • SonK.-H.ParkJ.-H.KimD.OhM.-M.2012Leaf shape, growth, and phytochemicals in two leaf lettuce cultivars grown under monochromatic light-emitting diodesKor. J. Hort. Sci. Technol.30664672

    • Search Google Scholar
    • Export Citation
  • StutteG.W.EdneyS.SkerrittT.2009Photoregulation of bioprotectant content of red leaf lettuce with light-emitting diodesHortScience447982

    • Search Google Scholar
    • Export Citation
  • TominagaM.KinoshitaT.ShimazakiK.2001Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal openingPlant Cell Physiol.42795802

    • Search Google Scholar
    • Export Citation
  • WangH.GuM.CuiJ.ShiK.ZhouT.YuJ.2009Effects of light quality on CO2 assimilation, chlorophyll-fluorescence quenching, expression of Calvin cycle genes and carbohydrate accumulation in Cucumis sativusJ. Photochem. Photobiol. B963037

    • Search Google Scholar
    • Export Citation
  • WuM.C.HouC.Y.JiangC.M.WangY.T.WangC.Y.ChenH.H.ChangH.M.2007A novel approach of LED light radiation improves the antioxidant activity of pea seedlingsFood Chem.10117531758

    • Search Google Scholar
    • Export Citation
  • YehN.ChungJ.-P.2009High-brightness LEDs-energy efficient lighting sources and their potential in indoor plant cultivationRenew. Sustain. Energy Rev.1321752180

    • Search Google Scholar
    • Export Citation
  • YorioN.C.GoinsG.D.SagerJ.C.WheelerR.M.SagerJ.C.2001Improving spinach, radish, and lettuce growth under red light-emitting diodes (LEDs) with blue light supplementationHortScience36380383

    • Search Google Scholar
    • Export Citation

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Contributor Notes

To whom reprint requests should be addressed; e-mail moh@cbnu.ac.kr.

Article Sections

Article Figures

  • View in gallery

    Relative spectral distribution of various combinations of blue and red light-emitting diodes (LEDs) used in this study. (A) blue:red = 0:100, (B) blue:red = 13:87, (C) blue:red = 26:74, (D) blue:red = 35:65, (E) blue:red = 47:53, (F) blue:red = 59:41, and (G) control (fluorescent lamp + high-pressure sodium lamp). Total photosynthetic photon flux (PPF) was 171 ± 7 μmol·m−2·s−1 in each treatment. Spectral scans were measured at 25 cm from LED lighting sources and at five points (a center and four edges of each tray of pots).

  • View in gallery

    SPAD value (chlorophyll content) of two lettuce cultivars grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 8). Significant at P = 0.001.

  • View in gallery

    Leaf shape index at 2 and 4 weeks after the onset of light-emitting diode (LED) treatment (left) and lettuce plants grown under various combinations of blue and red LEDs at 4 weeks after the onset of LED treatment (right) in both ‘Sunmang’ (A) and ‘Grand Rapid TBR’ (B). Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 8). Significant at P = 0.001.

  • View in gallery

    Total phenolic concentrations of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 4). Significant at P = 0.001.

  • View in gallery

    Antioxidant capacity of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 4). Significant at P = 0.01.

  • View in gallery

    Total flavonoid concentration of lettuce plants grown under various combinations of blue and red light-emitting diodes (LEDs) at 4 weeks after the onset of LED treatment. Control represents fluorescent lamp and high-pressure sodium lamp. The data indicate the means ± se (n = 4). Significant at P = 0.01.

  • View in gallery

    Correlation of total phenolic concentration and shoot fresh weight for ‘Sunmang’ red leaf lettuce (A) and ‘Grand Rapid TBR’ green leaf lettuce (B) grown under various combinations of blue and red light-emitting diodes (LEDs) for 4 weeks after the onset of LED treatment. The data indicate the means (n = 4).

Article References

  • AinsworthE.A.GillespieK.M.2007Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagentNat. Protoc.2875877

    • Search Google Scholar
    • Export Citation
  • BalasundramN.SundramK.SammanS.2006Phenolic compounds in plants and agri-industrial by-products: Antioxidant activity, occurrence, and potential usesFood Chem.99191203

    • Search Google Scholar
    • Export Citation
  • BanaśA.K.AggarwalC.ŁabuzJ.SztatelmanO.GabryśH.2012Blue light signaling in chloroplast movementsJ. Expt. Bot.6315591574

  • BrandtK.ChristensenL.P.Hansen-MøllerJ.HansenS.L.HaraldsdottirJ.JespersenL.PurupS.KharazmiA.BarkholtV.FrøkiaerH.Kobaek-LarsenM.2004Health promoting compounds in vegetables and fruits: A systematic approach for identifying plant components with impact on human healthTrends Food Sci. Technol.15384393

    • Search Google Scholar
    • Export Citation
  • BriggsW.R.ChristieJ.M.2002Phototropins 1 and 2: Versatile plant blue-light receptorsTrends Plant Sci.7204210

  • BroughamR.K.1960The relationship between the critical leaf area, total chlorophyll content, and maximum growth-rate of some pasture and crop plantsAnn. Bot. (Lond.)24463474

    • Search Google Scholar
    • Export Citation
  • BunningM.L.KendallP.A.StoneM.B.StonakerF.H.StushnoffC.2010Effects of seasonal variation on sensory properties and total phenolic content of 5 lettuce cultivarsJ. Food Sci.75156161

    • Search Google Scholar
    • Export Citation
  • ButteryB.R.BuzzellR.I.1977The relationship between chlorophyll content and rate of photosynthesis in soybeansCan. J. Plant Sci.5715

  • CarvalhoR.F.TakakiM.AzevedoR.A.2011Plant pigments: The many faces of light perceptionActa Physiol. Plant.33241248

  • DewantoV.WuX.AdomK.K.LiuR.H.2002Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activityJ. Agr. Food Chem.5030103014

    • Search Google Scholar
    • Export Citation
  • EbisawaM.ShojiK.KatoM.ShimomuraK.GotoF.YoshiharaT.2008Supplementary ultraviolet radiation B together with blue light at night increased quercetin content and flavonol synthase gene expression in leaf lettuce (Lactuca sativa L.)Envrion. Control Biol.46111

    • Search Google Scholar
    • Export Citation
  • EmersonR.1929The relation between maximum rate of photosynthesis and concentration of chlorophyllJ. Gen. Physiol.12609622

  • FoltaK.M.ChildersK.S.2008Light as a growth regulator: Controlling plant biology with narrow-bandwidth solid-state lighting systemsHortScience4319571964

    • Search Google Scholar
    • Export Citation
  • GoinsG.D.YorioN.C.SanwoM.M.BrownC.S.1997Photomorphogenesis, photosynthesis, and seed yield of wheat plants grown under red light-emitting diodes (LEDs) with and without supplemental blue lightingJ. Expt. Bot.4814071413

    • Search Google Scholar
    • Export Citation
  • HeoJ.W.KangD.H.BangH.S.HongS.G.ChunC.KangK.K.2012Early growth, pigmentation, protein content, and phenylalanine ammonia-lyase activity of red curled lettuces grown under different lighting conditionsKor. J. Hort. Sci. Technol.30612

    • Search Google Scholar
    • Export Citation
  • HichriI.BarrieuF.BogsJ.KappelC.DelrotS.LauvergeatV.2011Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathwayJ. Expt. Bot.6224652483

    • Search Google Scholar
    • Export Citation
  • HoeneckeM.E.BulaR.J.TibbittsT.W.1992Importance of ‘Blue’ photon levels for lettuce seedlings grown under red-light-emitting diodesHortScience27427430

    • Search Google Scholar
    • Export Citation
  • HogewoningS.W.TrouwborstG.MaljaarsH.PoorterH.van IeperenW.HarbinsonJ.2010Blue light dose–responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue lightJ. Expt. Bot.6131073117

    • Search Google Scholar
    • Export Citation
  • HooperL.CassidyA.2006A review of the health care potential of bioactive compoundsJ. Sci. Food Agr.8618051813

  • HopkinsW.G.HunerN.P.A.2004Introduction to plant physiology. 3rd Ed. John Wiley and Sons Hoboken NJ

  • JiaoY.LauO.S.DengX.W.2007Light-regulated transcriptional networks in higher plantsNat. Rev. Genet.8217230

  • JohkanM.ShojiK.GotoF.HashidaS.YoshiharaT.2010Blue light-emitting diode light irradiation of seedlings improves seedling quality and growth after transplanting in red leaf lettuceHortScience4518091814

    • Search Google Scholar
    • Export Citation
  • KimH.H.WheelerR.SagerJ.NorikaneJ.2005Photosynthesis of lettuce exposed to different short term light qualitiesEnviron. Control Biol.43113119

    • Search Google Scholar
    • Export Citation
  • LeeJ.G.OhS.S.ChaS.H.JangY.A.KimS.Y.UmY.C.CheongS.R.2010Effects of red/blue light ratio and short-term light quality conversion on growth and anthocyanin contents of baby leaf lettuceJ. Bio-Environ. Control19351359

    • Search Google Scholar
    • Export Citation
  • LichtenthalerH.K.BuschmannC.RahmsdorfU.1980The importance of blue light for the development of sun-type chloroplasts. In: Senger H. (ed.). The blue light syndrome. Springer-Verlag Berlin Germany

  • LiuX.ArdoS.BunningM.ParryJ.ZhouK.StushnoffC.StonikerF.YuL.KendallP.2007Total phenolic content and DPPH˙ radical scavenging activity of lettuce (Lactuca sativa L.) grown in ColoradoSwiss Soc. Food Sci. Technol.40552557

    • Search Google Scholar
    • Export Citation
  • MatsudaR.Ohashi-kanekoK.FujiwaraK.GotoE.KurataK.2004Photosynthetic characteristics of rice leaves grown under red light with or without supplemental blue lightPlant Cell Physiol.4518701874

    • Search Google Scholar
    • Export Citation
  • MatsudaR.Ohashi-kanekoK.FujiwaraK.KurataK.2007Analysis of the relationship between blue-light photon flux density and the photosynthetic properties of spinach (Spinacia oleracea L.) leaves with regard to the acclimation of photosynthesis to growth irradianceSoil Sci. Plant Nutr.53459465

    • Search Google Scholar
    • Export Citation
  • MaxwellK.JohnsonG.N.2000Chlorophyll fluorescence—A practical guideJ. Expt. Bot.51659668

  • McCreeK.J.1972Action spectrum, absorptance and quantum yield of photosynthesis in crop plantsAgr. Meteorol.9191216

  • MillerN.J.Rice-EvansC.A.1996Spectrophotometric determination of antioxidant activityRedox Rpt.2161171

  • MorrowR.C.2008LED lighting in horticultureHortScience4319471950

  • MortensenL.M.StrømmeE.1987Effects of light quality on some greenhouse cropsSci. Hort.332736

  • NishimuraT.OhyamaK.GotoE.IangakiN.2009Concentration of perillaldehyde, limonene, and anthocyanin of Perilla plants as affected by light quality under controlled environmentsSci. Hort.122134137

    • Search Google Scholar
    • Export Citation
  • NishimuraT.ZobayedS.M.A.KozaiT.GotoE.2007Medicinally important secondary metabolites and growth of Hypericum perforatum L. plants as affected by light quality and intensityEnvrion. Control Biol.45113120

    • Search Google Scholar
    • Export Citation
  • OhM.-M.CareyE.E.RajashekarC.B.2009Environmental stresses induce health-promoting phytochemicals in lettucePlant Physiol. Biochem.47578583

    • Search Google Scholar
    • Export Citation
  • OlsenR.L.PrattR.B.GumpP.KemperA.TallmanG.2002Red light activates a chloroplast-dependent ion uptake mechanism for stomatal opening under reduced CO2 concentrations in Vicia sppNew Phytol.153497508

    • Search Google Scholar
    • Export Citation
  • PenningtonJ.A.T.FisherR.A.2009Classification of fruits and vegetablesJ. Food Compost. Anal.222331

  • PennycookeJ.C.CoxS.StushnoffC.2005Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia × hybrida)Environ. Exp. Bot.53225232

    • Search Google Scholar
    • Export Citation
  • RajashekarC.B.CareyE.E.ZhaoX.OhM.-M.2009Health-promoting phytochemicals in fruits and vegetables: Impact of abiotic stresses and crop production practicesFunctional Plant Sci. Biotechnol.33038

    • Search Google Scholar
    • Export Citation
  • SavvidesA.FanourakisD.van IeperenW.2012Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leavesJ. Expt. Bot.6311351143

    • Search Google Scholar
    • Export Citation
  • SonK.-H.ParkJ.-H.KimD.OhM.-M.2012Leaf shape, growth, and phytochemicals in two leaf lettuce cultivars grown under monochromatic light-emitting diodesKor. J. Hort. Sci. Technol.30664672

    • Search Google Scholar
    • Export Citation
  • StutteG.W.EdneyS.SkerrittT.2009Photoregulation of bioprotectant content of red leaf lettuce with light-emitting diodesHortScience447982

    • Search Google Scholar
    • Export Citation
  • TominagaM.KinoshitaT.ShimazakiK.2001Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal openingPlant Cell Physiol.42795802

    • Search Google Scholar
    • Export Citation
  • WangH.GuM.CuiJ.ShiK.ZhouT.YuJ.2009Effects of light quality on CO2 assimilation, chlorophyll-fluorescence quenching, expression of Calvin cycle genes and carbohydrate accumulation in Cucumis sativusJ. Photochem. Photobiol. B963037

    • Search Google Scholar
    • Export Citation
  • WuM.C.HouC.Y.JiangC.M.WangY.T.WangC.Y.ChenH.H.ChangH.M.2007A novel approach of LED light radiation improves the antioxidant activity of pea seedlingsFood Chem.10117531758

    • Search Google Scholar
    • Export Citation
  • YehN.ChungJ.-P.2009High-brightness LEDs-energy efficient lighting sources and their potential in indoor plant cultivationRenew. Sustain. Energy Rev.1321752180

    • Search Google Scholar
    • Export Citation
  • YorioN.C.GoinsG.D.SagerJ.C.WheelerR.M.SagerJ.C.2001Improving spinach, radish, and lettuce growth under red light-emitting diodes (LEDs) with blue light supplementationHortScience36380383

    • Search Google Scholar
    • Export Citation

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