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Supplemental LED inter-lighting compensates for a shortage of light for plant growth and yield under the lack of sunshine

  • Fasil Tadesse Tewolde,

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Writing – original draft, Writing – review & editing

    Affiliations Graduate School of Horticulture, Chiba University, Matsudo, Japan, Center for Environment, Health and Field Science, Chiba University, Kashiwa, Japan, Ethiopian Institute of Agricultural Research, Addis Ababa, Ethiopia

  • Kouta Shiina,

    Roles Writing – review & editing

    Affiliation JA Zen-Noh, Kashiwa, Japan

  • Toru Maruo,

    Roles Writing – review & editing

    Affiliations Graduate School of Horticulture, Chiba University, Matsudo, Japan, Center for Environment, Health and Field Science, Chiba University, Kashiwa, Japan

  • Michiko Takagaki,

    Roles Writing – review & editing

    Affiliations Graduate School of Horticulture, Chiba University, Matsudo, Japan, Center for Environment, Health and Field Science, Chiba University, Kashiwa, Japan

  • Toyoki Kozai,

    Roles Writing – review & editing

    Affiliation Japan Plant Factory Association, Kashiwa, Japan

  • Wataru Yamori

    Roles Conceptualization, Supervision, Writing – original draft, Writing – review & editing

    wataru.yamori@bs.s.u-tokyo.ac.jp

    Affiliations Center for Environment, Health and Field Science, Chiba University, Kashiwa, Japan, Department of Biological Sciences, Faculty of Science, the University of Tokyo, Tokyo, Japan

Supplemental LED inter-lighting compensates for a shortage of light for plant growth and yield under the lack of sunshine

  • Fasil Tadesse Tewolde, 
  • Kouta Shiina, 
  • Toru Maruo, 
  • Michiko Takagaki, 
  • Toyoki Kozai, 
  • Wataru Yamori
PLOS
x

Abstract

Supplemental lighting can enhance yield when sunlight is limited, as in winter. As the effect of frequent cloudy or rainy days in other seasons on plant growth and yield remains unclear, we investigated the effect on tomato (Solanum lycopersicum) and compensation by supplemental LED inter-lighting. Plants were grown under 30% shade cloth on 0%, 40%, or 60% of days. Lower leaves were illuminated with red and blue LED inter-lighting modules from right after first anthesis, or not illuminated. Shading during 40% and 60% of days diminished daily light integral (DLI) by 26% and 40%, respectively, and reduced shoot dry weight by 22.0% and 23.3%, yield by 18.5% and 23.3%, and fruit soluble solids content by 12.3% and 9.3%. In contrast, supplemental inter-lighting improved the light distribution within plants and compensated DLI, and maintained similar yield and soluble solids content in both shade treatments as in the control. These results clearly show that supplemental LED inter-lighting could efficiently compensate for a shortage of light for plant growth, photosynthesis and thus yield under the lack of sunshine.

Introduction

Valued globally at 58.2 billion USD, tomato is ranked as the 4th most valuable agricultural commodity or crop after rice, wheat, and soybean [1]. Thus, economic benefits may accrue from investigating the effects of low solar radiation as a result of cloud cover on productivity of greenhouse tomatoes. Despite the “global brightening” reported in many places [2], some areas in East Asia still experience dimming characterized by the reduced in shortwave radiation due to the high or even increasing aerosol concentrations, especially in China and downstream in Japan [3]. In the past 50 years the reduction of solar radiation reaching Earth’s surface globally has averaged 0.51 ± 0.05 W m−2 per year, equivalent to a reduction of 2.7% per decade [4]. Thus, it’s important to understand whether cloud cover and low solar radiation limit carbon uptake, photosynthesis, and thus crop productivity despite the improvement in carbon gain in terrestrial ecosystems by an increased ratio of diffuse radiation [5].

Single-truss tomato production systems [6, 7] can reduce labor requirements for training, pruning, and harvesting. Moreover, single-truss tomato cultivation systems are superior to multi-truss tomato cultivation systems because they allow multiple cropping, predictable and consistent harvests, and use of moveable benches, and they have the potential for automation [611]. However, at high planting density, light becomes a limiting factor in the growth of single-truss tomato plants, as mutual shading prevents light from penetrating into the lower canopy [10]. This problem is exacerbated in winter [12]. Moreover, frequent cloudy or rainy days during spring to early summer could also affect plant growth and productivity. To maintain optimal growth, plants require optimal light, temperature, water, and nutrients. These factors have long been understood as primary determinants of agricultural productivity [1315]. In greenhouse horticulture, it is relatively easy to control water, nutrients, and temperature, but not irradiation [16, 17]. Plants experience a highly variable light environment over the course of the day, season, and year [18], and are highly sensitive to their light environment [19, 20], as irradiation directly affects photosynthesis, which determines plant growth and yield [18, 21, 22].

In tomato production, the understory leaves have a very low net photosynthetic rate due to both lower incident light and induced senescence [23, 24]. Frantz et al [25] found that supplemental light within a cowpea canopy significantly delayed senescence of the interior leaves. In addition, supplying upward lighting from underneath retarded the senescence of outer leaves of lettuce and increased photosynthetic rate, improving total plant growth [26, 27]. Many studies have shown that supplemental lighting above or within the canopy enhanced the yield of tomato plants when sunlight is limited, mainly in winter [2833]. In greenhouse crop production, the ‘1% rule of thumb’ says that a 1% reduction in the daily light integral (DLI) results in a 1% reduction in yield [34]. This rule was shown to hold for greenhouse crops such as cucumber and sweet pepper throughout the cropping period [35]. A similar relationship was found in tomato during winter and spring, although the yield reduction was slightly lower in summer [36]. Although it has been investigated a relationship between crop yield and DLI seasonally and/or annually, it would be difficult to eliminate differences in other environmental factors (i.e., temperature, VPD and so on) depending on the season and the year. Recurrent cloudy and rainy days in other seasons could reduce plant growth and thus productivity, however, there has been no research on how supplemental lighting can compensate under continuous cloudy conditions.

Crop productivity under limited light conditions can be enhanced by supplementation using fluorescent lamps, high-pressure sodium lamps, metal halide lamps, or LED lamps [2833]. LEDs are considered a suitable light source for inter-lighting (lighting within plant canopy) because they produce less heat and are therefore less likely to burn leaves than high-pressure sodium lamps [37]. LED inter-lighting module used in this experiment was found to increase temperature by about 1°C [33]. It has also been reported that temperatures above 33 oC must be avoided with most tomato cultivars when aiming to produce fruit [38]. Usually supplemental lighting should be turned off when solar irradiation exceeds a desired set point, which is about 1300 mmol m-2 s-1 in a greenhouse [39, 12]. Their development has enabled growers to control light spectral qualities by combining various light sources with different waveband emissions [40, 41, 9, 42, 43]. Our objective was to investigate how cloudy or rainy weather affect tomato plant growth and yield and how supplemental LED inter-lighting could compensate the DLI requirement and thus improve plant growth and yield in single-truss tomato production.

Materials and methods

2.1. Plant material and growth conditions

Seeds of tomato (Solanum lycopersicum L. ‘Sanbi’) were sown in 128-cell plug trays filled with vermiculite on 23 April 2014. After 2 days in the dark at 26°C, the trays were transferred to a walk-in environment-controlled growth chamber with environmental control unit (Nae Terrace, Mitsubishi Plastics Agri Dream Co., Ltd., Tokyo, Japan), and seedlings were grown as described [33]. After 3 weeks, on 15 May, the seedlings were transplanted at a density of 10 plants per m2 in a greenhouse. The greenhouse was equipped with heat pumps and a pad-and-fan system to control day/night temperatures at 26/18°C. Otsuka nutrient solution (Otsuka Chemical Co., Ltd., Osaka) was used with the application schedule, EC, and pH described by [33]. In high-density single-truss tomato cultivation, each plant is allowed to develop only a single fruit truss [9]. To achieve this, the apical meristem of each plant was pinched after first anthesis, leaving two leaves above and three leaves below the truss, and all flowers that set fruits were kept intact. To improve fruit set, fully blooming flowers were sprayed once with 4-chlorophenoxyacetic acid at 15 mg L−1 as described [33].

2.2. LED inter-lighting

The understory leaves were illuminated with LED modules (Green Power LED inter-lighting module DR/B, Philips, Eindhoven, the Netherlands. The modules combined blue (with a peak at 440 nm) and red light (with a peak at 632 nm) of 1:4 ratio, respectively, with a photosynthetic photon flux density (PPFD) of 220 μmol m−2 s−1 (for more, see [33]). They were positioned on both sides of the aisle at 50 cm from the stems (10 cm from the mid-canopy leaves), at a height of 60 cm above the polystyrene board under which the root system grew. As yield of single-truss tomato plants is positively correlated with the total incident light during the period from anthesis to harvest [7, 31, 42], we applied LED inter-lighting with a 12-h photoperiod from the very first anthesis until harvest in order to maximize yield while minimizing energy costs.

2.3. Cloud cover simulation

Between 40% and 60% of all days over the past 5 years in Japan were cloudy or rainy [44]. To simulate cloudy weather, we used 30% shade cloth to create treatments in which 40% or 60% of days within the growth period were ‘cloudy’ (Fig 1). We used five treatments: 40% and 60% cloudy days with and without supplemental LED inter-lighting, and a control (no shading, no inter-lighting). Each treatment had twenty-five tomato plants, of which fifteen plants were selected randomly and tagged for the measurement of growth and other parameters.

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Fig 1. Schematic diagram of experimental schedule and LED inter-lighting used.

LED inter-lighting was used when the shade cloth was applied.

https://doi.org/10.1371/journal.pone.0206592.g001

2.4. Measurements

Plant growth.

We measured internode length and stem diameter under the fruit truss, leaf chlorophyll content, leaf area, leaf mass per unit area (LMA), and shoot dry weight. Chlorophyll was determined by chlorophyll meter (SPAD-502 Plus, Konica Minolta, Tokyo, Japan). Leaf area was measured by leaf area meter (LI-3000C, Li-Cor, Lincoln, NE, USA).

Light distribution within the plant profile.

We measured the light intensity at the top (5th leaf), middle (3rd leaf), and bottom (1st leaf) of the canopy (Fig 2) with a quantum sensor (LI-190SA; Li-Cor). The sensor was angled the same as nearby leaves. The LED inter-lighting remained in use. Solar irradiance alone was measured as a control.

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Fig 2. Effects of LED inter-lighting on photosynthetic photon flux density (PPFD) within the plant canopy.

PPFD was measured by a quantum sensor held at the same angle as nearby leaves. Data are means ± SEM (n = 10). Values marked with the same letter are not significantly different (Tukey’s HSD at P < 0.05).

https://doi.org/10.1371/journal.pone.0206592.g002

Daily light integral (DLI).

DLI is an important variable to measure in a greenhouse because it directly influences plant growth, development, yield, and quality. DLI is the amount of photosynthetically active radiation received per day, as a function of light intensity (instantaneous light: μmol m-2 s-1) and duration (day).

Leaf gas exchange.

We measured the light-response curve of the photosynthetic rate from 10:00 to 14:00 with a portable gas exchange system (LI-6400; Li-Cor) as described [4547] in representative leaves from the top of the canopy (5th leaf from the bottom), the middle (3rd leaf from the bottom), and the bottom (1st leaf from the bottom).

Yield and fruit quality.

We recorded the fresh weight of each fruit and measured two quality parameters [33]: ascorbic acid content, using a reflectometer (RQ Flex Plus, Merck Co., Ltd., Darmstadt, Germany), and total soluble solids content, using a refractometer (Atago 3810 PAL-1, Atago Co., Ltd., Tokyo, Japan).

2.5. Statistical analysis

Data were tested in SPSS v. 21.0 software (SPSS, Chicago, IL, USA). The significance of differences between treated plants and controls was analyzed with Tukey’s HSD test. P < 0.05 was considered to be significant.

Results

Daily light integral (DLI)

Control plants (no shading, no supplemental inter-lighting) received a mean DLI of 8.4 mol m−2 (Table 1). Shading of plants for 40% and 60% of days decreased DLI to 6.2 and 5.0 mol m−2, respectively, thus decreasing DLI by 2.2 and 3.4 mol m−2. Supplemental LED inter-lighting contributed 2.8 and 4.2 mol m−2 DLI, respectively. It also increased light intensity and distribution among the middle and lower canopy leaves (Fig 2). In both shading treatments, it increased the light distribution within mid-canopy leaves by 165 μmol m−2 s−1. The estimated diurnal changes in PPFD indicated that only 30% of the incident light at the top of the canopy reached the middle, and only 15% reached the bottom (Fig 2).

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Table 1. Effects of shading and LED inter-lighting on daily light integral (mean ± SEM, n = 15).

https://doi.org/10.1371/journal.pone.0206592.t001

Leaf chlorophyll content

Leaves in the middle and lower canopy had significantly lower chlorophyll contents than leaves at the top. In the control, the content increased from 37.3 g m−2 in the bottom leaf to 45.6 g m−2 in the top leaf (Fig 3). In the shading treatments, it decreased further in the mid-canopy leaves, by 5% in the 40% treatment and by 7% in the 60% treatment, but did not differ significantly from the control in the top and lower canopy in either shading treatment (Fig 3). Supplemental LED inter-lighting increased the light distribution within the plants (Fig 2). It overcompensated the chlorophyll content of the mid-canopy leaves in both treatments increased it by 12% in the 40% treatment and by 13% in the 60% treatment of the lower canopy, but had no effect in the top canopy (Fig 3).

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Fig 3. Total chlorophyll contents of single-truss tomato leaves measured in three canopy layers in plants grown under shading during 0%, 40% and 60% of days, with or without LED inter-lighting.

Data are means ± SEM (n = 15). Values marked with the same letter are not significantly different for the same leaf number in different treatments (Tukey’s HSD at P < 0.05).

https://doi.org/10.1371/journal.pone.0206592.g003

Photosynthesis

Both shading treatments did not affect photosynthetic rate in the mid-canopy leaves at lower light intensity (< 100 μmol m−2 s−1), but significantly reduced at higher light intensity (> 200 μmol m−2 s−1) (Fig 4, S1 Table). The photosynthetic rate in the mid-canopy leaves was reduced by 12% at PPFD = 1000 μmol m−2 s−1 in the 40% treatment, and by 22% at PPFD = 1000 μmol m−2 s−1 in the 60% treatment. On the other hand, the supplemental LED inter-lighting compensated for the reduction of photosynthetic rate by both shading treatments. The effect in the lower canopy was similar, but the top canopy showed no difference from the control.

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Fig 4. Effects of LED inter-lighting on leaf photosynthetic capacity of single-truss tomato plants.

Light-response curve was measured from 10:00 to 14:00 in representative leaves in three canopy layers in plants grown under shading during 0%, 40% and 60% of days with or without LED inter-lighting. Data are means ± SEM (n = 5).

https://doi.org/10.1371/journal.pone.0206592.g004

Plant growth

Shading on 60% of days reduced stem diameter by 11.3% and truss diameter by 14.6%, but supplemental LED inter-lighting reversed these differences (Table 2). Inter-lighting increased leaf mass per unit area (LMA) significantly but had no significant effect on internode length or leaf area index (LAI) (Table 2). Shading reduced shoot dry weight by 22.0%–23.3%, but inter-lighting increased it by 19.1%–19.5% to levels similar to the control (Fig 5).

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Fig 5. Shoot dry weights and fruit yield of single-truss tomato plants grown under shading during 0%, 40% and 60% of days with or without LED inter-lighting.

Data are means ± SEM (n = 5). Values marked with the same letter are not significantly different (Tukey’s HSD at P < 0.05).

https://doi.org/10.1371/journal.pone.0206592.g005

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Table 2. Effect of shading and LED inter-lighting on growth of single-truss tomato plants (means ± SEM, n = 15).

https://doi.org/10.1371/journal.pone.0206592.t002

Fruit yield and quality

Shading decreased fruit yield by 18.5% in the 40% treatment and by 23.3% in the 60% treatment. Thus, a 1% reduction in DLI reduced yield by 0.7% in the 40% treatment and by 0.6% in the 60% treatment. However, supplemental LED inter-lighting compensated for the DLI requirement, improving plant growth and yield to the control levels (Fig 6). Shading also reduced the fruit soluble solids content, by 12.3% and 9.3%, respectively. However, inter-lighting completely compensated it (Fig 6). On the other hand, shading showed no significant effect on fruit ascorbic acid content.

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Fig 6. Ascorbic acid and total soluble solids contents of single-truss tomato plants grown under shading during 0%, 40% and 60% of days with or without LED inter-lighting.

Data are means ± SEM (n = 10). Bars with the same letter are not significantly different (Tukey’s HSD at P < 0.05). NS, no significant differences.

https://doi.org/10.1371/journal.pone.0206592.g006

Discussion

Supplemental LED inter-lighting enhanced daily light integral and vertical light distribution

Cloud-free weather is infrequent during spring and early summer in temperate regions such as Japan [48] and southern China [49]. Light is further reduced by the greenhouse glazing and structures [17]. In our experiment, shading during 40% and 60% of days diminished DLI by 26% and 40%, respectively (Table 1). A minimum of 4 mol m−2 d−1 is needed for single-truss tomato production [39]. Since our results show that supplemental LED inter-lighting increased DLI by 2.8 mol m−2 d−1 in the 40% treatment and 4.2 mol m−2 d−1 in the 60% treatment, the use of LED inter-lighting on cloudy days could supply plants with more than the minimum DLI requirement (Table 1). The light distribution among the middle and lower canopy leaves was greatly reduced with shading (Fig 2), but the inter-lighting improved it and DLI (Table 1), enhancing yield and fruit quality (Figs 5 and 6).

Supplemental LED inter-lighting improved photosynthesis, growth, and yield when daily light integral is limiting

Both 40% and 60% shading treatments reduced the chlorophyll content of middle and lower leaves, and consequently reduced leaf photosynthetic rate (Figs 3 and 4). Leaf chlorophyll content is one of the most important factors determining photosynthetic rate [50, 51] and dry matter production [52], since the contribution of leaves to crop yield through photosynthetic assimilation relies on the amount of radiant energy absorbed by chlorophyll [22]. LED inter-lighting during cloudy days increased leaf chlorophyll content and photosynthetic rate in the mid-canopy leaves (Figs 3 and 4). It also significantly increased LMA but not LAI, indicating that it enhanced shoot dry mass production by improving leaf photosynthetic capacity (Table 2; Fig 5).

Generally, yield has an inverse relationship with shading level [11]. Cloud cover also decreases productivity and daily carbon gain owing to a dramatic reduction in total DLI [53]. Shading can decrease the soluble solids content and increase the titratable acidity of fruits [11]. In humid subtropical Brazil, 52% shading of tomato between September and December after anthesis reduced yield by 20% [54]. In our results, 30% shading during 40% and 60% of days reduced yield by 18.5% and 23.3% (Fig 5). This indicated that tomato yield has directly a proportional relationship with DLI (Fig 7), as a 1% reduction in DLI reduced yield by 0.7% in the 40% treatment and by 0.6% in the 60% treatment. Similarly, in previous work, a 1% reduction in DLI results in a 1% reduction in yield for greenhouse crops such as cucumber and sweet pepper throughout the cropping period [35]. The observed decreases in photosynthetic rate, growth, and yield of tomato with decreasing solar radiation are consistent with common understanding. However, our data clearly show that supplemental lighting improved DLI (Table 1) and vertical light distribution within the canopy (Fig 2), resulting in increases in leaf photosynthetic rate (Fig 4), growth and yield (Fig 5). In addition, supplemental LED inter-lighting compensated for reductions in total soluble solids content of fruits (Fig 6). It has been reported that developmental triggers and environmental signals, particularly light, influence ascorbic acid accumulation in leaves [5557], however, the ascorbic acid concentration was not affected by the shading treatment in the present study. The ascorbic acid concentration might be affected not by DLI but by the maximum light intensities within a couple of days, since ascorbic acid can function as an antioxidant to alleviate the high-light stress for plants [58].

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Fig 7. Relation between yield and daily light integral (DLI).

Open circle: plants grown under shading during 0%, 40% and 60% of days, Filled triangle: plants grown under shading during 40% of days with supplemental LED inter-lighting, filled square: plants grown under shading during 60% of days with supplemental LED inter-lighting. The regression line among plants grown under shading during 0%, 40% and 60% of days is shown (y = 0.1869x + 1.0605, R2 = 0.97).

https://doi.org/10.1371/journal.pone.0206592.g007

Previous studies showed that supplemental lighting improved canopy light interception, leaf photosynthetic capacity, assimilate supply to fruits, and crop productivity [8, 29, 30, 33]. However, some studies reported that it did not significantly increase yield of tomato and cucumber [12, 35, 59]. Part of the reason for the difference could be reduced vertical and horizontal light interception caused by extreme leaf curling, the LED-light spectrum used, or low irradiance [59]. Another reason could be that some tomato cultivars grow equally well whether lit from above or within [12]. Recently, it has been reported that daytime inter-lighting during summer improved mid-canopy light distribution but also increased temperature significantly [33], so high temperatures and high solar irradiation during midday in summer could exceed the optimal range for tomato production and thus reduce yield. Thus, both the growth season and the time of day when the light is applied could also determine the effectiveness of supplemental inter-lighting.

Conclusion

Shading during both 40% and 60% of days significantly decreased DLI in the mid and lower canopy, resulting in reductions in tomato productivity. However, supplemental LED inter-lighting improved the light distribution within the plant profile and compensated for the DLI requirement of plants, improving plant growth and yield. These results clearly indicate that where cloudy or rainy days are frequent, supplemental LED inter-lighting could compensate for a shortage of light for plant growth and yield (both quantity and quality), allowing sustainable year-round tomato production.

Supporting information

S1 Table. Effects of LED inter-lighting on leaf photosynthetic capacity of single-truss tomato plants.

Light-response curve was measured from 10:00 to 14:00 in representative leaves in three canopy layers in plants grownunder shading during 0%, 40% and 60% of days with or without LED inter-lighting. Data are means ± SEM (n = 5). Different letters indicated significant difference within the column (Tukey’s HSD test, P <0.05).

https://doi.org/10.1371/journal.pone.0206592.s001

(PDF)

Acknowledgments

We would like to thank Philips Lighting for providing LED modules and Mr. Takakazu Iijima for his help during plant cultivation.

References

  1. 1. FAO. FAOSTAT database collections. Food and Agriculture Organization of the United Nations. 2012; Rome. Access date: 2016-04-22. URL: http://faostat.fao.org
  2. 2. Wild M., Gilen H., Roesch A., Ohumura A., Long C. N., et al., From dimming to brightening; decadal changes in solar radiation at Earth’s surface. Science. 2005; 308. 847–850, pmid:15879214
  3. 3. Wang K. C., Dickinson R. E., Wild M. and Liang S. Atmospheric impacts on climatic variability of surface incident solar radiation. Atmos. Chem. Phys. 2012; 12, 9581–9592.
  4. 4. Stanhill G., and Cohen S. Global dimming: a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences. Agricultural and Forest Meteorology. 2001; 107, 255–278.
  5. 5. Mercado L.M., Bellouin N., Sitch S., Boucher O., Huntingford C., Wild M. et al. Impact of changes in diffuse radiation on the global land carbon sink. Nature. 2009; 458, 1014–1017. pmid:19396143
  6. 6. Giniger M.S., McAvoy R.J., Giacomelli G.A., and Janes H.W. Computer simulation of a single truss tomato cropping system. American Society of Agricultural Engineers. 1988; 31, 1176–1179.
  7. 7. McAvoy R.J., Janes H.W., Godfriaux B.L., Secks M., Duchai D., and Wittman W.K). The effect of total available photosynthetic photon flux on single truss tomato growth and production. Journal of Horticultural Science. 1989; 64, 331–338.
  8. 8. McAvoy R.J., and Janes H.W. Alternative production strategies for greenhouse tomato using supplemental lighting. Scientia Horticulturae. 1988; 35, 161–166.
  9. 9. Giacomelli G.A., Ting K.C., and Mears D.R. Design of a single truss tomato production system (STTPS). Acta Horticulturae. 1994; 361, 77–84.
  10. 10. Okano K., Nakano Y., and Watanabe S. Single-truss tomato system-a labor-saving management system for tomato production. Jpn. Agric.Res.Q. 2001; 35, 177–184.
  11. 11. Wada T., Ikeda H., Matsushita K., Kambara A., Hirai H., and Abe K. Effect of shading in summer on yield and quality of tomatoes grown on a single-truss system. Journal of the Japanese Society for Horticultural Science. 2006; 75, 51–58.
  12. 12. Gunnlaugsson E., and Adalsteinsson S. Inter-lighting and plant density in year-round production of tomato at northern latitudes. In V International Symposium on Artificial Lighting in Horticulture 711, eds. Acta Horticulturae. 2006; 71–75. https://doi.org/10.17660/ActaHortic.2006.711.6
  13. 13. Fischer R.A., and Turner N.C. Plant productivity in the arid and semiarid zones. Annual Review of Plant Physiology. 1978; 29, 277–317.
  14. 14. Novoa R., and Loomis R.S. Nitrogen and plant production. Plant Soil. 1981; 58, 177–204.
  15. 15. Boyer J.S. Plant productivity and environment. Science. 1982; 218, 443–448. pmid:17808529
  16. 16. Wang H., Wang F.L., Wang G., and Majourhat K. The responses of photosynthetic capacity, chlorophyll fluorescence and chlorophyll content of nectarine (Prunus persica var. nectarina Maxim.) to greenhouse and field grown conditions. Scientia Horticulturae. 2007; 112, 66–72.
  17. 17. Hanan J.J. Greenhouses: Advanced technology for protected horticulture. 1998; CRC Press, Boca Raton, FL.
  18. 18. Yamori W. Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. Journal of Plant Research. 2016); 129:379–395 pmid:27023791
  19. 19. Yamori W., Shikanai T., and Makino A. Photosystem I cyclic electron flow via chloroplast NADH dehydrogenase-like complex performs a physiological role for photosynthesis at low light. Scientific Reports. 2015; 5, 13908. pmid:26358849
  20. 20. Yamori W., Makino A., and Shikanai T. A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Scientific Reports. 2016; 6, 20147. pmid:26832990
  21. 21. Yamori W. Improving photosynthesis to increase food and fuel production by biotechnological strategies in crops. J Plant Biochem & Physiol. 2013; 1: 113.
  22. 22. Yamori W., and Shikanai T. Physiological functions of cyclic electron transport around Photosystem I in sustaining photosynthesis and plant growth. Annual Review of Plant Biology. 2016; 67:81–106. pmid:26927905
  23. 23. Acock B., Charles-Edwards D.A., Fitter D.J., Hand D.W., Ludwig L.J., Warren Wilson J., et al. The contribution of leaves from different levels within a tomato crop to canopy net photosynthesis: an experimental examination of two canopy models. Journal of Experimental Botany. 1978; 111, 815–827.
  24. 24. Xu H.L., Gauthier L., Desjardins Y., and Gosselin A. (1997). Photosynthesis in leaves, fruits, stem and petioles of greenhouse-grown tomato plants. Photosynthetica. 1978; 33, 113–12.
  25. 25. Frantz J.M., Joly R.J., and Mitchell C.A. Intra-canopy lighting influences radiation capture, productivity, and leaf senescence in cowpea canopies. Journal of American Society for Horticulture Science. 2000; 125, 694–701.
  26. 26. Zhang G., Shen S., Takagaki M., Kozai T., and Yamori W. Supplemental upward lighting from underneath to obtain higher marketable lettuce (Lactuca sativa) leaf fresh weight by retarding senescence of outer leaves. Frontiers in Plant Science. 2015; 6, 1110. pmid:26697055
  27. 27. Joshi J., Zhang G., Shen S., Supaibulwatana K., Watanabe C. K., and Yamori W. A combination of downward lighting and supplemental upward lighting improves plant growth in a closed plant factory with artificial lighting. HortScience. 2017; 52(6), 831–835.
  28. 28. Hovi T., Nakkila J., and Tahvonen R. Intra-canopy lighting improves production of year-round cucumber. Scientia Horticulturae. 2004; 102, 283–294.
  29. 29. Hovi T., and Tahvonen R. Effect of inter-lighting on yield and external fruit quality in year-round cultivated cucumber. Scientia Horticulturae. 2008; 116, 152–161.
  30. 30. Pettersen R.I., Torre S., and Gislerod H.R. Effects of intra-canopy lighting on photosynthesis characteristics in cucumber. Scientia Horticulturae. 2010; 125, 77–81.
  31. 31. Lu N., Maruo T., Johkan M., Hohjo M., Tsukagoshi S., Ito Y., et al. Effects of supplemental lighting within the canopy at different developing stages on tomato yield and quality of single-truss tomato plants grown at high density. Environmental Control in Biology. 2012a; 50, 1–11.
  32. 32. Lu N., Maruo T., Johkan M., Hohjo M., Tsukagoshi S., Ito Y., et al. Effects of supplemental lighting with light-emitting diodes (LEDs) on tomato yield and quality of single-truss tomato plants grown at high planting density. Environmental Control in Biology. 2012b; 50, 63–74.
  33. 33. Tewolde F.T., Lu N., Shiina K., Maruo T., Takagaki M., Kozai T., et al. Nighttime supplemental LED inter-lighting improves growth and yield of single-truss tomatoes by enhancing photosynthesis in both winter and summer. Frontier in Plant Science. 2016; 7, 448. pmid:27092163
  34. 34. Marcelis L.F.M., Broekhuijsen A.G.M., Meinen E., Nijs L. and Raaphorst M.G.M. Quantification of the growth response to light quantity of greenhouse grown crops. Acta Horticulturae. 2006; 711, 97–104.
  35. 35. Heuvelink, E., Bakker, M.J., Hogendonk, L., Janse, J., Kaarsemaker, R., and Maaswinkel, R. Horticultural lighting in the Netherlands: new developments. In V International Symposium on Artificial Lighting in Horticulture 711, eds. Acta Horticulturae. 2006; 25–33. https://doi.org/10.17660/ActaHortic.2006.711.1
  36. 36. Cockshull K.E., Graves C.J. and Cave C.R.J. The influence of shading on yield of glasshouse tomatoes. Journal of Horticultural Science. 1992; 67, 11–24.
  37. 37. Hao X., Zheng J.M., Little C., and Khosla S. LED inter-lighting in year-round greenhouse mini-cucumber production. Acta Horticulturae. 2012; 335–340.
  38. 38. Adams S. R., Cockshull K.E., and Cave C.R.J. Effect of temperature on the growth and development of tomato fruits. Ann. Bot. 2001; 88, 869–877.
  39. 39. Dorais, M. The use of supplemental lighting for vegetable crop production: light intensity, crop response, nutrition, crop management, cultural practices. 2003; Canadian Greenhouse Conference, October 9, 2003, Toronto, Ontario.
  40. 40. Goto E. Effect of light quality on growth of crop plants under artificial lighting. Environmental Control in Biology. 2003; 41, 121–132.
  41. 41. Merrill B.F., Lu N., Yamaguchi T., Takagaki M., Maruo T., Kozai T., et al. The next revolution of agriculture: a review of innovations in Plant factories. In: Handbook of Photosynthesis, 3rd ed. 2016; CRC Press
  42. 42. Hisatomi T., and Fujimoto K. Studies on the single truss tomato culture. I. Growth and yield for sowing at different dates over the year. Journal of Japan Society of Horticultural Science. 1978; 46, 487–494.
  43. 43. Monostori I., Heilmann M., Kocsy G., Rakszegi M., Ahres M., Altenbach SB., et al. LED Lighting–Modification of Growth, Metabolism, Yield and Flour Composition in Wheat by Spectral Quality and Intensity. Frontier in Plant Science. 2018; 9, 605. pmid:29780400
  44. 44. JMA. Data on solar and infrared radiation. 2014; http://www.data.jma.go.jp/gmd/env/​radiation/en/data_rad_e.html Accessed 29 September 2014.
  45. 45. Yamori W., Noguchi K., and Terashima I. Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant, Cell & Environment. 2005; 28, 536–547.
  46. 46. Yamori W., Noguchi K., Hikosaka K., and Terashima I. Cold-tolerant crop species have greater temperature homeostasis of leaf respiration and photosynthesis than cold-sensitive species. Plant and Cell Physiology. 2009; 50, 203–215. pmid:19054809
  47. 47. Yamori W., Noguchi K., Hikosaka K., and Terashima I. Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant physiology. 2010; 152, 388–399. pmid:19880611
  48. 48. Takai T., Yano M., and Yamamoto T. Canopy temperature on clear and cloudy days can be used to estimate varietal differences in stomatal conductance in rice. Field Crops Research. 2010; 115, 165–170.
  49. 49. Xiaoying L., Shirong G., Taotao C. Zhigang X., and Tezuka T. Regulation of the growth and photosynthesis of cherry tomato seedlings by different light irradiations of light emitting diodes (LED). Africa Journal of Biotechnology. 2012; 11, 6169–6177.
  50. 50. Naidu R.A., Krishnan M., Nayudu M.V., and Gnanam A. Studies on peanut green mosaic virus infected peanut (Arachis hypogaea L.) leaves. II. Chlorophyll-protein complexes and polypeptide composition of thylakoid membranes. Physiological Plant Pathology. 1984; 25, 191–198.
  51. 51. Mao L.Z., Lu H.F., Wang Q., and Cai M.M. Comparative photosynthesis characteristics of Calycanthus chinensis and Chimonanthus praecox. Photosynthetica. 2007; 45, 601–605
  52. 52. Ghosh P.K., Bandyopadhyay K.K., Manna M.C., Mandal K.G., Misra A.K., Hati K.M. Comparative effectiveness of cattle manure, poultry manure, phosphocompost and fertilizer-NPK on three cropping systems in vertisols of semi-arid tropics. II. Dry matter yield, nodulation, chlorophyll content and enzyme activity. Bioresource Technology. 2004; 95, 85–93. pmid:15207300
  53. 53. Alton P.B. Reduced carbon sequestration in terrestrial ecosystems under overcast skies compared to clear skies. Agricultural and Forest Meteorology. 2008; 148, 1641–1653.
  54. 54. Sandra M.A., Andriolo J.L., Witter M., and Ross T.D. Effect of shading on tomato plants grown under greenhouse. Horticultura Brasileira. 2003; 21, 642–645.
  55. 55. Imai T., Kingston-Smith A., Foyer C.H. Ascorbate metabolism in potato leaves supplied with exogenous ascorbate. Free Radical Research. 1999; 31, 171–179.
  56. 56. Gatzek S., Wheeler G.L., Smirnoff N. Antisense suppression of L-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated L-galactose synthesis. The Plant Journal. 2002; 30, 541–553. pmid:12047629
  57. 57. Bartoli CG, Yu JP, Gomez F, Fernandez L, McIntosh L, and Foyer CH. Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. Journal of Experimental Botany. 2006; 57, 1621–1631. pmid:16714304
  58. 58. Foyer C. Ascorbic acid. In: Alscher RG, Hess JL, eds. Antioxidants in higher plants. CRC Press. 1993; 31–58
  59. 59. Trouwborst G., Oosterkamp J., Hogewoning S.W., Harbinson J., and Ieperen W.V. The response of light interception, photosynthesis and fruit yield of cucumber to LED-lighting within the canopy. Physiologia Plantrum. 2010; 138, 289–300. pmid:20051030