SYSTEMATIC REVIEW published: 29 April 2021 doi: 10.3389/fpls.2021.596927 Supplemental LED Lighting Effectively Enhances the Yield and Quality of Greenhouse Truss Tomato Production: Results of a Meta-Analysis Elisa Appolloni 1 , Francesco Orsini 1*, Giuseppina Pennisi 1 , Xavier Gabarrell Durany 2,3 , Ivan Paucek 1 and Giorgio Gianquinto 1 1 DISTAL – Department of Agricultural and Food Sciences, Alma Mater Studiorum – Università di Bologna, Bologna, Italy, 2 María de Maeztu Unit of Excellence, Institut de Ciència i Tecnologia Ambientals (ICTA-UAB), Universitat Autònoma de Barcelona, Barcelona, Spain, 3 Chemical, Biological and Environmental Engineering Department, Universitat Autònoma de Barcelona, Barcelona, Spain Intensive growing systems used for greenhouse tomato production, together with light interception by cladding materials or other devices, may induce intracanopy mutual Edited by: Bernard Grodzinski, shading and create suboptimal environmental conditions for plant growth. There are a University of Guelph, Canada large number of published peer-reviewed studies assessing the effects of supplemental Reviewed by: light-emitting diode (LED) lighting on improving light distribution in plant canopies, Mark Lefsrud, increasing crop yields and producing qualitative traits. However, the research results McGill University, Canada Jason Lanoue, are often contradictory, as the lighting parameters (e.g., photoperiod, intensity, and Agriculture and Agri-Food Canada quality) and environmental conditions vary among conducted experiments. This research (AAFC), Canada presents a global overview of supplemental LED lighting applications for greenhouse *Correspondence: Francesco Orsini tomato production deepened by a meta-analysis aimed at answering the following f.orsini@unibo.it research question: does supplemental LED lighting enhance the yield and qualitative traits of greenhouse truss tomato production? The meta-analysis was based on the differences Specialty section: This article was submitted to among independent groups by comparing a control value (featuring either background Crop and Product Physiology, solar light or solar + HPS light) with a treatment value (solar + supplemental LED light or a section of the journal solar + HPS + supplemental LED light, respectively) and included 31 published papers Frontiers in Plant Science and 100 total observations. The meta-analysis results revealed the statistically significant Received: 20 August 2020 Accepted: 06 April 2021 positive effects (p-value < 0.001) of supplemental LED lighting on enhancing the yield Published: 29 April 2021 (+40%), soluble solid (+6%) and ascorbic acid (+11%) contents, leaf chlorophyll content Citation: (+31%), photosynthetic capacity (+50%), and leaf area (+9%) compared to the control Appolloni E, Orsini F, Pennisi G, Gabarrell Durany X, Paucek I and conditions. In contrast, supplemental LED lighting did not show a statistically significant Gianquinto G (2021) Supplemental effect on the leaf stomatal conductance (p-value = 0.171). In conclusion, in addition LED Lighting Effectively Enhances the to some partial inconsistencies among the considered studies, the present research Yield and Quality of Greenhouse Truss Tomato Production: Results of a enables us to assert that supplemental LED lighting ameliorates the quantitative and Meta-Analysis. qualitative aspects of greenhouse tomato production. Front. Plant Sci. 12:596927. doi: 10.3389/fpls.2021.596927 Keywords: supplemental light, LED, greenhouse, Solanum lycopersicum, interlighting Frontiers in Plant Science | www.frontiersin.org 1 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review INTRODUCTION photomorphogenesis, and chlorophyll production (O’Carrigan et al., 2014b). Cryptochromes and phototropins are the main In greenhouse tomato (Solanum lycopersicum) production, photoreceptors stimulated by blue light (Christie et al., 2015); photosynthesis and carbon sequestration may be hindered by these photoreceptors go through a phosphorylation process cloud cover, shading systems, and variable solar radiation, as well and bind protein to trigger proton extrusion and K+ uptake as by plant mutual shading (e.g., when high vertical stem training in stomatal guard cells, with the consequent cell turgidity or increased crop densities are used) (Zhang et al., 2015; Tewolde and stomatal opening enabling gas exchange (Roelfsema and et al., 2018). Considering the non-uniform distribution of solar Hedrich, 2005: Shimazaki et al., 2007). Apparently, green and red radiation around the world, limitations may also occur in cases of light may also play roles in gas exchange by inducing stomatal high-latitude countries such as Canada, Japan, Norway, as well as closure, as green light may stop soluble uptake in guard cells in the northern areas of China and the United States, where long (Talbott et al., 2002), while red light may lead to K+ and winters and low DLIs (daily light integrals) may affect greenhouse solute losses (Zeiger, 1990). In tomato plants, studies that have production (Garland et al., 2010; Deram et al., 2014; Sun et al., applied blue, red, and green lighting in closed chambers seem 2015; Tewolde et al., 2016; Paponov et al., 2019). Supplemental to confirm such observations (O’Carrigan et al., 2014b; Bian artificial lighting can be applied to increase greenhouse yields and et al., 2019), opening the possibility of integrating green LED ensure stable year-round production regardless of environmental lighting to reduce drought stress in tomato plants (Bian et al., conditions (Ohashi-Kaneko et al., 2007), even in regions with 2019). However, it is important to consider that what is observed high DLIs, such as the Mediterranean and Jordan Valley (Israel) in growing chamber experiments is not always transferable to (Joshi et al., 2019; Paucek et al., 2020). Today, light-emitting the processes occurring in productive systems, where different diode (LED) lamps represent the most advantageous artificial environmental factors may affect plant responses. lighting systems in terms of energy use efficiency, with foreseen Greenhouse tomatoes represent one of the most relevant expectations for further reducing investments and running costs horticultural crops worldwide (Deram et al., 2014; FAO, 2018). In in the near future (Olle and Viršile, 2013). Additional advantages intensive greenhouse tomato production, high-wire single-truss also involve the functional aspects of LEDs that make the training systems are normally applied to enable labor reductions, technology suitable for cultivation, particularly thanks to their multiple harvests and possible automation (Giniger et al., 1988; possible miniaturization, light weight, and limited radiant heat Okano et al., 2001). Nonetheless, the high plant density required emissions (Ibaraki, 2017). Accordingly, LED lamps can be used for these systems can limit light penetration within canopies with in proximity to plant canopies without excessively increasing consequences on fruit quality and yield (Wada et al., 2006). In this the leaf temperature (Morrow, 2008), enabling inter-lighting context, several studies have already reported the usefulness of applications that reduce intracanopy shading conditions in high- LED lighting system applications for qualitative and quantitative stem-density plants (Jokinen et al., 2012, Gómez and Mitchell, improvements in greenhouse truss tomato production (Tewolde 2016a; Kumar et al., 2016; Hao et al., 2017). et al., 2016; Dzakovich et al., 2017; Jiang et al., 2017; Kim LED application can enable the fine tuning of combinations et al., 2019). However, inconsistencies among studies are also between light spectral compositions and light intensities, with present; non-significant effects of supplemental LED lighting, direct consequences not only on yield but also on structural especially on qualitative parameters (e.g., soluble solids, ascorbic and physiological plant aspects (Ouzounis et al., 2015; Hao acid) (Lu et al., 2012b; Hao et al., 2016), have been found. In et al., 2017; Ibaraki, 2017). In fact, the responses of plants most studies to date, researchers have integrated supplemental to light characteristics are regulated by photoreceptors that LED lighting technologies either in greenhouses where no reading specific wavelengths, intensities or photoperiods can supplemental lighting was formerly present or as additional trigger signals that modify plant metabolism (Christie et al., lighting sources in greenhouses where top artificial lights (e.g., 2015). Accordingly, light environmental management can lead high-pressure sodium lights, HPSs, lamps) were already installed to interesting commercial results. For instance, red light can and in operation. Accordingly, this study aims to offer an promote flower development (Liao et al., 2014), while the blue- overview of the recent topic of supplemental LED lighting for violet spectrum can increase plant protection from diseases greenhouse tomato production through the use of a meta- (Tokuno et al., 2012; Hui et al., 2017), preserving postharvest analysis as a statistical tool to summarize the results of published conservation and food safety through the inactivation of studies and understand the effectiveness of supplementary LED pathogen action (D’Souza et al., 2015). Moreover, specific light lighting in influencing the qualitative-quantitative aspects of spectra can improve the qualitative and nutraceutical aspects truss tomatoes. Consequently, the meta-analysis aims to answer of plants (Mempel and Wittmann, 2019), such as enhancing the following research question: does supplemental LED lighting antioxidant compound biosynthesis (e.g., flavonoids, ascorbic enhance the yield and qualitative traits of greenhouse truss acid) in various species (e.g., lettuce, basil, tomato) (Ebisawa tomato production? et al., 2008; Carvalho et al., 2016; Jiang et al., 2017; Pennisi et al., 2019a,b). MATERIALS AND METHODS Stomatal conductance is a specific physiological response that is guided by light. The wavelength mainly involved in this Data Collection process is blue light (450 and 495 n), which is also implicated in Article collection was conducted during the first half of 2020 other mechanisms, such as phototropism, chloroplast migration, using online databases (e.g., Google Scholar and Scopus). The Frontiers in Plant Science | www.frontiersin.org 2 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review following search string was applied to identify publications: information in cases of general descriptive data relative to the LED AND supplemental light∗ AND tomato∗ AND greenhouse. trials. Figure 1 shows the flow diagram applied for the data Only accessible published material in the English language was selection and evaluation. collected, including scientific articles, conference papers, book chapters, and thesis dissertations. The literature search results Meta-Analysis were then filtered to reduce heterogeneity in the studies and The response ratio [R] considered in the meta-analysis was to include only Solanum lycopersicum species cultivated in represented by the influence of supplemental LED lighting on greenhouses with supplemental LED lighting or supplemental the Yield, TSS, Asc, Chl, PN, gs , and LA of greenhouse-grown LED lighting combined with HPS lamps. All cultivar types, tomato plants. Since each study accounted for more than one growing systems and greenhouse typologies were considered. treatment, each trial was examined as a separate observation (k). Given that the presence of solar radiation was a requisite of the Accordingly, each study could have more than one observation. research question (targeting the effect of supplemental LEDs in For instance, if an article compared two different supplemental greenhouses), studies of indoor cultivation in which only artificial LED lighting treatments, one with a red spectrum and the lighting sources (e.g., indoor farming) were applied were not other with a blue spectrum, each treatment was considered an considered in the research. Overhead, intracanopy and bottom individual observation. Each treatment value was compared with lighting supplies were all included, as well as nighttime, end- a control value from the same article to perform a meta-analysis of-the-day, and continuous lighting treatments. Only one case based on the differences among independent groups. In the of night-break lighting supply was excluded from the research current study, the applied control treatment may be of two types: (Cao et al., 2016). Furthermore, studies reporting evaluations on solar light only or solar light + HPS light. In the first case, seedlings or transplants with short treatment periods were also the control was compared with solar light + supplemental LED excluded; only mature and productive plants were considered to light, while in the second case, the comparison involved solar accomplish the upstream objective of evaluating the qualitative light + HPS light + supplemental LED light. Only observations and quantitative effects of supplemental LED lighting on reporting a control, either with solar or solar + HPS light, were tomato production. used for the meta-analysis after a second selection phase. In one The collected data included both general information related case (Deram et al., 2014), the comparison between the control to trial conditions and more specific data used in the meta- and treatment showed extremely high values compared to other analysis. In particular, the general data were represented by results. In this case, the data were considered outliers and were intrinsic or environmental trial features (cultivar, location, excluded from the meta-analysis. maximum and minimum temperatures, relative humidity, The [R] of each observation was calculated as follows: nutrient solution electrical conductivity (EC) and pH, plant density, greenhouse typology, and growing system), as well as ln mt by the LED treatment characteristics (light spectrum, intensity ln R = ln (R) = = ln mt ln mc ln mc and photoperiod, treatment duration, and other eventual specific experimental conditions, e.g., nighttime treatments). All these where mt and mc represent the mean outcomes of the treatment general data were used in the descriptive statistical analysis and and control, respectively (Hedges et al., 1999; Borenstein et al., to identify factors of heterogeneity among different experiments 2009). Since most of the considered publications did not display during the meta-analysis. The natural lighting amount (e.g., DLI) standard error (SE), variance (Var), or standard deviation (S) was not considered due to the scarcity of articles reporting this values, an unweighted meta-analysis was applied to equally information. The specific data referred to precise information weight each observation (McDaniel et al., 2014; Qin et al., 2015). that was needed for the development of the meta-analysis, The data were analyzed using the online available software Meta- including the treatment and control mean outcomes as well Essential (Suurmond et al., 2017). A random effect model was as the sample size (or replicate number, in cases in which the chosen for each response value (Yield, TSS, Asc, Chl, PN, gs , sample size was not available). Studies not reporting specific and LA). The heterogeneity value (I 2 ) was used to evaluate the data were not used for the meta-analysis development. The percentage of variation among studies (Hak et al., 2016). Cases outcomes, also called the effect sizes or response ratios [R] reporting I 2 values higher than 25% were further investigated by (Hedges et al., 1999), used in the meta-analysis consisted of the applying a subgroup analysis (Borenstein et al., 2009; Hak et al., fresh fruit mass yield (yield, expressed as kg plant−1 of fresh fruit 2016). The subgroup analysis divided the observations into six mass), soluble solid content (TSS, expressed as ◦ Brix), ascorbic categories: solar light or solar light + HPS used as a control; acid content (Asc, expressed as mg Asc 100 g−1 of fruit fresh pure supplemental LED light or supplemental LED light + HPS; weight), chlorophyll content (Chl, expressed as Chl index), net artificial light supply (e.g., DLI ≥10 or <10 mol m−2 d−1 ); photosynthesis (PN, expressed as µmol CO2 m−2 s−1 ), stomatal seasonality (whether the hours of natural light were increasing, conductance (gs , expressed as mmol H2 O m−2 s−1 ), and leaf e.g., during spring in the Northern Hemisphere, or decreasing, area (LA, expressed as m2 per plant). Only physiological and e.g., during fall in Northern Hemisphere, along the experiment); vegetative outcomes directly influencing tomato productivity and photoperiod ≥16 or <16 h d−1 ; lighting supplied as intracanopy quality were considered, while other information (e.g., stem or others. In the last case, “others” were intended to include diameter, internode length) was not investigated. Outcome values overhead, bottom or combined lighting supplies, which were were extracted from both tables and graphs, integrating textual grouped together due to the low number of singular categories. Frontiers in Plant Science | www.frontiersin.org 3 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review FIGURE 1 | Flow diagram showing the steps of the study selection and analysis. Hedges’ g was applied as the measurement of the effect size in the registered, occurring for 22% of cited cases with sand, perlite, meta-analysis model. The [R] value was accepted as significant vermiculite or peat applied as growing substrates. The use of with a p-value < 0.05, considering a confidence interval (CI) of bags filled with substrate (peat, vermiculite or perlite) was also 95%. Since the results showed high heterogeneity, no publication identified in 3 out of 36 cases. Finally, only two soil-based bias analysis was performed, assuming its absence (Hak et al., cultivation cases and one nutrient film technique (NFT) case 2016). A graphic representation of the study distribution per year were reported. and country was realized using Gephi software (Bastian et al., Concerning the planting density, the 45 studies showed a 2009) (Figure 2). mean of ∼5 plants m−2 , a mode of 2.7 plants m−2 and a median of 2.7 plants m−2 , with values ranging from 1.5 to 16.6 plants RESULTS m−2 . The average maximum and minimum temperatures were 23 and 19◦ C, respectively, while the average relative humidity The literature search results are included in was 69%. The applied nutrient solutions had a mean EC value Supplementary Material 1, attached as an Excel file to the of 2.4 dS m−1 and a mean pH value of 6. Different cultivars present manuscript. The preliminary literature search resulted of truss tomato were used in the trials (33), and the highest in 45 studies following the selection criteria. These publications recurrence was observed for Solanum lycopersicum cv Komeett were used for the descriptive statistical analysis. The results (De Ruiter, Amstelveen, The Netherlands), which was mentioned showed that the majority of trials took place in North America, in 10 publications. with 38% of the total cases (USA n = 9, Canada n = 8), while In total, 161 supplemental LED lighting treatments were Europe (Netherlands n = 8, Norway n = 3, Poland n = 2, observed within the 45 collected publications. Of those Belgium n = 1, Germany n = 1, and Italy n = 1) and Asia (Japan treatments, 57% applied intracanopy LED lighting, 8% applied n = 6, China n = 4, and South Korea n = 2) reported frequencies bottom lighting, 17% applied overhead lamps, 13% applied a of 35 and 27%, respectively. No cases were registered in other combination of supply methods (e.g., intracanopy + overhead continents. No collected publication was released before 2011, lighting), and 6% of cases did not clearly report the type and the collected studies showed the highest frequencies in 2019 of lighting supply. Furthermore, 20% of revised observations (29%) and 2016 (18%) (Figure 2). applied a combination of LED and HPS lighting as the Although not always stated, most experiments were supplemental treatment. Regarding the daily lighting duration, conducted in technologically advanced greenhouses applying the mean photoperiod used was 15 h d−1 , while the mode and soilless growing methods, and the studies often mentioned median durations were both 16 h d−1 . Within the collected controlled environmental systems. When reported, the highest- literature, two extreme cases of 24 h of continuous lighting and frequency growing methods reported were substrate cultivation 2 h of end-of-the-day lighting were also found. The average on slabs (61% of 36 cases reported this growing method). Slab photosynthetic photon flux density (PPFD) and DLI supplied materials were mainly represented by rockwool, although two through lighting were also registered, showing values of 165 cases of coir use were also reported. Pot employment was also µmol m−2 s−1 and 9.5 mol m−2 d−1 , respectively, while the mode Frontiers in Plant Science | www.frontiersin.org 4 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review FIGURE 2 | Graphical distribution of 45 selected studies grouped by country and publication year. and median were 160 and 165 µmol m−2 s−1 for PPFD and 11.5 LED lighting, although different tendencies and significances and 9.8 mol m−2 d−1 for DLI, respectively. Spectral compositions were observed depending on the evaluated [R] (Figure 3). occurred in numerous combinations and ratios depending on PN (k = 45) and Yield (k = 68) were the parameters most the trial. The absolute frequencies of the red, blue, white, far- affected by supplemental LED treatments, reporting the highest red, and UV spectral components were registered separately, standardized mean differences (Hedges’ g) of 2.70 and 1.75, and each component was counted each time it appeared in respectively. Both response ratios were significantly influenced a treatment independently from the combinations. The count by supplemental lighting, with one-tailed p-values < 0.001. resulted in red light supplies recurring in 128 cases, while light Conversely, gs (k = 26) showed a standardized mean difference in the blue, white and far-red spectra were adopted 115, 24 of 0.83, although no significant effect was reported (p = 0.171). and 20 times, respectively. UV application was only used 3 Asc (k = 20) and TSS (k = 38) presented standardized mean times, while green light occurred once. Both UV and green light differences of 0.81 and 0.34, with significant p-values of 0.001 were always applied in combination with other light spectral and <0.001, respectively. Finally, Chl (k = 40) and LA (k = 38) components. Furthermore, 68% of the reviewed observations recorded similar values, showing Hedges’ g values of 0.74 and used a combination of red and blue diodes, while monochromatic 0.75, respectively, while the p-values were <0.001 for both cases. red or blue diodes were applied in 6 and 2% of total observations, Figure 3 displays a summary of the combined effect sizes. respectively. The average duration of treatments was 5 months, The I 2 value, which describes the percentage of variation with the durations ranging from 2 to 8 months. among studies, was the main investigated factor used to After a second selection phase, 10 studies not reporting any understand the heterogeneity in the results (Hak et al., 2016). In control, as well as one outlier case concerning the reported particular, fruit yield (Yield) showed a heterogeneity of 89.18%. yield values (Deram et al., 2014), were excluded from the The qualitative effects, measured as TSS and Asc, reported meta-analysis. This selection resulted in 31 studies, and 100 I 2 values of 29.27 and 75.97%, respectively. The physiological total observations were used for the further analyses. The parameters showed I 2 values equal to 91.66% for gs , 91.15% results revealed the generally positive effects of supplemental for PN, and 73.23% for Chl. Finally, the LA heterogeneity Frontiers in Plant Science | www.frontiersin.org 5 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review FIGURE 3 | Forest plot showing the combined effect sizes and main meta-analysis parameters of the investigated response ratios (Yield, Yield; TSS, soluble solid content; Asc, ascorbic acid content; Chl, chlorophyll content; PN, photosynthetic capacity; gs , stomatal conductance; LA, leaf area). Numbers within brackets refer to k response ratios. The meta-analysis parameters are the effect size value (Hedges’g), low and high confidence intervals (CI), and tests of the null hypothesis (one-tailed p-value and z-value) (Hak et al., 2016). TABLE 1 | Heterogeneity evaluation of response ratios. Q pq I2 T2 T Yield 619 <0.001 89.18 3.45 1.86 TSS 52.31 0.049 29.27 0.10 0.31 Asc 79.07 <0.001 75.97 0.86 0.93 gs 299.70 <0.001 91.66 4.07 2.02 PN 497.14 <0.001 91.15 4.18 2.05 Chl 145.67 <0.001 73.23 0.76 0.87 LA 185.33 <0.001 80.04 1.09 1.05 Yield, Yield; TSS, soluble solid content; Asc, ascorbic acid content; Chl, chlorophyll content; PN, photosynthetic capacity; gs , stomatal conductance; LA, leaf area. Q, The heterogeneity parameters are the weighted sum-of-squared differences between the observed effects and the weighted-average effects; pq , the test of the null hypothesis; I2 , the measure of the proportion of observed variance that reflects the real differences in the effect size; T2 and T, the measure of the dispersion of the true effect sizes between studies in terms of the scale of the effect size (Hak et al., 2016). was 80.04%. The other parameters explaining heterogeneity are DISCUSSION reported in Table 1. All response ratios showed high heterogeneity, with I 2 values The worldwide distribution of the 45 identified studies showed >25%. Accordingly, a subgroup analysis was performed for a prevalence of trials in countries of the boreal hemisphere each outcome. Low heterogeneity was observed for Yield in occurring at latitudes above 43◦ N, falling within the temperate cases of light supplies different from intracanopy supplies (I 2 climatic zone (Fischer et al., 2012). Geographical latitude is = 18.7%) and cases using solar + HPS lighting as controls one of the main factors constraining daily solar radiation (I 2 = 12.7%); for TSS in cases with increased natural lighting during the year, thus affecting the minimal light requirements (I 2 = 21.2%) and lighting supplies other than intracanopy of most horticultural crops (∼2.34 kWh m−2 d−1 , which supplies (I 2 = 0.0%); and for Chl in cases with decreased translates to ∼8.5 MJ m−2 day−1 ) and, consequently, affecting natural lighting (I 2 = 0.0%). Table 2 shows the I 2 heterogeneity climatic suitability for greenhouse cultivation (Castilla and values identified for each [R] value and subgroup, as well Baeza, 2013). Accordingly, supplemental lighting can be as the percentages of each subgroup both relative to the particularly appropriate to guarantee better light distributions single response ratios and to the total number of meta- and longer cultivation spans in high-tech greenhouses in analysis observations. Cases not reporting a sufficient number northern countries, although useful applications were also of observations (k ≥ 5) within each subgroup division were observed within the Mediterranean area (Paucek et al., 2020). not reported. Although Mediterranean greenhouse cultivation is mainly Frontiers in Plant Science | www.frontiersin.org 6 April 2021 | Volume 12 | Article 596927 Frontiers in Plant Science | www.frontiersin.org Appolloni et al. TABLE 2 | Subgroup analysis reporting heterogeneity (I2 ) and percentage (P) by response ratio (Yield, Yield; TSS, soluble solid content; Asc, ascorbic acid content; Chl, chlorophyll content; PN, photosynthetic capacity; gs , stomatal conductance; LA, leaf area) and total percentage (Tot P) of subgroups considering 104 total observations used in the meta-analysis. Yield TSS Asc gs PN Chl LA Tot (k = 68) (k = 38) (k = 20) (k = 26) (k = 45) (k = 40) (k = 38) (k = 104) I2 (%) P(%) I2 (%) P (%) I2 (%) P (%) I2 (%) P(%) I2 (%) P (%) I2 (%) P(%) I2 (%) P(%) Tot P (%) Control type Solar light 92.2 69.1 - 97.4 - 85.0 - 100.0 - 97.8 - 90.0 79.8 86.8 80 Solar + HPS 12.7 30.9 - 2.6 - 15.0 - 0.0 - 2.2 - 10.0 77.5 13.2 20 Lamp type LED 92.6 64.7 - 94.7 - 80.0 - 92.3 - 93.3 75.1 87.5 78.9 86.8 76 LED+HPS 28.9 35.3 - 5.3 - 20.0 - 7.7 - 6.7 49.9 12.5 67.5 13.2 24 DLI <10 76.9 52.9 34.4 44.1 81.6 45.0 88.1 65.4 87.6 55.6 81.1 50.0 72.5 50.0 42 >=10 93.2 47.1 36.7 55.9 71.2 55.0 93.7 34.6 92.2 44.4 56.9 50.0 83.5 50.0 58 Photoperiod <16 80.8 35.3 45.5 41.9 84.4 45.0 92.8 34.6 90.3 37.8 88.5 30.0 35.8 34.2 30 >=16 91.1 64.7 28.6 58.1 71.3 55.0 91.4 65.4 90.4 62.2 43.2 70.0 84.9 65.8 70 Natural light 7 Decreasing 86.6 30.5 52.9 33.3 84.9 38.9 91.2 28.0 95.8 27.0 0.0 16.1 - 11.1 30 Increasing 91.2 69.5 21.2 66.7 67.7 61.1 90.4 72.0 83.2 73.0 66.2 83.9 - 88.9 70 Light supply Intracanopy 91.9 72.1 36.9 84.2 - 80.0 92.6 62.2 92.9 68.9 73.4 57.5 86.7 57.9 77 Others 7.4 27.9 0.0 15.8 - 20.0 84.7 30.8 81.6 31.1 71.7 42.5 45.0 42.1 23 I2 values <25% are reported in bold. LED Lighting for Greenhouse Tomato: A Review April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review characterized by applications of low-tech solutions (Fernández fruit production phase, suggesting a mean temperature of 21– et al., 2018), some examples of technologically advanced high- 18◦ C, with nutrient solutions featuring ECs of 2.7–4.0 dS m−1 density greenhouse farms also exist in this region (Meneses and a pH value of 5.8 (OMAFRA, 2001). When a supplemental and Castilla, 2009; Tuzel and Oztekin, 2014). In these LED lighting system is adopted, temperature management cases, supplemental lighting may be applied to improve off- becomes a key factor. Dueck et al. (2011) observed that tomato season production. Indeed, research on the application of plants grown under LED lighting receive less radiative energy supplemental LED lighting in the Mediterranean region has than when other lamp typologies (such as HPS lamps) are already demonstrated the capability of this technology to used, thus requiring more thermal heat during cold seasons improve yields and anticipate the ripening of truss tomatoes to maintain an optimal temperature within the greenhouse. during spring and summer (Paucek et al., 2020), although further On the other hand, Verheula et al. (2019) pointed out that research should be conducted in the fall season. Furthermore, it is the addition of supplemental LED inter-lighting to HPS lamps important to consider that Mediterranean greenhouse cultivation can increase the temperature by 1–2◦ C, leading to increased can suffer from excessive sun radiation and temperatures ventilation requirements for greenhouse production during during summertime, making external shading a necessary summer. Furthermore, considering that the lifespans of LED technique to ensure good internal growing conditions (Castilla lamps are halved when the working temperature increases by et al., 2002). However, sunlight screening may also reduce 10◦ C, a cooling system may also be necessary (Nelson and plant photosynthesis, especially in cases of low-cost permanent Bugbee, 2014; Hinov et al., 2019). The average planting density solutions (e.g., whitewashing) (Garcia et al., 2011). Tewolde value adopted in the considered studies was higher than the et al. (2018) demonstrated the feasibility of supplemental suggested greenhouse standards (2.5 plants m−2 for northern LED inter-lighting on tomato production in cases of shading Europe) (Kubota et al., 2018), even reaching 16.6 plants m−2 in cover applications, obtaining the same qualitative-quantitative some studies (Song et al., 2016; Johkan et al., 2017). Elevated performances as those observed in the naturally lighted control. planting densities may negatively affect light absorption in Although LED use was identified as an effective artificial lighting tomato plants (Sarlikioti et al., 2011), but the use of supplemental source for horticultural purposes (Heuvelink and Gonzalez-Real, lighting can compensate for the lower light availability caused 2007; Gupta and Agarwal, 2017), research on greenhouse-grown by an increased planting density, also enabling higher annual tomato production using supplemental LED lighting seems to be production compared to systems with lower planting densities relatively recent, as evidenced by the higher number of studies (Dorais et al., 1991). published during the last 5 years (Figure 2). Nevertheless, earlier The lighting distribution is a fundamental factor associated studies on seedlings and transplants are also present (Brazaityte with optimizing the effectiveness of supplemental lighting et al., 2009; Suzuki et al., 2009), though they were not considered systems. Traditionally, overhead lamps were used in greenhouse within this research. production systems, resulting in increased upper leaf interception High-tech solutions characterized by the use of soilless and intracanopy shading (Gomez et al., 2013). Although an cultivation systems, controlled climates and high plant densities overhead lighting supply may be preferred by growers due were mainly adopted in the evaluated trials. Although not always to both its easy installation in greenhouses and reduced mentioned, some studies reported high-wire growing methods labor requirements for crop management (Gunnlaugsson and based on plant lowering, allowing for production throughout Adalsteinsson, 2005), intracanopy lighting can increase light several seasons (Kubota et al., 2018). This training system, interception within a canopy, enhance light use efficiency thanks in association with advanced protected growing technologies, to better lighting distribution and maintain the photosynthetic can ensure increased productivity despite flourishing vegetation capacities of lower leaves (Trouwborst et al., 2011). The efficacy causing inner canopy shading (Hamamoto and Yamazaki, of intracanopy lighting on tomato production has already been 2009) and light quality modifications that occur due to ascertained by using HPS and fluorescent lamps (Gunnlaugsson both greenhouse cladding materials and shading items (Kittas and Adalsteinsson, 2005; Lu et al., 2012a), although its feasibility et al., 1999; Petropoulos et al., 2019). An economic analysis for technological uptake emerged only after the introduction demonstrated that these highly productive systems, together of low-surface-temperature LEDs (Hao et al., 2012; Guo et al., with efficient lighting technologies, can make supplemental 2016). In our research, the majority of considered trials applied lighting more effective for greenhouse tomato production than intracanopy LED lighting alone, sometimes combined with for the production of other species (Kubota et al., 2016). overhead HPS lamps. However, few cases of overhead LED With reference to both the technical and environmental aspects lighting alone against a control were also registered. Although not of trial management, the analysis of the results showed that statistically significant differences could be observed, intracanopy most supplemental LED lighting studies followed the optimal lighting tended to have a larger impact on yield than overhead growth conditions suggested for intensive greenhouse tomato lighting alone when compared to the controls. Finally, LEDs can production (Schwarz et al., 2014; Kubota et al., 2018). For also be applied as below-canopy lighting. Supplemental lighting instance, rockwool was found to be the most-applied growing strategies have been shown to increase photosynthesis both substrate, as is commonly observed in greenhouse tomato soilless below and within the canopy. However, two studies comparing cultivation systems (Kubota et al., 2018). The environmental intracanopy light with below-canopy lighting found that the growth conditions also followed the recommendations for the latter technology can promote CO2 assimilation and stomatal Frontiers in Plant Science | www.frontiersin.org 8 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review conductance by providing stable light penetration even at low resistance to Botrytis cinerea (Ji et al., 2019). Finally, Hao et al. canopy levels (Song et al., 2016; Johkan et al., 2017). (2018) investigated the effects of UV light on tomato yield and Deram et al. (2014) observed that the responses of plants to did not confirm any significant increase compared to other supplemental lighting also depended on the spectral components wavelengths. It should be noted that UV light is traditionally of the lighting system adopted. Red and blue wavelengths, alone not considered within photosynthetic active radiation (PAR), or combined in different ratios, were mainly used in the studies although recent studies have also attributed the capacity of UV evaluated in our research. In general, red light was mostly light to foster photosynthesis and growth in plants, e.g., in basil efficient in enhancing photosynthesis (McCree, 1971; Kaiser (Dou et al., 2019). Moreover, Tokuno et al. (2012) demonstrated et al., 2019a), while blue light was shown to play an important the effectiveness of supplemental UV LED radiation in reducing role in controlling plant morphology, biomass accumulation phytopathological diseases in greenhouse tomato plants. Further and stomatal conductance (Ménard et al., 2005; Johkan et al., research should also specifically target the effect of UV radiation 2010; Ieperen et al., 2012). Monochromatic lighting may be less on inducing secondary metabolite production in greenhouse- effective than a combination of red and blue light, since combined grown tomato plants, as already observed in several crops blue light can mitigate the so-called “red light syndrome” (seen (Schreiner et al., 2014). with monochromatic red lighting), which manifests itself in In addition to lighting quality, the intensity and photoperiod reduced leaf growth and decreased stomatal conductance and of lighting are also fundamental aspects. Deram et al. (2014) photosynthetic capacity (Miao et al., 2019). Lu et al. (2012b) investigated different supplemental LED lighting intensities (135, observed the effects of monochromatic supplemental lighting on 115, and 100 µmol m−2 s−1 ), although no statistically significant greenhouse truss tomato plants, showing higher yields in cases differences in plant productivity were observed. However, studies of red light application compared to pure blue light application. on light intensity are still limited, and further investigations However, good results were also obtained by using white light of the optimization of plant photosynthetic responses while containing both red and blue spectral regions in addition to minimizing energy costs are needed (Weaver et al., 2019). an abundant presence of green light, which may favor light Concerning the photoperiod, the tomato is a photosensitive penetration within a canopy and be particularly suitable for species with an optimal photoperiod identified at ∼14 h d−1 single-truss growing systems (Lu et al., 2012b). Deram et al. (Dorais et al., 1996; Demers et al., 1998; Demers and Gosselin, (2014) and Kaiser et al. (2019a) highlighted the effectiveness of 2000). Continuous lighting (24 h d−1 ) for 5–7 weeks may red and blue combinations for tomato production, suggesting improve tomato plant growth and tomato yield, while a longer red:blue = 4 and red:blue = 1.2–2.4 as optimal ratios for yield supply period can have negative effects, likely caused by improvement, respectively. Kaiser et al. (2019b) also evaluated accumulations of sucrose and starch affecting the maximum the partial replacement of red:blue LED lights with different quantum efficiency of photosystem II (PSII) with consequent leaf percentages of green light (7, 20, and 39%) in cases of greenhouse chlorosis (Demers et al., 1998; Demers and Gosselin, 2000; Velez- tomato production with supplemental artificial lighting. The Ramirez et al., 2017). However, the alternation of red and blue results showed that the highest studied green percentage (39%), continuous LED lighting was reported to reduce plant injuries, which was similar to the sunlight spectrum, showed the best with potential applications for long-term yield improvements effects on plant biomass and yield, suggesting that plants may (Lanoue et al., 2019). Additionally, the period of the day (daytime use sunlight-combined wavelengths more efficiently for growth or nighttime) in which additional lighting is supplied may affect than other wavelength combinations (Kaiser et al., 2019b). The plant production. Particularly, Tewolde et al. (2016) confronted far-red wavelength was also investigated by several studies on daytime vs. nighttime (applying light from 4:00 am to 4:00 pm in greenhouse tomato supplemental LED lighting (Pepin et al., the case of daytime supply and from 10:00 am to 10:00 pm for 2014; Hao et al., 2015, 2016; Gómez and Mitchell, 2016b; Song nighttime treatment) supplemental LED lighting applications, et al., 2016; Dzakovich et al., 2017; Fanwoua et al., 2019; Ji reporting a significant increase in yield, as well as of soluble solids et al., 2019; Kalaitzoglou et al., 2019; Kim et al., 2019, 2020; and ascorbic acid, during wintertime in the case of nighttime Zhang et al., 2019). The far-red ratio, particularly the red:far- supply and also observing better cost-effectiveness of nighttime red ratio, influences phytochrome regulation and has effects on supply compared to diurnal applications. plant architectural development, flower induction, germination, The meta-analysis results showed that the application of photosynthetic capacity, and nutrition (Demotes-Mainard et al., supplemental LED lighting on greenhouse tomato plants has 2016). Zhang et al. (2019) evaluated the effects of different a statistically significant tendency toward enhancing Yield, durations of the far-red lighting supply (namely, 0.5, 1.5, or 12 h TSS, Asc, Chl, PN, and LA, while no significant results were day−1 ) on greenhouse tomato cultivation, concluding that even observed for gs (Figure 3). With reference to Yield, although when adopting the lowest supply time, plant stem elongation the tendency revealed a global positive effect (with an average was stimulated, thus enhancing light penetration within the yield increase of +40% from the control conditions), some canopy. Kalaitzoglou et al. (2019) also highlighted similar far-red- studies reported negative or equal output values compared induced morphological and productive effects on tomato plants, with their control treatments. These inconsistencies may be although pointing out the necessity for long-term far-red supplies attributed to different trial management aspects and should be during the day to obtain optimal performances. Furthermore, far- considered to obtain the best tomato cultivation performance red light may also improve the hedonic perception of tomato using supplemental LED lighting. Tewolde et al. (2016) observed fruit (Kim et al., 2020), despite the potential reduction of that daytime LED inter-lighting during summer may reduce Frontiers in Plant Science | www.frontiersin.org 9 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review tomato yield compared to a solar light control, probably due light qualities, intensities, growing systems, etc.) but also the to the excessive temperature and radiation around the mid- absence of common meta-data protocols for data collection and canopy area caused by lamps. A similar effect was also observed presentation. The last can be seen as one of the main issues by Verheula et al. (2019), equally pointing out the need for hindering the development of agricultural meta-analyses, and ventilation during summer, although with lower energy savings. this challenge should be overcome by always presenting all the Additionally, Gómez et al. (2016) reinforced these observations, statistical values needed for a meta-analysis evaluation (e.g., the concluding that supplemental LED lighting may not be a feasible standard error, standard deviation, variance, and sample size), solution during summer even when a root cooling system as well as by applying common measurement methods (Eagle is used. et al., 2017). The lower heterogeneity observed for TSS than Looking at qualitative parameters, while most of the analyzed for the other factors may be attributed to different measuring studies associated supplemental lighting with positive effects systems or units, while the other evaluated effect sizes utilized (increasing TSS by 6% and Asc by 11%), some inconsistent different measurement standards that required unit conversions results were also found. Accordingly, Dzakovich et al. (2015, in some cases. Concerning the subgroup analysis, most of the 2017) reported that supplemental lighting did not increase confronted group showed high heterogeneity, indicating the the TSS values. Similarly, supplemental lighting on tomato absence of influences determined by specific trial characteristics. plants was not associated with increased TSS values or Asc However, low heterogeneity was observed for Yield in cases of contents (Lu et al., 2012b) or with the sugar or acid contents, lighting supplies different from intracanopy lighting or pure according to Gautier et al. (2005). However, it is important HPS lamps used as controls, for TSS in cases of increased to consider that in addition to light access, other factors may natural light or other lighting supplies, and for Chl in cases affect the qualitative parameters of tomato fruits (e.g., genotype, of decreased natural lighting. Accordingly, the analysis revealed environmental conditions, nutrient solution EC) (Kubota et al., common trends of results in these specific subgroups. However, 2012; Dzakovich et al., 2015; Ouzounis et al., 2016). Furthermore, further targeted assumptions regarding the effect of specific LED it must be acknowledged that the parameters used for the purpose lighting features (e.g., decreasing or increasing natural sunlight; of this research (e.g., TSS and Asc) do not entirely describe intracanopy or other light supplies) on the combined effect sizes tomato fruit quality from a sensorial or nutraceutical standpoint. cannot be hypothesized due to the absence of homogeneity in the For instance, due to the scarcity of studies, some qualitative confronted group. aspects (e.g., antioxidant content) were not evaluated in the present research. Further research on the antioxidant response to supplemental LED lighting is therefore needed, also considering that a potential increase in carotenoids induced by using far-red CONCLUSION light has already been reported (Hao et al., 2016). In this study, the leaf response to supplemental LED lighting Despite some limitations commonly occurring in agricultural was evaluated in terms of Chl, PN, LA, and gs . As already meta-analyses, the research conducted herein revealed that presented within the results (Figure 3), the response ratios [R] supplemental LED lighting may be effective in improving the for Chl, PN, and LA globally reported statistically significant quantitative and qualitative aspects of greenhouse-grown truss increases when supplemental LED lighting was applied (on tomato production. Significant positive results were observed average, increasing Chl by 31%, PN by 50%, and LA by 9%). for both direct qualitative-quantitative parameters (Yield, TSS, Additionally, for these parameters, however, inconsistencies Asc) and crop photosynthetic properties (Chl, PN, LA), were observed among studies. In particular, Kim et al. (2019) while only stomatal conductance (gs ) was not significantly observed reductions in Chl and LA in plants treated with low affected by supplemental LED lighting. Further research is red:far-red levels for long durations, which may be attributed needed regarding product quality, particularly focusing on the to major biomass allocations in reproductive structures during unexplored effects of LED lighting on nutraceutical properties plant growth and development. Other authors also observed and organoleptic features. Moreover, most studies considered non-statistically significant differences in both the chlorophyll herein applied red and blue spectra, although preliminary content and total leaf area (Jiang et al., 2017) or in the studies have also introduced promising results by applying leaf area only (Gómez and Mitchell, 2016b) when applying UV or green light. Finally, the collected studies were mainly supplemental lighting treatments. No statistically significant concentrated in the northern part of the boreal hemisphere, effect of supplemental LED lighting application on PN was where the presence of technologically advanced greenhouses, observed by Gajc-Wolska et al. (2013) or by Gómez et al. as well as some favorable environmental conditions due to (2016) compared to the control conditions. From the meta- lower temperatures and sun radiation, have induced the wide analysis, a non-significant effect of supplemental lighting on gs uptake of horticultural LED technology. However, interesting was observed, possibly suggesting that excessive light irradiance applications may also be hypothesized for milder climates such could also lead to stomatal closure (O’Carrigan et al., 2014a). as those of the Mediterranean area, in which supplemental The evaluation of heterogeneity among the studies showed LED lighting could improve the quantitative and qualitative high values for each response ratio [R] (Table 1). Such results aspects of greenhouse tomato plants both during the off-season were, however, expected, considering not only the variability and when extremely hot summers occur and intensive shading in trial management (e.g., diverse locations and technologies, is needed. Frontiers in Plant Science | www.frontiersin.org 10 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review DATA AVAILABILITY STATEMENT All authors contributed to the article and approved the submitted version. The authors confirm that the data supporting the findings of this study are available within the article and its FUNDING Supplementary Materials. The research leading to this publication has received funding from the European Union’s Horizon 2020 research and AUTHOR CONTRIBUTIONS innovation programme under grant agreement No 862663. EA designed and performed the data collection and meta SUPPLEMENTARY MATERIAL data analysis, and drafted the manuscript. GP and FO contributed to the research design and the drafting of The Supplementary Material for this article can be found the manuscript. IP revised the manuscript. XG and GG online at: https://www.frontiersin.org/articles/10.3389/fpls.2021. supervised the research and critically revised the manuscript. 596927/full#supplementary-material REFERENCES Dorais, M., Gosselin, A., and Trudel, M. J. (1991). Annual greenhouse tomato production under a sequential intercropping system using supplemental light. Bastian, M., Heymann, S., and Jacomy, M. (2009). “Gephi: an open source software Sci. Hortic. 45, 225–234. doi: 10.1016/0304-4238(91)90067-9 for exploring and manipulating networks,” in International AAAI Conference on Dorais, M., Yelle, S., and Gosselin, A. (1996). Influence of extended photoperiod Weblogs and Social Media (San Jose, CA). on photosynthate partitioning and export in tomato and pepper plants. N. Z. J. Bian, Z., Zhang, X., Wang, Y., and Lu, C. (2019). Improving drought Crop Hort. 24, 29–37. doi: 10.1080/01140671.1996.9513932 tolerance by altering the photosynthetic rate and stomatal aperture via Dou, H., Niu, G., and Gu, M. (2019). Pre-harvest UV-B radiation and green light in tomato (Solanum lycopersicum L.) seedlings under drought photosynthetic photon flux density interactively affect plant photosynthesis, conditions. Environ. Exp. Bot. 167:103844. doi: 10.1016/j.envexpbot.2019. growth, and secondary metabolites accumulation in basil (Ocimum basilicum) 103844 plants. Agronomy 9:434. doi: 10.3390/agronomy9080434 Borenstein, M., Hedges, L. V., Higgins, J. P. T., and Rothstein, H. R. (2009). D’Souza, C., Yuk, H. G., Khoo, G. H., and Zhou, W. (2015). Application Introduction to Meta-Analysis. Chichester: Wiley. doi: 10.1002/9780470743386 of light-emitting diodes in food production, postharvest preservation, Brazaityte, A., Duchovskis, P., Urbonavičiute, A., Samuoliene, G., Jankauskiene, and microbiological food safety. Compr. Rev. Food Sci. F 14, 719–740. J., Kazenas, V., et al. (2009). After-effect of light-emitting diodes lighting doi: 10.1111/1541-4337.12155 on tomato growth and yield in greenhouse. Sodininkyste ir darŽininkyste Dueck, T. A., Janse, J., Eveleens, B. A., Kempkes, F. L. K., and Marcelis, L. F. M. 28, 115–126. (2011). Growth of tomatoes under hybrid LED and HPS lighting. Acta Hortic. Cao, K., Cui, L., Ye, L., Zhou, X., Bao, E., Zhao, H., et al. (2016). Effects of red light 952, 335–342. doi: 10.17660/actahortic.2012.952 night break treatment on growth and flowering of tomato plants. Front. Plant Dzakovich, M. P., Gómez, C., Ferruzzi, M. G., and Mitchell, C. A. (2017). Chemical Sci. 7:527. doi: 10.3389/fpls.2016.00527 and sensory properties of greenhouse tomatoes remain unchanged in response Carvalho, S. D., Schwieterman, M. L., Abrahan, C. E., Colquhoun, T. to Red, Blue, and Far Red supplemental light from Light-Emitting Diodes. A., and Folta, K. M. (2016). Light quality dependent changes in HortScience 52, 1734–1741. doi: 10.21273/hortsci12469-17 morphology, antioxidant capacity, and volatile production in sweet basil Dzakovich, M. P., Gómez, C., and Mitchell, C. A. (2015). Tomatoes grown (Ocimum basilicum). Front. Plant Sci. 7:1328. doi: 10.3389/fpls.2016. with light-emitting diodes or high-pressure sodium supplemental 01328 lights have similar fruit-quality attributes. HortScience 50, 1498–1502. Castilla, N., and Baeza, E. (2013). Greenhouse site selection. Good Agricultural doi: 10.21273/hortsci.50.10.1498 Practices for greenhouse vegetable crops: principles for mediterranean climate Eagle, A. J., Christianson, L. E., Cook, R. L., Harmel, R. D., Miguez, F. E., and Qian, areas. FAO plant production and protection paper, FAO, 21–34. S. S., et al. (2017). Meta-analysis constrained by data: recommendations to Castilla, N., Hernández, J., and Abou-Hadid, A. F. (2002). Strategic crop and improve relevance of nutrient management research. J. Agron. 109, 2441–2449. greenhouse management in mild winter climate areas. Acta Hortic. 633, doi: 10.2134/agronj2017.04.0215 183–196. doi: 10.17660/actahortic.2004.633.22 Ebisawa, M., Shoji, K., Kato, M., Shimomura, K., Goto, F., and Yoshihara, T. Christie, J. M., Blackwood, L., Petersen, J., and Sullivan, S. (2015). (2008). Supplementary ultraviolet radiation B together with blue light at night Plant flavoprotein photoreceptors. Plant Cell Physiol. 56, 401–413. increased quercetin content and flavonol synthase gene expression in leaf doi: 10.1093/pcp/pcu196 lettuce (Lactuca sativa L.). Environ. Control Biol. 46, 1–11. doi: 10.2525/ecb.46.1 Demers, D. A., Dorais, M., Wien, C. H., and Gosselin, A. (1998). Effects Fanwoua, J., Vercambre, G., Buck-Sorlin, G., Dieleman, J. A., de Visser, of supplemental light duration on greenhouse tomato (Lycopersicon P., and Génard, M. (2019). Supplemental LED lighting affects the esculentum Mill.) plants and fruit yields. Sci. Hortic. 74, 295–306. dynamics of tomato fruit growth and composition. Sci. Hortic. 256:108571. doi: 10.1016/s0304-4238(98)00097-1 doi: 10.1016/j.scienta.2019.108571 Demers, D. A., and Gosselin, A. (2000). Growing greenhouse tomato and FAO (2018). FAOSTAT database collections. Rome: Food and Agriculture sweet pepper under supplemental lighting: optimal photoperiod, negative Organization of the United Nations. Available online at: http://faostat.fao.org effects of long photoperiod and their causes. Acta Hortic. 580, 83–88. (accessed June 24, 2020). doi: 10.17660/actahortic.2002.580.9 Fernández, J. A., Orsini, F., Baeza, E., Oztekin, G. B., Muñoz, P., Contreras, J., et al. Demotes-Mainard, S., Péron, T., Corot, A., Bertheloot, J., Le Gourrierec, (2018). Current trends in protected cultivation in Mediterranean climates. Eur. J., and Pelleschi-Travier, S., et al. (2016). Plant responses to red and J. Hortic. Sci. 83, 294–305. doi: 10.17660/ejhs.2018/83.5.3 far-red lights, applications in horticulture. Environ. Exp. Bot. 121, 4–21. Fischer, G., Nachtergaele, F. O., Prieler, S., Teixeira, E., Tóth, G., and Van doi: 10.1016/j.envexpbot.2015.05.010 Velthuizen, H., et al. (2012). Global agro-ecological zones (GAEZ v3. 0) - Model Deram, P., Lefsrud, M. G., and Orsat, V. (2014). Supplemental lighting Documentation. IIASA, FAO, Rome, Italy. orientation and red-to-blue ratio of light-emitting diodes for greenhouse Gajc-Wolska, J., Kowalczyk, K., Metera, A., Mazur, K., Bujalski, D., and tomato production. HortScience 49, 448–452. doi: 10.21273/hortsci.49.4.448 Hemka, L. (2013). Effect of supplementary lighting on selected physiological Frontiers in Plant Science | www.frontiersin.org 11 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review parameters and yielding of tomato plants. Folia Horticult. 25, 153–159. Hedges, L. V., Gurevitch, J., and Curtis, P. S. (1999). The meta-analysis of response doi: 10.2478/fhort-2013-0017 ratios in experimental ecology. Ecology 80, 1150–1156. doi: 10.1890/0012- Garcia, M. L., Medrano, E., Sanchez-Guerrero, M. C., and Lorenzo, P. (2011). 9658(1999)080[1150:TMAORR]2.0.CO;2 Climatic effects of two cooling systems in greenhouses in the Mediterranean Heuvelink, E., and Gonzalez-Real, M. M. (2007). Innovation in plant- area: external mobile shading and fog system. Biosyst. Eng. 108, 133–143. greenhouse interactions and crop management. Acta Hortic. 80, 63–74. doi: 10.1016/j.biosystemseng.2010.11.006 doi: 10.17660/actahortic.2008.801.2 Garland, K. F., Burnett, S. E., Stack, L. B., and Zhang, D. (2010). Minimum daily Hinov, N., Tsankov, P., and Ibrishimov, H. (2019). “Innovative LED lighting,” in light integral for growing high-quality coleus. Horttechnology 20, 929–933. 2019 International Conference on Creative Business for Smart and Sustainable doi: 10.21273/HORTTECH.20.5.929 Growth (CREBUS) (Sandanski), 1–5. doi: 10.1109/CREBUS.2019.8840095 Gautier, H., Rocci, A., Buret, M., Grasselly, D., Dumas, Y., and Causse, M. Hui, X., Fu, Y. N., Li, T. L., and Rui, W. (2017). Effects of different LED (2005). Effect of photoselective filters on the physical and chemical traits of light wavelengths on the resistance of tomato against Botrytis cinerea and vine-ripened tomato fruits. Can. J. Plant Sci. 85, 439–446. doi: 10.4141/p03-163 the corresponding physiological mechanisms. J. Integr. Agric. 16, 106–114. Giniger, M. S., McAvoy, R. J., Giacomelli, G. A., and Janes, H. W. (1988). doi: 10.1016/s2095-3119(16)61435-1 Computer simulation of a single truss tomato cropping system. Trans. ASAE Ibaraki, Y. (2017). “LED supplementary lighting,” in Light Emitting 31, 1176–1179. doi: 10.13031/2013.30840 Diodes for Agriculture, ed S. D. Gupta (Singapore: Springer), 27–36. Gómez, C., Clark, M., and Mitchell, C. A. (2016). Effect of intracanopy doi: 10.1007/978-981-10-5807-3_2 lighting and/or root-zone temperature on high-wire tomato production Ieperen, W. V., Savvides, A., and Fanourakis, D. (2012). Red and blue under supra-optimal air temperature. Acta Hortic. 1134, 63–70. light effects during growth on hydraulic and stomatal conductance doi: 10.17660/ActaHortic.2016.1134.9 in leaves of young cucumber plants. Acta Hortic. 956, 223–230. Gómez, C., and Mitchell, C. A. (2016a). Physiological and productivity doi: 10.17660/actahortic.2012.956.24 responses of high-wire tomato as affected by supplemental light source Ji, Y., Ouzounis, T., Courbier, S., Kaiser, E., Nguyen, P. T., Schouten, H. J., and distribution within the canopy. J. Am. Soc. Hortic. Sci. 141, 196–208. et al. (2019). Far-red radiation increases dry mass partitioning to fruits but doi: 10.21273/jashs.141.2.196 reduces Botrytis cinerea resistance in tomato. Environ. Exp. Bot. 168:103889. Gómez, C., and Mitchell, C. A. (2016b). In search of an optimized supplemental doi: 10.1016/j.envexpbot.2019.103889 lighting spectrum for greenhouse tomato production with intracanopy lighting. Jiang, C., Johkan, M., Hohjo, M., Tsukagoshi, S., Ebihara, M., Nakaminami, Acta Hortic. 1134, 57–62. doi: 10.17660/actahortic.2016.1134.8 A., et al. (2017). Photosynthesis, plant growth, and fruit production Gomez, C., Morrow, R. C., Bourget, C. M., Massa, G. D., and Mitchell, C. A. of single-truss tomato improves with supplemental lighting provided (2013). Comparison of intracanopy light-emitting diode towers and overhead from underneath or within the inner canopy. Sci. Hort. 222, 221–229. high-pressure sodium lamps for supplemental lighting of greenhouse-grown doi: 10.1016/j.scienta.2017.04.026 tomatoes. Horttechnology 23, 93–98. doi: 10.21273/HORTTECH.23.1.93 Johkan, M., Hohjo, T., Tsukagoshi, S., Ebihara, M., Nakaminami, A., Maruo, M., Gunnlaugsson, B., and Adalsteinsson, S. (2005). Interlight and plant density in et al. (2017). Supplemental lighting applied within or underneath the canopy year-round production of tomato at northern latitudes. Acta Hortic. 711, 71–76. enhances leaf photosynthesis, stomatal regulation and plant development doi: 10.17660/actahortic.2006.711.6 of tomato under limiting light conditions. Acta Hortic. 1227, 645–652. Guo, X., Hao, X., Khosla, S., Kumar, K. G. S., Cao, R., and Bennett, N. (2016). doi: 10.17660/actahortic.2018.1227.82 Effect of LED interlighting combined with overhead HPS light on fruit yield Johkan, M., Shoji, K., Goto, F., Hashida, S. N., and Yoshihara, T. (2010). Blue and quality of year-round sweet pepper in commercial greenhouse. Acta Hortic. light-emitting diode light irradiation of seedlings improves seedling quality 1134, 71–78. doi: 10.17660/actahortic.2016.1134.10 and growth after transplanting in red leaf lettuce. HortScience 45, 1809–1814. Gupta, S. D., and Agarwal, A. (2017). “Artificial lighting system for plant doi: 10.21273/hortsci.45.12.1809 growth and development: Chronological advancement, working principles, Jokinen, K., Särkkä, L. E., and Näkkilä, J. (2012). Improving sweet and comparative assessmen,” in Light Emitting Diodes for Agriculture, pepper productivity by LED interlighting. Acta Hortic. 956, 59–66. ed S. D. Gupta (Singapore: Springer), 1–25. doi: 10.1007/978-981-10-580 doi: 10.17660/actahortic.2012.956.4 7-3_1 Joshi, N. C., Ratner, K., Eidelman, O., Bednarczyk, D., Zur, N., Many, Y., et al. Hak, T., Van Rhee, H. J., and Suurmond, R. (2016). How to Interpret Results (2019). Effects of daytime intra-canopy LED illumination on photosynthesis of Meta-Analysis. (Version 1.3). Rotterdam: Erasmus Rotterdam Institute of and productivity of bell pepper grown in protected cultivation. Sci. Hort. 250, Management. doi: 10.2139/ssrn.3241367 81–88. doi: 10.1016/j.scienta.2019.02.039 Hamamoto, H., and Yamazaki, K. (2009). Supplemental lighting inside the Kaiser, E., Ouzounis, T., Giday, H., Schipper, R., Heuvelink, E., and Marcelis, L. F. plant canopy increased the yield and quality of three-truss-ordered (2019a). Adding blue to red supplemental light increases biomass and yield of tomato. Acta Hortic. 907, 283–286. doi: 10.17660/actahortic.2011. greenhouse-grown tomatoes, but only to an optimum. Front. Plant Sci. 9:2002. 907.45 doi: 10.3389/fpls.2018.02002 Hao, X., Cao, R., Zheng, J., Little, C., Kholsa, S., and Yelton, M. (2018). Kaiser, E., Weerheim, K., Schipper, R., and Dieleman, J. A. (2019b). Partial Optimizing vertical light spectral distribution to improve yield and quality replacement of red and blue by green light increases biomass and in greenhouse fruit vegetable production. Acta Hortic. 1271, 141–148. yield in tomato. Sci. Hort. 249, 271–279. doi: 10.1016/j.scienta.2019. doi: 10.17660/actahortic.2020.1271.20 02.005 Hao, X., Guo, X., Lanoue, J., Zhang, Y., Cao, R., Zheng, J., et al. Kalaitzoglou, P., Van Ieperen, W., Harbinson, J., van der Meer, M., Martinakos, S., (2017). A review on smart application of supplemental lighting in Weerheim, K., et al. (2019). Effects of continuous or end-of-day far-red light greenhouse fruiting vegetable production. Acta Hortic. 1227, 499–506. on tomato plant growth, morphology, light absorption and fruit production. doi: 10.17660/ActaHortic.2018.1227.63 Front. Plant Sci. 10:322. doi: 10.3389/fpls.2019.00322 Hao, X., Guo, X., Zheng, J., Celeste, L., Kholsa, S., and Chen, X. (2015). Response of Kim, H. J., Lin, M. Y., and Mitchell, C. A. (2019). Light spectral and greenhouse tomato to different vertical spectra of LED lighting under overhead thermal properties govern biomass allocation in tomato through high pressure sodium and plasma lighting. Acta Hortic. 1170, 1003–1110. morphological and physiological changes. Environ. Exp. Bot. 157, 228–240. doi: 10.17660/actahortic.2017.1170.129 doi: 10.1016/j.envexpbot.2018.10.019 Hao, X., Little, C., Zheng, J. M., and Cao, R. (2016). Far-red LEDs Kim, H. J., Yang, T., Choi, S., Wang, Y. J., Lin, M. Y., and Liceaga, A. improve fruit production in greenhouse tomato grown under high-pressure M. (2020). Supplemental intracanopy far-red radiation to red LED light sodium lighting. Acta Hortic. 1134, 95–102. doi: 10.17660/actahortic.2016. improves fruit quality attributes of greenhouse tomatoes. Sci. Hort. 261:108985. 1134.13 doi: 10.1016/j.scienta.2019.108985 Hao, X., Zheng, J., Little, C., and Khosla, S. (2012). LED inter-lighting in year- Kittas, C., Baille, A., and Giaglaras, P. (1999). Influence of covering material and round greenhouse mini-cucumber production. Acta Hortic. 956, 335–340. shading on the spectral distribution of light in greenhouses. J. Agric. Eng. Res. doi: 10.17660/ActaHortic.2012.956.38 73, 341–351. doi: 10.1006/jaer.1999.0420 Frontiers in Plant Science | www.frontiersin.org 12 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review Kubota, C., de Gelder, A., and Peet, M. M. (2018). “Greenhouse tomato Olle, M., and Viršile, A. (2013). The effects of light-emitting diode lighting production,” in Tomatoes, ed E. Heuvelink (Wageningen: CABI), 276–314. on greenhouse plant growth and quality. Agr. Food Sci. 22, 223–234. doi: 10.1079/9781780641935.0276 doi: 10.23986/afsci.7897 Kubota, C., Kroggel, M., Both, A. J., Burr, J. F., and Whalen, M. (2016). Does OMAFRA (2001). Growing Greenhouse Vegetables. Publication 371. Ontario supplemental lighting make sense for my crop? – empirical evaluations. Acta Ministry of Agriculture, Food and Rural Affairs, Toronto, Canada, 116. Hortic. 1134, 403–412. doi: 10.17660/actahortic.2016.1134.52 Ouzounis, T., Heuvelink, E., Ji, Y., Schouten, H. J., Visser, R. G. F., and Marcelis, Kubota, C., Kroggel, M., Torabi, M., Dietrich, K. A., Kim, H. J., Fonseca, J., L. F. M. (2016). Blue and red LED lighting effects on plant biomass, stomatal et al. (2012). Changes in selected quality attributes of greenhouse tomato fruit conductance, and metabolite content in nine tomato genotypes. Acta Hortic. as affected by pre-and postharvest environmental conditions in year-round 1134, 251–258. doi: 10.17660/actahortic.2016.1134.34 production. HortScience 47, 1698–1704. doi: 10.21273/hortsci.47.12.1698 Ouzounis, T., Rosenqvist, E., and Ottosen, C. O. (2015). Spectral effects of artificial Kumar, K. G. S., Hao, X., Khosla, S., Guo, X., and Bennett, N. (2016). Comparison light on plant physiology and secondary metabolism: a review. HortScience 50, of HPS lighting and hybrid lighting with top HPS and intra-canopy LED 1128–1135. doi: 10.21273/hortsci.50.8.1128 lighting for high-wire mini-cucumber production. Acta Hortic. 1134, 111–118. Paponov, M., Kechasov, D., Lacek, J., Verheul, M., and Paponov, I. A. (2019). doi: 10.17660/actahortic.2016.1134.15 Supplemental LED inter-lighting increases tomato fruit growth through Lanoue, J., Zheng, J., Little, C., Thibodeau, A., Grodzinski, B., and Hao, X. enhanced photosynthetic light use efficiency and modulated root activity. (2019). Alternating Red and Blue Light-Emitting Diodes allows for injury- Front. Plant Sci. 10:1656. doi: 10.3389/fpls.2019.01656 free tomato production with continuous lighting. Front. Plant Sci. 10:1114. Paucek, I., Pennisi, G., Pistillo, A., Appolloni, E., Crepaldi, A., Calegari, doi: 10.3389/fpls.2019.01114 B., et al. (2020). Supplementary LED interlighting improves yield and Liao, Y., Suzuki, K., Yu, W., Zhuang, D., Takai, Y., Ogasawara, R., et al. precocity of greenhouse tomatoes in the mediterranean. Agron 10:1002. (2014). Night break effect of LED light with different wavelengths on floral doi: 10.3390/agronomy10071002 bud differentiation of Chrysanthemum morifolium ramat ‘Jimba’and Iwa no Pennisi, G., Blasioli, S., Cellini, A., Maia, L., Crepaldi, A., Braschi, I., et al. (2019b). hakusen. Environ. Exp. Bot. 52, 45–50. doi: 10.2525/ecb.52.45 Unravelling the role of red:blue LED lights on resource use efficiency and Lu, N., Maruo, T., Johkan, M., Hohjo, M., Tsukagoshi, S., Ito, Y., et al. (2012a). nutritional properties of indoor grown sweet basil. Front. Plant Sci. 10: 305. Effects of supplemental lighting within the canopy at different developing stages doi: 10.3389/fpls.2019.00305 on tomato yield and quality of single-truss tomato plants grown at high density. Pennisi, G., Orsini, F., Blasioli, S., Cellini, A., Crepaldi, A., Braschi, I., et al. Environ. Exp. Bot. 50, 1–11. doi: 10.2525/ecb.50.1 (2019a). Resource use efficiency of indoor lettuce (Lactuca sativa L.) cultivation Lu, N., Maruo, T., Johkan, M., Hohjo, M., Tsukagoshi, S., Ito, Y., et al. (2012b). as affected by red:blue ratio provided by LED lighting. Sci. Rep. 9:14127. Effects of supplemental lighting with light-emitting diodes (LEDs) on tomato doi: 10.1038/s41598-019-50783-z yield and quality of single-truss tomato plants grown at high planting density. Pepin, S., Fortier, E., Béchard-Dubé, S. A., Dorais, M., Ménard, C., and Bacon, R. Environ. Exp. Bot. 50, 63–74. doi: 10.2525/ecb.50.63 (2014). Beneficial effects of using a 3-D LED interlighting system for organic McCree, K. J. (1971). The action spectrum, absorptance and quantum greenhouse tomato grown in Canada under low natural light conditions. Acta yield of photosynthesis in crop plants. J. Agric. Meteorol. 9, 191–216. Hortic. 1041, 239–246. doi: 10.17660/actahortic.2014.1041.28 doi: 10.1016/0002-1571(71)90022-7 Petropoulos, S. A., Fernandes, Â., Katsoulas, N., Barros, L., and Ferreira, I. C. McDaniel, M. D., Tiemann, L. K., and Grandy, A. S. (2014). Does agricultural (2019). The effect of covering material on the yield, quality and chemical crop diversity enhance soil microbial biomass and organic matter dynamics? composition of greenhouse-grown tomato fruit. J. Sci. Food Agric. 99, A meta-analysis. Ecol. Appl. 24, 560–570. doi: 10.1890/13-0616.1 3057–3068. doi: 10.1002/jsfa.9519 Mempel, H., and Wittmann, S. (2019). Potential and use of artificial lighting in Qin, W., Hu, C., and Oenema, O. (2015). Soil mulching significantly enhances horticulture. Light Eng. 27, 31–41. yields and water and nitrogen use efficiencies of maize and wheat: a meta- Ménard, C., Dorais, M., Hovi, T., and Gosselin, A. (2005). Developmental and analysis. Sci. Rep. 5:16210. doi: 10.1038/srep16210 physiological responses of tomato and cucumber to additional blue light. Acta Roelfsema, M. R. G., and Hedrich, R. (2005). In the light of stomatal Hortic. 711, 291–296. doi: 10.17660/actahortic.2006.711.39 opening: new insights into ‘the Watergate’. New Phytol. 167, 665–691. Meneses, J. F., and Castilla, N. (2009). Protected cultivation in Iberian horticulture. doi: 10.1111/j.1469-8137.2005.01460.x Chron. Horticult. 49, 37–39. Sarlikioti, V., de Visser, P. H., Buck-Sorlin, G. H., and Marcelis, L. F. M. (2011). Miao, Y., Chen, Q., Qu, M., Gao, L., and Hou, L. (2019). Blue light alleviates How plant architecture affects light absorption and photosynthesis in tomato: ‘red light syndrome’ by regulating chloroplast ultrastructure, photosynthetic towards an ideotype for plant architecture using a functional–structural plant traits and nutrient accumulation in cucumber plants. Sci. Hort. 257:108680. model. Ann. Bot. 108, 1065–1073. doi: 10.1093/aob/mcr221 doi: 10.1016/j.scienta.2019.108680 Schreiner, M., Martínez-Abaigar, J., Glaab, J., and Jansen, M. (2014). UV-B induced Morrow, R. C. (2008). LED lighting in horticulture. HortScience 43, 1947–1950. secondary plant metabolites: potential benefits for plant and human health. doi: 10.21273/hortsci.43.7.1947 Optik (Stuttg) 9, 34–37. doi: 10.1002/opph.201400048 Nelson, J. A., and Bugbee, B. (2014). Economic analysis of greenhouse lighting: Schwarz, D., Thompson, A. J., and Kläring, H. P. (2014). Guidelines to use light emitting diodes vs. high intensity discharge fixtures. PLoS ONE 9:e99010. tomato in experiments with a controlled environment. Front. Plant Sci. 5:625. doi: 10.1371/journal.pone.0099010 doi: 10.3389/fpls.2014.00625 O’Carrigan, A., Babla, M., Wang, F., Liu, X., Mak, M., Thomas, R., et al. Shimazaki, K. I., Doi, M., Assmann, S. M., and Kinoshita, T. (2007). Light (2014b). Analysis of gas exchange, stomatal behaviour and micronutrients regulation of stomatal movement. Ann. Rev. Plant Biol. 58, 219–247. uncovers dynamic response and adaptation of tomato plants to doi: 10.1146/annurev.arplant.57.032905.105434 monochromatic light treatments. Plant Physiol. Biochem. 82, 105–115. Song, Y., Jiang, C., and Gao, L. (2016). Polychromatic supplemental lighting from doi: 10.1016/j.plaphy.2014.05.012 underneath canopy is more effective to enhance tomato plant development by O’Carrigan, A., Hinde, E., Lu, N., Xu, X. Q., Duan, H., Huang, G., et al. improving leaf photosynthesis and stomatal regulation. Front. Plant Sci. 7:1832. (2014a). Effects of light irradiance on stomatal regulation and growth doi: 10.3389/fpls.2016.01832 of tomato. Environ. Exp. Bot. 98, 65–73. doi: 10.1016/j.envexpbot.2013. Sun, Y., Sun, Y., Sun, Z., Li, P., and Li, C. (2015). “Mapping monthly distribution of 10.007 daily light integrals across China,” in Annual Conference of ASHS (New Orleans). Ohashi-Kaneko, K., Takase, M., Kon, N., Fujiwara, K., and Kurata, K. (2007). Effect Suurmond, R., van Rhee, H., and Hak, T. (2017). Introduction, comparison and of light quality on growth and vegetable quality in leaf lettuce, spinach and validation of Meta-Essentials: a free and simple tool for meta-analysis. Res. komatsuna. Envrion. Control Biol. 45, 189–198. doi: 10.2525/ecb.45.189 Synth. Methods 8, 537–553. doi: 10.1002/jrsm.1260 Okano, K., Nakano, Y., and Watanabe, S. I. (2001). Single-truss tomato system—a Suzuki, K., Yasuba, K., Takaichi, M., Takahashi, T., and Hoshi, T. (2009). Effect of labor-saving management system for tomato production. Jpn. Agr. Res. Q. 35, the supplemental lighting on the growth of young plants in second nursery in 177–184. doi: 10.6090/jarq.35.177 tomato. Acta Hortic. 907, 269–276. doi: 10.17660/actahortic.2011.907.43 Frontiers in Plant Science | www.frontiersin.org 13 April 2021 | Volume 12 | Article 596927 Appolloni et al. LED Lighting for Greenhouse Tomato: A Review Talbott, L. D., Nikolova, G., Ortiz, A., Shmayevich, I., and Zeiger, E. (2002). Green Wada, T., Ikeda, H., Matsushita, K., Kambara, A., Hirai, H., and Abe, K. (2006). light reversal of blue-light-stimulated stomatal opening is found in a diversity Effect of shading in summer on yield and quality of tomatoes grown on a of plant species. Am. J. Bot. 89, 366–368. doi: 10.3732/ajb.89.2.366 single-truss system. J. Jpn. Soc. Hortic. Sci. 75, 51–58. doi: 10.2503/jjshs.75.51 Tewolde, F. T., Lu, N., Shiina, K., Maruo, T., Takagaki, M., Kozai, T., et al. (2016). Weaver, G. M., van Iersel, M. W., and Velni, J. M. (2019). A photochemistry-based Nighttime supplemental LED inter-lighting improves growth and yield of method for optimising greenhouse supplemental light intensity. Biosyst. Eng. single-truss tomatoes by enhancing photosynthesis in both winter and summer. 182, 123–137. doi: 10.1016/j.biosystemseng.2019.03.008 Front. Plant Sci. 7:448. doi: 10.3389/fpls.2016.00448 Zeiger, E. (1990). Light perception in guard cells. Plant, Cell Environ. 13, 739–744. Tewolde, F. T., Shiina, K., Maruo, T., Takagaki, M., Kozai, T., and Yamori, W. doi: 10.1111/j.1365-3040.1990.tb01088.x (2018). Supplemental LED inter-lighting compensates for a shortage of light Zhang, G., Shen, S., Takagaki, M., Kozai, T., and Yamori, W. (2015). Supplemental for plant growth and yield under the lack of sunshine. PLoS ONE 13:e0206592. upward lighting from underneath to obtain higher marketable lettuce (Lactuca doi: 10.1371/journal.pone.0206592 sativa) leaf fresh weight by retarding senescence of outer leaves. Front. Plant Tokuno, A., Iaraki, Y., Ito, S. I., Araki, H., Yoshimura, K., and Osaki, K. Sci. 6:1110. doi: 10.3389/fpls.2015.01110 (2012). Disease suppression in greenhouse tomato by supplementary lighting Zhang, Y. T., Zhang, Y. Q., Yang, Q. C., and Tao, L. I. (2019). with 405 nm LED. Environ. Control. Biol. 50, 19–29. doi: 10.2525/ecb. Overhead supplemental far-red light stimulates tomato growth 50.19 under intra-canopy lighting with LEDs. J. Integr. Agric. 18, 62–69. Trouwborst, G., Sander, W. H., Harbinson, J., and Wim Van, I. (2011). The doi: 10.1016/s2095-3119(18)62130-6 influence of light intensity and leaf age on the photosynthetic capacity of leaves within a tomato canopy. J. Hortic. Sci. Biotech. 86, 403–407. Disclaimer: The publication reflects the author’s views. The Research Executive doi: 10.1080/14620316.2011.11512781 Agency (REA) is not liable for any use that may be made of the information Tuzel, Y., and Oztekin, G. B. (2014). Recent developments of vegetables contained therein. protected cultivation in Turkey. Acta Hortic. 1142, 435–442. doi: 10.17660/actahortic.2016.1142.66 Conflict of Interest: The authors declare that the research was conducted in the Velez-Ramirez, A. I., Carreño-Quintero, N., Vreugdenhil, D., Millenaar, F. F., and absence of any commercial or financial relationships that could be construed as a van Ieperen, W. (2017). Sucrose and starch content negatively correlates with potential conflict of interest. PSII maximum quantum efficiency in tomato (Solanum lycopersicum) exposed to abnormal light/dark cycles and continuous light. Plant Cell Physiol. 58, Copyright © 2021 Appolloni, Orsini, Pennisi, Gabarrell Durany, Paucek and 1339–1349. doi: 10.1093/pcp/pcx068 Gianquinto. This is an open-access article distributed under the terms of the Creative Verheula, M. J., Maessen, H. F. R., Panosyan, A., Paponov, M., and Paponov, I. Commons Attribution License (CC BY). The use, distribution or reproduction in A. (2019). Effects of supplemental light and temperature on summer production other forums is permitted, provided the original author(s) and the copyright owner(s) of tomato in Norway. Available online at: https://vb.northsearegion.eu/public/ are credited and that the original publication in this journal is cited, in accordance files/repository/20190925153007_2019-10m%C3%B8de.pdf (accessed June 24, with accepted academic practice. 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