Effect of Light-emitting Diodes, Ultraviolet-B, and Fluorescent Supplemental Greenhouse Lights on Strawberry Plant Growth and Response to Infection by the Anthracnose Pathogen Colletotrichum gloeosporioides

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Barbara J. SmithU.S. Department of Agriculture, Agriculture Research Service, Poplarville, MS 39470

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Amir RezazadehUniversity of Florida/IFAS, St. Lucie County Extension, Fort Pierce, FL 34945

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Eric T. StafneMississippi State University, South Mississippi Branch Experiment Station, Poplarville, MS 39470

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Hamidou F. SakhanokhoU.S. Department of Agriculture, Agriculture Research Service, Poplarville, MS 39470

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Supplemental lighting is frequently used to extend daylength for strawberries (Fragaria ×ananassa) grown in greenhouses and high tunnels; however, information is limited on the effect of these lights on disease development. We evaluated the effect of ambient light and six supplemental light treatments [red, blue, and white light-emitting diodes (LEDs), separately; a combination of red, blue, and white LEDs; wide-spectrum fluorescent (WSF); and WFS + ultraviolet B (UV-B)] on plant growth and disease response of strawberries grown in a greenhouse. Plants were exposed to supplemental light treatments for 17 h each day. In the WSF+UV-B treatment, plants were exposed to WSF light during the day and to UV-B light for 3 hours during the night. Two trials were conducted; each trial contained five or six cultivars and was replicated three times. Twice during each trial, detached leaves from each cultivar in each light treatment were inoculated with a conidial suspension of the anthracnose crown rot pathogen, Colletotrichum gloeosporioides and rated for disease severity 10 days later. There was a significant difference due to light treatment and to cultivar in relative chlorophyll content and plant growth parameters. Plant injury ratings were lowest in the white LED, WSF, and WSF+UV-B treatments. Plants in the combination LED and red LED light treatments received higher injury, lower vigor scores, and lower relative chlorophyll content values than plants in all other light treatments. After inoculation of detached strawberry leaves with C. gloeosporioides in Trial 1, there was a significant effect due to light treatments on disease severity ratings (DSRs) after 18 weeks’ exposure to light treatments with the DSRs in the WSF+UV-B treatment being lower than those in all other treatments except those in the red LED treatment. There was not a significant effect in DSRs due to light treatments after 24 weeks in Trial 1 or after 4 or 22 weeks in Trial 2. There were significant effects due to cultivar on DSRs in both trials: ‘Strawberry Festival’, ‘Pelican’, and ‘Seascape’ received the lowest DSRs. This study showed an effect of supplemental light on several strawberry plant growth parameters, including a harmful effect of high-intensity red LED irradiation.

Abstract

Supplemental lighting is frequently used to extend daylength for strawberries (Fragaria ×ananassa) grown in greenhouses and high tunnels; however, information is limited on the effect of these lights on disease development. We evaluated the effect of ambient light and six supplemental light treatments [red, blue, and white light-emitting diodes (LEDs), separately; a combination of red, blue, and white LEDs; wide-spectrum fluorescent (WSF); and WFS + ultraviolet B (UV-B)] on plant growth and disease response of strawberries grown in a greenhouse. Plants were exposed to supplemental light treatments for 17 h each day. In the WSF+UV-B treatment, plants were exposed to WSF light during the day and to UV-B light for 3 hours during the night. Two trials were conducted; each trial contained five or six cultivars and was replicated three times. Twice during each trial, detached leaves from each cultivar in each light treatment were inoculated with a conidial suspension of the anthracnose crown rot pathogen, Colletotrichum gloeosporioides and rated for disease severity 10 days later. There was a significant difference due to light treatment and to cultivar in relative chlorophyll content and plant growth parameters. Plant injury ratings were lowest in the white LED, WSF, and WSF+UV-B treatments. Plants in the combination LED and red LED light treatments received higher injury, lower vigor scores, and lower relative chlorophyll content values than plants in all other light treatments. After inoculation of detached strawberry leaves with C. gloeosporioides in Trial 1, there was a significant effect due to light treatments on disease severity ratings (DSRs) after 18 weeks’ exposure to light treatments with the DSRs in the WSF+UV-B treatment being lower than those in all other treatments except those in the red LED treatment. There was not a significant effect in DSRs due to light treatments after 24 weeks in Trial 1 or after 4 or 22 weeks in Trial 2. There were significant effects due to cultivar on DSRs in both trials: ‘Strawberry Festival’, ‘Pelican’, and ‘Seascape’ received the lowest DSRs. This study showed an effect of supplemental light on several strawberry plant growth parameters, including a harmful effect of high-intensity red LED irradiation.

Light plays an important role in plant growth, development, photosynthesis, nutritional quality, and secondary metabolism (Kondo et al., 2014; Lee et al., 2013; Muneer et al., 2014). Specific light wavelengths can influence seed germination, stem growth, and plant biomass (Kim et al., 2004; Parks et al., 2001). Various types of light sources, including incandescent, fluorescent, metal halide, high-pressure sodium lamps, and LEDs have been used as either the sole source of light or as a supplement to ambient light for cultivation of strawberries (Fragaria ×ananassa) grown in protected culture. Red and blue wavelengths are often used to optimize photosynthesis and enhance plant quality. Red light is important for shoot/stem elongation, phytochrome responses, and changes in plant anatomy (Schuerger et al., 1997) but may negatively affect flower bud initiation in fall-flowering strawberry cultivars (Takeda et al., 2008). Blue light promotes plant growth, increases biomass, and has a role in chlorophyll biosynthesis, stomatal opening, enzyme synthesis, phototropism, and photosynthesis (Johkan et al., 2010; Muneer et al., 2014).

Although supplemental lighting, especially LED lighting, has become common as a means of extending daylength of strawberries grown in greenhouses and high tunnels or as the sole light source in growth chambers, there is little information on the effect of these lights on disease development. Light quality is an important factor in plant disease management and may influence plant disease through suppression of pathogen growth (Suthaparan et al., 2010, 2012), induction of resistance to disease within plants (Imada et al., 2014; Kim et al., 2013) or modification of morphogenesis and pathogenicity in fungal pathogens (Canessa et al., 2013). Exposure to LED lights (particularly blue and red LED light) and limited exposure to UV-B light reduced disease severity in several crops grown in growth chambers, greenhouses, and tunnels (Ahn et al., 2015). Red LED light [625–740 nm (Jones, 2020)] has been reported to induce resistance to powdery mildew (Sphaerotheca fuliginea) (Wang et al., 2010), gray mold (Botrytis cinerea) (Islam et al., 1999), leaf spot (Alternaria alternatae and A. tenuissima) (Rahman et al., 2003; Tabira et al., 1989), and damping off (Phytophthora capsica) (Islam et al., 2004). Red LED light also inhibited sporulation of the downy mildew pathogen (Peronospora belbahrii) (Patel et al., 2016) and reduced severity of tomato bacterial wilt (Pseudomonas solanacearum) (Schuerger and Brown, 1997). Blue LED light (435–500 nm) significantly reduced gray mold on tomato (Solanum lycopersicum) (Imada et al., 2014). Green LED light (500–570 nm) reduced anthracnose lesions and incidence of the pathogen (Glomerella cingulata) in strawberry fields while promoting growth of plants and enlargement of fruits (Kudo et al., 2011). Several studies have reported the effect of combinations of LED lights on infection and disease development by the gray mold pathogen B. cinerea: blue and red LED light inhibited lesion development and induced an accumulation of stilbenes and expression of defense-related genes in detached grapevine (Vitis vinifera) leaves inoculated with B. cinerea (Ahn et al., 2015); yellow and red LED lights inhibited the formation of infection by B. cinerea hypha on broad bean (Vicia faba) leaflets (Islam et al., 1998); and red and purple LED lights suppressed gray mold in tomatoes (Xu et al., 2017).

Many studies reported harmful effects of UV-B irradiation (280–320 nm) on plants (Pancotto et al., 2005; Rousseauxy et al., 2004), but others reported that UV-B irradiation may be used to control pathogens and increase plant resistance to disease (Manning and Tiedeman, 1995). UV-B radiation was lethal for conidia of Trichoderma spp. and Clonostachys rosea (Costa, 2011) and reduced powdery mildew infections both via direct (fungicidal effect) and indirect mechanisms (induction of plant resistance) in grapevines (Keller et al., 2003). On strawberry fruit, UV-B radiation suppressed powdery mildew symptoms and induced expression of a disease-resistance gene (Kanto et al., 2009, 2014). Because prolonged exposure to UV irradiation may damage plants, it is critical to establish the exposure time sufficient to kill a pathogen without injury to the host (Suthaparan et al., 2016). Night irradiation with UV-B for 2 h was more effective than 4-h irradiation during the day in suppression development of powdery mildew in greenhouse roses (Rosa ×hybrida) while causing less damage to the plants (Suthaparan et al., 2012). Short exposure to UV-C (254 nm) irradiation followed by a dark period has potential use in intensive field and indoor production of other fruits and vegetables. It reduced petal infection and fruit decay (B. cinerea and Colletotrichum sp.) of strawberries grown in a high tunnel with no negative effects on fruit yield or quality (Janisiewicz et al., 2016) and killed several fungal pathogens (B. cinerea, Podosphaera aphanis, C. gloeosporioides, and C. fragariae) without damaging strawberry plants (Takeda et al., 2019). The dark period following irradiation probably prevents activation of the light-induced DNA repair mechanism in these fungi (Takeda et al., 2019). Recently, Janisiewicz et al. (2021) reported that far UV (222 nm) was much more effective than UV-C (254 nm) in killing conidia of several fungal pathogens of strawberry, including B. cinerea, Penicillium expansum, and several Colletotrichum species, but was not detrimental to plant photosynthesis, pollen germ tube growth, and fruit set at the doses required to kill these pathogens.

Anthracnose crown rot, primarily caused by the fungus C. gloeosporioides, is a serious disease of strawberries grown in warm, humid areas (Dowling et al., 2020; Louws et al., 2019; Peres et al., 2017; Smith, 2008). This pathogen is most often associated with crown rot but also may incite fruit rots and leaf spots. In the southeastern United States, anthracnose crown rot can be especially severe on California strawberry cultivars grown on black plastic (Louws et al., 2019). In Florida, anthracnose crown rot is sometimes seen in winter production fields but is more common in nurseries (Peres et al., 2017). Several effective fungicides labeled for use on strawberries are available; however, anthracnose crown rot is difficult to control if environmental conditions are favorable for its development. Furthermore, frequent use of the same class fungicides often results in the development of resistance in Colletotrichum sp. (Dowling et al., 2020; Smith et al., 2013).

Supplemental light offers a potential alternative to chemical sprays for control of some plant diseases while eliminating the negative environmental effects of chemical fungicides and slowing the development of pesticide-resistant pathogens of strawberries grown in greenhouses. The objective of this greenhouse study was to investigate the effect of LED, UV-B, and WSF supplemental lights on strawberry plant growth and on plant response to infection following the inoculation of detached strawberry leaves with the anthracnose crown rot pathogen, C. gloeosporioides.

Materials and Methods

Greenhouse light treatments.

Six light treatments (red LED; blue LED; white LED; a combination of red, blue, and white LEDs; WSF; and WSF+UV-B) were used to evaluate the effect of supplemental lighting on plant growth and plant response to infection of strawberries grown in a greenhouse located in Poplarville, MS (30.84° N, 89.5° W). LED lights (Pro325 HV; LumiGrow, Emeryville, CA); WSF (GroLux, 20W T12 Wide Spectrum Fluorescent; Sylvania, Wilmington, MA), and WSF+UV-B (UV-B, Philips Broadband Ultraviolet-B TL 20W/12 RS, Hamburg, Germany) were suspended ≈1.2 m above strawberry plants. The light intensity adjustment of the adjustable spectrum LumiGrow Pro 325 LED grow lights was used to set the intensity of the red, blue, and white LED lights at their highest intensity setting (10) for each individual LED light treatment and for each of the three spectra in the combination LED treatment. Light treatments were placed on each of three greenhouse benches in a randomized complete block design and separated on each bench by 1.2 m high by ≈1.5 m square barriers constructed from rigid 2.5-cm insulation board with foil on both sides (R-6 Polyisocyanurate Rigid Foam insulation board; RMax Corp, Dallas, TX). Plants received natural light supplemented by treatment lights for a photoperiod of 17 h of light, approximately the number of daylight hours in south Mississippi in July. In addition to the 17 h WSF light exposure during the day, plants in the WSF+UV-B treatment were also exposed to UV-B irradiation for 3 h beginning 1 h after the WSF exposure ended (Janisiewicz et al., 2016; Suthaparan et al., 2012). In the second trial, an additional treatment was added, ambient light (i.e., no supplemental light). All other light treatment conditions were the same. Trial 1 ran for 24 weeks from early December until late May, and Trial 2 ran for 23 weeks from mid-January until the end of June.

Strawberry cultivars.

Strawberry plants (Table 1) were obtained from commercial nurseries or established from runners rooted locally, potted in 9 cm pots in a 1:1 mixture of Jiffy-Mix (JPA, West Chicago, IL) and sand; grown in a warm greenhouse (28 °C day/12 °C night, ± 10 °C) for a minimum of 4 weeks before initiation of each trial; and watered via drip emitters. Each plant was pruned back to the four youngest leaves before the start of each trial and about every 6 weeks during each trial. Trial 1 included six strawberry cultivars (Camarosa, Chandler, Pelican, Seascape, Strawberry Festival, and Sweet Charlie) with four plants of each cultivar in each replication of each light treatment for a total of 432 plants in the trial. Trial 2 included five cultivars (Albion, Allstar, Jewel, Seascape, and Strawberry Festival) with one plant of each cultivar in each replication of each light treatment for a total of 105 plants in the trial. Plants in Trial 1 were fertilized every 14 d with a liquid fertilizer [Miracle-Gro (24–8–16) Water-Soluble All Purpose Plant Fertilizer, Marysville, OH] at the labeled rate (40 mL per pot of 2.5 mL/4 L solution), and plants in Trial 2 were fertilized with Osmocote Classic (3- to 4-month) Slow Release 19–6–12 fertilizer (5 g per pot; ICL Fertilizers, Dublin, OH) applied 1 month before the start of the trial. Sixteen weeks after trial initiation, these plants were fertilized with Miracle-Gro (24–8–16) Water-Soluble All Purpose Plant Fertilizer at the labeled rate.

Table 1.

Strawberry cultivars used in Trials 1 and 2, their type, fruiting season, susceptibility to Colletotrichum spp., and the location of their release.

Table 1.

Light quality.

Light intensity (lumens/m2), temperature, and relative humidity data were recorded continuously throughout Trial 1 using a HOBO U12-012 Data Logger (Onset Computer Corporation, Bourne, MA). In both trials, photosynthetic photon flux density (PPFD, μmol·m−2·s−1), illuminance (lux), and peak wavelength (nm) of treatment lights were measured using a portable handheld spectrometer (Spectromaster C-7000; Sekonic Corporation Nerima-Ku, Tokyo, Japan). In Trial 1 spectrometer readings were taken during full sun near noon in midwinter, and during Trial 2, spectrometer readings were taken at noon CST (± 1 h) three times during each of four weather conditions (sunny, overcast, cloudy, rain and/or very cloudy) between January and June.

Plant growth data.

A soil plant analysis development (SPAD) chlorophyll meter (SPAD-502; Konica Minolta Sensing, Osaka, Japan) was used to determine relative chlorophyll concentration as an indicator of the foliar nitrogen level of plants (Wang et al., 2012). The vigor of each plant was rated visually on a subjective scale that ranged from 1 (least vigorous) to 10 (most vigorous). Plant injury was rated visually on a subjective scale that ranged from 0 (no visible damage) to 5 (extreme damage, including stunted plants with red, yellow, and/or necrotic foliage). The number of flowers and leaves on each plant were counted every 6 weeks. In Trial 1, each plant was photographed after 8 weeks of exposure to light treatments, and the photographs were used to electronically evaluate plant growth (plant area and density) using image analysis software (Assess 2.0, APS, St. Paul, MN). At the end of Trial 1 (after 24 weeks of exposure to light treatments), leaf samples were collected from each plant, dried, and sent to the Mississippi State University Extension Soil Testing Laboratory (Mississippi State, MS) for elemental analysis.

Detached leaf inoculation.

The effect of light treatments on the response of strawberry plants to infection by the anthracnose pathogen, C. gloeosporioides (= C. fructicola) isolate CG162 (Miller-Butler et al., 2018), was assessed using a detached leaf assay. One young, fully developed, blemish-free leaf was removed from a plant of each cultivar in each light treatment in each replication. The leaf petiole was inserted into a 10 × 150-mm test tube filled with sterile deionized water. Detached leaves were inoculated with a conidial suspension (1.5 × 106 conidia/mL) of the pathogen by misting the adaxial surface of each leaflet to the point of runoff using a hand pump sprayer. Leaves were immediately placed in a dew chamber at 100% relative humidity (RH) and 30 °C, incubated in the dark for 48 h, then transferred to sealed, clear plastic containers at 100% RH and 30 °C with continuous fluorescent light for an additional 8 days. Disease symptoms on each leaf blade were visually assessed 7 and 10 d after inoculation (dai) using a DSR scale of 0 = no visible disease symptom on any leaflet, 1 through 4 = increasing disease symptom severity, and 5 = total area of leaflets necrotic (Miller-Butler et al., 2018). Leaves in Trial 1 were collected and inoculated after 18 and 24 weeks of exposure to light treatments. In Trial 2, leaves were collected after 4 and 22 weeks of exposure to light treatments, inoculated with C. gloeosporioides isolate CG-162 and immediately placed in a dew chamber as in Trial 1. Two days later, inoculated leaves were removed from the dew chamber, placed into clear plastic boxes with glass lids, and returned to the same treatment location in the greenhouse as the plants from which they were taken. This was a variation from Trial 1 in which inoculated leaves were incubated in clear humidity boxes in the laboratory. Visual disease severity ratings were made 7 and 10 dai as in Trial 1.

Statistical analysis.

The experimental design of each trial was a randomized complete block with two main effects (light treatment and cultivar) and three replications. Analyses of variance was used to determine the effects of light treatments and cultivars on light quality, plant growth, plant vigor, plant injury, SPAD, and disease severity ratings. Main effect means were separated by Fisher’s protected least significant difference method at P < 0.05 using SAS statistical software (version 8.2; SAS Institute, Cary, NC). If the Pr > F value of light treatment by cultivar interaction was P < 0.05, analyses of variance and mean separation was rerun by cultivar to perform the contrasts.

Results

Light quality.

During Trial 1, average greenhouse temperatures in midwinter ranged from lows during the night of 15 °C to highs during the day of 27 °C with the highest temperature readings occurring in the white LED, WSF, and WSF+UV-B treatments (data not shown). Average light brightness during midwinter within light treatments varied from the lowest (red LED = 1870 lm/m2) to the highest (white LED = 4025 lm/m2) and within time periods from the lowest (night, 20:00–04:30 hr with all treatment lights off = 283 lm/m2) to the highest (full daylight, 08:00–16:30 hr = 9597 lm/m2) (data not shown). During time periods when there was an absence of full daylight [dawn (05:00–7:30 hr) and evening (17:00–19:30 hr)], average light brightness was 944 lm/m2 and 400 lm/m2, respectively (data not shown). There were no significance differences in average PPFD or illuminance (lux) in Trial 1 when spectrometer readings were taken during full sun near noon in midwinter (Table 2).

Table 2.

Spectrometer readings [photosynthetic photon flux density (PPFD), illuminance, and peak wavelength] of six supplemental light treatments, taken during full sun near noon in midwinter in Trial 1, and average spectrometer readings taken during Trial 2 near noon on 12 dates between January and June during various weather conditions (sunny, overcast, cloudy, rain/very cloudy).

Table 2.

During Trial 2, spectrometer readings were recorded near noon three times during each of four weather conditions (sunny, overcast, cloudy, rain, and/or very cloudy) between January and June. The overall average of the 12 readings of PPFD and illuminance was highest in the Combination LED light treatment (369 μmol·m−2·s−1, 13130 lx) and lowest in the ambient and WSF treatments (132 μmol·m−2·s−1, 7664 lx; and 145 μmol·m−2·s−1, 8229 lx, respectively) (Table 2). PPFD and illuminance were highest during sunny and cloudy weather conditions (251 μmol·m−2·s−1, 12,091 lx; and 261 μmol·m−2·s−1, and 12,341 lx, respectively) and lowest in rain and/or very cloudy conditions (145 μmol·m−2·s−1, 5708 lx) (Table 2).

Relative chlorophyll content.

Relative chlorophyll content of each plant was measured using a SPAD chlorophyll meter. Eleven weeks after initiation of Trial 1, the relative chlorophyll content of plants in the combination LED and red LED light treatments was lower than that of plants in all other light treatments (Table 3). At the initiation of Trial 2, there were no significant differences in SPAD values due to light treatments. At the 5- and 23-week evaluations, plants in the red LED and combination LED treatments had the lowest SPAD readings. In both trials, SPAD readings varied among cultivars at each evaluation (Table 3). In Trial 1, the relative chlorophyll content of ‘Pelican’ was lower than that of ‘Sweet Charlie’. In Trial 2, ‘Seascape’ had higher SPAD readings than ‘Strawberry Festival’ at the 5- and 23-week evaluations. SPAD readings declined as Trial 2 progressed (data not shown) probably due to decreasing nitrogen levels in the potting media. There was not a significant (P < 0.05) difference in light treatment by cultivar interaction in relative chlorophyll content in either trial.

Table 3.

Relative chlorophyll content, as determined by SPAD, 11 and 18 weeks after initiation of Trial 1 and 0, 5, and 23 weeks after initiation of Trial 2.

Table 3.

Plant growth and injury.

Significant differences occurred in plant growth and injury ratings due to light treatments and cultivars in both trials; however, the interactions between light treatments and cultivars were not significant for plant growth or injury in either trial (Table 4). In Trial 1, plant size, density, and vigor data were taken 11 weeks after trial initiation, and plant injury, leaf count and flower count data were taken after 18 weeks. The most vigorous plants at the 11-week evaluation were those in the WSF and WSF+UV-B light treatments, and the larger plants were those in the WSF, WSF+UV-B, and white LED light treatments (Table 4). Plants in the combination LED and red LED light treatments were less vigorous and smaller than plants in the other light treatments. ‘Strawberry Festival’ and ‘Sweet Charlie’ plants were significantly more vigorous and denser but smaller than ‘Pelican’ plants. At the 18-week evaluation, plants in the blue LED treatment had more flowers than those in the combination LED treatment, even though the combination LED treatment included a blue LED at the same intensity as in the blue LED treatment (Table 4). ‘Strawberry Festival’ had the most leaves. Plant injury ratings were lowest in white LED, WSF, and WSF+UV-B treatments. ‘Sweet Charlie’ plants had the least signs of injury and ‘Strawberry Festival’ plants had the most signs of injury.

Table 4.

Trial 1, plant size, density, and vigor ratings 11 weeks after initiation of light treatments; and plant injury, leaf count, and flower count 18 weeks after initiation of light treatments. Trial 2, plant vigor and plant injury ratings 0, 8 and 21 weeks after initiation of light treatments.

Table 4.

Plant vigor and plant injury data were taken at the beginning of Trial 2, 2 and 8 weeks later, and at the end of the trial. At the start of Trial 2, all plants received a vigor rating of ≈3.0 (data not shown). After 2- and 8-week exposure to the light treatments, plants in the combination and red LED treatments had the highest vigor ratings, whereas plants in the ambient, WSF, and WSF+UV-B treatments had the lowest vigor ratings (Table 4). By the 21 week evaluation, plants in the WSF treatment had significantly lower vigor ratings than plants in the white LED and WSF+UV-B treatment. ‘Albion’ plants received low vigor ratings and ‘Jewel’ plants received high vigor ratings at the 8- and 21-week evaluations. Plant injury ratings were very low, but plants in the combination and red LED treatments received significantly higher ratings at the 8- and 23-week evaluations than plants in all other light treatments (Table 4). ‘Strawberry Festival’ plants received higher injury scores than ‘Allstar’ plants at the 8-week evaluation. At the 23-week evaluation, plant injury scores were higher for ‘Strawberry Festival’ plants than for ‘Allstar’ and ‘Jewel’ plants (Table 4).

Foliar leaf analysis.

Elemental content of leaves harvested from each plant at the end of Trial 1 showed lower levels of N, K, Ca, and Fe in plants in the combination LED and red LED treatments than in plants from all other light treatments (Table 5). Leaves from plants in the WSF+UV-B light treatment had greater levels of Zn than leaves from plants in the combination LED, red LED, white LED, and WSF treatments. Among cultivars, K, Ca, Fe, and Mn levels were lowest in ‘Pelican’ leaves. There were no significant differences in elemental P or Mg (sufficiency range P = 0.2% to 0.4%, average foliar content of P = 0.21%; sufficiency range Mg = 0.25% to 0.45%, average foliar content of Mg = 0.28%) due to light treatment or cultivar, and no significant differences in elemental N content of leaves due to cultivar. The average foliar contents of N (1.4%), Fe (42 ppm), and Zn (4.9 ppm) of the plants in this study were well below the North Carolina Department of Agriculture nutrient sufficiency ranges for strawberry of N (3% to 4%), Fe (50 to 300 ppm), and Zn (15 to 60 ppm) (Campbell and Miner, 2000).

Table 5.

Nutrient sufficiency ranges for strawberry grown in the southern U.S., and elemental analysis of strawberry leaf tissue following 24 weeks exposure to light treatments during Trial 1.

Table 5.

Detached leaf inoculations.

After 18 weeks exposure to light treatments in Trial 1, there was a significant effect due to light treatment on DSRs 10 days after inoculation of detached strawberry leaves with C. gloeosporioides (Table 6). The DSRs in the WSF+UV-B treatment were lower than those in all other treatments except those in the red LED treatment. However, there were no significant effects due to light treatment in DSRs 10 days after inoculation after 24 weeks exposure to light treatments in Trial 1 or after 22-week exposure in Trial 2 (Table 6). There were significant effects due to cultivar at each evaluation date. In Trial 1, detached ‘Strawberry Festival’ and ‘Pelican’ leaves had the lowest DSRs (<1.0) at each evaluation date; in Trial 2, ‘Albion’, ‘Allstar’, and ‘Jewel’ leaves had significantly higher DSRs than ‘Seascape’ leaves after 22 weeks exposure to light treatments. There was a significant light by cultivar interaction at the 22 week evaluation in Trial 2 (Table 6), and there were significant differences in the DSRs within the cultivars, ‘Allstar’ and ‘Jewel’ due to light treatments (Table 7).

Table 6.

Main effects of light treatments and cultivar following 18 and 24 weeks (Trial 1) and 4 and 22 weeks (Trial 2) exposure to light treatments on disease severity ratings (DSRsz) 10 d after inoculation (dai) of detached leaves with Colletotrichum gloeosporioides Isolate CG162.

Table 6.
Table 7.

Effects of light treatments by cultivar following 22 weeks exposure to light treatments on disease severity ratings (DSRsz) 10 d after inoculation (dai) of detached leaves with Colletotrichum gloeosporioides Isolate CG162 in Trial 2.

Table 7.

Discussion

In this greenhouse study, we evaluated the effect of ambient and supplemental lights on plant growth and disease response of strawberries grown in a greenhouse. Supplemental lights had their greatest effect on plant growth during time periods when there was an absence of full daylight (i.e., dawn, evening, or during very cloudy or rainy conditions). Significant differences occurred among light treatments in PPFD and illuminance—that is, PPFD and illuminance were lowest in the ambient and WSF light treatments, highest in the combination LED and red LED light treatments, and, among the various weather conditions, lowest in rain and/or very cloudy conditions.

In each of the two trials, there were significant effects due to light treatment on strawberry plant growth, injury, foliar leaf analysis, and SPAD values. Significant differences occurred in disease severity ratings of inoculated detached leaves due to light treatment at one evaluation date in one trial. In Trial 1, Plants in the WSF and WSF+UV-B light treatments were the most vigorous, whereas those in the combination LED and red LED light treatments were the least vigorous. Plants in the combination LED treatment had fewer flowers probably due to the negative affect of the red LED light (Takeda et al., 2008). At the 21 week evaluation in Trial 2, plants in the combination and red LED treatments were significantly less vigorous than plants in the WSF+UV-B treatment. Plant injury ratings were very low in both trials; however, plants in the combination LED and red LED treatments consistently displayed more severe signs of injury.

The relative chlorophyll content of leaves (as determined by a SPAD meter) of plants in the combination LED and red LED light treatments was lower than that of plants in all other light treatments at both evaluation dates in both trials. At the end of Trial 1, foliar analysis of plants in the combination LED and red LED treatments had lower levels of N, K, Ca, and Fe than plants from all other light treatments. This nutrient deficiency is consistent with the high injury, low vigor, and low SPAD values of plants in the red LED and combination LED treatments and is probably due to the high intensity of the red LED light in each of these two treatments; that is, a PPFD ≈400 µmol·m−2·s−1 compared with that of the other four light treatments (PPFD ≈318 µmol·m−2·s−1) and to ambient light (PPFD = 169 µmol·m−2·s−1).

A significant effect due to light treatments on DSRs was found at one inoculation date in Trial 1. After 18 weeks of exposure to light treatments, detached strawberry leaves were inoculated with the anthracnose pathogen C. gloeosporioides and rated for anthracnose symptoms 10 days later. Significantly lower DSRs occurred in the WSF+UV-B and Red LED treatments. The low DSR of the leaves in the WSF+UV-B treatment may have been due to the UV-B irradiation which has been shown to increase plant resistance to disease (Kanto et al., 2014; Keller et al., 2003; Manning and Tiedeman, 1995). The low DSR of the leaves in the red LED treatment corelates with the low SPAD values and low elemental leaf nitrogen levels of plants in the red LED treatment because anthracnose crown rot is known to be less severe when strawberries are grown on soils with low nitrogen fertility (Howard et al., 1992; Smith, 2008).

The LumiGrow Pro325 HV LED light fixtures used in these trials feature independently adjustable knobs for each of three light spectra (red, blue, or white) that allowed the intensity of each light spectrum in each light fixture to be set individually or in combinations at intensities from 1 to 10, or to be turned off. We measured the PPFD readings in the laboratory at each light intensity setting of the LED fixtures using a portable handheld spectrometer located 1.2 m directly below each light fixture. The PPFD readings emitted by the white LED, blue LED, red LED, and combination LED lights ranged from 6.3, 6.7, 10.3, and 10.5 µmol·m−2·s−1, respectively, when each spectrum was set at 1 compared with PPFD readings of 20.0, 31.8, 141.5, and 178.3 µmol·m−2·s−1, respectively, when each spectrum was set at 10 (Table 8). For the light treatments in the two trials in our study, each individual light spectrum was set at an intensity of 10, and all three light spectra were set at “10” in the combination LED treatment. Our results indicate that the intensity of the red LED light in the red LED and combination LED treatments were too strong for the strawberry plants in this study.

Table 8.

Photosynthetic photon flux density (PPFD, μmol·m–2·s–1) readings at various light intensity settings of the LED fixtures (LumiGrow Pro325 HV, Emeryville, CA) measured using a portable handheld spectrometer (Spectromaster C-7000, Sekonic Corporation Nerima-Ku, Tokyo, Japan), which was located 1.2 m directly below each light. Readings were taken in the laboratory. PPFD readings of wide spectrum fluorescent light (GroLux) located 1.2 m directly below each light was 3.9 PPFD (μmol·m−2·s−1).

Table 8.

Various cultivars representing day neutral and June-bearing types released from the eastern, western, and southern United States were evaluated in each of the two trials. Significant differences in the relative chlorophyll content, plant growth, plant injury, and disease severity ratings occurred among cultivars in each trial. The light treatment by cultivar interaction for DSR was significant at the 22 week evaluation in the second trial. In Trial 1, ‘Sweet Charlie’ plants had significantly higher SPAD readings and were smaller, denser, and more vigorous than ‘Pelican’ plants which is consistent with the dark green foliage and compact growth characteristic of ‘Sweet Charlie’ (Chandler et al., 2009) compared with the pale green foliage and open growth habit characteristic of ‘Pelican’ (Smith et al., 1998). In Trial 2, ‘Albion’ plants were the least vigorous and ‘Jewel’ plants were the most vigorous. ‘Sweet Charlie’ (Trial 1), ‘Allstar’ and ‘Jewel’ (Trial 2) plants displayed the least signs of plant injury. In Trial 1, ‘Strawberry Festival’ and ‘Pelican’ had the lowest DSRs (<1.0) at each evaluation date. The low DSR for ‘Pelican’ was expected because of its known level of resistance to anthracnose (Miller-Butler et al., 2018; Smith et al., 1998); however, it was unexpected for ‘Strawberry Festival’ which is more susceptible to anthracnose (Chandler, 2004; Miller-Butler et al., 2018).

Many types of supplemental lighting are available for use in commercial greenhouses and grow rooms. Growers often choose LED lights where options range from spectrum-specific LED light bulbs that can be placed in standard incandescent sockets, to T8 LED retrofits that can replace standard T8 fluorescent tubes, to fixtures with adjustable spectra and wireless software-based controls. Within each type, a single spectrum up to a full spectrum of red, white, and blue LEDs are available. Some have a preset spectrum for either/or both vegetative and flowering stages, whereas others feature individually, fully adjustable wavelengths with software controlled via Wi-Fi so that growers can adjust lights to their crop. The cost of supplemental lighting varies greatly and represents a significant investment by the grower. Detailed research data are needed on the effect of various lighting options on plant growth, diseases, and insects so that strawberry growers can make informed decisions on the best supplemental light and light spectra for each phase of strawberry production (plant growth, flowering, and fruiting).

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Contributor Notes

We gratefully acknowledge the technical support of J.B. Carroll and R. Davis. The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the U.S. Department of Agriculture or the Agricultural Research Service, University of Florida/IFAS, or Mississippi State University of any product or service to the exclusion of others that may be suitable.

B.S., E.S., H.S., and A.R. contributed equally to this work.

B.J.S. is the corresponding author. E-mail: Barbara.Smith6@usda.gov.

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  • Ahn, S.Y., Kim, S.A. & Yun, H.K. 2015 Inhibition of Botrytis cinerea and accumulation of stilbene compounds by light-emitting diodes of grapevine leaves and differential expression of defense-related genes Eur. J. Plant Pathol. 143 753 765 https://doi.org/10.1007/s10658-015-0725-5

    • Search Google Scholar
    • Export Citation
  • Bringhurst, R.S. & Voth, V. 1991 U.S. Patent Plant 7,614. Date of Patent: 6 Aug. 1991 Strawberry plant named ‘Seascape’

  • Campbell, C.R. & Miner, G.S. 2000 Strawberry, annual hill culture Campbell, C.R. Reference sufficiency ranges for plant analysis in the southern region of the United States. NC Dept of Agriculture & Consumer Services Raleigh, N.C. Southern Cooperative Series Bulletin 394: www.ncagr.gov/agronomi/saaesd/scsb394.pdf

    • Search Google Scholar
    • Export Citation
  • Canessa, P., Schumacher, J., Hevia, M.A., Tudzynski, P. & Larrondo, L.F. 2013 Assessing the effects of light on differentiation and virulence of the plant pathogen Botrytis cinerea: Characterization of the white-collar complex PLoS One 8 e84223 https://doi.org/10.1371/journal.pone.0084223

    • Search Google Scholar
    • Export Citation
  • Chandler, C.K. 2004 ‘Strawberry Festival’ Strawberry Plant U.S. Patent PP14,739 P2. 27 Apr. 2004

  • Chandler, C.K, Albregts, E.E., Howard, C.M. & Brecht, J.K. 2009 ‘Sweet Charlie’ Strawberry University of Florida IFAS Extension HS820

  • Costa, L.B. 2011 Efeito da radical ultravioleta-B sobre Trichoderma spp. Clonostachysrosea, agentes de biocontrole de fitopatógenos MS dissertation Universidade Federal de Lavras Lavras MG

    • Search Google Scholar
    • Export Citation
  • Dowling, M., Peres, N., Villani, S. & Schnabel, G. 2020 Managing Colletotrichum on fruit crops: A “complex” challenge Plant Dis. 04 2301 2316 https://doi.org/10.1094/PDIS-11-19-2378-FE

    • Search Google Scholar
    • Export Citation
  • Galletta, G.J. 1981 ‘Allstar’ strawberry HortScience 16 792 794

  • Howard, C.M., Maas, J.L., Chandler, C.K. & Albregts, E.E. 1992 Anthracnose of strawberry caused by the Colletotrichum complex in Florida Plant Dis. 76 976 981 https://doi.org/10.1094/PD-76-0976

    • Search Google Scholar
    • Export Citation
  • Imada, K., Tanaka, S., Ibaraki, Y., Yoshimura, K. & Ito, S. 2014 Antifungal effect of 405-nm light on Botrytis cinerea Lett. Appl. Microbiol. 59 670 676 https://doi.org/10.1111/lam.12330

    • Search Google Scholar
    • Export Citation
  • Islam, S.Z., Babadoost, M. & Honda, Y. 2004 Optimization of red-light irradiation in inducing resistance in vegetable seedlings against Phytophthora apsica Phytopathology 94 S44

    • Search Google Scholar
    • Export Citation
  • Islam, S.Z., Honda, Y. & Arase, S. 1998 Light induced resistance of broad bean against Botrytis cinerea J. Phytopathol. 146 479 485 https://doi.org/10.1111/j.1439-0434.1998.tb04609.x

    • Search Google Scholar
    • Export Citation
  • Islam, S.Z., Honda, Y. & Arase, S. 1999 Some characteristics of red light-induced substance(s) against Botrytis cinerea produced in broad bean leaflets J. Phytopathol. 147 65 70 https://doi.org/10.1046/j.1439-0434.1999.147002065

    • Search Google Scholar
    • Export Citation
  • Janisiewicz, W., Takeda, F., Evans, B. & Camp, M. 2021 Potential of far ultraviolet (UV) 222 nm light for management of strawberry fungal pathogens Crop Prot. 05791 1 10 https://doi.org/10.1016/j.cropro.2021.105791

    • Search Google Scholar
    • Export Citation
  • Janisiewicz, W.J., Takeda, F., Glenn, D.M., Camp, M.J. & Jurick, M. II 2016 Dark period following UV-C treatment enhances killing of Botrytis cinerea conidia and controls gray mold of strawberries Phytopathology 106 386 394 https://doi.org/10.1094/PHYTO-09-15-0240-R

    • Search Google Scholar
    • Export Citation
  • Johkan, M., Shoji, K., Goto, F., Hashida, S. & Yoshihara, T. 2010 Blue light-emitting diode light irradiation of seedlings improves seedling quality and growth after transplanting in red leaf lettuce HortScience 45 1809 1814 https://doi.org/10.21273/HORTSCI.45.12.1809

    • Search Google Scholar
    • Export Citation
  • Jones, A.Z. 2020 What is the visible light spectrum? ThoughtCo. Feb. 14, 2020, thoughtco.com/the-visible-light-spectrum-2699036

  • Kanto, T., Matsuura, K., Yamada, M., Usami, T. & Amemiya, Y. 2009 UV-B radiation for control of strawberry powdery mildew Acta Hort. 842 359 362 https://doi.org/10.17660/ActaHortic.2009.842.68

    • Search Google Scholar
    • Export Citation
  • Kanto, T., Matsuura, K., Ogawa, T., Yamada, M., Ishiwata, M., Usami, T. & Amemiya, Y. 2014 A new UV-B lighting system controls powdery mildew of strawberry Acta Hort. 1049 655 660 https://doi.org/10.17660/ActaHortic.2014.1049.101

    • Search Google Scholar
    • Export Citation
  • Keller, M., Rogiers, S. & Schultz, H. 2003 Nitrogen and ultraviolet radiation modify grapevines’ susceptibility to powdery mildew Vitis Geilweilerhof 42 87 94

    • Search Google Scholar
    • Export Citation
  • Kim, H.H., Goins, G.D., Wheeler, R.M. & Sager, J.C. 2004 Green light supplementation for enhanced lettuce growth under red and blue light-emitting diodes HortScience 39 1617 1622 https://doi.org/10.21273/HORTSCI.39.7.161

    • Search Google Scholar
    • Export Citation
  • Kim, K., Kook, H.-S., Jang, Y.-J., Lee, W.-H., Kamala-Kannan, S., Chae, J.-C. & Lee, K.-J. 2013 The effect of blue-light-emitting diodes on antioxidant properties and resistance to Botrytis cinerea in tomato J. Plant Pathol. Microbiol. 4 203 208

    • Search Google Scholar
    • Export Citation
  • Kondo, S., Tomiyama, H., Rodyoung, A., Okawa, K., Ohara, H., Sugaya, S., Terahara, N. & Hirai, N. 2014 Abscisic acid metabolism and anthocyanin synthesis in grape skin are affected by light emitting diode (LED) irradiation at night J. Plant Physiol. 171 823 829 https://doi.org/10.1016/j.jplph.2014.01.001

    • Search Google Scholar
    • Export Citation
  • Kudo, R., Ishida, Y. & Yamamoto, K. 2011 Effects of green light irradiation on induction of disease resistance in plants Acta Hort. 907 251 254 https://doi.org/10.17660/ActaHortic.2011.907.39

    • Search Google Scholar
    • Export Citation
  • Lee, M.J., Son, J.E. & Oh, M.M. 2013 Growth and phenolic content of sowthistle grown in a closed-type plant production system with a UV-A or UV-B lamp Hortic. Environ. Biotechnol. 54 492 500 https://doi.org/10.1007/s13580-013-0097-8C

    • Search Google Scholar
    • Export Citation
  • Louws, F., Ridge, G., Harrison, J. & Cline, B. 2019 Anthracnose Crown Rot of Strawberry NC State Extension Publications, Raleigh, NC. https://content.ces.ncsu.edu/anthracnose-crown-rot-of-strawberry#

    • Search Google Scholar
    • Export Citation
  • Manning, W.J. & Tiedeman, A.V. 1995 Climate change: Potential effects of increased atmospheric carbon dioxide (CO2), ozone (O3), and Ultraviolet-B (UV-B) radiation on plant diseases Environ. Pollut. 88 219 245 https://doi.org/10.1016/0269-7491(95)91446-r

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