Testing Cultivar-specific Tipburn Sensitivity of Lettuce for Indoor Vertical Farms

Authors:
John Ertle 224 Howlett Hall, 2001 Fyffe Court, Columbus, OH 43210, USA

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Chieri Kubota 330 Howlett Hall, 2001 Fyffe Court, Columbus, OH 43210, USA

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Abstract

Low evaporative conditions in indoor (vertical) farms reduce mass-flow–driven transport of calcium (Ca), resulting in tipburn of lettuce. Lettuce tipburn symptoms develop along the margins of young leaves and the growing shoot tip, where necrotic tissue forms as a result of Ca deficiency. For indoor farms, lettuce tipburn poses a major economic risk because the crop becomes unmarketable as a result of its appearance. Difference in tipburn sensitivity among cultivars has been thought to be related to differences in growth rate, morphology, or anthocyanin production, whereas most commercial lettuce cultivars have been known to express tipburn symptoms in the indoor farm setting. We created a tipburn-inducing growing condition in walk-in growth chambers that limits plant potential transpiration rate while achieving relatively high growth rates, and examined 10 commercial cultivars selected for tipburn sensitivity. Selected cultivars differ in morphology (butterhead, romaine, and leafy type) and color (red or green; resulting from anthocyanin production). All cultivars expressed visually detectable tipburn symptoms 22 ± 2.6 days after transplanting, and varied tipburn rates of 7% to 41% of all leaves at the time of harvest (28 days after transplanting). Despite cultivar-specific variation, neither lettuce morphology nor anthocyanin content were significantly correlated with the incidence or severity of tipburn. However, cultivars recommended for “indoor” production by seed suppliers had less tipburn severity than those recommended for outdoor or both indoor and outdoor production systems. Although tipburn risk may vary under other environmental conditions, low evaporative conditions in this experiment caused tipburn symptoms in all tested cultivars at varying degrees of severity. Cultivar-specific average yield and tipburn severity were not correlated with the Ca concentrations in the inner leaves, suggesting that the amount of tissue Ca required to prevent tipburn is cultivar specific and not related to yield. Our selected tipburn-inducing condition was found to be effective in comparing tipburn sensitivity of lettuce cultivars for indoor farm settings, and similar fast-growing but low-evaporative conditions should be used to assess cultivars for indoor farm production.

During the past decade, dozens of indoor (vertical) farms (IF) have been founded throughout the world. Relying on environmental controls, electric lighting, and hydroponic growing systems, IFs have begun to supplement the existing agricultural industry by producing leafy greens such as lettuce and herbs near urban settings (Takagaki et al. 2020). Through indoor growing, crops can be produced year-round, unaffected by weather, seasons, or daylength. Indoor farms typically use hydroponic systems to grow plants rapidly using nutrient solutions instead of traditional soil systems, allowing for maximized growth rates and reduced waste (Kozai et al. 2022). In addition, IFs have the capacity to operate in highly urban settings using minimal space, allowing for hyperlocalized production and distribution of produce near consumers (Specht et al. 2014). As a result, transport costs are reduced and product shelf life is increased, minimizing food waste while creating a high-quality product (Mempel et al. 2021).

Indoor farms reportedly can be 100 times more productive per square foot than open-field farms (Kozai et al. 2022), but they also have many unique challenges. An understanding of engineering principles, plant physiology, and pest and disease management techniques is crucial to the success of IFs (Geelen et al. 2018). Much research is conducted to establish best practices within IFs. However, a calcium (Ca) deficiency in IF-grown lettuce, called tipburn, persists for many growers. Tipburn is a localized Ca deficiency caused by a limited supply of Ca relative to fast-growing lettuce shoot tips (Barta and Tibbitts 2000). Although the supply of Ca in hydroponics is sufficient, as evidenced by a lack of Ca-deficient symptoms in the roots (Petrazzini et al. 2014), necrotic tissue forms along the edges of leaves, which is characteristic of a Ca deficiency (Brumm and Schenk 1993). Lettuce tipburn is caused when Ca translocated to the growing shoot tip does not meet the demand for new growth (Barta and Tibbitts 2000). This disorder causes lower yields because the necrotic tissue prevents full expansion of new leaves and low marketable quality as a result of the poor visual appearance (Frantz et al. 2004).

The growing conditions known for increasing the risk of inducing tipburn are those promoting a fast-growth rate during the day, while also limiting transpiration. Lettuce is reported to have maximum net photosynthesis (Pn) at 24 ± 1 °C (Seginer et al. 1991), and has optimal growth between 22 and 25 °C under elevated (1000–1500 μmol⋅mol–1) carbon dioxide (CO2) conditions (Ahmed et al. 2020). When grown at higher temperatures, Lee et al. (2013) reported greater tipburn incidence in two green-leaf lettuce cultivars, presumably as a result of a greater growth rate under these temperatures. Elevated CO2 of ∼1000 μmol⋅mol–1 is a widely adopted practice in greenhouse and IFs, as it is known to increase the growth rate and yield of lettuce over ambient conditions (Park and Lee 2001). However, increase in tipburn incidence (percentage of plants with tipburn symptoms) has been reported under greater CO2 concentrations (700–1300 μmol⋅mol–1) compared with less CO2 (< 700 μmol⋅mol–1) or without CO2 enrichment (Caplan 2018). Both et al. (1997) examined varied daily light integrals (DLIs) for ‘Ostinata’ lettuce in a greenhouse equipped with supplemental lighting and reported that tipburn was not induced at a DLI of ≤ 16 mol⋅m–2⋅d–1.

Vapor pressure deficit in the air (VPD) is known to be highly correlated with transpiration rate. Although a greater daytime relative humidity (RH) of 74% (0.73 kPa VPD) reportedly increased tipburn incidence of lettuce (compared with 51% RH), increasing nighttime humidity to a near-saturation level (> 95%) reduced tipburn compared with ≤ 90% nighttime RH (Collier and Tibbitts 1984). During the night, root pressure plays a key role; enhancing nonstomatal (cuticular) transpiration at night is known to reduce the contribution of root pressure and thereby increase tipburn (Vanhassel et al. 2015). Nearly saturated humidity at nighttime is known to limit nonstomatal nighttime transpiration, which can increase xylem pressure, which drives water and Ca to the leaves to mitigate tipburn risk. Therefore, a combination of high daytime humidity and low nighttime humidity is considered a tipburn-inducing humidity environment. Similarly, airflow rate significantly affects transpiration rate. For lettuce, the rate as well as the direction of airflow relative to the plant canopy have been considered factors affecting tipburn incidence (Ahmed et al. 2020). Goto and Takakura (1992) demonstrated that perforated tubes supplying 1 L⋅min–1 (or 1.33 m⋅s–1) of airflow continuously to the inner leaves was able to eliminate tipburn of lettuce, but not when the same airflow was applied to the outer leaves or when plants were grown without this airflow. Shibata et al. (1995) suggested downward vertical airspeeds greater than 0.3 m⋅s–1 to facilitate transpiration of inner leaves, and Ahmed et al. (2022) recommended an airflow speed of 0.5 m⋅s–1, specifically to reduce or eliminate tipburn in lettuce.

A main challenge for growers deciding which cultivars to produce is comparing the tipburn risk of cultivars offered by different seed companies. Many tipburn sensitivity assessments are performed in greenhouses rather than true IFs, which likely underestimate the tipburn risk in indoor settings. A testing condition within environments such as IFs (e.g., growth chambers) would allow for more direct comparisons among lettuce cultivars offered by different seed companies.

Although there is a foundational knowledge base of tipburn-inducing environmental conditions, testing environments and consistent metrics for assessing tipburn sensitivity of lettuce cultivars are not well developed. Therefore, the objectives of this study were 1) to present a selected tipburn-inducing growing condition that can be used to evaluate tipburn sensitivity of lettuce and 2) to assess the tipburn risk of 10 commercial lettuce cultivars known to be tipburn sensitive.

Materials and Methods

Growth chamber setup.

The experiment was conducted in two identical walk-in growth chambers (Conviron, Winnipeg, ON, Canada) located in Columbus, OH, USA (lat. 40°N, long. 83°W, elevation 275 m above sea level). The floor area was 2.74 × 3.32 m, with a growing area (per chamber) of 2.83 m2 at 1 m above the floor, spread across four identical carts. Each growth chamber had dedicated heating, ventilation, and air conditioning controlled by an aspirated temperature sensor located centrally 1.4 m above the floor. The chambers also had additive CO2 control based on an aspirated probe (EE872; E+E Elektronik, Engerwitzdorf, Austria). The horizontal and vertical airflow speeds were 0.09 ± 0.08 and 0.08 ± 0.02 m⋅s–1, respectively, when measured across the growing area in both chambers (192 points, measured before and after the experiment).

Sole-source lighting was provided by light-emitting diode (LED) lighting modules with adjustable spectra (GPL PM 168 DRBWFR L120 G3.0 C4 NA; Philips Signify, Eindhoven, Netherlands). Two modules were mounted per cart, 50 cm above the channel surface. The light spectra were 19% blue (400–500 nm), 10% green (500–600 nm), and 71% red (600–700 nm) in a photon flux ratio, with a small amount of far-red light (∼1%, 700–750 nm). Between both chambers, light intensity across the channel surface at the canopy height averaged 289.4 ± 2.3 μmol⋅m–2⋅s–1 photosynthetic photon flux density (PPFD), with an additional far-red light intensity of 4 μmol⋅m–2⋅s–1 when measured at the height of a well-developed lettuce canopy (30 cm below the fixtures) in an empty shelf with black cloth covering the shelf surface to limit the reflection.

Environmental conditions were monitored throughout the experiment using two CR1000X Dataloggers (Campbell-Scientific, Logan, UT, USA), one for each growth chamber. Air temperature was measured at lettuce canopy level at the center of each of the eight carts using calibrated T-type thermocouples (gauge, 36). Additional air temperature and RH (converted to air temperature-based VPD) values were measured using a fan-aspirated HMP-60 probe (Vaisala, Vantaa, Helsinki, Finland) located centrally, opposite the growth chamber doors. The datalogger in each chamber added humidity with an ultrasonic humidifier (Optimus U-31002; Optimus Enterprise Inc., Anaheim, CA, USA).

Tipburn-inducing conditions.

Table 1 shows the environmental conditions achieved in this experiment. Targeted temperatures were 23 and 19 °C for day and night, respectively, with an RH target of 75% (VPD = 0.7 kPa) during the daytime and untargeted nighttime venting to reduce humidity. Liquid CO2 was injected during the daytime to elevate the concentration to 1000 μmol⋅mol–1. The average DLI was 16.7 mol⋅m–2⋅d–1, with a maximum DLI of 19.6 mol⋅m–2⋅d–1 at the center of the growing area.

Table 1.

Environmental conditions achieved for each experimental repeat during the day and night for each growth chamber.i

Table 1.

Plant materials and seedling growing conditions.

A combination of eight commercial lettuce cultivars (Rijk Zwaan, De Lier, Netherlands) known to be tipburn sensitive were used in this experiment (Table 2). In addition, two cultivars (Rex and Rouxai) were added because they were referred to as relatively tipburn tolerant, according to a seed distributor’s information (for ‘Rex’) and our own experience (for ‘Rouxai’). The selected cultivar types include three Romaine (Claudius, Rafael, and Tuccadona), three butterhead (Cecilia, Flandria, and Rex), and four other leafy types (Haldane, Kalat, Klee, and Rouxai) (Table 2). Kalat, Klee, and Rouxai are red-lettuce cultivars.

Table 2.

Names, colors, types, and seed company–recommended production systems for the 10 commercial lettuce cultivars used in this experiment.

Table 2.

Seeds were covered with an opaque plastic tray and germinated in rockwool cubes (3.8 × 3.8 cm; Grodan Inc., ON, Canada) for 2 d at 20 °C inside of a continuously lit (120 μmol⋅m–2⋅s–1 PPFD) growth chamber (E15; Conviron, Winnipeg, MB, Canada). After germination, the seedlings were uncovered and grown in the same growth chamber for 12 d with the same light intensity under a 16-h photoperiod, with day and night temperatures of 23 and 19 °C, respectively. Lights were white fluorescent lamps (120 μmol⋅m–2⋅s–1 PPFD). Seedlings were watered once a day with a half-strength nutrient solution described later.

Post-transplanting growing conditions.

Two-week old seedlings with three to four true leaves were transplanted into nutrient film technique channels (Cropking Inc., Lodi, OH, USA) made of food-grade polyvinyl chloride inside of the two identical walk-in growth chambers described earlier. Channels measured 9.5 × 4 × 123 cm, with six 2.5- × 2.5-cm square holes punched in the channel cover. Four channels were mounted on each of four wire-frame carts in each chamber, totaling eight carts, which we considered blocks. Each channel held six plants, resulting in 24 plants grown per cart, or 96 plants per chamber, and 192 total plants between the two chambers. The planting density was 34 plants/m2. Channels were rotated every other day to account for light uniformity and to limit the number of true border plants. Because of the alternating arrangement of the square hole punches per channel, one plant at the end of each channel was considered a border plant and was removed from analysis. Thus, 160 of 192 total plants were used for data collection and analysis.

For the first week of growth, channels were closed off and filled to 80% of their volume (∼3.74 L) with a modified leafy green hydroponic solution (M. Jensen, University of Arizona, Tucson, AZ, USA), containing 173 mg⋅L–1 total nitrogen (N) (166 nitrate-N), 37 mg⋅L–1 phosphorus, 157 mg⋅L–1 potassium, 186 mg⋅L–1 Ca, 38 mg⋅L–1 magnesium, 64 mg⋅L–1 sulfur, 91 mg⋅L–1 chloride, and micronutrients. The pH and electrical conductivity of the nutrient solution were adjusted as needed to maintain values of 6.0 ± 0.5 and 2.0 ± 0.2 dS⋅m–1, respectively. Channels were filled to enhance root contact with the solution and were drained completely and refilled once per day to maintain dissolved oxygen levels (> 5 mg⋅L–1). After 1 week, the channels were opened completely and a nutrient film was allowed to flow continuously within the channels through the end of the experiment. The entire nutrient solution was replaced once per week.

Across all four reps and both chambers, the average day- and nighttime temperatures were within 0.3 °C of the set points across all thermocouples (Table 1). The aggregate average temperatures [mean ± standard deviation (SD)] were 23.1 ± 0.3 and 19.3 ± 0.8 °C for day and night, respectively. The average day- and nighttime VPD was 0.52 ± 0.24 and 0.72 ± 0.31 kPa, or 81.5 ± 8.7 and 67.6 ± 14.1% RH, respectively. Although temperatures were uniform, VPD varied throughout the course of the experimental repeats, which is reflected in the SD. Humidity control in the chambers was difficult because the air conditioner removed little water as a result of its large size. The daytime humidity target of 0.70 kPa was greater than the achieved conditions in this experiment (Table 1). Average PPFD from the LED lighting modules varied by < 9.1 μmol⋅m–2⋅s–1 across all blocks in both chambers for each of the four experimental repeats (n = 96 observations per chamber or 24 observations per block), resulting in an average DLI of 16.7 mol⋅m–2⋅d–1. Carbon dioxide levels averaged 982 μmol⋅mol–1 and varied by 148 μmol⋅mol–1 within both chambers across all experimental repeats.

Data collection.

Evaporation rates in the chamber were measured before transplant using a petri and deep dish tool developed by Papio (2021). The petri dish is useful for estimating evaporation resulting from horizontal and vertical airflow directions, whereas the deep dish estimates evaporation more adequately as a result of the vertical airflow, because the higher sidewalls function as a barrier for horizontal flow. Across all channel surfaces, the evaporation rate during the day was 3.7 ± 0.1 and 5.9 ± 0.2 mol⋅m–2⋅h–1 for deep and petri dishes, respectively. At night, the evaporation rate was 3.0 ± 0.2 and 4.3 ± 0.3 mol⋅m–2⋅h–1, respectively. These tools are used to compare the relative maximum evapotranspiration rate of plants in the same system. Evaporation rates < 10 mol⋅m–2⋅h–1 are low for a controlled environment setting and are indicative of a low transpiration potential (Papio 2021).

After transplanting, plants were assessed for visual tipburn symptoms daily. Visual inspection was done by the same person. Tipburn emergence is noted in this study as the number of days from transplant to visible tipburn symptoms [days after transplant (DAT)]. Each plant was considered to have tipburn when necrotic tissue formed along the margins of young leaves (typically near the meristem) and was visible to the human eye, and is referred to as tipburn incidence. Tipburn severity was rated at final harvest as the percentage of leaves expressing tipburn symptoms out of the total number of leaves per plant (percentage of leaves with tipburn symptoms).

Leaf gas exchange was collected during experimental repeats 3 and 4 at 26 to 27 DAT using a Ciras-3 portable photosynthesis system and a CFM-3 chlorophyll fluorescence module (PPSystems, Amesbury, MA, USA). The CFM-3 is an adjustable spectra and intensity LED unit that was calibrated to 350 μmol⋅m–2⋅s–1 (the maximum PPFD in the growing environment) and matched the light quality used in this experiment (2:1:7 blue:green:red).

At harvest, shoot and root fresh mass were collected. The number of leaves, and the number of leaves with tipburn symptomology, were counted for each plant. Plants were dried at 55 °C for at least 3 d before collecting shoot and root dry mass. For two plants of each cultivar (one from each chamber; 20 plants total), a sample of inner leaves of ∼10 g fresh mass, or ∼8 to 15 inner leaves (depending on the cultivar) nearest the meristem, were dried separately from the outer leaves at harvest. Both inner and outer leaf samples from each selected plant were sent for mineral nutrient composition analysis (JR Peters, Allentown, PA, USA).

Experimental design and statistical analysis.

The four experimental repeats were conducted in 2021, from 18 Mar to 29 Apr, 6 May to 17 Jun, 5 Aug to 16 Sep, and 21 Sep to 2 Nov. Transplanting was conducted 14 d after the start date of each repeat, and all repeats were harvested after a total of 42 d. The fourth experimental repeat was not replicated in both chambers, and only used one chamber to evaluate post-transplanting growth (n = 80 plants for this repeat only).

The experimental model was a randomized complete block design, with factors including the experimental replication [random; degrees of freedom (df) = 3] growth chambers (random, nested in the experimental replication; df = 1), carts (random, nested in chamber; df = 6), cultivars (fixed; df = 9), and residual error (df = 254). Carts were considered blocks within each chamber. Individual plants were considered sampling units, and experimental units were the combined values of treatments within each block (n = 280, or n = 28 per cultivar).

All statistical analyses were conducted using R (ver. 4.2.3; R Foundation for Statistical Computing, Vienna, Austria) and RStudio (ver. 2023.03; RStudio, Boston, MA, USA). Mixed linear model analysis and Tukey’s honestly significant difference (HSD) tests were used to determine significance (α ≤ 0.05) and separate means. Specific packages include lme4 (ver. 1.1-33) and agricolae (ver. 1.3-5) for mixed linear models and HSD tests, respectively (Bates et al. 2015; de Mendiburu 2019), and ggplot2 (ver. 3.4.2) for plotting regression analyses (Wickham 2016).

Results

Plant growth.

Table 3 contains the Tukey’s letter report, marking significant differences determined by Tukey’s HSD and mixed linear model (P ≤ 0.05) of shoot and root fresh and dry mass, root-to-shoot (fresh mass) ratio, and number of leaves. Plant growth differences were expected among different cultivars.

Table 3.

All plant growth values (mean ± standard error).

Table 3.

‘Tuccadona’ had the greatest root and shoot fresh and dry mass, making it the greatest yielding cultivar (shoot fresh mass = 285 ± 13.9 g). ‘Haldane’ had the lowest shoot and root fresh mass, and the lowest shoot dry mass, making it the lowest yielding cultivar (shoot fresh mass = 95 ± 3.1 g). The average yield of all cultivars was 162.4 ± 63.1 g. ‘Klee’ had the most leaves (74 ± 2.6 per plant), whereas ‘Flandria’ had the least (34 ± 0.9 per plant).

Leaf gas exchange.

Healthy leaves without tipburn were selected for gas exchange measurements, including Pn, transpiration, water use efficiency (WUE) (equation: WUE = Pn/E, where E is transpiration), and stomatal conductance (gs) (Table 4). Significant differences in these values occurred only for measures of Pn, and they ranged from 7.0 ± 1.1 (‘Rouxai’) to 11.9 ± 1.4 (‘Cecilia’) mmol⋅m–2⋅s–1. Photosynthetic rate was not correlated with fresh or dry shoot mass, and there were no differences in Pn found between red- and green-leaf cultivars.

Table 4.

Mean ± standard error for measured calcium (Ca) concentration, tipburn incidence, tipburn severity, and gas exchange measurements.

Table 4.

Tissue calcium.

Inner and outer leaf samples in experimental repeats 2, 3, and 4 were assessed for elemental concentrations including Ca. Inner leaves were found to have a lower leaf tissue Ca concentration than outer leaves in each cultivar (Table 4). The ratio of Ca concentration in the inner and outer leaves was not significantly different among cultivars and averaged 0.33 ± 0.02 (mean ± standard error) (Supplemental Fig. 1).

Tipburn incidence, emergence, and severity.

Of all 560 lettuce plants grown in this study, 86.3% had tipburn symptoms (incidence) at the time of harvest. Tipburn incidence varied among cultivars, from 49% of individual plants with tipburn symptoms (‘Rouxai’) to 100% (‘Kalat’ and ‘Tuccadona’) (Table 4).

Tipburn emergence and severity at harvest varied among cultivars (Table 4). ‘Tuccadona’ had the earliest emergence of tipburn symptoms, at 20.7 ± 2.8 DAT, whereas ‘Rouxai’ developed visible symptoms at 27.2 ± 0.4 DAT. The average tipburn emergence for all cultivars was 22.2 ± 2.6 DAT, or 22.0 ± 2.5 DAT when ‘Rouxai’ is excluded. ‘Klee’ had the most severe tipburn expression, with 40.5 ± 3.5% of leaves showing tipburn at the time of harvest (28 DAT). ‘Rouxai’ had the least amount of tipburn, at 7.1 ± 10.8% of leaves. The average tipburn severity for all cultivars was 23.8 ± 16.9% of all leaves, or 25.7 ± 16.4% when ‘Rouxai’ is excluded.

Discussion

Leaf gas exchange.

Although all three types of cultivars had similar ranges of Pn, romaine cultivars Claudius, Rafael, and Tuccadona had significantly greater fresh and dry shoot mass compared with butterhead and leafy types, which had similar biomass. It is likely that differences in cultivar yield are linked closely to morphology, and the tall but also wide structure of leaf development in romaine lettuce types allowed significantly greater photon capture than shorter, compact butterhead or leaf-type counterparts. Johnson et al. (2017) similarly reported greater yields for four romaine cultivars over eight butterhead, four crisphead, and 12 leaf-type lettuce cultivars grown hydroponically in a high tunnel.

We found that red-leaf lettuce cultivars did not differ significantly in Pn or yield from green-leaf cultivars (data not shown). Red-leaf lettuce produces more anthocyanins and pigments than green lettuce, partitioning more resources toward production of these compounds even within the same cultivar, leading to a reduction in both Pn and yield (Carillo et al. 2020). Although we did not observe differences during our study, it is likely that we would also observe greater Pn among the red-leaf cultivars we grew if we had selected a different lighting spectrum that limited anthocyanin production.

Measures of gs, transpiration, and WUE did not vary among cultivars in this experiment (Table 4). A greater value of transpiration would indicate that more Ca is being transported throughout the plant, and we would expect reduced tipburn incidence. Many have found that increasing transpiration through targeted downward airflow can greatly reduce or eliminate tipburn (Ahmed et al. 2020, 2022; Frantz et al. 2004; Goto and Takakura 1992), as does the reduction of aerial humidity (Collier and Tibbitts 1984). A greater gs value is indicative of greater transpiration, as these two values are closely correlated (Ahmed et al. 2022). Furthermore, a lower value for WUE would indicate that transpiration is relatively high compared with Pn, suggesting that Ca transport is more likely to be adequate to prevent tipburn. Although we did not see significant differences in these values, each of which may indicate tipburn risk, we did observe a large range of tipburn incidence, emergence, and severity (Table 4) among the tested cultivars. We believe that those cultivars with a greater tipburn incidence, later tipburn emergence, and greater tipburn severity can be considered higher risk cultivars to grow than those with opposite trends. Because gas exchange did not vary, except for Pn, the relative risk of these cultivars may be linked genetically and may not be heavily influenced by environmental variation or error in our study.

Tissue calcium.

In this experiment, the inner leaves of lettuce were found to have a lower Ca concentration than outer leaves, which agrees with previous reports (Barta and Tibbitts 1986; Collier and Tibbitts 1984; Sago 2016). The oldest leaves of the lettuce head are known to have the greatest Ca concentration, with each newly initiated leaf having a linear decrease in Ca concentration (Collier and Huntington 1983; Sago 2016). A low air speed limits the transpiration rate, reducing the Ca supply and increasing tipburn risk for young leaves. The low air speed (< 0.1 m⋅s–1 in the horizontal and vertical directions) in this experiment combined with low daytime VPD (Table 1) resulted in low evaporation, as demonstrated by the petri- and deep-dish tests. A limited evaporation rate measured by these tools can indicate limited lettuce leaf transpiration (Papio 2021) and therefore Ca transport. This is especially true near the meristem, where the boundary layer experiences little agitation as a result of the crowding of mature leaves. The environmental conditions selected create a fast-growing environment, which drives the demand for Ca further. Under this condition, demand for Ca is high, whereas transportation of Ca is low. Although Ca concentration is demonstrated to decline with each newly initiated leaf, we believe the combination of the fast growth rate and low transpiration condition caused young leaves (Fig. 1) to have significantly less Ca accumulation than would be expected. As a result, inner leaves had roughly one-third the leaf Ca concentration of outer leaves (Fig. 2), leading to severe tipburn for most cultivars.

Fig. 1.
Fig. 1.

Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. inner leaf calcium concentration (measured in grams per kilogram dry leaves) of the same sampled plants from experimental replications 2, 3, and 4 (n = 31). Error bars are standard error.

Citation: HortScience 58, 10; 10.21273/HORTSCI17313-23

Fig. 2.
Fig. 2.

Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. outer leaf calcium concentration (measured in grams per kilogram dry leaves) of the same sampled plants from experimental replications 2, 3, and 4 (n = 70). Error bars are standard error.

Citation: HortScience 58, 10; 10.21273/HORTSCI17313-23

Tipburn incidence, emergence, and severity.

Tipburn incidence, emergence, and severity varied within reported cultivars both within and among experimental repeats. This produced a wide range of values, which are reflected in Table 4. Variation in plant growth values were also found within and among experimental repeats for all reported cultivars (Table 3). In controlled environments, uniformity of aerial conditions, including light, temperature, VPD, and CO2, can affect the growth rate of plants at various stages. Microclimatic variations in the environment (Table 1), especially PPFD and VPD, could contribute to differences in plant growth and tipburn symptomology. However, it is also likely that genetic variation within cultivars influenced plant growth and tipburn risk, as reported by Beacham et al. (2023) in a study evaluating tipburn susceptibility of 20 lettuce accessions. Therefore, it is likely that a combination of genetic variation and microclimatic variation led to differences in plant growth and tipburn symptomology within our experiment.

Correlations of tipburn sensitivity with growth parameters, cultivar type, recommended production systems, and tissue Ca concentrations.

Some analyses have found that greater yielding lettuce cultivars have a greater tipburn risk (Wissemeier and Zühlke 2002). However, in the experiment by Wissemeier and Zühlke (2002), greater yield and tipburn occurred when sunlight radiation was greater. In our experiment, shoot fresh mass within cultivars correlated significantly with tipburn severity (Fig. 3). We believe that microclimatic variations of light intensity and environmental conditions were not great enough to cause large differences in tipburn severity within observations of each cultivar. Rather, this variation could be attributed to variation in plant growth and tipburn of individual plants under similar environmental and light conditions. Although this variation could help explain differences in tipburn, neither fresh nor dry mass of shoots or roots, or the root-to-shoot ratio within each cultivar, correlated with tipburn severity (Tables 3 and 4, Fig. 4). Therefore, it appears that individual plant variation within the same cultivar could produce a range of tipburn risk (e.g., severity). However, each cultivar’s ability to support growth sufficiently determined the overall tipburn risk, and the high-yielding trait alone does not increase tipburn severity (Fig. 4). The growth rate of lettuce increases exponentially during the final 2 weeks of growth (5–6 weeks after seeding), which requires more Ca transport to meet the growing demand. This leads to greater rates of tipburn severity within cultivars when plant growth is promoted (Fig. 3). For example, ‘Klee’ was the eighth highest-yielding cultivar, but first in tipburn severity, whereas the highest-yielding cultivar Tuccadona was third in tipburn severity. Therefore, yield is only a good predictor of tipburn risk within, but not among, cultivars.

Fig. 3.
Fig. 3.

Shoot fresh mass (measured in grams) vs. tipburn severity (percentage of leaves) for all 10 cultivars. Regression lines are significant by analysis of variance. Significant P values (α ≤ 0.05) and R2 reported.

Citation: HortScience 58, 10; 10.21273/HORTSCI17313-23

Fig. 4.
Fig. 4.

Shoot fresh mass (measured in grams) vs. tipburn severity (percentage of leaves) for all 10 cultivars. Error bars are standard error. Regression analysis is nonsignificant.

Citation: HortScience 58, 10; 10.21273/HORTSCI17313-23

Gas exchange measurements of Pn, transpiration, gs, and WUE had no significant relationship with tipburn incidence or severity (Table 4). Plants with adequate capacity to move Ca through transpiration can produce biomass effectively to support the plant growth rate without tipburn risk. A cultivar’s capacity to transport Ca relies on the genetics of that cultivar as well as the environmental conditions, reflecting the results of tipburn susceptibility of different cultivars in different geographic locations as reported by Lafta et al. (2021) and Jenni and Hayes (2010). For each cultivar, the transpiration rate to supply Ca must be adequate to support leaf expansion, which may vary among the genetics of each cultivar. However, we found no association of tipburn risk with the measured gas exchange of sampled plants. Although average gas exchange did not vary significantly among cultivars (except for Pn) (Table 4), we also found that a linear regression analysis of transpiration and inner leaf Ca concentrations did not correlate with tipburn severity (data not shown). Therefore, it is likely that the amount of Ca required for each cultivar to support adequate growth varies among cultivars, as does the rate of transpiration that may supply adequate Ca.

There were no significant correlations between tipburn incidence or severity with lettuce type (morphology) (data not shown). Although morphologically different, all lettuce cultivars did demonstrate tipburn regardless of whether the leaves enclosed the meristem. ‘Klee’ had the greatest tipburn severity, yet the shoot tip was plainly visible and unobstructed throughout harvest, whereas ‘Rouxai’ had the lowest severity and a fully enclosed shoot tip. Practically, it has been proposed that leaves enclosing the shoot tip may cause or worsen lettuce tipburn (Barta and Tibbitts 2000). Although we agree that leaves enveloping the shoot tip can limit transpiration of young, expanding leaves, leading to worsening tipburn symptoms, we found that morphology alone is not a predictor of tipburn risk (data not shown).

There was no effect between lettuce leaf color and tipburn incidence, emergence, or severity. Greater lettuce productivity would indicate that green lettuce types have a greater tipburn risk, although we did not find that tipburn incidence or severity was different between lettuce of different colors. Jenni et al. (2013) did find that red-leaf lettuce cultivars had a lower tipburn incidence than green-leaf cultivars in the open field across multiple locations. Within a controlled environment, lettuce typically produces significantly less pigmentation than in the open field, which could account for this difference (Brücková et al. 2016). Therefore, lettuce color appears not to be a good predictor of tipburn risk within controlled environments as a result of a reduction in total anthocyanin concentrations. Rather, tipburn sensitivity in a controlled environment is most associated with the genotype of each cultivar.

The 10 cultivars grown in our experiment were originally recommended for outdoor (open-field) production systems, indoor (greenhouse or vertical farm) systems, or both according to Rijk Zwaan (Table 2). As we expected, cultivars recommended for indoor production systems had a lower percentage of leaves with tipburn at the time of harvest than those recommended for outdoor or both types of systems (P < 0.0001; Fig. 5). Regardless for which production system cultivars were recommended, tipburn emergence was similar among each group (22.2 ± 2.6 d; mean ± SD). Commonly, seed companies recommend tipburn-resistant cultivars based on greenhouse cultivation trials (HB, personal communication). However, environmental conditions of IFs may permit faster growth rates than those of greenhouses, increasing tipburn risk. Furthermore, greenhouses may also feature enhanced air circulation and a greater sunlight spectrum, which drives more transpiration than electric lighting (Nelson and Bugbee 2015) to reduce tipburn risk. Therefore, it is likely that there are fewer cultivars appropriate for IF-specific production than those recommended for greenhouse production.

Fig. 5.
Fig. 5.

Tipburn severity (percentage of leaves with tipburn symptoms at harvest) vs. the suggested production system for the 10 cultivars used in this experiment (n = 280). Boxplots represent the median (line in box), quartiles (upper and lower bounds of box), and maximum and minimum values (whiskers). Tukey’s honestly significant difference letter report significant at P < 0.0001.

Citation: HortScience 58, 10; 10.21273/HORTSCI17313-23

For the plants used for Ca analysis (n = 51), greater cultivar-average Ca concentrations of inner leaves resulted in later tipburn emergence (Fig. 1; P = 0.018). To delay tipburn emergence by 1 d, inner leaves would require 0.12 g⋅kg–1 more Ca. The same analysis of cultivar-specific outer leaf Ca content showed a weaker trend of increasing the number of days to tipburn incidence (Fig. 2; P = 0.01), but this is not representative of the tipburn-affected inner leaves because this value reflects whole-plant transpiration. Therefore, we do not believe outer leaf Ca concentrations should be evaluated to determine tipburn risk. Similarly, the ratio of inner to outer leaf Ca concentrations correlated loosely (Supplemental Fig. 1; P = 0.085) with tipburn incidence. However, because outer leaf Ca has no correlation with inner leaf Ca concentration (data not shown), we do not think this analysis is representative of Ca requirements to prevent tipburn.

The ability of each cultivar to drive xylem transport of Ca is linked to genotype, environment, and genotype × environment interactions when comparing cultivars across multiple open-field locations (Jenni and Hayes 2010; Lafta et al. 2021). In our experiment, leaf tissue Ca concentration for inner and outer leaves varied among and within cultivars, but the inner-to-outer Ca ratio was similar. Variation across genotype alone would produce clusters of inner and outer Ca concentration data points for each cultivar. However, variation by environment resulted in a wide distribution of data points within cultivars (represented by horizontal error bars in Figs. 1, 2, and Supplemental Fig. 1). Inner leaf Ca was highly variable in our experiment, suggesting that inner leaf Ca transport is highly linked to the microclimate varying both spatially and temporally, as discussed earlier. Although inner leaf Ca concentrations had a large variation, tipburn emergence and severity had little variation (Table 4). Therefore, it is difficult to propose a target inner leaf Ca concentration for specific cultivars to avoid tipburn entirely, because the required amount of Ca varies considerably by genotype, environment, and the genotype × environment interaction. A sufficient cultivar-specific leaf Ca concentration to reduce tipburn risk under one condition may not be adequate under a different environmental condition. Instead of targeting a specific Ca concentration, steps should be taken to enhance Ca transport to the inner leaves to meet the demand of growth. For example, targeted airflow to the inner leaves increases xylem-driven Ca transport to decrease tipburn risk under any condition, as has been demonstrated by others (Ahmed et al. 2020; Frantz et al. 2004; Goto and Takakura 1992; Lee et al. 2013).

Conclusion

Tipburn sensitivity is an important characteristic of lettuce cultivars for IF producers. Currently, the evaluation of tipburn sensitivity seems to take place under greenhouse conditions that do not induce tipburn as severely as conditions within IFs. In our experiment, we assessed tipburn emergence (days to the onset of tipburn after transplant) and severity (percentage of leaves with tipburn symptoms at the time of harvest) of 10 commercially available cultivars under a tipburn-inducing growing condition similar to IFs within growth chambers. Our environmental condition was designed to achieve high growth rates (and Ca demand) while limiting transpiration during the day and night to promote Ca deficiency. All cultivars grown in our experiment, and most individual plants (86%), had tipburn at the time of harvest, demonstrating that the selected environmental conditions were effective in inducing tipburn in lettuce. Although tipburn sensitivity was cultivar specific, none of the growth or morphological characteristics of the cultivars was attributable to tipburn sensitivity. However, the recommended production system was predictive of tipburn severity risk. Cultivars with the ability to transport more Ca under this condition had greater concentrations in the inner leaves and were found to have delayed tipburn incidence, but not reduced tipburn severity. This indicates that the tissue Ca requirement to prevent tipburn is cultivar specific, highly related to growth rate, and different among microclimates and likely other growing conditions. However, tipburn risk should generally be reduced when conditions favor enhanced transpiration of the inner leaves to promote Ca transport, as others have reported (Ahmed et al. 2020; Frantz et al. 2004; Goto and Takakura 1992; Lee et al. 2013). We recommend that lettuce marketed or developed for IFs be evaluated and reported publicly using environmental conditions promoting fast growth, but limiting transpiration, to provide an adequate comparison of tipburn risk among cultivars.

References Cited

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    • Search Google Scholar
    • Export Citation
  • Ahmed HA, Yu-Xin T, Qi-Chang Y. 2020. Optimal control of environmental conditions affecting lettuce plant growth in a controlled environment with artificial lighting: A review. S Afr J Bot. 130:7589. https://doi.org/10.1016/j.sajb.2019.12.018.

    • Search Google Scholar
    • Export Citation
  • Barta DJ, Tibbitts TW. 1986. Effects of artificial enclosure of young lettuce leaves on tipburn incidence and leaf calcium concentration. J Am Soc Hortic Sci. 111(3):413416.

    • Search Google Scholar
    • Export Citation
  • Barta DJ, Tibbitts TW. 2000. Calcium localization and tipburn development in lettuce leaves during early enlargement. J Am Soc Hortic Sci. 125(3):294298. https://doi.org/10.21273/jashs.125.3.294.

    • Search Google Scholar
    • Export Citation
  • Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw. 67(1):148. https://doi.org/10.18637/jss.v067.i01.

    • Search Google Scholar
    • Export Citation
  • Beacham AM, Hand P, Teakle GR, Barker GC, Pink DAC, Monaghan JM. 2023. Tipburn resilience in lettuce (Lactuca spp.): The importance of germplasm resources and production system‐specific assays. J Sci Food Agric. 103(9):44814488. https://doi.org/10.1002/jsfa.12523.

    • Search Google Scholar
    • Export Citation
  • Both AJ, Albright LD, Langhans RW, Reiser RA, Vinzant BG. 1997. Hydroponic lettuce production influenced by integrated supplemental light levels in a controlled environment agriculture facility: Experimental results. Acta Hortic. 418:4552. https://doi.org/10.17660/ActaHortic.1997.418.5.

    • Search Google Scholar
    • Export Citation
  • Brumm I, Schenk M. 1993. Influence of nitrogen supply on the occurrence of calcium deficiency in field grown lettuce. Acta Hortic. 339:125136. https://doi.org/10.17660/ActaHortic.1993.339.11.

    • Search Google Scholar
    • Export Citation
  • Brücková K, Sytar O, Ţivčák M, Brestic M, Lebeda A. 2016. The effect of growth conditions on flavonols and anthocyanins accumulation in green and red lettuce. J Cent Eur Agric. 17(4):986997. https://doi.org/10.5513/JCEA01/17.4.1802.

    • Search Google Scholar
    • Export Citation
  • Caplan B. 2018. Optimizing carbon dioxide concentration and daily light integral combination in a multi-level electrically lighted lettuce production system (Masters thesis). University of Arizona, Tucson, AZ, USA.

  • Carillo P, Giordano M, Raimondi G, Napolitano F, Di Stasio E, Kyriacou MC, Sifola MI, Rouphael Y. 2020. Physiological and nutraceutical quality of green and red pigmented lettuce in response to NaCl concentration in two successive harvests. Agronomy (Basel). 10(9):1358. https://doi.org/10.3390/agronomy10091358.

    • Search Google Scholar
    • Export Citation
  • Collier GF, Huntington VC. 1983. The relationship between leaf growth, calcium accumulation and distribution, and tipburn development in field-grown butterhead lettuce. Sci Hortic. 21(2):123128. https://doi.org/10.1016/0304-4238(83)90157-7.

    • Search Google Scholar
    • Export Citation
  • Collier GF, Tibbitts TW. 1984. Effects of relative humidity and root temperature on calcium concentration and tipburn development in lettuce. J Am Soc Hortic Sci. 109(2):128131.

    • Search Google Scholar
    • Export Citation
  • de Mendiburu F. 2019. agricolae: Statistical procedures for agricultural research. R package. Lima, Peru.

  • Frantz JM, Ritchie G, Cometti NN, Robinson J, Bugbee B. 2004. Exploring the limits of crop productivity: Beyond the limits of tipburn in lettuce. J Am Soc Hortic Sci. 129(3):331338. https://doi.org/10.21273/jashs.129.3.0331.

    • Search Google Scholar
    • Export Citation
  • Geelen PAM, Voogt JO, van Weel PM. 2018. Plant empowerment: The basic principles. Letsgrow, Vlaardingen, Netherlands.

  • Goto E, Takakura T. 1992. Prevention of lettuce tipburn by supplying air to inner leaves. Am Soc Agric Eng. 35(2):641645.

  • Jenni S, Hayes RJ. 2010. Genetic variation, genotype × environment interaction, and selection for tipburn resistance in lettuce in multi-environments. Euphytica. 171(3):427439. https://doi.org/10.1007/s10681-009-0075-5.

    • Search Google Scholar
    • Export Citation
  • Jenni S, Truco MJ, Michelmore RW. 2013. Quantitative trait loci associated with tipburn heat stress induced physiological disorders and maturity traits in crisphead lettuce. Theor Appl Genet. 126:30653079. https://doi.org/10.1007/s00122-013-2193-7.

    • Search Google Scholar
    • Export Citation
  • Johnson GE, Buzby KM, Semmens KJ, Holaskova I, Waterland NL. 2017. Evaluation of lettuce between spring water, hydroponic, and flow-through aquaponic systems. Int J Veg Sci. 23(5):456470. https://doi.org/10.1080/19315260.2017.1319888.

    • Search Google Scholar
    • Export Citation
  • Kozai T, Niu G, Masabni J (eds). 2022. Plant factory: Basics, applications and advances. Academic Press, London, UK.

  • Lafta A, Sandoya G, Mou B. 2021. Genetic variation and genotype by environment interaction for heat tolerance in crisphead lettuce. HortScience. 56(2):126135. https://doi.org/10.21273/HORTSCI15209-20.

    • Search Google Scholar
    • Export Citation
  • Lee JG, Choi CS, Jang YA, Jang SW, Lee SG, Um YC. 2013. Effects of air temperature and air flow rate control on the tipburn occurrence of leaf lettuce in a closed type plant factory system. Hortic Environ Biotechnol. 54:303310. https://doi.org/10.1007/s13580-013-0031-0.

    • Search Google Scholar
    • Export Citation
  • Mempel H, Jüttner I, Wittmann S. 2021. The potentials of indoor farming for plant production. AUTO 69(4):287296. https://doi.org/10.1515/auto-2020-0044.

    • Search Google Scholar
    • Export Citation
  • Nelson JA, Bugbee B. 2015. Analysis of environmental effects on leaf temperature under sunlight, high pressure sodium and light emitting diodes. PLoS One. 10(10):e0138930. https://doi.org/10.1371/journal.pone.0138930.

    • Search Google Scholar
    • Export Citation
  • Papio GA. 2021. Development of a new hydroponic nutrient management strategy and a tool to assess microclimate conditions in indoor leafy green production (Masters thesis). Ohio State University, Columbus, OH, USA.

  • Park MH, Lee YB. 2001. Effects of CO2 concentration, light intensity and nutrient level on growth of leaf lettuce in a plant factory. Acta Hortic. 548:377384. https://doi.org/10.17660/ActaHortic.2001.548.43.

    • Search Google Scholar
    • Export Citation
  • Petrazzini LL, Souza GA, Rodas CL, Emrich EB, Carvalho JG, Souza RJ. 2014. Nutritional deficiency in crisphead lettuce grown in hydroponics. Hortic Bras. 32:310313.

    • Search Google Scholar
    • Export Citation
  • Sago Y. 2016. Effects of light intensity and growth rate on tipburn development and leaf calcium concentration in butterhead lettuce. HortScience. 51(9):10871091. https://doi.org/10.21273/HORTSCI10668-16.

    • Search Google Scholar
    • Export Citation
  • Seginer I, Shina G, Albright LD, Marsh LS. 1991. Optimal temperature setpoints for greenhouse lettuce. J Agric Eng Res. 49:209226. https://doi.org/10.1016/0021-8634(91)80040-L.

    • Search Google Scholar
    • Export Citation
  • Shibata T, Iwao K, Takano T. 1995. Effect of vertical air flowing on lettuce growing in a plant factory. Acta Hortic. 399:175182. https://doi.org/10.17660/ActaHortic.1995.399.20.

    • Search Google Scholar
    • Export Citation
  • Specht K, Siebert R, Hartmann I, Freisinger UB, Henckel D, Walk H, Dierich A. 2014. Urban agriculture of the future: an overview of sustainability aspects of food production in and on buildings. Agric Human Values. 31:3351. https://doi.org/10.1007/s10460-013-9448-4.

    • Search Google Scholar
    • Export Citation
  • Takagaki M, Hara H, Kozai T. 2020. Micro- and mini PFALS for improving the quality of life in urban areas, p 91–104. In: Kozai T, Niu G, Takagaki M (eds). Plant factory: An indoor vertical farming system for efficient quality food production. Academic Press, San Diego, CA, USA. https://doi.org/10.1016/B978-0-12-816691-8.00006-6.

  • Vanhassel P, Bleyaert P, Van Lommel J, Vandevelde I, Crappé S, Van Hese N, Hanssens J, Steppe K, Van Labeke MC. 2015. Rise of nightly air humidity as a measure for tipburn prevention in hydroponic cultivation of butterhead lettuce. Acta Hortic. 1107:195201. https://doi.org/10.17660/ActaHortic.2015.1107.26.

    • Search Google Scholar
    • Export Citation
  • Wickham H. 2016. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York, NY, USA.

  • Wissemeier AH, Zühlke G. 2002. Relation between climatic variables, growth and the incidence of tipburn in field-grown lettuce as evaluated by simple, partial and multiple regression analysis. Sci Hortic. 93(3–4):193204.

    • Search Google Scholar
    • Export Citation

Supplemental Fig. 1.
Supplemental Fig. 1.

Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. the ratio of the inner to outer leaf calcium (Ca) concentration (dry leaf ratio) of the same sampled plants from experimental replications 2, 3, and 4 (n = 70). Error bars are standard error.

Citation: HortScience 58, 10; 10.21273/HORTSCI17313-23

  • Fig. 1.

    Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. inner leaf calcium concentration (measured in grams per kilogram dry leaves) of the same sampled plants from experimental replications 2, 3, and 4 (n = 31). Error bars are standard error.

  • Fig. 2.

    Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. outer leaf calcium concentration (measured in grams per kilogram dry leaves) of the same sampled plants from experimental replications 2, 3, and 4 (n = 70). Error bars are standard error.

  • Fig. 3.

    Shoot fresh mass (measured in grams) vs. tipburn severity (percentage of leaves) for all 10 cultivars. Regression lines are significant by analysis of variance. Significant P values (α ≤ 0.05) and R2 reported.

  • Fig. 4.

    Shoot fresh mass (measured in grams) vs. tipburn severity (percentage of leaves) for all 10 cultivars. Error bars are standard error. Regression analysis is nonsignificant.

  • Fig. 5.

    Tipburn severity (percentage of leaves with tipburn symptoms at harvest) vs. the suggested production system for the 10 cultivars used in this experiment (n = 280). Boxplots represent the median (line in box), quartiles (upper and lower bounds of box), and maximum and minimum values (whiskers). Tukey’s honestly significant difference letter report significant at P < 0.0001.

  • Supplemental Fig. 1.

    Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. the ratio of the inner to outer leaf calcium (Ca) concentration (dry leaf ratio) of the same sampled plants from experimental replications 2, 3, and 4 (n = 70). Error bars are standard error.

  • Ahmed HA, Li Y, Shao L, Tong Y. 2022. Effect of light intensity and air velocity on the thermal exchange of indoor-cultured lettuce. Hortic Environ Biotechnol. 63(3):375390. https://doi.org/10.1007/s13580-021-00410-6.

    • Search Google Scholar
    • Export Citation
  • Ahmed HA, Yu-Xin T, Qi-Chang Y. 2020. Optimal control of environmental conditions affecting lettuce plant growth in a controlled environment with artificial lighting: A review. S Afr J Bot. 130:7589. https://doi.org/10.1016/j.sajb.2019.12.018.

    • Search Google Scholar
    • Export Citation
  • Barta DJ, Tibbitts TW. 1986. Effects of artificial enclosure of young lettuce leaves on tipburn incidence and leaf calcium concentration. J Am Soc Hortic Sci. 111(3):413416.

    • Search Google Scholar
    • Export Citation
  • Barta DJ, Tibbitts TW. 2000. Calcium localization and tipburn development in lettuce leaves during early enlargement. J Am Soc Hortic Sci. 125(3):294298. https://doi.org/10.21273/jashs.125.3.294.

    • Search Google Scholar
    • Export Citation
  • Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw. 67(1):148. https://doi.org/10.18637/jss.v067.i01.

    • Search Google Scholar
    • Export Citation
  • Beacham AM, Hand P, Teakle GR, Barker GC, Pink DAC, Monaghan JM. 2023. Tipburn resilience in lettuce (Lactuca spp.): The importance of germplasm resources and production system‐specific assays. J Sci Food Agric. 103(9):44814488. https://doi.org/10.1002/jsfa.12523.

    • Search Google Scholar
    • Export Citation
  • Both AJ, Albright LD, Langhans RW, Reiser RA, Vinzant BG. 1997. Hydroponic lettuce production influenced by integrated supplemental light levels in a controlled environment agriculture facility: Experimental results. Acta Hortic. 418:4552. https://doi.org/10.17660/ActaHortic.1997.418.5.

    • Search Google Scholar
    • Export Citation
  • Brumm I, Schenk M. 1993. Influence of nitrogen supply on the occurrence of calcium deficiency in field grown lettuce. Acta Hortic. 339:125136. https://doi.org/10.17660/ActaHortic.1993.339.11.

    • Search Google Scholar
    • Export Citation
  • Brücková K, Sytar O, Ţivčák M, Brestic M, Lebeda A. 2016. The effect of growth conditions on flavonols and anthocyanins accumulation in green and red lettuce. J Cent Eur Agric. 17(4):986997. https://doi.org/10.5513/JCEA01/17.4.1802.

    • Search Google Scholar
    • Export Citation
  • Caplan B. 2018. Optimizing carbon dioxide concentration and daily light integral combination in a multi-level electrically lighted lettuce production system (Masters thesis). University of Arizona, Tucson, AZ, USA.

  • Carillo P, Giordano M, Raimondi G, Napolitano F, Di Stasio E, Kyriacou MC, Sifola MI, Rouphael Y. 2020. Physiological and nutraceutical quality of green and red pigmented lettuce in response to NaCl concentration in two successive harvests. Agronomy (Basel). 10(9):1358. https://doi.org/10.3390/agronomy10091358.

    • Search Google Scholar
    • Export Citation
  • Collier GF, Huntington VC. 1983. The relationship between leaf growth, calcium accumulation and distribution, and tipburn development in field-grown butterhead lettuce. Sci Hortic. 21(2):123128. https://doi.org/10.1016/0304-4238(83)90157-7.

    • Search Google Scholar
    • Export Citation
  • Collier GF, Tibbitts TW. 1984. Effects of relative humidity and root temperature on calcium concentration and tipburn development in lettuce. J Am Soc Hortic Sci. 109(2):128131.

    • Search Google Scholar
    • Export Citation
  • de Mendiburu F. 2019. agricolae: Statistical procedures for agricultural research. R package. Lima, Peru.

  • Frantz JM, Ritchie G, Cometti NN, Robinson J, Bugbee B. 2004. Exploring the limits of crop productivity: Beyond the limits of tipburn in lettuce. J Am Soc Hortic Sci. 129(3):331338. https://doi.org/10.21273/jashs.129.3.0331.

    • Search Google Scholar
    • Export Citation
  • Geelen PAM, Voogt JO, van Weel PM. 2018. Plant empowerment: The basic principles. Letsgrow, Vlaardingen, Netherlands.

  • Goto E, Takakura T. 1992. Prevention of lettuce tipburn by supplying air to inner leaves. Am Soc Agric Eng. 35(2):641645.

  • Jenni S, Hayes RJ. 2010. Genetic variation, genotype × environment interaction, and selection for tipburn resistance in lettuce in multi-environments. Euphytica. 171(3):427439. https://doi.org/10.1007/s10681-009-0075-5.

    • Search Google Scholar
    • Export Citation
  • Jenni S, Truco MJ, Michelmore RW. 2013. Quantitative trait loci associated with tipburn heat stress induced physiological disorders and maturity traits in crisphead lettuce. Theor Appl Genet. 126:30653079. https://doi.org/10.1007/s00122-013-2193-7.

    • Search Google Scholar
    • Export Citation
  • Johnson GE, Buzby KM, Semmens KJ, Holaskova I, Waterland NL. 2017. Evaluation of lettuce between spring water, hydroponic, and flow-through aquaponic systems. Int J Veg Sci. 23(5):456470. https://doi.org/10.1080/19315260.2017.1319888.

    • Search Google Scholar
    • Export Citation
  • Kozai T, Niu G, Masabni J (eds). 2022. Plant factory: Basics, applications and advances. Academic Press, London, UK.

  • Lafta A, Sandoya G, Mou B. 2021. Genetic variation and genotype by environment interaction for heat tolerance in crisphead lettuce. HortScience. 56(2):126135. https://doi.org/10.21273/HORTSCI15209-20.

    • Search Google Scholar
    • Export Citation
  • Lee JG, Choi CS, Jang YA, Jang SW, Lee SG, Um YC. 2013. Effects of air temperature and air flow rate control on the tipburn occurrence of leaf lettuce in a closed type plant factory system. Hortic Environ Biotechnol. 54:303310. https://doi.org/10.1007/s13580-013-0031-0.

    • Search Google Scholar
    • Export Citation
  • Mempel H, Jüttner I, Wittmann S. 2021. The potentials of indoor farming for plant production. AUTO 69(4):287296. https://doi.org/10.1515/auto-2020-0044.

    • Search Google Scholar
    • Export Citation
  • Nelson JA, Bugbee B. 2015. Analysis of environmental effects on leaf temperature under sunlight, high pressure sodium and light emitting diodes. PLoS One. 10(10):e0138930. https://doi.org/10.1371/journal.pone.0138930.

    • Search Google Scholar
    • Export Citation
  • Papio GA. 2021. Development of a new hydroponic nutrient management strategy and a tool to assess microclimate conditions in indoor leafy green production (Masters thesis). Ohio State University, Columbus, OH, USA.

  • Park MH, Lee YB. 2001. Effects of CO2 concentration, light intensity and nutrient level on growth of leaf lettuce in a plant factory. Acta Hortic. 548:377384. https://doi.org/10.17660/ActaHortic.2001.548.43.

    • Search Google Scholar
    • Export Citation
  • Petrazzini LL, Souza GA, Rodas CL, Emrich EB, Carvalho JG, Souza RJ. 2014. Nutritional deficiency in crisphead lettuce grown in hydroponics. Hortic Bras. 32:310313.

    • Search Google Scholar
    • Export Citation
  • Sago Y. 2016. Effects of light intensity and growth rate on tipburn development and leaf calcium concentration in butterhead lettuce. HortScience. 51(9):10871091. https://doi.org/10.21273/HORTSCI10668-16.

    • Search Google Scholar
    • Export Citation
  • Seginer I, Shina G, Albright LD, Marsh LS. 1991. Optimal temperature setpoints for greenhouse lettuce. J Agric Eng Res. 49:209226. https://doi.org/10.1016/0021-8634(91)80040-L.

    • Search Google Scholar
    • Export Citation
  • Shibata T, Iwao K, Takano T. 1995. Effect of vertical air flowing on lettuce growing in a plant factory. Acta Hortic. 399:175182. https://doi.org/10.17660/ActaHortic.1995.399.20.

    • Search Google Scholar
    • Export Citation
  • Specht K, Siebert R, Hartmann I, Freisinger UB, Henckel D, Walk H, Dierich A. 2014. Urban agriculture of the future: an overview of sustainability aspects of food production in and on buildings. Agric Human Values. 31:3351. https://doi.org/10.1007/s10460-013-9448-4.

    • Search Google Scholar
    • Export Citation
  • Takagaki M, Hara H, Kozai T. 2020. Micro- and mini PFALS for improving the quality of life in urban areas, p 91–104. In: Kozai T, Niu G, Takagaki M (eds). Plant factory: An indoor vertical farming system for efficient quality food production. Academic Press, San Diego, CA, USA. https://doi.org/10.1016/B978-0-12-816691-8.00006-6.

  • Vanhassel P, Bleyaert P, Van Lommel J, Vandevelde I, Crappé S, Van Hese N, Hanssens J, Steppe K, Van Labeke MC. 2015. Rise of nightly air humidity as a measure for tipburn prevention in hydroponic cultivation of butterhead lettuce. Acta Hortic. 1107:195201. https://doi.org/10.17660/ActaHortic.2015.1107.26.

    • Search Google Scholar
    • Export Citation
  • Wickham H. 2016. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York, NY, USA.

  • Wissemeier AH, Zühlke G. 2002. Relation between climatic variables, growth and the incidence of tipburn in field-grown lettuce as evaluated by simple, partial and multiple regression analysis. Sci Hortic. 93(3–4):193204.

    • Search Google Scholar
    • Export Citation
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Contributor Notes

This work was supported financially by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture Specialty Crop Research Initiative (grant no. 2019-51181-30017).

We acknowledge and thank members of the Kubota lab and The Ohio State University Department of Horticulture and Crop Science, the members of the Optimia project, and the USDA for their support of this research.

C.K. is the corresponding author. E-mail: kubota.10@osu.edu.

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  • Fig. 1.

    Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. inner leaf calcium concentration (measured in grams per kilogram dry leaves) of the same sampled plants from experimental replications 2, 3, and 4 (n = 31). Error bars are standard error.

  • Fig. 2.

    Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. outer leaf calcium concentration (measured in grams per kilogram dry leaves) of the same sampled plants from experimental replications 2, 3, and 4 (n = 70). Error bars are standard error.

  • Fig. 3.

    Shoot fresh mass (measured in grams) vs. tipburn severity (percentage of leaves) for all 10 cultivars. Regression lines are significant by analysis of variance. Significant P values (α ≤ 0.05) and R2 reported.

  • Fig. 4.

    Shoot fresh mass (measured in grams) vs. tipburn severity (percentage of leaves) for all 10 cultivars. Error bars are standard error. Regression analysis is nonsignificant.

  • Fig. 5.

    Tipburn severity (percentage of leaves with tipburn symptoms at harvest) vs. the suggested production system for the 10 cultivars used in this experiment (n = 280). Boxplots represent the median (line in box), quartiles (upper and lower bounds of box), and maximum and minimum values (whiskers). Tukey’s honestly significant difference letter report significant at P < 0.0001.

  • Supplemental Fig. 1.

    Tipburn emergence (the number of days from transplant to visible tipburn symptomology) of sampled plants vs. the ratio of the inner to outer leaf calcium (Ca) concentration (dry leaf ratio) of the same sampled plants from experimental replications 2, 3, and 4 (n = 70). Error bars are standard error.

 

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