Nutrient Solution Application of a Calcium-mobilizing Biostimulant Mitigates Tipburn without Decreasing Biomass of Greenhouse Hydroponic Lettuce

Authors:
Kishan Biradar Department of Plant and Soil Sciences, University of Delaware, 531 South College Avenue, Newark, DE 19716, USA

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Qingwu Meng Department of Plant and Soil Sciences, University of Delaware, 531 South College Avenue, Newark, DE 19716, USA

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Abstract

Lettuce tipburn is a physiological disorder characterized by marginal necrosis and curling of inner, younger leaves caused by localized calcium deficiency, especially in low evapotranspiration environments that restrict mass flow and thus calcium mobility. Severe tipburn negatively affects the marketability and quality of greenhouse-grown hydroponic lettuce. We aimed to assess the effectiveness of a chemical-based, calcium-mobilizing biostimulant for mitigating lettuce tipburn when applied in hydroponic nutrient solutions. Butterhead lettuce (Lactuca sativa ‘Rex’) was grown indoors under warm-white light-emitting diodes at a mean photosynthetic photon flux density of 300 μmol⋅m−2⋅s−1 for 11 days. Subsequently, we transplanted seedlings into deep-water-culture hydroponic trays in a greenhouse at an air temperature of 24.6 ± 1.2 °C, relative humidity of 76.2% ± 7.4%, and 20-hour photoperiod with supplemental lighting from high-pressure sodium lamps. The plants were grown in nutrient solutions with and without the biostimulant codenamed CC US-2105 at two concentrations (22 and 220 μL⋅L−1). Data were collected from plant samples at three harvests at 14, 21, and 28 days after transplant (DAT). At 14 DAT, there was no tipburn under any treatments. Compared with the control, the biostimulant at 22 μL⋅L−1 increased shoot dry mass by 31%. At 21 DAT, the biostimulant at 220 μL⋅L−1 eliminated tipburn, and the biostimulant increased shoot fresh weight by 28%, irrespective of the concentration. At 28 DAT, despite sufficient calcium in the whole plant and the remaining nutrient solution, severe tipburn still occurred in plants that did not receive the biostimulant (control). Compared with the control, the biostimulant at the higher concentration of 220 μL⋅L−1 decreased the tipburn rating by 88% and the number of leaves with tipburn by 85%, increased the plant diameter by 11%, increased the total leaf number by six, and accumulated higher levels of manganese and zinc. In contrast, these parameters remained unaffected at the lower biostimulant concentration of 22 μL⋅L−1. At 28 DAT, shoot biomass was unaffected by the biostimulant. In conclusion, the calcium-mobilizing biostimulant is an effective strategy to mitigate hydroponic lettuce tipburn without decreasing biomass accumulation in greenhouse conditions.

Controlled-environment agriculture has enabled year-round cultivation of high-value, fresh, nutritious, and local food crops, including leafy vegetables, culinary herbs, and small fruits, inside greenhouses and indoor vertical farms. Lettuce (Lactuca sativa) is especially popular because of its high consumer demand, high harvest index, and short growth cycles. However, lettuce cultivation in controlled environments is limited by tipburn, which is a physiological disorder caused by localized calcium (Ca) deficiency (Lee et al. 2013). Characterized by symptoms including marginal necrosis and curling of the inner, younger leaves, tipburn negatively affects lettuce quality, marketability, and profitability. The symptoms occur mainly because of weak cell walls and/or excessive turgor pressure in the laticifer cells causing them to rupture (Frantz et al. 2004). As an essential plant macronutrient, Ca is indispensable to cell walls and the plant structure. Because it is not translocated from older leaves to newer leaves as the plant continues to grow (Kerton et al. 2009), symptoms of Ca deficiency first appear on emerging leaves. Similar physiological disorders related to localized Ca deficiency are observed in other horticultural crops, such as tipburn in Chinese cabbage (Brassica rapa ssp. pekinensis) (Wang et al. 2019) and brussels sprouts (Brassica oleracea) (Drost and Johnson 2020), black heart in celery (Apium graveolens) (Yahia et al. 2019), bitter pit in apple (Malus domestica) (De Freitas et al. 2010), spongy tissue in mango (Mangifera indica) (Ma et al. 2023), and blossom end rot in tomato (Solanum lycopersicum) (Hagassou et al. 2019).

Tipburn is typically caused by environmental factors and plant growth patterns that limit Ca availability in the actively growing tissue instead of the lack of sufficient Ca in the root zone. Additionally, Ca is not readily mobile in the phloem and is mainly transported through the xylem tissue by mass flow, which is primarily driven by transpiration and root pressure (Barta and Tibbitts 1986). High relative humidity during the day can increase tipburn occurrence and severity by decreasing the transpiration rate (Palzkill et al. 1980), whereas low humidity at night can increase tipburn occurrence and severity by decreasing root pressure and, thus, mass flow (Vanhassel et al. 2014). Lower daytime relative humidity reduces tipburn occurrence by increasing transpiration, thereby increasing Ca transport to young developing leaf tissues (Collier and Tibbitts 1984). Providing adequate airflow at the growing tip can reduce tipburn incidence by reducing boundary layer resistance around the leaf, thereby increasing the transpiration rate (Frantz et al. 2004; Zhang et al. 2016). Although mass flow facilitates the Ca supply, during the exponential growth phase of lettuce, the Ca demand at the growing meristem becomes increasingly high, which can exceed the Ca supply, thus eliciting localized Ca deficiency (Su et al. 2019). Therefore, lettuce plants are especially prone to tipburn under environmental conditions optimal for high plant growth rates, including high daily light integrals (DLIs) and temperature (Both et al. 1997; Lee et al. 2019; Sago 2016).

Current tipburn mitigation strategies are mainly centered around humidity and airflow control in addition to practices of slowing plant growth rates and early harvesting to avoid crop loss (Kaufmann 2023; Kubota et al. 2023). However, controlling relative humidity in greenhouses and vertical farms can be challenging because of ventilation limitations, variable environmental conditions, equipment performance, and energy overload (Van Delden et al. 2021; Weidner et al. 2021). Moreover, the growing tip of lettuce is often enclosed by surrounding leaves, which creates a microclimate of high humidity conducive to tipburn, regardless of the ambient humidity. Although using vertical airflow fans directly above plants is a common practice among greenhouse lettuce growers to increase transpiration at the growing tip and thus reduce tipburn, it is challenging to install these fans in indoor vertical farms because of limited headspace (Kubota 2016). Lowering the DLI and/or temperature to slow plant growth slows tipburn development but limits the grower’s ability to maximize yield potential and shorten crop cycles. Finally, although certain lettuce cultivars are marketed as “tipburn-tolerant,” tipburn can still occur with conducive environmental conditions and high plant growth rates.

Biostimulants are broadly defined beneficial substances to plant growth and health that can be derived from chemicals, bacteria, algae, seaweed, or plants. Their primary functions are to improve crop yield, nutrient use efficiency, secondary metabolite accumulation, and abiotic stress tolerance, which have been studied in lettuce production (Bulgari et al. 2019; Di Mola et al. 2019; El-Nakhel et al. 2023). For example, nutrient solution treatment with a biostimulant derived from extracts of sea bamboo (Ecklonia maxima), a type of kelp, at 2 and 4 mL⋅L−1 increased lettuce shoot fresh weight by 33% and 38%, respectively (Miceli et al. 2021). Extracts of the seaweed Ascophyllum nodosum improved lettuce biomass under salt stress, but not under nonsaline conditions (Guinan et al. 2012). Additionally, plant-derived protein hydrolysates applied as a combination of foliar and nutrient solution treatment increased lettuce biomass more than either treatment alone (Cristofano et al. 2021). Nonetheless, few biostimulants have been developed to mitigate lettuce tipburn in controlled-environment agriculture.

A potential alternative solution to tipburn is a chemical-based, water-soluble biostimulant product based on proprietary Ca mobility technology (codenamed CC US-2105 and hereafter referred to as 2105; Croda, Inc., New Castle, DE, USA). The objective of this study was to evaluate the efficacy of this Ca-mobilizing biostimulant for mitigating lettuce tipburn when applied in the hydroponic nutrient solution in greenhouse conditions. We hypothesized that adding this biostimulant to the hydroponic nutrient solution would improve Ca mobility within the plant, thereby reducing lettuce tipburn and improving produce quality without compromising biomass accumulation.

Materials and Methods

Seedling propagation.

Seeds of green butterhead lettuce ‘Rex’ (Johnny’s Selected Seeds, Winslow, ME, USA) were sown in rockwool cubes (one seed per cube; 25 × 25 × 40 mm; AO 25/40, Grodan, Milton, ON, Canada) that were premoistened with reverse-osmosis water and placed in trays. The trays were covered with transparent humidity domes in darkness for 4 d after sowing. Once humidity domes were removed on day 4, the seedlings were placed under sole-source lighting from warm-white light-emitting diode fixtures with an 11-h photoperiod at a mean photosynthetic photon flux density (PPFD) (400–700 nm) of 300 μmol⋅m−2⋅s−1. The seedlings were sub-irrigated with a nutrient solution [pH = 5.7–5.9; electrical conductivity (EC) = 1.2–1.4 dS⋅m−1] to supply the following nutrients (in mg⋅L−1): 125 N, 18 P, 138 K, 72 Ca, 48 Mg, 39 S, 1.8 Fe, 0.52 Mn, 0.56 Zn, 0.12 B, 0.47 Cu, and 0.13 Mo. The nutrient solution used from days 4 to 12 was prepared by dissolving a water-soluble base fertilizer (12N–2P–13K RO; JR Peters, Inc., Allentown, PA, USA) and magnesium sulfate (JR Peters, Inc.) sequentially in reverse-osmosis water. The pH and EC were measured with a portable meter (HI9814; Hanna Instruments, Smithfield, RI, USA).

Transplant and nutrient solution treatments.

On day 12, we transplanted 108 lettuce seedlings into six deep-water-culture hydroponic trays (122-cm length × 61-cm width × 20-cm depth) on concrete benches in a glass-glazed research greenhouse. Each hydroponic tray had a foam raft with 18 planting sites floating in a nutrient solution with a depth of 12 cm. The initial nutrient solution in each tray comprised the same two fertilizer parts as used for seedlings dissolved sequentially in 89.11 L of municipal water, which provided (in mg⋅L−1): 150 N, 22 P, 166 K, 88 Ca, 58 Mg, 47 S, 2.1 Fe, 0.63 Mn, 0.68 Zn, 0.15 B, 0.56 Cu, and 0.15 Mo. The pH of the initial nutrient solution in each tray was adjusted to 5.8 with commercial liquid buffering solutions pH Up and pH Down (General Hydroponics, Inc., Santa Rosa, CA, USA). The nutrient solution was not actively aerated.

Using a randomized complete block design, two greenhouse benches were designated as two experimental blocks (replications), with each containing three nutrient solution treatments with the same fertilizer inputs but different amounts of the biostimulant (2105). This chemical-based biostimulant contained a mixture of calcium ammonium nitrate, zinc nitrate, and ethoxylated branched C11–14, C13-rich alcohols (the specific chemical identity and exact percentage of composition were withheld as a trade secret). Plants were grown without (control) and with the biostimulant at two concentrations of 22 and 220 μL⋅L−1. To deliver the biostimulant before transplanting, after 500 mL of the nutrient solution from each tray was placed into a beaker, the specified volume of the biostimulant was added to the beaker. Once the combined solution was thoroughly mixed until fully dissolved, it was added back to the tray and thoroughly mixed with the rest of the nutrient solution. There were no further additions of water, fertilizers, or the biostimulant after transplanting. The nutrient solution was not replenished because the deep-water-culture hydroponic trays held sufficient nutrient solution volumes for the entire production phase.

Production phase and greenhouse environment.

After transplanting, plants were grown under sunlight with supplemental lighting from high-pressure sodium lamps, which turned on when the PPFD from sunlight was below a set threshold (≈925 μmol⋅m−2⋅s−1) to provide a 20-h photoperiod. In the middle of each greenhouse bench, we placed a full-spectrum quantum sensor (SQ-500; Apogee Instruments, Inc., Logan, UT, USA) to measure the PPFD and a temperature and relative humidity sensor (HOBO MX2301; Onset Computer Corporation, Bourne, MA, USA) to monitor the growing environment at 10-min logging intervals. During the production phase (between transplant and the last harvest), the DLI, air temperature, and relative humidity (mean±SD) were 22.7 ± 5.3 mol⋅m−2⋅d−1, 24.8 ± 2.5 °C, and 75.3% ± 10.4%, respectively, in block 1, and 22.3 ± 5.3 mol⋅m−2⋅d−1, 24.5 ± 2.4 °C, and 76.5% ± 10.6%, respectively, in block 2.

Data collection and analysis.

Four randomly selected plants per tray were harvested from each treatment and block for data collection at each of three time points: 14, 21, and 28 d after transplant (DAT). At each harvest, we photographed a representative plant from each treatment and block. Shoot fresh weight at harvest, shoot dry mass, and root dry mass after ≥5 d in a forced-air drying oven (SMO28–2; Sheldon Manufacturing, Inc., Cornelius, OR, USA) were recorded using an analytical balance. The plant diameter (longest horizontal distance between leaf peripheries) and root length (distance between the bottom of a rockwool cube and the root tip) were measured using a ruler. Each plant was also given a visual rating based on the severity of tipburn symptoms (scale of 0 to 5: 0 = no tipburn; 1 = mild tipburn; 3 = moderate tipburn; 5 = severe tipburn). The number of leaves with visible tipburn symptoms and the total number of leaves (≥5 cm in length) per plant were recorded to calculate the ratio of the former to the latter as an additional indicator of tipburn severity. The chlorophyll concentration index was measured at three random positions on the fifth most mature leaf of each plant using a handheld chlorophyll meter (MC-100, Apogee Instruments). Oven-dried whole-plant tissue samples from the last harvest were homogenized and nutrient solution samples were collected at the beginning and end of the experiment were submitted to an analytical laboratory (JR Peters, Inc.) for nutrient analysis. The symptomatic and nonsymptomatic plant tissues of each whole plant were mixed homogenously and not separated before nutrient analysis. The nutrient analysis was performed with an inductively coupled plasma atomic emission spectrometer for most nutrients and the combustion method for N according to the same procedures described by a previous study (Levine and Mattson 2021). For each parameter, including the tipburn visual rating, pairwise comparisons among treatments were performed using a parametric Tukey’s honest significant difference test (P ≤ 0.05) and statistical software JMP Pro (version 17.0.0; SAS Institute, Inc., Cary, NC, USA).

Results

Tipburn and shoot and root biomass.

Lettuce tipburn was effectively controlled with the biostimulant at the higher concentration of 220 μL⋅L−1 compared with the control, whereas the biostimulant at the lower concentration of 22 μL⋅L−1 did not affect the tipburn incidence or severity (Figs. 1 and 2). At 14 DAT, there was no tipburn under any treatment (Fig. 2). At 21 DAT, moderate tipburn developed with and without the biostimulant at 22 μL⋅L−1, whereas no tipburn was observed with the biostimulant at 220 μL⋅L−1. At 28 DAT, severe tipburn developed with and without the biostimulant at 22 μL⋅L−1, whereas little tipburn was observed with the biostimulant at 220 μL⋅L−1. Compared with the control, the biostimulant at 220 μL⋅L−1 decreased the tipburn rating and the percentage of leaves with tipburn by 88% and 85%, respectively.

Fig. 1.
Fig. 1.

Top and side views of representative plants of lettuce ‘Rex’ grown in hydroponic nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. The images share the same scale within a single harvest, whereas the scale varies across different harvests.

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

Fig. 2.
Fig. 2.

Tipburn rating (0 = no tipburn; 1 = mild tipburn; 5 = severe tipburn) and percentage of leaves with tipburn of lettuce ‘Rex’ grown in hydroponic nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05).

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

Compared with the control, the biostimulant increased shoot fresh weight by 28% regardless of the concentration at 21 DAT, but did not affect it at 14 or 28 DAT (Fig. 3). Shoot dry mass was unaffected by the biostimulant regardless of the concentration at 21 and 28 DAT, although the biostimulant at 22 μL⋅L−1 increased shoot dry mass by 31% compared with the control at 14 DAT.

Fig. 3.
Fig. 3.

Shoot fresh and dry mass of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

In general, plants developed similarly healthy roots under all the treatments. The biostimulant at 22 μL⋅L−1 slightly increased the root length but did not affect it at 220 μL⋅L−1 at 28 DAT (Fig. 4). There were no treatment effects on the root dry mass of lettuce plants.

Fig. 4.
Fig. 4.

Root length and dry mass of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

Plant diameter, total leaf number, and chlorophyll concentration index.

Although the biostimulant at either concentration did not influence the plant diameter at 14 or 21 DAT, the biostimulant at 220 μL⋅L−1, but not at 22 μL⋅L−1, increased it by 11% compared with the control at 28 DAT (Fig. 5). Plants treated with the biostimulant at 220 μL⋅L−1 developed four and six more leaves than those under the control at 21 and 28 DAT, respectively. In contrast, the biostimulant at 22 μL⋅L−1 did not affect the total leaf number. The chlorophyll concentration index was similar across all treatments at 14 and 21 DAT, although it was 12% lower under the biostimulant at 220 μL⋅L−1 than under the control at 28 DAT (Fig. 6).

Fig. 5.
Fig. 5.

Plant diameter and leaf number of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

Fig. 6.
Fig. 6.

Chlorophyll concentration index of lettuce ‘Rex’ lettuce grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

Plant tissue nutrient compositions.

The whole-plant tissue nutrient compositions from all treatments at 28 DAT are shown in Fig. 7. The biostimulant at either concentration did not affect the concentrations of any macronutrients, Fe, B, and Cu. Plants treated with the biostimulant at 220 μL⋅L−1, but not at 22 μL⋅L−1, accumulated 115% and 496% higher Mn and Zn, respectively, than those under the control. Plants treated with the biostimulant at 22 μL⋅L−1 had 53% lower Mo than those under the control.

Fig. 7.
Fig. 7.

Concentrations of macronutrients (N, K, P, Ca, Mg, and S) and micronutrients (Fe, Mn, Zn, B, Cu, and Mo) in lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

Citation: HortScience 59, 1; 10.21273/HORTSCI17507-23

Nutrient solutions.

The nutrient solution compositions at the beginning and end of the experiment are shown in Table 1. Despite higher Ca concentrations at the end than at the beginning of the experiment in all nutrient solutions, severe tipburn still occurred under the control and the biostimulant at 22 μL⋅L−1. This indicates that tipburn was likely caused by insufficient Ca uptake and movement rather than the lack of Ca in the root zone. At the end of the experiment, nutrient solution Ca and Zn concentrations increased with increasing biostimulant concentrations.

Table 1.

Nutrient solution compositions at the beginning and the end of the experiment without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1.

Table 1.

Discussion

The biostimulant 2105 at the concentration of 220 μL⋅L−1 inhibited tipburn occurrence and severity effectively without compromising edible biomass of butterhead lettuce ‘Rex’ grown hydroponically in greenhouse conditions favorable to high plant growth rates, such as high DLIs and optimal temperature. We did not separate leaf tissues with and without tipburn during the tissue nutrient analysis; therefore, we could not determine the Ca concentration at the growing meristem of the plant. Nonetheless, because tipburn is caused by localized Ca deficiency at the growing meristem of the plant, the lack of tipburn under the biostimulant at the 220 μL⋅L−1 treatment indicates sufficient Ca there. Because the biostimulant did not influence the overall Ca concentration in the leaf tissues sampled from the entire plant, which was dried, homogenized, and analyzed for its nutrient composition, we inferred that the biostimulant improved Ca mobility within the plant and allocated sufficient Ca to the inner, younger leaves.

The Ca ions enter the xylem through either the apoplastic pathway (between cells or through cell walls) or the symplastic pathway (through the cytoplasm of cells connected by plasmodesmata), although uptake of Ca by the root and movement of Ca from the xylem to the leaf tissues typically occur via the apoplastic pathway (Thor 2019; Yang and Jie 2005). Because the Ca flux via the apoplastic pathway is mainly influenced by transpiration and restricted under low transpiration conditions (White and Broadley 2003), the symplastic pathway is an alternative that allows for sufficient Ca movement. Based on its mode of action, the biostimulant 2105 can improve Ca mobility within the plant by stimulating selective ion transport channels in cell membranes, increasing the Ca concentration in the cytoplasm of cells, and subsequently promoting Ca movement via the symplastic pathway (Croda, Inc. 2020). Therefore, the biostimulant was effective at mobilizing Ca to the actively growing young leaf tissue, meeting its Ca demand, and mitigating tipburn.

Although the biostimulant did not affect whole-plant tissue macronutrient concentrations, the biostimulant at 220 μL⋅L−1 increased the accumulation of Mn and Zn in the leaf tissues compared with the control. Because Mn uptake is also mediated by Ca channels of the plasma membrane (Alejandro et al. 2020), the Ca-mobilizing biostimulant likely increased Mn uptake. The elevated Zn concentration can be attributed to the inclusion of Zn in the biostimulant formulation, which contained zinc nitrate. In addition to zinc nitrate, the biostimulant contained calcium ammonium nitrate, which can explain the generally increased N, Ca, and Zn concentrations in the nutrient solution at the end of the experiment with increasing biostimulant concentrations. Furthermore, variations in the nutrient concentrations can be partly attributed to different rates of water and nutrient uptake across treatments with different plant growth rates. In the nutrient solution, the final Ca concentrations under all treatments were higher than the initial Ca concentration under the control, which was sufficient for lettuce growth. In addition, compared with the initial nutrient solution under the control, the nutrient solution ratio of Ca to K increased over time under all treatments, whereas the ratio of Ca to Mg remained similar, indicating that Ca uptake was not limited by cation competition. Therefore, tipburn was not caused by a lack of Ca availability in the nutrient solution, but rather by low transpiration conditions (high humidity) that limit Ca movement through mass flow and unmet demand of Ca in the central fast-growing region under high light.

The biostimulant in this study effectively controlled greenhouse hydroponic lettuce tipburn without decreasing harvestable biomass in contrast to existing strategies that may mitigate lettuce tipburn at the expense of harvestable biomass and/or increased energy consumption and operating costs. For example, foliar spray of CaCl2 twice per week reduced tipburn but also reduced yield in greenhouse lettuce production (Samarakoon et al. 2020). Limiting the DLI at the end of the production cycle delayed the onset of tipburn symptoms but also incurred a 22% to 26% yield penalty in indoor lettuce production (Ertle 2023). In addition, although the tipburn incidence increased with increasing light intensities, it decreased by 87% when the air velocity increased from 0.25 to 0.75 m⋅s−1 (Ahmed et al. 2022). Vertical airflow fans were more effective than horizontal airflow fans at reducing tipburn severity but reduced the fresh weight of two lettuce cultivars in indoor vertical farming conditions (Kaufmann 2023). Alternatively, increasing relative humidity (90%–95%) at night increased the root pressure, which increased the Ca concentration of inner leaves, thus reducing the tipburn incidence (Collier and Tibbitts 1984).

The biostimulant at both concentrations tested during this study increased lettuce shoot fresh weight at the second harvest (21 DAT) but did not affect it at the final harvest (28 DAT) compared with the control. Because shoot dry mass was unaffected at 21 DAT, the biostimulant increased plant water uptake and moisture content at 21 DAT compared with the control. Because Ca not only contributes to cell wall integrity and structure but also promotes tissue and organ growth (Kleinhenz and Palta 2002), the biostimulant increased the plant diameter (at 28 DAT) and leaf number (at 21 and 28 DAT), likely by increasing Ca availability at the meristem. At 28 DAT, despite the increases in extension growth and the leaf developmental rate in plants treated with the biostimulant at 220 μL⋅L−1 compared with the control, shoot fresh weight was unaffected. This could be partly attributed to the lower chlorophyll concentration in plants treated with the biostimulant at 220 μL⋅L−1 compared with the control, which was likely caused by the dilution effect because of increased extension growth (Amaro de Sales et al. 2021). However, the plant canopy had closed by 28 DAT given a planting density of 24.2 plants/m2. Because neighboring plants started to shade each other, the light capture per plant became saturated regardless of the actual individual plant size. Therefore, the increases in the plant diameter and leaf number likely did not contribute to whole-plant photosynthesis late in the growing cycle. Future research can evaluate whether the biostimulant increases crop biomass throughout the growing cycle when adjacent plants are sufficiently spaced apart.

Because tipburn is associated with leaf deformation and necrosis, plants under different treatments varied in their morphological traits depending on tipburn severity. Lettuce ‘Rex’ treated with the biostimulant at 220 μL⋅L−1 had a higher plant diameter at the final harvest compared with the control, likely because of low tipburn occurrence and severity. In addition, the biostimulant at 220 μL⋅L−1 increased the total leaf number at the second and final harvests compared with the control. Others biostimulants can also improve plant morphology and development. For example, a plant-derived biostimulant increased the total leaf number and leaf area of greenhouse-grown lettuce (Cozzolino et al. 2020). Foliar application of a biostimulant that regulates nitrogen use also increased the plant diameter by 5% and total leaf number by 10% in high-tunnel-grown lettuce (Ottaiano et al. 2021). Moreover, biostimulants derived from extracts of plant and seaweed sources increased the leaf area but did not affect the total leaf number in greenhouse-grown spinach (Rouphael et al. 2018).

In conclusion, applying the Ca-mobilizing biostimulant in the hydroponic nutrient solution was an effective solution to control lettuce tipburn in greenhouse conditions. Compared with the control, the biostimulant increased shoot fresh weight at 21 DAT, but not at 28 DAT. It also increased the plant diameter and total leaf number as plants matured. Finally, the adoption of this biostimulant can benefit hydroponic lettuce growers in controlled environments by reducing tipburn-related crop losses, thus increasing profitability.

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  • De Freitas ST, do Amarante CV, Labavitch JM, Mitcham EJ. 2010. Cellular approach to understand bitter pit development in apple fruit. Postharvest Biol Technol. 57(1):613. https://doi.org/10.1016/j.postharvbio.2010.02.006.

    • Search Google Scholar
    • Export Citation
  • Di Mola I, Cozzolino E, Ottaiano L, Giordano M, Rouphael Y, Colla G, Mori M. 2019. Effect of vegetal-and seaweed extract-based biostimulants on agronomical and leaf quality traits of plastic tunnel-grown baby lettuce under four regimes of nitrogen fertilization. Agronomy. 9(10):571. https://doi.org/10.3390/agronomy9100571.

    • Search Google Scholar
    • Export Citation
  • Drost D, Johnson M. 2020. Brussels sprouts in the garden. Utah State University Extension, Logan, UT, USA.

  • El-Nakhel C, Cristofano F, Colla G, Pii Y, Secomandi E, De Gregorio M, Buffagni V, Garcia-Perez P, Lucini L, Rouphael Y. 2023. Vegetal-derived biostimulants distinctively command the physiological and metabolomic signatures of lettuce grown in depleted nitrogen conditions. Scientia Hortic. 317:112057. https://doi.org/10.1016/j.scienta.2023.112057.

    • Search Google Scholar
    • Export Citation
  • Ertle JM. 2023. Tipburn management through controlled environment for indoor vertical farm lettuce production (PhD Diss). The Ohio State University, Columbus, Ohio, USA.

  • 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
  • Guinan KJ, Sujeeth N, Copeland RB, Jones PW, O’Brien NM, Sharma H, Prouteau P, O’Sullivan JT. 2012. Discrete roles for extracts of Ascophyllum nodosum in enhancing plant growth and tolerance to abiotic and biotic stresses. Acta Hortic. 1009:127135. https://doi.org/10.17660/ActaHortic.2013.1009.15.

    • Search Google Scholar
    • Export Citation
  • Hagassou D, Francia E, Ronga D, Buti M. 2019. Blossom end-rot in tomato (Solanum lycopersicum L.): A multi-disciplinary overview of inducing factors and control strategies. Scientia Hortic. 249:4958. https://doi.org/10.1016/j.scienta.2019.01.042.

    • Search Google Scholar
    • Export Citation
  • Kaufmann CJ. 2023. Reducing tipburn in lettuce grown in an indoor vertical farm: Comparing the impact of vertically distributed airflow vs. horizontally distributed airflow in the growth of Lactuca sativa (MS thesis). University of Arizona, Tucson, Arizona, USA.

  • Kerton M, Newbury HJ, Hand D, Pritchard J. 2009. Accumulation of calcium in the centre of leaves of coriander (Coriandrum sativum L.) is due to an uncoupling of water and ion transport. J Expt Bot. 60(1):227235. https://doi.org/10.1093/jxb/ern279.

    • Search Google Scholar
    • Export Citation
  • Kleinhenz MD, Palta JP. 2002. Root zone calcium modulates the response of potato plants to heat stress. Physiol Plant. 115(1):111118. https://doi.org/10.1034/j.1399-3054.2002.1150113.x.

    • Search Google Scholar
    • Export Citation
  • Kubota C. 2016. Growth, development, transpiration and translocation as affected by abiotic environmental factors, p 151–164. In: Kozai T, Niu G, Takagaki M (eds). Plant factory. Academic Press, Cambridge, MA, USA. https://doi.org/10.1016/B978-0-12-801775-3.00010-X.

  • Kubota C, Papio G, Ertle J. 2023. Technological overview of tipburn management for lettuce (Lactuca sativa) in vertical farming conditions. Acta Hortic. 1369:6574. https://doi.org/10.17660/ActaHortic.2023.1369.8.

    • 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
  • Lee RJ, Bhandari SR, Lee G, Lee JG. 2019. Optimization of temperature and light, and cultivar selection for the production of high-quality head lettuce in a closed-type plant factory. Hortic Environ Biotechnol. 60:207216. https://doi.org/10.1007/s13580-018-0118-8.

    • Search Google Scholar
    • Export Citation
  • Levine CP, Mattson NS. 2021. Potassium-deficient nutrient solution affects the yield, morphology, and tissue mineral elements for hydroponic baby leaf spinach (Spinacia oleracea L.). Horticulturae. 7(8):213. https://doi.org/10.3390/horticulturae7080213.

    • Search Google Scholar
    • Export Citation
  • Ma X, Liu B, Zhang Y, Su M, Zheng B, Wang S, Wu H. 2023. Unraveling correlations between calcium deficiency and spongy tissue in mango fruit flesh. Scientia Hortic. 309:111694. https://doi.org/10.1016/j.scienta.2022.111694.

    • Search Google Scholar
    • Export Citation
  • Miceli A, Vetrano F, Moncada A. 2021. Influence of Ecklonia maxima extracts on growth, yield, and postharvest quality of hydroponic leaf lettuce. Horticulturae. 7(11):440. https://doi.org/10.3390/horticulturae7110440.

    • Search Google Scholar
    • Export Citation
  • Ottaiano L, Di Mola I, Cozzolino E, El-Nakhel C, Rouphael Y, Mori M. 2021. Biostimulant application under different nitrogen fertilization levels: Assessment of yield, leaf quality, and nitrogen metabolism of tunnel-grown lettuce. Agronomy. 11(8):1613. https://doi.org/10.3390/agronomy11081613.

    • Search Google Scholar
    • Export Citation
  • Palzkill DA, Tibbitts TW, Struckmeyer BE. 1980. High relative humidity promotes tipburn on young cabbage plants. HortScience. 15(5):659660. https://doi.org/10.21273/HORTSCI.15.5.659.

    • Search Google Scholar
    • Export Citation
  • Rouphael Y, Giordano M, Cardarelli M, Cozzolino E, Mori M, Kyriacou MC, Bonini P, Colla G. 2018. Plant-and seaweed-based extracts increase yield but differentially modulate nutritional quality of greenhouse spinach through biostimulant action. Agronomy. 8(7):126. https://doi.org/10.3390/agronomy8070126.

    • 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
  • Samarakoon U, Palmer J, Ling P, Altland J. 2020. Effects of electrical conductivity, pH, and foliar application of calcium chloride on yield and tipburn of Lactuca sativa grown using the nutrient-film technique. HortScience. 55(8):12651271. https://doi.org/10.21273/HORTSCI15070-20.

    • Search Google Scholar
    • Export Citation
  • Su T, Li P, Wang H, Wang W, Zhao X, Yu Y, Zhang D, Yu S, Zhang F. 2019. Natural variation in a calreticulin gene causes reduced resistance to Ca2+ deficiency‐induced tipburn in chinese cabbage (Brassica rapa ssp. pekinensis). Plant Cell Environ. 42(11):30443060. https://doi.org/10.1111/pce.13612.

    • Search Google Scholar
    • Export Citation
  • Thor K. 2019. Calcium—nutrient and messenger. Front Plant Sci. 10:440. https://doi.org/10.3389/fpls.2019.00440.

  • Van Delden SH, SharathKumar M, Butturini M, Graamans LJA, Heuvelink E, Kacira M, Kaiser E, Klamer RS, Klerkx L, Kootstra G, Loeber A. 2021. Current status and future challenges in implementing and upscaling vertical farming systems. Nat Food. 2(12):944956. https://doi.org/10.1038/s43016-021-00402-w.

    • Search Google Scholar
    • Export Citation
  • Vanhassel P, Bleyaert P, Van Lommel J, Vandevelde I, Crappé S, Van Hese N, Hanssens J, Steppe K, Van Labeke M. 2014. Rise of nightly air humidity as a measure for tipburn prevention in hydroponic cultivation of butterhead lettuce. Acta Hortic. 1107:195202. https://doi.org/10.17660/ActaHortic.2015.1107.26.

    • Search Google Scholar
    • Export Citation
  • Wang W, Wang J, Wei Q, Li B, Zhong X, Hu T, Hu H, Bao C. 2019. Transcriptome-wide identification and characterization of circular RNAs in leaves of Chinese cabbage (brassica rapa L. ssp. pekinensis) in response to calcium deficiency-induced tip-burn. Sci Rep. 9:14544. https://doi.org/10.1038/s41598-019-51190-0.

    • Search Google Scholar
    • Export Citation
  • Weidner T, Yang A, Hamm MW. 2021. Energy optimisation of plant factories and greenhouses for different climatic conditions. Energy Convers Manage. 243:114336. https://doi.org/10.1016/j.enconman.2021.114336.

    • Search Google Scholar
    • Export Citation
  • White PJ, Broadley MR. 2003. Calcium in plants. Ann Bot. 92(4):487511. https://doi.org/10.1093/aob/mcg164.

  • Yahia EM, Carrillo-López A, Sañudo A. 2019. Physiological disorders and their control, p 499–527. In: Yahia EM (ed). Postharvest technology of perishable horticultural commodities. Woodhead Publishing, Sawston, UK. https://doi.org/10.1016/B978-0-12-813276-0.00015-8.

  • Yang H, Jie Y. 2005. Uptake and transport of calcium in plants. J Plant Physiol Mol Biol. 31(3):227234. https://www.researchgate.net/profile/Hq-Yang-2/publication/7781249_Uptake_and_transport_of_calcium_in_plants/links/5ebbccac92851c11a8654f0e/Uptake-and-transport-of-calcium-in-plants.pdf. [accessed 24 Sep 2023].

    • Search Google Scholar
    • Export Citation
  • Zhang Y, Kacira M, An L. 2016. A CFD study on improving air flow uniformity in indoor plant factory system. Biosyst Eng. 147:193205. https://doi.org/10.1016/j.biosystemseng.2016.04.012.

    • Search Google Scholar
    • Export Citation
  • Fig. 1.

    Top and side views of representative plants of lettuce ‘Rex’ grown in hydroponic nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. The images share the same scale within a single harvest, whereas the scale varies across different harvests.

  • Fig. 2.

    Tipburn rating (0 = no tipburn; 1 = mild tipburn; 5 = severe tipburn) and percentage of leaves with tipburn of lettuce ‘Rex’ grown in hydroponic nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05).

  • Fig. 3.

    Shoot fresh and dry mass of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 4.

    Root length and dry mass of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 5.

    Plant diameter and leaf number of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 6.

    Chlorophyll concentration index of lettuce ‘Rex’ lettuce grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 7.

    Concentrations of macronutrients (N, K, P, Ca, Mg, and S) and micronutrients (Fe, Mn, Zn, B, Cu, and Mo) in lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • 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.

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  • Alejandro S, Höller S, Meier B, Peiter E. 2020. Manganese in plants: From acquisition to subcellular allocation. Front Plant Sci. 11:300. https://doi.org/10.3389/fpls.2020.00300.

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  • 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. https://doi.org/10.21273/JASHS.111.3.413.

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  • 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.

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  • Bulgari R, Trivellini A, Ferrante A. 2019. Effects of two doses of organic extract-based biostimulant on greenhouse lettuce grown under increasing NaCl concentrations. Front Plant Sci. 9:1870. https://doi.org/10.3389/fpls.2018.01870.

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  • 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. https://doi.org/10.21273/JASHS.109.2.128.

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  • Cozzolino E, Giordano M, Fiorentino N, El-Nakhel C, Pannico A, Di Mola I, Mori M, Kyriacou MC, Colla G, Rouphael Y. 2020. Appraisal of biodegradable mulching films and vegetal-derived biostimulant application as eco-sustainable practices for enhancing lettuce crop performance and nutritive value. Agronomy. 10(3):427. https://doi.org/10.3390/agronomy10030427.

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  • Cristofano F, El-Nakhel C, Pannico A, Giordano M, Colla G, Rouphael Y. 2021. Foliar and root applications of vegetal-derived protein hydrolysates differentially enhance the yield and qualitative attributes of two lettuce cultivars grown in floating system. Agronomy. 11(6):1194. https://doi.org/10.3390/agronomy11061194.

    • Search Google Scholar
    • Export Citation
  • Croda, Inc. 2020. Importance of calcium and CaT mode of action. https://www.plantimpact.com/mediaassets/files/plant-impact/cat-mode-of-action.pdf. [accessed 20 Aug 2023].

  • De Freitas ST, do Amarante CV, Labavitch JM, Mitcham EJ. 2010. Cellular approach to understand bitter pit development in apple fruit. Postharvest Biol Technol. 57(1):613. https://doi.org/10.1016/j.postharvbio.2010.02.006.

    • Search Google Scholar
    • Export Citation
  • Di Mola I, Cozzolino E, Ottaiano L, Giordano M, Rouphael Y, Colla G, Mori M. 2019. Effect of vegetal-and seaweed extract-based biostimulants on agronomical and leaf quality traits of plastic tunnel-grown baby lettuce under four regimes of nitrogen fertilization. Agronomy. 9(10):571. https://doi.org/10.3390/agronomy9100571.

    • Search Google Scholar
    • Export Citation
  • Drost D, Johnson M. 2020. Brussels sprouts in the garden. Utah State University Extension, Logan, UT, USA.

  • El-Nakhel C, Cristofano F, Colla G, Pii Y, Secomandi E, De Gregorio M, Buffagni V, Garcia-Perez P, Lucini L, Rouphael Y. 2023. Vegetal-derived biostimulants distinctively command the physiological and metabolomic signatures of lettuce grown in depleted nitrogen conditions. Scientia Hortic. 317:112057. https://doi.org/10.1016/j.scienta.2023.112057.

    • Search Google Scholar
    • Export Citation
  • Ertle JM. 2023. Tipburn management through controlled environment for indoor vertical farm lettuce production (PhD Diss). The Ohio State University, Columbus, Ohio, USA.

  • 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
  • Guinan KJ, Sujeeth N, Copeland RB, Jones PW, O’Brien NM, Sharma H, Prouteau P, O’Sullivan JT. 2012. Discrete roles for extracts of Ascophyllum nodosum in enhancing plant growth and tolerance to abiotic and biotic stresses. Acta Hortic. 1009:127135. https://doi.org/10.17660/ActaHortic.2013.1009.15.

    • Search Google Scholar
    • Export Citation
  • Hagassou D, Francia E, Ronga D, Buti M. 2019. Blossom end-rot in tomato (Solanum lycopersicum L.): A multi-disciplinary overview of inducing factors and control strategies. Scientia Hortic. 249:4958. https://doi.org/10.1016/j.scienta.2019.01.042.

    • Search Google Scholar
    • Export Citation
  • Kaufmann CJ. 2023. Reducing tipburn in lettuce grown in an indoor vertical farm: Comparing the impact of vertically distributed airflow vs. horizontally distributed airflow in the growth of Lactuca sativa (MS thesis). University of Arizona, Tucson, Arizona, USA.

  • Kerton M, Newbury HJ, Hand D, Pritchard J. 2009. Accumulation of calcium in the centre of leaves of coriander (Coriandrum sativum L.) is due to an uncoupling of water and ion transport. J Expt Bot. 60(1):227235. https://doi.org/10.1093/jxb/ern279.

    • Search Google Scholar
    • Export Citation
  • Kleinhenz MD, Palta JP. 2002. Root zone calcium modulates the response of potato plants to heat stress. Physiol Plant. 115(1):111118. https://doi.org/10.1034/j.1399-3054.2002.1150113.x.

    • Search Google Scholar
    • Export Citation
  • Kubota C. 2016. Growth, development, transpiration and translocation as affected by abiotic environmental factors, p 151–164. In: Kozai T, Niu G, Takagaki M (eds). Plant factory. Academic Press, Cambridge, MA, USA. https://doi.org/10.1016/B978-0-12-801775-3.00010-X.

  • Kubota C, Papio G, Ertle J. 2023. Technological overview of tipburn management for lettuce (Lactuca sativa) in vertical farming conditions. Acta Hortic. 1369:6574. https://doi.org/10.17660/ActaHortic.2023.1369.8.

    • 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
  • Lee RJ, Bhandari SR, Lee G, Lee JG. 2019. Optimization of temperature and light, and cultivar selection for the production of high-quality head lettuce in a closed-type plant factory. Hortic Environ Biotechnol. 60:207216. https://doi.org/10.1007/s13580-018-0118-8.

    • Search Google Scholar
    • Export Citation
  • Levine CP, Mattson NS. 2021. Potassium-deficient nutrient solution affects the yield, morphology, and tissue mineral elements for hydroponic baby leaf spinach (Spinacia oleracea L.). Horticulturae. 7(8):213. https://doi.org/10.3390/horticulturae7080213.

    • Search Google Scholar
    • Export Citation
  • Ma X, Liu B, Zhang Y, Su M, Zheng B, Wang S, Wu H. 2023. Unraveling correlations between calcium deficiency and spongy tissue in mango fruit flesh. Scientia Hortic. 309:111694. https://doi.org/10.1016/j.scienta.2022.111694.

    • Search Google Scholar
    • Export Citation
  • Miceli A, Vetrano F, Moncada A. 2021. Influence of Ecklonia maxima extracts on growth, yield, and postharvest quality of hydroponic leaf lettuce. Horticulturae. 7(11):440. https://doi.org/10.3390/horticulturae7110440.

    • Search Google Scholar
    • Export Citation
  • Ottaiano L, Di Mola I, Cozzolino E, El-Nakhel C, Rouphael Y, Mori M. 2021. Biostimulant application under different nitrogen fertilization levels: Assessment of yield, leaf quality, and nitrogen metabolism of tunnel-grown lettuce. Agronomy. 11(8):1613. https://doi.org/10.3390/agronomy11081613.

    • Search Google Scholar
    • Export Citation
  • Palzkill DA, Tibbitts TW, Struckmeyer BE. 1980. High relative humidity promotes tipburn on young cabbage plants. HortScience. 15(5):659660. https://doi.org/10.21273/HORTSCI.15.5.659.

    • Search Google Scholar
    • Export Citation
  • Rouphael Y, Giordano M, Cardarelli M, Cozzolino E, Mori M, Kyriacou MC, Bonini P, Colla G. 2018. Plant-and seaweed-based extracts increase yield but differentially modulate nutritional quality of greenhouse spinach through biostimulant action. Agronomy. 8(7):126. https://doi.org/10.3390/agronomy8070126.

    • 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
  • Samarakoon U, Palmer J, Ling P, Altland J. 2020. Effects of electrical conductivity, pH, and foliar application of calcium chloride on yield and tipburn of Lactuca sativa grown using the nutrient-film technique. HortScience. 55(8):12651271. https://doi.org/10.21273/HORTSCI15070-20.

    • Search Google Scholar
    • Export Citation
  • Su T, Li P, Wang H, Wang W, Zhao X, Yu Y, Zhang D, Yu S, Zhang F. 2019. Natural variation in a calreticulin gene causes reduced resistance to Ca2+ deficiency‐induced tipburn in chinese cabbage (Brassica rapa ssp. pekinensis). Plant Cell Environ. 42(11):30443060. https://doi.org/10.1111/pce.13612.

    • Search Google Scholar
    • Export Citation
  • Thor K. 2019. Calcium—nutrient and messenger. Front Plant Sci. 10:440. https://doi.org/10.3389/fpls.2019.00440.

  • Van Delden SH, SharathKumar M, Butturini M, Graamans LJA, Heuvelink E, Kacira M, Kaiser E, Klamer RS, Klerkx L, Kootstra G, Loeber A. 2021. Current status and future challenges in implementing and upscaling vertical farming systems. Nat Food. 2(12):944956. https://doi.org/10.1038/s43016-021-00402-w.

    • Search Google Scholar
    • Export Citation
  • Vanhassel P, Bleyaert P, Van Lommel J, Vandevelde I, Crappé S, Van Hese N, Hanssens J, Steppe K, Van Labeke M. 2014. Rise of nightly air humidity as a measure for tipburn prevention in hydroponic cultivation of butterhead lettuce. Acta Hortic. 1107:195202. https://doi.org/10.17660/ActaHortic.2015.1107.26.

    • Search Google Scholar
    • Export Citation
  • Wang W, Wang J, Wei Q, Li B, Zhong X, Hu T, Hu H, Bao C. 2019. Transcriptome-wide identification and characterization of circular RNAs in leaves of Chinese cabbage (brassica rapa L. ssp. pekinensis) in response to calcium deficiency-induced tip-burn. Sci Rep. 9:14544. https://doi.org/10.1038/s41598-019-51190-0.

    • Search Google Scholar
    • Export Citation
  • Weidner T, Yang A, Hamm MW. 2021. Energy optimisation of plant factories and greenhouses for different climatic conditions. Energy Convers Manage. 243:114336. https://doi.org/10.1016/j.enconman.2021.114336.

    • Search Google Scholar
    • Export Citation
  • White PJ, Broadley MR. 2003. Calcium in plants. Ann Bot. 92(4):487511. https://doi.org/10.1093/aob/mcg164.

  • Yahia EM, Carrillo-López A, Sañudo A. 2019. Physiological disorders and their control, p 499–527. In: Yahia EM (ed). Postharvest technology of perishable horticultural commodities. Woodhead Publishing, Sawston, UK. https://doi.org/10.1016/B978-0-12-813276-0.00015-8.

  • Yang H, Jie Y. 2005. Uptake and transport of calcium in plants. J Plant Physiol Mol Biol. 31(3):227234. https://www.researchgate.net/profile/Hq-Yang-2/publication/7781249_Uptake_and_transport_of_calcium_in_plants/links/5ebbccac92851c11a8654f0e/Uptake-and-transport-of-calcium-in-plants.pdf. [accessed 24 Sep 2023].

    • Search Google Scholar
    • Export Citation
  • Zhang Y, Kacira M, An L. 2016. A CFD study on improving air flow uniformity in indoor plant factory system. Biosyst Eng. 147:193205. https://doi.org/10.1016/j.biosystemseng.2016.04.012.

    • Search Google Scholar
    • Export Citation
Kishan Biradar Department of Plant and Soil Sciences, University of Delaware, 531 South College Avenue, Newark, DE 19716, USA

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Qingwu Meng Department of Plant and Soil Sciences, University of Delaware, 531 South College Avenue, Newark, DE 19716, USA

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Contributor Notes

We thank the University of Delaware Department of Plant and Soil Sciences Innovations in Plant Science Fellowship for partial funding, Drs. Susan Sun and Jason Wall at Croda, Inc., for technical input and support, and William Bartz at the University of Delaware for experimental assistance.

Q.M. is the corresponding author. E-mail: qwmeng@udel.edu.

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  • Fig. 1.

    Top and side views of representative plants of lettuce ‘Rex’ grown in hydroponic nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. The images share the same scale within a single harvest, whereas the scale varies across different harvests.

  • Fig. 2.

    Tipburn rating (0 = no tipburn; 1 = mild tipburn; 5 = severe tipburn) and percentage of leaves with tipburn of lettuce ‘Rex’ grown in hydroponic nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05).

  • Fig. 3.

    Shoot fresh and dry mass of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 4.

    Root length and dry mass of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 5.

    Plant diameter and leaf number of lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 6.

    Chlorophyll concentration index of lettuce ‘Rex’ lettuce grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 14, 21, and 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

  • Fig. 7.

    Concentrations of macronutrients (N, K, P, Ca, Mg, and S) and micronutrients (Fe, Mn, Zn, B, Cu, and Mo) in lettuce ‘Rex’ grown in nutrient solutions without (control) and with the biostimulant CC US-2105 at two concentrations of 22 and 220 μL⋅L−1 28 d after transplant. Means (±SE) followed by different letters are statistically different based on Tukey’s honest significant difference test (α = 0.05). NS = nonsignificant.

 

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Longwood Gardens Fellows Program 2024

 

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