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ASHS 2024 Annual Conference

 

Copper Can Be Elevated in Hydroponics and Peat-based Media for Potential Disease Suppression: Concentration Thresholds for Lettuce and Tomato

Authors:
Mackenzie G. Dey Department of Plants, Soils, and Climate, Utah State University, Crop Physiology Laboratory, 1410 N. 800 E., Logan, UT 84322-4820, USA

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Noah J. Langenfeld Department of Plants, Soils, and Climate, Utah State University, Crop Physiology Laboratory, 1410 N. 800 E., Logan, UT 84322-4820, USA

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Bruce Bugbee Department of Plants, Soils, and Climate, Utah State University, Crop Physiology Laboratory, 1410 N. 800 E., Logan, UT 84322-4820, USA

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Abstract

Copper (Cu) is typically adequate at 0.5 μM (0.03 ppm) in hydroponics and at 2 μM (0.125 ppm) in soilless media, but elevated levels can be used to inhibit pathogenic fungal growth. We studied the effect of elevated Cu on the growth of lettuce and tomato in peat-based media and deep-flow hydroponics. Lettuce growth in hydroponics was not hindered until a concentration greater than 4 μM (0.25 ppm) Cu was used, which is eight times greater than the adequate level. Tomato was more tolerant of elevated Cu, with no growth suppression up to 8 μM (0.5 ppm) in hydroponics. Organic matter tightly binds Cu, and bioavailability is thus determined by organic components in soilless media. We confirmed an adsorption capacity of 19 mg Cu per g of peat, which explains why there was no inhibition of lettuce or tomato growth up to 1000 μM (64 ppm) Cu in peat-based media. When chelated with ethylenediaminetetraacetic acid, Cu binding to organic matter was reduced and growth was decreased in lettuce but not tomato. Both species tolerated a 100-fold greater concentration of Cu in peat-based media than in deep-flow hydroponics. Elevated Cu in solution increased concentrations 20 times greater in root tissue than in leaves. These solution and tissue concentrations are greater than identified toxicity thresholds of pathogenic fungal and fungal-like organisms, and could thus be used to suppress root-borne fungal and fungal-like diseases.

Copper (Cu) is a metal essential to plants for its inclusion in the electron transport chain, lignin synthesis, and as a cofactor for many proteins (Yruela 2005). Most field soils contain adequate Cu for plant growth, but it is typically a component of greenhouse fertilizers at micronutrient levels. The optimal concentration of Cu in the fertilizer solution can be determined using a mass–balance approach by multiplying an average desired leaf tissue concentration of 10 mg⋅kg–1 Cu by an estimated water-use efficiency of 3 g of dry biomass per liter of water transpired (Langenfeld et al. 2022). The minimum Cu concentration in a nutrient solution is therefore only 0.5 μM (0.03 ppm). However, many commercial fertilizers contain up to 2 μM (0.125 ppm) Cu to ensure bioavailability in the presence of organic substances.

Soilless media often contains high levels of organic matter (OM) from coco coir, peat, pine bark, and/or sawdust. Organic matter has a uniquely high adsorption capacity for Cu (Bolan et al. 2003; Silber 2019). The acidic side chains in OM are rich in carboxylic and phenolic functional groups with negative charges that have a high affinity to adsorb Cu (Gardea-Torresdey et al. 1996). Leaf curling and chlorotic and necrotic leaf margins in young tissue are common in Cu-deficient plants, which leads to impaired growth (Adams et al. 1978; Robinson 1987; Yruela 2005). Copper deficiency also restricts enzymatic activity and the efficiency of photosystem II (Printz et al. 2016).

An excessive Cu concentration in the root zone can be toxic to plants by overwhelming transporters that guard against excessive Cu uptake. Plants have evolved specific Cu-binding chaperone proteins that guide Cu to transport electrons within mitochondria and chloroplasts (Printz et al. 2016; Yruela 2009). Excess Cu is free within plant tissues and catalyzes the formation of reactive oxygen species (Aust et al. 1985). This leads to oxidative stress that damages proteins, lipids, and DNA (Hänsch and Mendel 2009; Thounaojam et al. 2012). Common toxicity symptoms in most plants include brown root tips, root dieback, and stunted plant growth. Shams et al. (2019) saw 14% less shoot growth in lettuce (Lactuca sativa L. cv. Yedikule) from 0.2 (0.01 ppm) to 400 μM (25 ppm) Cu as Cu sulfate in peat-based media, but Mukherji and Gupta (1972) saw complete inhibition of lettuce (cv. Suttons Unrivalled) root growth at 100 μM (6.4 ppm) Cu in petri dishes. Rhoads et al. (1989) studied Cu soil application in tomato (Solanum lycopersicum L. cv. Sunny) and found growth was suppressed above 150 mg Cu per kg of loamy-fine soil, whereas Sonmez et al. (2006) saw hindered growth in tomato (cv. F144) when fertilized with more than 1000 mg Cu per kg of calcareous soil. These studies show variability in crop response to elevated Cu.

Although excessive Cu is toxic, increasing Cu concentrations up to the toxicity threshold in the root zone can be beneficial. Root membranes filter Cu to minimize excess concentrations in leaf tissue. Root-surface Cu concentrations can be as high as 0.1% (1000 mg⋅kg–1), which can mitigate fungal and fungal-like infections (Cervantes and Gutierrez-Corona 1994). The effect of Cu on fungal and fungal-like pathogens has been well studied in petri dishes. Liu et al. (2020) found that Fusarium graminearum biomass decreased by 25 to 35% at 20 μM (1.2 ppm) Cu and was prevented at 100 μM (6.4 ppm) compared with 0-μM Cu treatments. Ribeiro et al. (2017) found that Pythium insidiosum growth was suppressed by 13% at 63 μM (4 ppm) Cu and was inhibited completely at 1000 μM (64 ppm) compared with 31-μM (2-ppm) treatments. Zabrieski et al. (2015) found that 786 μM (50 ppm) Cu nanoparticles suppressed growth of Pythium aphanidermatum by about 23% and Pythium ultimum by about 27%. Some studies have shown the effects of elevated Cu in soilless media on increasing crop resistance to fungal and fungal-like diseases. Lopez-Lima et al. (2021) saw that when treated with 7868 μM (500 ppm) Cu nanoparticles, tomato (cv. Rio Grande) infected with Fusarium oxysporum f. sp. lycopersici had about 56% more biomass than contaminated controls without Cu. Shang et al. (2021) also found that 31 mg Cu nanoparticles/kg soilless media increased lettuce (cv. Black Seeded Simpson) biomass by 26% when contaminated with Fusarium oxysporum f. sp. lactucae compared with infected controls. Elevated Cu in the root zone could therefore suppress disease caused by Pythium and Fusarium, but may be more effective depending on species.

The chelate ethylenediaminetetraacetic acid (EDTA) complexes readily with Cu and can help buffer against toxicity. Chelation minimizes the binding of Cu to OM and increases bioavailability compared with unchelated Cu (Tills 1987). Chelates also minimize Cu binding to hydroxide and phosphate ions (Jurinak and Inouye 1962). Chelation can decrease Cu availability in hydroponics because it must be extracted from the chelate.

Elevated silicon (Si) in the root zone can regulate the uptake of micronutrients (El-Beltagi et al. 2020) and can mitigate Cu toxicity (Frantz et al. 2011; Li et al. 2008). For this reason, it is now common to add Si to both hydroponics and soilless media (Langenfeld et al. 2022).

Although Cu tolerance of some species has been studied in the field, and the adsorption of Cu to some media components are known, little work has been done to examine the tolerance of common crops to elevated Cu in controlled-environment systems.

The objective of our study was to compare a range of Cu concentrations on the growth and Cu tissue concentration of lettuce and tomato grown in deep-flow hydroponics and peat-based media with and without chelated Cu.

Methods

Hydroponics.

Lettuce (cv. Grand Rapids) and tomato (cv. Better Boy) were germinated with tap water on germination paper (Germination blue blotter; Seedburo Equipment Company, Des Plaines, IL, USA) using a slant board (Langenfeld and Bugbee 2022) for 7 d (lettuce) and 11 d (tomato). Seedlings were then transplanted into foam collars in 2-L opaque plastic bottles (Nalgene; Thermo Fisher Scientific, Waltham, MA, USA), for deep-flow hydroponics, filled with a nutrient solution containing 1.5 mM calcium nitrate tetrahydrate, 2 mM potassium nitrate, 0.4 mM monopotassium phosphate, 0.8 mM magnesium sulfate heptahydrate, 0.6 mM potassium silicate, 1 mM nitric acid, 7 μM iron diethylenetriaminepentaacetic acid, 3 μM manganese (II) chloride, 3 μM zinc (II) chloride, 40 μM boric acid, 0.1 μM sodium molybdate, 0.1 μM nickel (II) chloride, and 5 mM 2-(N-morpholino)ethanesulfonic acid buffer (Bugbee and Langenfeld 2022). The nutrient solution was prepared using reverse-osmosis water.

Treatments used Cu disodium EDTA at concentrations of 0, 4, 8, 12, 16, 20, 32, and 64 μM (0, 0.3, 0.5, 0.8, 1, 2, and 4 ppm) Cu (for replicates, see Supplemental Tables S1 and S2). The lowest levels bracketed the Cu concentration in commercial fertilizers (0.5 μM in hydroponics and 2 μM in soilless media). Preliminary studies indicated minimal differences in growth among these low concentrations. Plants were grown in the bottles for 28 d across four trials for lettuce (Feb–Jun 2022) and one trial for tomato (Sep–Oct 2022) in a glass greenhouse at Utah State University (Logan, UT, USA). Mean air temperature was controlled at 25 ± 3 °C and mean relative humidity was 35 ± 10%. Environmental conditions were set and maintained by a data logger (CR1000; Campbell Scientific, Inc., Logan, UT, USA). The carbon dioxide (CO2) concentration was 450 ± 50 ppm CO2. The 16-h photoperiod resulted in a daily light integral of 25 to 35 mol⋅m–2⋅d–1 (model SQ-500, full-spectrum quantum sensor; Apogee Instruments, Logan, UT, USA) with supplemental lighting provided by light-emitting diodes (model LUXX-200-277-88/80R Spectrum; LUXX Lighting Systems, Los Angeles, CA, USA).

Fresh weight was measured and plants were dried for 48 h at 80 °C to obtain dry mass. Composite samples were made of all replicates per treatment. Leaf and root tissues were ground separately to a fine powder, digested in nitric acid and hydrogen peroxide [method B-4.25 in Gavlak et al. (2005)], and analyzed for elemental concentrations using inductively coupled plasma optical emission spectroscopy by the Utah State University Analytical Laboratory (Logan, UT, USA).

Peat-based media.

Lettuce and tomato seeds were sown directly in media with 75% sphagnum peat moss (Premier Pro-Moss TBK; Premier Horticulture, Inc., Quakertown, PA, USA), 13% vermiculite (horticultural coarse vermiculite; Perlite Vermiculite Packaging Industries, North Bloomfield, OH, USA), and 12% parboiled rice hulls (PBH Nature’s media amendment; Riceland Foods, Inc., Stuttgart, AR, USA) by volume. Hydrated lime (Chemstar® Type S lime; Chemstar Products, Minneapolis, MN, USA) was added at a rate of 1.5 g per liter of media to increase the initial pH to 6.0. Wetting agent (AquaGro® 2000 G; Aquatrols, Paulsboro, NJ, USA) was added at a rate of 0.75 g per liter of media to increase wetting ability of the hydrophobic peat.

Treatments consisted of 0, 16, 32, 64, 128, 250, 500, and 1000 μM (0, 1, 2, 4, 8, 16, and 64 ppm) Cu from Cu disodium EDTA or unchelated Cu (II) chloride (for replicates, see Supplemental Tables S5 and S6). The base nutrient solution was the same as in the hydroponics experiment. Plants were watered with liquid fertilization as needed to minimize water stress.

Lettuce was grown in 1.7-L pots for 35 d from May to Jun 2021 in a closed growth chamber (model PGR15; Controlled Environments Inc., Pembia, ND, USA) with a photosynthetic photon flux density of 300 µmol⋅m–2⋅s–1 under a 16-h photoperiod from full-spectrum, high-pressure sodium lights; 35 ± 10% relative humidity; and 450 ppm CO2, with a set 25/23 °C day/night temperature. A second trial was conducted from May to Jun 2022 using the same greenhouse and environmental conditions as the hydroponics study. Tomato was also grown in this greenhouse from Sep to Oct 2022 in 1.7-L pots. Seedlings were thinned to one plant per container 7 d after sowing, after which treatments were initiated. Fresh weight was measured, and plants were then dried for 48 h at 80 °C to obtain dry mass. Composite samples were made of all replicates per treatment. Leaf tissue was analyzed using the same method as in the hydroponics study.

Adsorption of Cu to peat moss.

A 1-L glass jar containing 50 g of air-dry peat (Premier Pro-Moss TBK, Premier Horticulture, Inc.) was filled with 500 mL deionized water containing either 0, 500, 5000, or 50,000 μM Cu (II) chloride. This equated to 0, 0.318, 3.18, or 31.8 mg Cu per gram of peat in each jar, with one replicate per treatment. The contents were mixed well and placed on an orbital shaker (SI-1700 Orbital Genie; Scientific Industries, Inc., Bohemia, NY, USA) at 75 rpm. Measurements were collected 1, 24, and 48 h after the addition to each jar. The content of each jar was filtered (Whatman grade 1 filter paper, 0.45 μM; Cytiva, Marlborough, MA, USA) and measured colorimetrically for Cu using the bicinchoninic acid method (Brenner and Harris 1995).

Statistical analysis.

Dry masses were normalized to the average dry mass of plants grown with 0 μM Cu within each trial to account for growth differences resulting from variable lighting throughout the year. Data were analyzed using regression fitting in SigmaPlot 13 (Systat Software Inc., San Jose, CA, USA) at an alpha level of 0.05. Linear, quadratic, power, exponential, and rational regression were used to generate best-fit equations.

Results

Hydroponics.

Lettuce plants with added Cu up to 4 μM, and 8 μM in tomato, had a greater dry mass than plants with no Cu, but normalized dry shoot mass decreased as Cu concentration increased beyond these concentrations (Fig. 1). Normalized dry shoot mass increased and then decreased as Cu concentrations increased from 4 to 8 μM Cu in lettuce and 8 to 16 μM Cu in tomato. Tomato was more tolerant of elevated Cu than lettuce. A concentration of 64 μM Cu decreased growth by 85% in lettuce compared with 4-μM Cu plants, and 71% in tomato compared with 8-μM Cu plants. All dry mass data for hydroponic plants are shown in Supplemental Tables S1 and S2.

Fig. 1.
Fig. 1.

Normalized dry shoot mass of lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) grown in deep-flow hydroponics with increasing concentrations of copper (Cu) ethylenediaminetetraacetic acid (EDTA). Masses were normalized to the average dry mass of the 0 μM Cu controls within each trial (four trials for lettuce and one trial for tomato). Dry masses increased from 0 to 4 μM Cu (0.25 ppm) for lettuce (n = 58) and 8 μM Cu (0.5 ppm) for tomato (n = 13), but were correlated with negative linear regressions at greater Cu concentrations. The dashed vertical line in the graph denotes the typical Cu concentration in hydroponic nutrient solution.

Citation: HortScience 58, 4; 10.21273/HORTSCI17048-22

The Cu concentration in lettuce leaf tissue increased from about 3 to 12 mg⋅kg–1 as the Cu concentration in the nutrient solution increased from 0 to 32 μM Cu-EDTA (Fig. 2). Plants grown with 64 μM Cu were chlorotic and too small to be sampled for tissue analysis. The accumulation rate of Cu was greater in leaf tissue when nutrient solution Cu increased from 0 to 12 μM Cu compared with 12 to 32 μM Cu. Root tissue Cu concentration of lettuce increased exponentially from about 15 to 450 mg⋅kg–1 as nutrient solution Cu concentration increased from 0 to 32 μM. The Cu concentration in tomato leaf tissue increased from 7 to 20 mg⋅kg–1 as the Cu-EDTA concentration increased from 0 to 4 μM. Additional increases in Cu-EDTA had smaller effects on the Cu in the leaf tissue. All leaf tissue Cu concentrations for plants grown in hydroponics are shown in Supplemental Tables S3 and S4. Tomato root tissue Cu was greater than lettuce roots from 0 to 16 μM Cu and similar at 16 μM Cu.

Fig. 2.
Fig. 2.

Concentration of copper (Cu) in leaf (A) and root (B) tissue of lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) grown in a deep-flow hydroponic solution with increasing concentrations of Cu ethylenediaminetetraacetic acid (EDTA). Lettuce leaf tissue data were correlated (P < 0.001, n = 20) with a rational regression (r2 = 0.91); tomato leaf tissue data were correlated (P = 0.01, n = 5) with a power regression (r2 = 0.99). Lettuce root tissue data were correlated (P < 0.001, n = 20) with a quadratic regression (r2 = 0.99); tomato root tissue data were correlated (P = 0.03, n = 5) with a power regression (r2 = 0.97). Data points represent leaf tissue from all replicate plants within each treatment for a composite sample. Copper concentration in leaf tissue is considered optimal from 5 to 20 mg⋅kg–1 (Marschner and Marschner 2012; Robinson 1987).

Citation: HortScience 58, 4; 10.21273/HORTSCI17048-22

Peat-based media.

Dry shoot mass of each plant grown in peat-based media was normalized as in the hydroponics experiment. Dry shoot mass of lettuce increased when grown with up to 16 μM Cu with (+EDTA) and without (–EDTA) chelate, but there was then a linear decrease as Cu increased up to 1000 μM Cu (Fig. 3). Dry shoot mass decreased more in the +EDTA treatments than in the –EDTA treatments. Chelation and Cu concentration had no effect on the growth of tomato, but plants grown with Cu had a greater dry shoot mass than plants grown with no Cu. The 1000-μM Cu +EDTA treatment in lettuce had significantly suppressed growth and chlorotic leaves in all the replicates, but there were no visual signs of Cu toxicity in tomato (Fig. 4). All dry mass data for plants grown in peat-based media are shown in Supplemental Tables S5 to S7.

Fig. 3.
Fig. 3.

Normalized dry shoot mass of lettuce (Lactuca sativa) (A) and tomato (Solanum lycopersicum) (B) grown in peat-based media with increasing concentrations of copper (Cu) with ethylenediaminetetraacetic acid (+EDTA) and without (–EDTA) chelation. Masses were normalized to the average dry mass of the zero Cu controls within each trial. Biomass accumulation for –EDTA lettuce (n = 27) decreased to a greater extent with increasing Cu concentration than +EDTA masses (n = 26). Masses for –EDTA tomato were correlated (P = 0.002, n = 15) with a rational regression (r2 = 0.65); and +EDTA masses were correlated (P < 0.001, n = 15) with a power regression (r2 = 0.74).

Citation: HortScience 58, 4; 10.21273/HORTSCI17048-22

Fig. 4.
Fig. 4.

Lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) grown in a peat-based media with a nutrient solution containing 1000 μM copper (Cu; 64 ppm) without chelation by ethylenediaminetetraacetic acid (–EDTA) (left) and with (+EDTA) (right). Toxicity effects were visually noticeable with chelation in lettuce, but not in tomato.

Citation: HortScience 58, 4; 10.21273/HORTSCI17048-22

Accumulation of Cu in leaf tissue grown in peat-based media was similar to hydroponic-grown lettuce, with a steep increase in Cu leaf concentration at low Cu nutrient solution levels followed by smaller increases as Cu concentrations in nutrient solution increased (Fig. 5). Plants grown with EDTA accumulated Cu in the leaves up to 46 mg⋅kg–1 Cu. Tomato leaf Cu content was similar to lettuce leaf Cu concentration at about 18 mg⋅kg–1 at 1000 μM Cu –EDTA, but accumulated up to 72 mg⋅kg–1 at 1000 μM Cu +EDTA, whereas lettuce accumulated 46 mg⋅kg–1 at 1000 μM Cu. Roots were not analyzed because of the difficulty in removing them from the media. All leaf tissue Cu concentrations for plants grown in the peat-based media are shown in Supplemental Tables S8 and S9.

Fig. 5.
Fig. 5.

Concentration of copper (Cu) in leaf tissue of lettuce (Lactuca sativa) (A) and tomato (Solanum lycopersicum) (B) grown in a peat-based media with increasing Cu concentrations with ethylenediaminetetraacetic acid (+EDTA) and without (–EDTA) chelation. Lettuce treatments were correlated (P = 0.01, n = 5) with power regressions (r2 = 0.99 for both). Tomato treatments were correlated (+EDTA, P = 0.002, n = 5; –EDTA, P = 0.04, n = 5) with power regressions (+EDTA, r2 = 0.99; –EDTA, r2 = 0.96). Leaf tissue from multiple plants within each treatment was combined in each data point. Copper concentration in leaf tissue is considered optimal from 5 to 20 mg⋅kg–1 (Marschner and Marschner 2012; Robinson 1987).

Citation: HortScience 58, 4; 10.21273/HORTSCI17048-22

Adsorption of Cu to peat moss.

The sorption study showed that all Cu was adsorbed by the peat after 1 h in both the 0.318- and 3.18-mg Cu treatments (Table 1). About 19.7 mg Cu was adsorbed per gram of peat in the 31.8-mg Cu treatment 1 h after addition, and no additional Cu was adsorbed after 24 and 48 h. This equates to an adsorption capacity of about 19 mg of Cu per gram of peat.

Table 1.

The concentration of copper (Cu) in the filtered leachate of jars filled with 50 g peat moss and 500 mL of the Cu-containing solution with one replicate per treatment. The 0 and 0.318 mg⋅g–1 Cu of the peat treatments were not measured after 24 h because all Cu was adsorbed by the peat after 1 h.

Table 1.

Discussion

Nutrients, including Cu, are highly bioavailable in hydroponics. Nonchelated Cu was not studied in hydroponics because unchelated Cu binds to phosphorus in solution (Jurinak and Inouye 1962). Although chelation reduces ion activity and thus reduces bioavailability, it also reduces the chance of Cu forming insoluble precipitates. Chelation is therefore beneficial to maintain bioavailability in hydroponics.

Lettuce and tomato were tolerant of higher levels of Cu in peat-based media than deep-flow hydroponics. We hypothesized that chelation in the presence of OM would increase Cu availability and lower the toxicity threshold compared with nonchelated Cu. Without chelation, there was no decrease in biomass up to 1000 μM (64 ppm), but biomass decreased with increasing Cu with chelation in lettuce. Gharbi et al. (2005) saw a similar lack of Cu toxicity up to 1000 μM in lettuce (cv. Grosse Blonde) when grown in field soils with high OM content. This means lettuce was tolerant of Cu concentrations several times greater when grown in peat (Fig. 3) compared with deep-flow hydroponics (Fig. 1), especially when Cu was chelated. Tomato showed no change in growth between either chelated or unchelated treatments, which corroborates the greater Cu threshold in hydroponics. In the peat-based media, growth was reduced slightly in the absence of Cu. Environmental conditions alter water-use efficiency and thus nutrient accumulation. Nutrients with passive uptake, such as Cu, can accumulate in tissue under high transpiration conditions. Changes in seasonal light intensities among trials could have affected our results, but increased transpiration from greater light intensity is correlated with increased growth, so the impact on water-use efficiency, and thus Cu accumulation rate, was likely minimal (Langenfeld et al. 2022).

Our results indicate the adsorption capacity of our peat is 19 mg Cu per gram of peat (Table 1). This is consistent with the results of Sen Gupta et al. (2009), who found an adsorption capacity of 18 mg Cu per gram of peat. Most commercial fertilizers contain about 8 μM (0.5 ppm) of unchelated Cu, which means that all Cu will be bound initially by the peat. In the absence of plant growth, 37 L of 8-μM Cu nutrient solution would need to be added per 1 g of peat to overcome the saturation capacity. This value implies plants can extract Cu from the media. The high adsorption capacity of the peat likely led to Cu being adsorbed, and thus reduced toxicity.

Soilless media may include other OM-rich substrates, such as coconut coir and sawdust. Shukla et al. (2009) found a maximum adsorption of 2.5 mg Cu adsorbed per gram of coconut coir. Shukla and Pai (2005) saw 8.1 mg Cu per gram of sawdust. Both coir and sawdust therefore have lower adsorption capacities for Cu than peat, but still bind appreciable levels of Cu. For any OM-rich media, the form and concentration of Cu supplied by the fertilizer should be assessed to achieve an optimal application rate.

Chelates can be used to increase bioavailability in OM-rich media because they reduce adsorption to OM functional groups (Tills 1987). We used EDTA because it is a common chelate with a high affinity for Cu.

Tomato was more tolerant to greater concentrations of Cu than lettuce. The biomass accumulation of lettuce grown in deep-flow hydroponics decreased at Cu concentrations greater than 4 μM (0.25 ppm), but tomato was tolerant up to 8 μM. This shows a species difference in tolerance to Cu. The concentration of Cu can be increased to eight times greater than normal levels in tomato, but only four times greater for lettuce.

The optimal leaf tissue concentration of Cu in lettuce and tomato is generally considered to be 5 to 20 mg⋅kg–1 (Marschner and Marschner 2012; Robinson 1987). Elevated Cu concentrations in the hydroponic nutrient solution led to increased accumulations of Cu and toxicity symptoms in leaves (up to 26 mg⋅kg–1 Cu) and roots (up to 465 mg⋅kg–1 Cu) of tomato. Roots at lower Cu levels were bright white, whereas roots at the highest Cu level (64 μM) were light brown. However, toxicity levels vary among crops. MacKay et al. (1966) saw toxicity in lettuce (cv. Premier) starting at 13 mg⋅kg–1 Cu in leaf tissue, which is close to the toxicity levels in this study. Carrot (Daucus carota L. var. sativa D. C. cv. Nantes), onion (Allium cepa L. cv. Autumn Spice), and cauliflower (Brassica oleracea, var. botrytis L. cv. Primosnow) had similar toxicity thresholds; Cu toxicity in spinach (Spinacia oleracea L. cv. Wisconsin Bloomsdale) occurred at about 64 mg⋅kg–1 Cu in the leaf tissue (MacKay et al. 1966). If substrates with an adsorptive capacity for Cu are used, greater concentrations may be supplied in the nutrient solution without toxic accumulation in leaf tissue.

The use of hydroponics facilitates the analysis of nutrients in root tissue without damaging the roots. At elevated Cu concentrations, root concentrations of Cu were more than an order of magnitude greater than in leaf tissue. Many of the most detrimental fungal and fungal-like diseases (e.g., Pythium and Fusarium) attack the plants through the roots. This elevated concentration in root tissue should be even more effective in inhibiting root fungal and fungal-like diseases.

We have long added Si to both hydroponic solutions and peat-based media (Bugbee 2004) because of the reduction of disease and tolerance of drought stress [see references cited in Langenfeld et al. (2022)]. Elevated Si in the root zone can also help regulate the uptake of micronutrients (El-Beltagi et al. 2020; Nowakowski and Nowakowska 1997) and can mitigate heavy metal toxicity, such as Cu (Frantz et al. 2011; Li et al. 2008). Copper thresholds may be affected based on the bioavailability of Si in the growing medium.

Conclusion

The toxicity threshold for elevated Cu is dependent on species, substrate type, and chelation. Copper toxicity thresholds were 100-fold less in deep-flow hydroponics than in peat-based media. Concentrations greater than 4 to 8 μM began to suppress growth in hydroponics. Copper chelated with EDTA increased bioavailability in peat-based media, but tomato was tolerant of high Cu in the peat-based media regardless of chelation. An elevated Cu concentration in the root zone has the potential to suppress fungal and fungal-like infections.

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  • Langenfeld, NJ, Pinto, DF, Faust, JE, Heins, R & Bugbee, B 2022 Principles of nutrient and water management for indoor agriculture Sustainability. 14 16 10204 https://doi.org/10.3390/su141610204

    • Search Google Scholar
    • Export Citation
  • Li, J, Leisner, SM & Frantz, J 2008 Alleviation of copper toxicity in Arabidopsis thaliana by silicon addition to hydroponic solutions J Am Soc Hortic Sci. 133 5 670 677 https://doi.org/10.21273/JASHS.133.5.670

    • Search Google Scholar
    • Export Citation
  • Liu, X, Jiang, Y, He, D, Fang, X, Xu, J, Lee, Y-W, Keller, NP & Shi, J 2020 Copper tolerance mediated by FgAceA and FgCrpA in Fusarium graminearum Front Microbiol. 11 1392 https://doi.org/10.3389/fmicb.2020.01392

    • Search Google Scholar
    • Export Citation
  • Lopez-Lima, D, Mtz-Enriquez, AI, Carrión, G, Basurto-Cereceda, S & Pariona, N 2021 The bifunctional role of copper nanoparticles in tomato: Effective treatment for Fusarium wilt and plant growth promoter Sci Hortic. 277 109810 https://doi.org/10.1016/j.scienta.2020.109810

    • Search Google Scholar
    • Export Citation
  • MacKay, DC, Chipman, EW & Gupta, UC 1966 Copper and molybdenum nutrition of crops grown on acid sphagnum peat soil Soil Sci Soc Am J. 30 6 755 759 https://doi.org/10.2136/sssaj1966.03615995003000060028x

    • Search Google Scholar
    • Export Citation
  • Marschner, H & Marschner, P 2012 Mineral nutrition of higher plants 3rd ed Elsevier/Academic Press Waltham, MA, USA https://doi.org/10.1016/C2009-0-63043-9

    • Search Google Scholar
    • Export Citation
  • Mukherji, S & Gupta, BD 1972 Characterization of copper toxicity in lettuce seedlings Physiol Plant. 27 2 126 129 https://doi.org/10.1111/j.1399-3054.1972.tb03588.x

    • Search Google Scholar
    • Export Citation
  • Nowakowski, W & Nowakowska, J 1997 Silicon and copper interaction in the growth of spring wheat seedlings Biol Plant. 39 463 466 https://doi.org/10.1023/A:1001009100026

    • Search Google Scholar
    • Export Citation
  • Printz, B, Lutts, S, Hausman, J-F & Sergeant, K 2016 Copper trafficking in plants and its implication on cell wall dynamics Front Plant Sci. 7 601 https://doi.org/10.3389/fpls.2016.00601

    • Search Google Scholar
    • Export Citation
  • Rhoads, FM, Olson, SM & Manning, A 1989 Copper toxicity in tomato plants J Environ Qual. 18 2 195 197 https://doi.org/10.2134/jeq1989.00472425001800020011x

    • Search Google Scholar
    • Export Citation
  • Ribeiro, TC, Weiblen, C, Botton, S de A, Pereira, DIB, de Jesus, FPK, Verdi, CM, Gressler, LT, Sangioni, LA & Santurio, JM 2017 In vitro susceptibility of the oomycete Pythium insidiosum to metallic compounds containing cadmium, lead, copper, manganese or zinc Med Mycol. 55 6 669 672 10.1093/mmy/myw115

    • Search Google Scholar
    • Export Citation
  • Robinson, JD 1987 Diagnosis of mineral disorders in plants: Glasshouse crops 1st ed Her Majesty’s Stationary Office Richmond, UK

  • Sen Gupta, B, Curran, M, Hasan, S & Ghosh, TK 2009 Adsorption characteristics of Cu and Ni on Irish peat moss J Environ Manage. 90 2 954 960 https://doi.org/10.1016/j.jenvman.2008.02.012

    • Search Google Scholar
    • Export Citation
  • Shams, M, Ekinci, M, Turan, M, Dursun, A, Kul, R & Yildirim, E 2019 Growth, nutrient uptake and enzyme activity response of lettuce (Lactuca sativa L.) to excess copper Environ Sustain. 2 1 67 73 https://doi.org/10.1007/s42398-019-00051-7

    • Search Google Scholar
    • Export Citation
  • Shang, H, Ma, C, Li, C, Zhao, J, Elmer, W, White, JC & Xing, B 2021 Copper oxide nanoparticle-embedded hydrogels enhance nutrient supply and growth of lettuce (Lactuca sativa) infected with Fusarium oxysporum f. sp. lactucae Environ Sci Technol. 55 20 13432 13442 https://doi.org/10.1021/acs.est.1c00777

    • Search Google Scholar
    • Export Citation
  • Shukla, SR, Gaikar, VG, Pai, RS & Suryavanshi, US 2009 Batch and column adsorption of Cu(II) on unmodified and oxidized coir Sep Sci Technol. 44 1 40 62 10.1080/01496390802281984

    • Search Google Scholar
    • Export Citation
  • Shukla, SR & Pai, RS 2005 Adsorption of Cu(II), Ni(II) and Zn(II) on dye loaded groundnut shells and sawdust Separ Purif Tech. 43 1 1 8 https://doi.org/10.1016/j.seppur.2004.09.003

    • Search Google Scholar
    • Export Citation
  • Silber, A 2019 Chemical characteristics of soilless media 113 148 Raviv, M, Lieth, H & Bar-Tal, A Soilless culture: Theory and practice. Elsevier Amsterdam, Netherlands https://doi.org/10.1016/B978-0-444-63696-6.00004-9

    • Search Google Scholar
    • Export Citation
  • Sonmez, S, Kaplan, M, Sonmez, NK, Kaya, H & Uz, I 2006 High level of copper application to soil and leaves reduce the growth and yield of tomato plants Sci Agric. 63 3 213 218 https://doi.org/10.1590/S0103-90162006000300001

    • Search Google Scholar
    • Export Citation
  • Thounaojam, TC, Panda, P, Mazumdar, P, Kumar, D, Sharma, GD, Sahoo, L & Sanjib, P 2012 Excess copper induced oxidative stress and response of antioxidants in rice Plant Physiol Biochem. 53 33 39 https://doi.org/10.1016/j.plaphy.2012.01.006

    • Search Google Scholar
    • Export Citation
  • Tills, AR 1987 Chelates in horticulture Chartered Inst Hortic. 1 4 120 125

  • Yruela, I 2005 Copper in plants Braz J Plant Physiol. 17 1 145 156 https://doi.org/10.1590/S1677-04202005000100012

  • Yruela, I 2009 Copper in plants: Acquisition, transport and interactions Funct Plant Biol. 36 5 409 https://doi.org/10.1071/FP08288

  • Zabrieski, Z, Morrell, E, Hortin, J, Dimkpa, C, McLean, J, Britt, D & Anderson, A 2015 Pesticidal activity of metal oxide nanoparticles on plant pathogenic isolates of Pythium Ecotoxicol. 24 6 1305 1314 https://doi.org/10.1007/s10646-015-1505-x

    • Search Google Scholar
    • Export Citation

Supplemental Table S1.

Dry shoot mass of hydroponic lettuce grown under increasing concentrations of copper (Cu).

Supplemental Table S1.
Supplemental Table S2.

Dry shoot mass of hydroponic tomato grown under increasing concentrations of copper (Cu).

Supplemental Table S2.
Supplemental Table S3.

Leaf and root tissue copper (Cu) concentrations of hydroponic lettuce grown under increasing concentrations of Cu.

Supplemental Table S3.
Supplemental Table S4.

Leaf and root tissue copper (Cu) concentrations of tomato grown in liquid hydroponics under increasing concentrations of Cu.

Supplemental Table S4.
Supplemental Table S5.

Dry shoot mass of lettuce grown in peat-based media in a growth chamber under increasing concentrations of copper (Cu) with and without the presence of the chelate ethylenediaminetetraacetic acid (EDTA).

Supplemental Table S5.
Supplemental Table S6.

Dry shoot mass of lettuce grown in peat-based media in a greenhouse under increasing concentrations of copper (Cu) with and without the presence of the chelate ethylenediaminetetraacetic acid (EDTA).

Supplemental Table S6.
Supplemental Table S7.

Dry shoot mass of tomato grown in peat-based media in a greenhouse under increasing concentrations of copper (Cu) with and without the presence of the chelate ethylenediaminetetraacetic acid (EDTA).

Supplemental Table S7.
Supplemental Table S8.

Leaf tissue copper (Cu) concentrations of lettuce grown in peat-based media under increasing concentrations of Cu with and without the presence of the chelate ethylenediaminetetraacetic acid (EDTA).

Supplemental Table S8.
Supplemental Table S9.

Leaf tissue copper (Cu) concentrations of tomato grown in peat-based media under increasing concentrations of Cu with and without the presence of the chelate ethylenediaminetetraacetic acid (EDTA).

Supplemental Table S9.
  • Fig. 1.

    Normalized dry shoot mass of lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) grown in deep-flow hydroponics with increasing concentrations of copper (Cu) ethylenediaminetetraacetic acid (EDTA). Masses were normalized to the average dry mass of the 0 μM Cu controls within each trial (four trials for lettuce and one trial for tomato). Dry masses increased from 0 to 4 μM Cu (0.25 ppm) for lettuce (n = 58) and 8 μM Cu (0.5 ppm) for tomato (n = 13), but were correlated with negative linear regressions at greater Cu concentrations. The dashed vertical line in the graph denotes the typical Cu concentration in hydroponic nutrient solution.

  • Fig. 2.

    Concentration of copper (Cu) in leaf (A) and root (B) tissue of lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) grown in a deep-flow hydroponic solution with increasing concentrations of Cu ethylenediaminetetraacetic acid (EDTA). Lettuce leaf tissue data were correlated (P < 0.001, n = 20) with a rational regression (r2 = 0.91); tomato leaf tissue data were correlated (P = 0.01, n = 5) with a power regression (r2 = 0.99). Lettuce root tissue data were correlated (P < 0.001, n = 20) with a quadratic regression (r2 = 0.99); tomato root tissue data were correlated (P = 0.03, n = 5) with a power regression (r2 = 0.97). Data points represent leaf tissue from all replicate plants within each treatment for a composite sample. Copper concentration in leaf tissue is considered optimal from 5 to 20 mg⋅kg–1 (Marschner and Marschner 2012; Robinson 1987).

  • Fig. 3.

    Normalized dry shoot mass of lettuce (Lactuca sativa) (A) and tomato (Solanum lycopersicum) (B) grown in peat-based media with increasing concentrations of copper (Cu) with ethylenediaminetetraacetic acid (+EDTA) and without (–EDTA) chelation. Masses were normalized to the average dry mass of the zero Cu controls within each trial. Biomass accumulation for –EDTA lettuce (n = 27) decreased to a greater extent with increasing Cu concentration than +EDTA masses (n = 26). Masses for –EDTA tomato were correlated (P = 0.002, n = 15) with a rational regression (r2 = 0.65); and +EDTA masses were correlated (P < 0.001, n = 15) with a power regression (r2 = 0.74).

  • Fig. 4.

    Lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) grown in a peat-based media with a nutrient solution containing 1000 μM copper (Cu; 64 ppm) without chelation by ethylenediaminetetraacetic acid (–EDTA) (left) and with (+EDTA) (right). Toxicity effects were visually noticeable with chelation in lettuce, but not in tomato.

  • Fig. 5.

    Concentration of copper (Cu) in leaf tissue of lettuce (Lactuca sativa) (A) and tomato (Solanum lycopersicum) (B) grown in a peat-based media with increasing Cu concentrations with ethylenediaminetetraacetic acid (+EDTA) and without (–EDTA) chelation. Lettuce treatments were correlated (P = 0.01, n = 5) with power regressions (r2 = 0.99 for both). Tomato treatments were correlated (+EDTA, P = 0.002, n = 5; –EDTA, P = 0.04, n = 5) with power regressions (+EDTA, r2 = 0.99; –EDTA, r2 = 0.96). Leaf tissue from multiple plants within each treatment was combined in each data point. Copper concentration in leaf tissue is considered optimal from 5 to 20 mg⋅kg–1 (Marschner and Marschner 2012; Robinson 1987).

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  • Langenfeld, NJ, Pinto, DF, Faust, JE, Heins, R & Bugbee, B 2022 Principles of nutrient and water management for indoor agriculture Sustainability. 14 16 10204 https://doi.org/10.3390/su141610204

    • Search Google Scholar
    • Export Citation
  • Li, J, Leisner, SM & Frantz, J 2008 Alleviation of copper toxicity in Arabidopsis thaliana by silicon addition to hydroponic solutions J Am Soc Hortic Sci. 133 5 670 677 https://doi.org/10.21273/JASHS.133.5.670

    • Search Google Scholar
    • Export Citation
  • Liu, X, Jiang, Y, He, D, Fang, X, Xu, J, Lee, Y-W, Keller, NP & Shi, J 2020 Copper tolerance mediated by FgAceA and FgCrpA in Fusarium graminearum Front Microbiol. 11 1392 https://doi.org/10.3389/fmicb.2020.01392

    • Search Google Scholar
    • Export Citation
  • Lopez-Lima, D, Mtz-Enriquez, AI, Carrión, G, Basurto-Cereceda, S & Pariona, N 2021 The bifunctional role of copper nanoparticles in tomato: Effective treatment for Fusarium wilt and plant growth promoter Sci Hortic. 277 109810 https://doi.org/10.1016/j.scienta.2020.109810

    • Search Google Scholar
    • Export Citation
  • MacKay, DC, Chipman, EW & Gupta, UC 1966 Copper and molybdenum nutrition of crops grown on acid sphagnum peat soil Soil Sci Soc Am J. 30 6 755 759 https://doi.org/10.2136/sssaj1966.03615995003000060028x

    • Search Google Scholar
    • Export Citation
  • Marschner, H & Marschner, P 2012 Mineral nutrition of higher plants 3rd ed Elsevier/Academic Press Waltham, MA, USA https://doi.org/10.1016/C2009-0-63043-9

    • Search Google Scholar
    • Export Citation
  • Mukherji, S & Gupta, BD 1972 Characterization of copper toxicity in lettuce seedlings Physiol Plant. 27 2 126 129 https://doi.org/10.1111/j.1399-3054.1972.tb03588.x

    • Search Google Scholar
    • Export Citation
  • Nowakowski, W & Nowakowska, J 1997 Silicon and copper interaction in the growth of spring wheat seedlings Biol Plant. 39 463 466 https://doi.org/10.1023/A:1001009100026

    • Search Google Scholar
    • Export Citation
  • Printz, B, Lutts, S, Hausman, J-F & Sergeant, K 2016 Copper trafficking in plants and its implication on cell wall dynamics Front Plant Sci. 7 601 https://doi.org/10.3389/fpls.2016.00601

    • Search Google Scholar
    • Export Citation
  • Rhoads, FM, Olson, SM & Manning, A 1989 Copper toxicity in tomato plants J Environ Qual. 18 2 195 197 https://doi.org/10.2134/jeq1989.00472425001800020011x

    • Search Google Scholar
    • Export Citation
  • Ribeiro, TC, Weiblen, C, Botton, S de A, Pereira, DIB, de Jesus, FPK, Verdi, CM, Gressler, LT, Sangioni, LA & Santurio, JM 2017 In vitro susceptibility of the oomycete Pythium insidiosum to metallic compounds containing cadmium, lead, copper, manganese or zinc Med Mycol. 55 6 669 672 10.1093/mmy/myw115

    • Search Google Scholar
    • Export Citation
  • Robinson, JD 1987 Diagnosis of mineral disorders in plants: Glasshouse crops 1st ed Her Majesty’s Stationary Office Richmond, UK

  • Sen Gupta, B, Curran, M, Hasan, S & Ghosh, TK 2009 Adsorption characteristics of Cu and Ni on Irish peat moss J Environ Manage. 90 2 954 960 https://doi.org/10.1016/j.jenvman.2008.02.012

    • Search Google Scholar
    • Export Citation
  • Shams, M, Ekinci, M, Turan, M, Dursun, A, Kul, R & Yildirim, E 2019 Growth, nutrient uptake and enzyme activity response of lettuce (Lactuca sativa L.) to excess copper Environ Sustain. 2 1 67 73 https://doi.org/10.1007/s42398-019-00051-7

    • Search Google Scholar
    • Export Citation
  • Shang, H, Ma, C, Li, C, Zhao, J, Elmer, W, White, JC & Xing, B 2021 Copper oxide nanoparticle-embedded hydrogels enhance nutrient supply and growth of lettuce (Lactuca sativa) infected with Fusarium oxysporum f. sp. lactucae Environ Sci Technol. 55 20 13432 13442 https://doi.org/10.1021/acs.est.1c00777

    • Search Google Scholar
    • Export Citation
  • Shukla, SR, Gaikar, VG, Pai, RS & Suryavanshi, US 2009 Batch and column adsorption of Cu(II) on unmodified and oxidized coir Sep Sci Technol. 44 1 40 62 10.1080/01496390802281984

    • Search Google Scholar
    • Export Citation
  • Shukla, SR & Pai, RS 2005 Adsorption of Cu(II), Ni(II) and Zn(II) on dye loaded groundnut shells and sawdust Separ Purif Tech. 43 1 1 8 https://doi.org/10.1016/j.seppur.2004.09.003

    • Search Google Scholar
    • Export Citation
  • Silber, A 2019 Chemical characteristics of soilless media 113 148 Raviv, M, Lieth, H & Bar-Tal, A Soilless culture: Theory and practice. Elsevier Amsterdam, Netherlands https://doi.org/10.1016/B978-0-444-63696-6.00004-9

    • Search Google Scholar
    • Export Citation
  • Sonmez, S, Kaplan, M, Sonmez, NK, Kaya, H & Uz, I 2006 High level of copper application to soil and leaves reduce the growth and yield of tomato plants Sci Agric. 63 3 213 218 https://doi.org/10.1590/S0103-90162006000300001

    • Search Google Scholar
    • Export Citation
  • Thounaojam, TC, Panda, P, Mazumdar, P, Kumar, D, Sharma, GD, Sahoo, L & Sanjib, P 2012 Excess copper induced oxidative stress and response of antioxidants in rice Plant Physiol Biochem. 53 33 39 https://doi.org/10.1016/j.plaphy.2012.01.006

    • Search Google Scholar
    • Export Citation
  • Tills, AR 1987 Chelates in horticulture Chartered Inst Hortic. 1 4 120 125

  • Yruela, I 2005 Copper in plants Braz J Plant Physiol. 17 1 145 156 https://doi.org/10.1590/S1677-04202005000100012

  • Yruela, I 2009 Copper in plants: Acquisition, transport and interactions Funct Plant Biol. 36 5 409 https://doi.org/10.1071/FP08288

  • Zabrieski, Z, Morrell, E, Hortin, J, Dimkpa, C, McLean, J, Britt, D & Anderson, A 2015 Pesticidal activity of metal oxide nanoparticles on plant pathogenic isolates of Pythium Ecotoxicol. 24 6 1305 1314 https://doi.org/10.1007/s10646-015-1505-x

    • Search Google Scholar
    • Export Citation
Mackenzie G. Dey Department of Plants, Soils, and Climate, Utah State University, Crop Physiology Laboratory, 1410 N. 800 E., Logan, UT 84322-4820, USA

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Noah J. Langenfeld Department of Plants, Soils, and Climate, Utah State University, Crop Physiology Laboratory, 1410 N. 800 E., Logan, UT 84322-4820, USA

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Bruce Bugbee Department of Plants, Soils, and Climate, Utah State University, Crop Physiology Laboratory, 1410 N. 800 E., Logan, UT 84322-4820, USA

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Contributor Notes

This research was supported by the Utah Agricultural Experiment Station, Utah State University (approved as journal paper no. 9619); and the National Aeronautics and Space Administration, Center for the Utilization of Biological Engineering in Space (grant no. NNX17AJ31G).

We acknowledge conscientious technical assistance from our undergraduate students to execute this study. We also acknowledge the anonymous reviewers who provided helpful feedback to improve this manuscript and broaden its reach.

Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

M.G.D. is the corresponding author. E-mail: jones.mack12@gmail.com.

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