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ASHS 2024 Annual Conference

 

Identifying Lettuce Accessions for Efficient Use of Phosphorus in Hydroponics

Authors:
Gustavo F. Kreutz Horticultural Sciences Department, Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA

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Jehangir H. Bhadha Department of Soil, Water, and Ecosystem Sciences, Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA

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Guodong D. Liu Horticultural Sciences Department, University of Florida, 2550 Hull Road, Gainesville, FL 32611, USA

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Germán V. Sandoya Horticultural Sciences Department, Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA

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Abstract

Lettuce (Lactuca sativa L.) is the most common leafy vegetable produced hydroponically in the United States. Although hydroponic systems are advantageous due to lower pest and disease pressure, and reduced water and nutrient requirements, the increasing prices of fertilizers, including phosphorus (P), still influences the profitability of hydroponic production of lettuce. Characterizing lettuce germplasm capable of producing high yield using less P inputs may help reduce fertilizer use, production costs, and P loads in wastewater. In this study, 12 lettuce accessions were grown in four experiments in a nutrient film technique system. In the first two experiments, the treatments consisted of two P concentrations (3.1 and 31 mg·L−1). Lettuce cultivated with 3.1 mg·L−1 of P had variable shoot and root biomass, root–shoot ratio, P uptake efficiency, and P utilization efficiency, indicating the existence of genetic variation. Five accessions (‘Little Gem’, 60183, ‘Valmaine’, BG19-0539, and ‘Green Lightning’) were considered efficient to P because produced similar shoot biomass with the low and high P treatments. In the third and fourth experiments, the treatments consisted of two P sources (monosodium phosphate (NaH2PO4) and tricalcium phosphate [TCP; Ca3(PO4)2]. Initially, extra 5 mM of calcium (Ca) was added to the TCP solution to reduce the TCP solubility and, hence, P bioavailability to plants. All accessions produced similar shoot and root weight with both treatments, indicating that the TCP treatment did not cause low-P stress to the plants. After, the extra Ca concentration added to TCP was increased to 10 mM, resulting in low-P stress and a significant reduction in shoot weight of all accessions. Despite the severe P stress, ‘Little Gem’ and 60183 were among the accessions with the least shoot weight reduction in the TCP treatment. Variability was observed in root biomass root–shoot ratio among accessions under the TCP treatment, suggesting that lettuce accessions responded differently to P stress conditions. The genetic variation for P use efficiency (PUE) and PUE-related traits in lettuce grown hydroponically suggests the feasibility of breeding new lettuce cultivars from elite lettuce germplasm adapted to low P availability in hydroponics.

Lettuce (Lactuca sativa L.), one of the most consumed vegetables worldwide, is a versatile crop that can be produced in a wide range of production systems, from field to greenhouse (Ahmed et al. 2021; Sandoya 2019; Sandoya et al. 2021). In recent years, hydroponic systems such as floating raft, nutrient film technique, and vertical towers have been increasingly adopted for lettuce production in the United States (Resh 2022). This phenomenon is, in part, a result of the identification of lettuce cultivars suitable for hydroponic production that allow growers to achieve yields similar to those observed in field cultivation (Resh 2022). Hydroponic systems allow cultivation of lettuce with better management of water, nutrients, light and temperature, lower pressure from pests and diseases, greater yield per unit area, and shorter life cycle (Resh 2022; Sharma et al. 2018).

Despite the many advantages, hydroponic farming presents some constraints especially regarding the high capital costs to establish and operate these systems (Resh 2022). Additional challenges include the high costs of fertilizers and the environmental risks associated with nutrient losses, especially in open systems such as rockwool, sand, and sawdust cultures that are incapable of recycling them (Choi et al. 2011; Resh 2022). Among these nutrients, phosphorus (P) is an element essential to plants that derive from nonrenewable sources and is commonly associated with eutrophication (Raghothama 1999). Moreover, the high global demand for phosphate fertilizers and their price fluctuations cause risks to farming operations due to increased production costs (Sarvajayakesavalu et al. 2018). The drawbacks of P fertilizer use in hydroponic systems can be mitigated by breeding and adopting P-efficient cultivars that produce similar yield in solutions with lower nutrient inputs.

Phosphorus use efficiency (PUE), a concept defined as higher capacity of plants to produce economic yield per unit of applied P, could reduce P inputs in crop production while maximizing productivity (Fageria et al. 2017). P-efficient cultivars may present higher capacity to absorb P from growth medium due to improved morphological and physiological mechanisms such as superior root architecture and density (Lan et al. 2015; Wen et al. 2019). Alternatively, P-efficient cultivars may use internal P more efficiently through higher capacity of internal P transport, distribution, allocation, and remobilization (Parentoni et al. 2012). For instance, higher root-to-shoot (R–S) biomass ratio in rye (Secale cereale L.) and wheat (Triticum spp.) confer these crop species with superior P uptake efficiency, whereas less efficient crops such as bean (Phaseolus vulgaris L.), onion (Allium cepa L.), and tomato (Lycopersicon esculentum Mill.) tend to show low R–S ratios (Raghothama 1999). In potato (Solanum tuberosum L.), PUE was correlated with total plant biomass and total P uptake (Sandaña, 2016). Similarly, higher P uptake and P utilization were associated with increased PUE in mustard (Brassica juncea L.) (Aziz et al. 2006).

Hydroponic studies have been conducted to understand the effect of P limitation on physiological parameters and growth of maize (Zea mays L.), sorghum [Sorghum bicolor (L.) Moench], potato, rice (Oryza sativa L.), and lettuce (Bera et al. 2018; Delaide et al. 2016; Islam et al. 2019; Lee et al. 2021; Neocleous and Savvas 2019; Nirubana et al. 2020; Sapkota et al. 2019). Nevertheless, further research is needed to identify and characterize lettuce accessions with higher PUE in hydroponics. P-efficient lettuce accessions could benefit hydroponic growers by reducing P inputs and/or improving the efficiency of P fertilizers applied to the nutrient solutions, especially in systems like aquaponics where P solubility is reduced due to high pH (Anderson et al. 2017). There is already identified lettuce that responds differently to a 50% reduction of the recommended P rate application in field conditions (Kreutz et al. 2022); therefore, genetic variation for PUE in greenhouse can exist but warrants research. However, PUE in field does not often correlate with PUE in a greenhouse in a variety of crops (Parentoni et al. 2012); consequently, accessions with higher PUE in field might not be efficient in low P in greenhouse and vice versa. In field, PUE is conditioned by environmental factors (e.g., rainfall and soil temperature), plant–soil interactions, and pest, weed and disease incidence (Parentoni et al. 2012). In contrast to fields, greenhouses allow for a more controlled growing environment for lettuce, especially in terms of temperature, water availability, and pest and disease control. Therefore, the objective of this study was to identify and characterize lettuce accessions capable of producing acceptable yield in suboptimal P conditions. To identify elite lettuce genotypes, mimicked soil solutions with low-P bioavailability were employed; a set of lettuce accessions was tested for PUE and PUE-related traits with two P concentrations and two different P sources in hydroponics.

Materials and Methods

Plant material.

A set of 12 lettuce accessions were tested for PUE in hydroponic settings in a glasshouse at the University of Florida Institute of Food and Agricultural Sciences (UF/IFAS) Everglades Research and Education Center (EREC), in Belle Glade, FL. Most accessions, except for one (BG19-0539), were previously tested for PUE in field conditions and considered as P-efficient or P-inefficient (Kreutz et al. 2022). Seeds of all accessions, that included six romaine, five crisphead, and one Latin (Table 1), were previously increased by the UF/IFAS Lettuce Breeding Program.

Table 1.

Lettuce accessions grown in four hydroponic experiments.

Table 1.

Experiment description.

Four experiments (E1, E2, E3, E4) were conducted from Oct through Dec 2020 (E1), from Dec 2020 through Feb 2021 (E2), from Dec 2021 through Jan 2022 (E3), and from Jan through Mar 2022 (E4), respectively. Seeds of the 12 accessions were germinated in rockwool cubes (Gro-Block, Grodan Rockwool B.V., The Netherlands), and seedlings were transferred to two nutrient film technique (NFT) structures (CropKing Inc., Lodi, OH, USA) at 10–16 d after sowing and at a plant density of 26 plants/m2. The two NFT systems were located inside of a glasshouse with natural sunlight and semicontrolled temperature adjusted by an air-conditioner.

Both NFT systems were supplied with a modified Howard Resh solution (Resh, 2022) with the following composition: 7.5 mM KNO3, 4 mM Ca(NO3)2·4H2O, 0.5 mM NH4NO3, 0.5 mM NaNO3, 2 mM MgSO4·7H2O, 50 µM KCl, 50 µM H3BO3, 12 µM MnSO4·4H2O, 2 µM ZnSO4·7H2O, 1.5 µM CuSO4·5H2O, 0.1 µM (NH4)6Mo7O24·4H2O, and 10 µM NaFeEDTA. In E1 and E2, treatments consisted of two P levels; each NFT system was supplied with a unique concentration of phosphoric acid (H3PO4): 0.1 mM (3.1 mg·L−1) or 1 mM (31 mg·L−1), herein named low P and high P, respectively. In E3 and E4, each NFT system was supplied with a unique P source: 1 mM NaH2PO4 (monosodium phosphate; MSP) or 0.5 mM Ca3(PO4)2 (tricalcium phosphate; TCP; Ksp = 2.7 × 10−33). In E3, an additional 5 mM of Ca was added to the TCP treatment in the form of CaCl2 to limit the availability of P. Because differences in plant biomass among the two P treatments were not significant in E3, 10 mM of Ca was added to the TCP treatment in E4 to reduce P availability.

In all experiments, nutrient solutions were prepared using deionized water obtained from the Soil, Water, and Nutrient Management Laboratory at EREC. Each NFT system was connected to a 100-L reservoir containing the nutrient solution. The 12 lettuce accessions in all experiments were arranged in a completely randomized design with three replicates on each P treatment, and each replicate consisted of a single plant. Electrical conductivity (EC) of the solutions was monitored daily and maintained within a range of 1.4 to 1.8 dS/m, and pH was adjusted to 6.0 ± 0.1 (optimal pH range for lettuce) by adding hydrochloric acid (HCl) or sodium hydroxide (NaOH). Nutrient solutions were discarded, and tanks were recharged every 2 weeks to avoid any unbalance of ions.

Data collection.

According to horticultural maturity, plants were harvested at 51, 58, 42, and 41 d after sowing in E1, E2, E3, and E4, respectively. Plants were evaluated for root and shoot fresh weight (grams), root and shoot dry weight (DW, grams). To measure shoot and root weight, plants were harvested, separated into roots and shoots, and weighed. Following harvest, roots and shoots were oven-dried at 65 °C for 5 d to obtain shoot and root DW. Shoot and root tissue samples were then subjected to total-P (TP) extraction to determine P concentration.

Briefly, the TP extraction protocol consisted of weighing 0.4 g of dried ground plant tissue into a 20-mL glass scintillation vial. Samples were then placed in a muffle furnace and burnt to ashes at 550 °C for 5 h 30 min. Once samples reached room temperature, they were moistened by adding five drops of deionized water. Each sample then received 2 mL of 6 M hydrochloric acid (HCl) and was maintained at room temperature for 2 h. The volume of each vial was then gaged to 20 mL, filtered with qualitative P5 filter paper (12.5 cm in diameter), and transferred to 15-mL polypropylene test tubes. The total P concentration of samples was determined using an inductively coupled plasma optical emission spectrometer (ICP-OES Agilent Technologies 5110, Santa Clara, CA, USA) at the UF/IFAS Soil, Water, and Nutrient Management Laboratory.

The following PUE parameters were estimated for all accessions in each of the P treatments: R–S biomass ratio, represented by the proportion of root biomass relative to shoot biomass; relative P uptake efficiency (PUpE; mg P mg·L−1 P), characterized by the total plant P content per unit of applied P; P utilization efficiency (PutE), characterized by the total biomass produced per unit of absorbed P (g DW mg·P−1), as described by Hammond et al. (2009) and Neto et al. (2016) (Table 2).

Table 2.

Definition, abbreviation, formula, and unit of phosphorus use efficiency parameters estimated for 12 lettuce accessions grown in four hydroponic experiments.

Table 2.

Statistical analyses.

For E1 and E2, analyses of variance (ANOVAs) for shoot weight, root weight, shoot TP, and root TP were performed among accessions, P treatments, experiments, and their respective interactions. All factors were treated as fixed effects. Because the concentration of Ca added to the TCP treatment in E4 was twice the Ca concentration used in E3, data from E3 and E4 were analyzed separately. Thus, ANOVA for shoot weight, root weight, shoot TP, and root TP was performed among accessions, P treatments, and the accession × P treatment interaction. All factors were considered as fixed effects. For all experiments, an additional ANOVA was conducted to identify differences in PUpE and PUtE following the model previously described.

Accessions were then pairwise compared (t tests) to identify nonsignificant differences for each trait among P rates. One accession was considered as P-efficient when its head weight reduction under P stress was less than 20% compared with the optimal P treatment.

In all analyses, least square means were generated using the lsmeans statement and differences for accessions within each treatment were determined by using Fisher’s protected least significant difference test at a level of significance of P = 0.05. Pearson correlation coefficients were calculated between shoot weight reduction, R–S biomass ratio, PUpE, and PUtE for each of the two P treatments. The coefficients were based on genotypic means across experiments and replicates. All analyses were carried out using GLIMMIX and CORR procedures in SAS software ver. 9.4 (SAS Institute Inc., Cary, NC, USA).

Results

Lettuce responds to different phosphorus levels (E1 and E2).

Applying only 10% of the optimal P level in the P solution aided to characterize germplasm that produced similar yield at low P compared with high P treatment in the NFT system. Significant differences (P < 0.05) were detected for shoot and root weight among accession (G), P treatment (T), experiment (E), and the interactions G×E and T×E (Supplemental Table 1). The G×T interaction was found to be slightly significant (P = 0.0434) for shoot weight, but not for root weight (P = 0.3033) (Supplemental Table 1).

Although lettuce shoot weight decreased when plants were grown at low P concentration, five lettuce accessions (‘Little Gem’, 60183, ‘Valmaine’, BG19-0539, and ‘Green Lightning’) presented a shoot weight reduction of 20% or less with low P as compared with high P. ‘Little Gem’ and 60183 were the accessions with the most similar shoot weight across the two treatments (shoot weight reduction of –6% and 11%, respectively) (Table 3; Fig. 1).

Fig. 1.
Fig. 1.

Least square means of shoot and root weight (g/plant) with 95% confidence intervals of 12 lettuce accessions grown under low and high P in E1 and E2. Shoot weight means with different lowercase letters and root weight means with different uppercase letters within an accession are significantly different at P ≤ 0.05 using the least significant difference test.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

Table 3.

Shoot and root weight reduction (%) and respective standard error and P values, root-to-shoot (R–S) biomass ratio, P uptake efficiency (PUpE, mg P mg·L−1 P applied), and P utilization efficiency (PUtE, g DW mg−1 P) of 12 lettuce accessions grown under low and high P in E1 and E2.

Table 3.

In contrast to shoot weight, the reduction in P concentration from 31 to 3.1 mg·L−1 caused a highly significant increase (P < 0.0001) in the overall root biomass in lettuce. Five accessions (H1078, ‘Honcho II’, ‘Little Gem’, ‘Okeechobee’, ‘Sun Devil’) showed similar (P > 0.75) root weight in low and high P (Table 3; Fig. 1). At low P, the romaine breeding line 60183 and cv. Valmaine had a significantly higher root weight compared with high P treatment (P = 0.0040 and P = 0.0086, respectively), indicating root growth promotion of these accessions when subjected to P stress (Fig. 1).

The 10% of P in the nutrient solution led to significant differences in shoot TP among accessions (P < 0.0001), P treatments (P < 0.0001), experiments (P < 0.0001), and the interactions G×E (P = 0.0002), T×E (P < 0.0001), and G×T×E (P < 0.0001). Meanwhile, P treatment (P < 0.0001), experiment (P = 0.0179), and the interaction T×E (P < 0.0001) were the only statistically significant factors for root TP of lettuce (Supplemental Table 1). With low P, all accessions showed a significant (P < 0.05) reduction in shoot TP compared with high P treatment. ‘Little Gem’ showed the greatest shoot TP concentration with both, low and high P (Supplemental Fig. 1). These results indicate the presence of genetic variation for shoot TP concentration in lettuce grown under suboptimal and optimal conditions. Considering root TP, a significant decrease was observed under low P vs. high P for most accessions, except for ‘Floricos 83’ and ‘Lantana’ (P = 0.0890 and P = 0.0752, respectively) (Supplemental Fig. 1). While no significant differences (P > 0.05) in root TP were detected among accessions at low P treatment, accessions ‘Sun Devil’, ‘Green Lightning’, and 60183 had the greatest root TP concentration at high P (Supplemental Fig. 1).

In lettuce, PUE is dependent on multiple plant traits, including root morphology, PUpE, PUtE. P-efficient accessions tend to produce greater root biomass when grown in P-deficient conditions, as noted by the greater root weight of lettuce plants with low P compared with high P. As a consequence, 10 of 12 accessions showed a greater R–S biomass ratio at low P. Among these, the crisphead ‘Green Lightning’ had the greatest R–S ratio under low P, indicating that this accession responded the most to the low-P stress by increasing its root biomass relative to the shoot biomass (Table 3).

It was also found that accessions differed significantly (P < 0.05) in PUpE and PUtE at low P treatment. However, PUpE and PUtE were associated with specific accessions. For instance, the romaine breeding line 60183 and ‘Manatee’ were the most efficient accessions at absorbing P from the solution (PUpE), whereas romaine ‘Okeechobee’ and ‘Floricos 83’ used internal P more efficiently (PUtE) (Table 3).

The shoot weight reduction of plants under low P relative to high P was negatively correlated with R–S ratio (r = –0.62; P = 0.0318) in this study. This suggests that accessions with greater R–S ratio in optimal P conditions are less affected by shoot biomass reduction when grown with low P. In contrast, shoot weight reduction was found to be positively correlated with PUpE at high P (r = 0.58; P = 0.0496), and with PUtE at low P (r = 0.70; P = 0.0116) and high P (r = 0.62; P = 0.0321). These results indicate that the reduction in shoot weight of lettuce grown under P-deprived conditions is inversely proportional to the capacity of plants to absorb P (under high P conditions) and/or use P internally. Additionally, a positive and slightly significant correlation between PUtE of lettuce grown at low and high P treatments was observed (r = 0.60; P = 0.0412). At low P treatment, a negative, nonsignificant correlation (r = –0.45; P = 0.1428) between PUpE and PUtE was observed. The lack of correlation between PUpE and PUtE indicates that these two parameters may be driven by independent mechanisms in lettuce.

Lettuce responds to different phosphorus sources (E3 and E4).

Although differences were found to be significant for both shoot and root weight (P < 0.0001 and P < 0.0001, respectively) among accessions, the G×T interaction was not significant for both traits (P > 0.05) in E3. The utilization of TCP as a source of P plus an additional 5 mM of Ca did not significantly (P > 0.05) affect the shoot and root weight of lettuce (Supplemental Table 2; Supplemental Fig. 2). All the 12 tested accessions produced statistically the same (P > 0.05) shoot weight under the TCP and MSP treatments (Fig. 2).

Fig. 2.
Fig. 2.

Least square means of shoot and root weight (g/plant) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3. Shoot weight means with different lowercase letters and root weight means with different uppercase letters within an accession are significantly different at P ≤ 0.05 using the least significant difference test.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

Only slight differences were found for root weight in the romaine accessions BG19-0539 and ‘Valmaine’, which produced less root biomass when grown in the TCP treatment (P = 0.0181 and P = 0.0494, respectively); the opposite was true for the romaine breeding line 60183 that had significantly higher root weight when cultivated in the TCP treatment (P = 0.0262) (Fig. 2). Likewise, no significant differences (P > 0.05) were detected for shoot TP and root TP among accessions, P treatments, and the G×T interaction in E3 (Supplemental Table 2). Most accessions presented statistically the same (P > 0.05) shoot TP and root TP under both P treatments, except for the romaine cv. Okeechobee that had significantly less shoot TP at the TCP treatment (Supplemental Fig. 3).

Due to the nonsignificant differences between the two initial P sources, the concentration of Ca added to the TCP treatment was raised to 10 mM in E4. The addition of 10 mM of Ca caused the shoot weight and root weight of lettuce to drastically decrease (P < 0.0001 and P < 0.0001, respectively) compared with the MSP treatment (Supplemental Table 2; Supplemental Fig. 2). As a consequence, all 12 accessions experienced significant (P < 0.05) shoot weight reduction when grown under TCP (Fig. 3). The cv. Manatee, cv. Little Gem, and breeding line BG19-0539 showed a highly similar (P > 0.50) root weight under TCP and MSP treatments (Fig. 3). In contrast, five lettuce accessions (‘Green Lightning’, H1078, ‘Lantana’, ‘Okeechobee’, and ‘Sun Devil’) yielded significantly less (P < 0.05) root weight when cultivated in TCP vs. MSP (Fig. 3).

Fig. 3.
Fig. 3.

Least square means of shoot and root weight (g/plant) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E4. Shoot weight means with different lowercase letters and root weight means with different uppercase letters within an accession are significantly different at P ≤ 0.05 using the least significant difference test.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

The addition of extra Ca into the TCP treatment in E4 significantly influenced lettuce tissue P concentration, as observed by the differences in shoot TP and root TP among accessions (P < 0.05) and P treatment (P < 0.05) (Supplemental Table 2). The G×T interaction was found to be nonsignificant (P > 0.05) for both shoot TP and root TP. All accessions showed a significant reduction in shoot TP when grown under the TCP source compared with the MSP treatment (Supplemental Fig. 4). Meanwhile, only three accessions (60183, ‘Little Gem’, and ‘Manatee’) experienced a significant decrease in root TP in the roots under the TCP treatment (P = 0.0294, P = 0.0228, and P = 0.0063, respectively) (Supplemental Fig. 4).

Lettuce plants cultivated in the TCP treatment did not present a higher root growth as nonsignificant differences in the overall R–S ratio of lettuce were observed between the two P sources (TCP and MSP) in both experiments, E3 (P = 0.1615) and E4 (P = 0.1669). However, significant (P < 0.05) genetic variability for R–S ratio was found within the germplasm evaluated in the TCP treatment (Tables 4 and 5). In E4, crisphead cv. Honcho II obtained the highest R–S ratio among all accessions, whereas the romaine breeding lines 60183 and BG19-0539 had the lowest R–S ratio (Table 5). These results indicate that under the TCP treatment, some accessions were more responsive to the lower P availability in the solution than others, as observed by the higher root biomass relative to the shoot biomass.

Table 4.

Shoot and root weight reduction (%) and respective standard error and P values, root-to-shoot (R–S) biomass ratio, P uptake efficiency (PUpE, mg P mg·L−1 P applied), and P utilization efficiency (PUtE, g DW mg·P−1) of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3.

Table 4.
Table 5.

Shoot and root weight reduction (%) and respective standard error and P values, root-to-shoot (R–S) biomass ratio, PUpE (mg P mg·L−1 P applied), and PUtE (g DW mg P−1) of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E4.

Table 5.

In E4, lettuce accessions significantly (P < 0.05) differed in P uptake efficiency (PUpE) only under the MSP treatment. Despite the genetic variability in PUpE under optimum P conditions, TCP with 10 mM of Ca caused severe P stress to the plants, likely leading to nonsignificant differences (P > 0.05) in P uptake among accessions. Under MSP, the crisphead cv. Green Lightning and the romaine cv. Manatee had the highest PUpE scores, indicating that these accessions were able to uptake more P under optimum conditions than the other accessions. The crisphead cv. Honcho II had the lowest PUpE among all the accessions (Table 5). No significant differences (P > 0.05) in PUtE were detected among accessions in both MSP and TCP treatments (Table 5).

In both experiments (E3 and E4), PUpE and PUtE of lettuce accessions grown with the MSP treatment were found to be negatively correlated (r = –0.68; P = 0.0304 in E3 and r = –0.62; P = 0.0327 in E4). In addition, the lack of correlation between both parameters under TCP treatment in E3 and E4 could be an affirmation that PUpE and PUtE might be controlled by independent mechanisms in lettuce when grown under suboptimal P conditions.

In E3 and E4, shoot weight reduction was not correlated with R–S ratio, PUpE, or PUtE, regardless of the P solution in which plants were grown. Nevertheless, R–S ratio of lettuce was found to be negatively correlated (r = –0.67; P = 0.0168) with PUpE at the TCP treatment in E4, suggesting that accessions with greater root biomass relative to the shoot biomass had a smaller P uptake efficiency, and vice versa. In E4, PUpE under TCP and MSP were positively correlated (r = 0.67; P = 0.0169), denoting that those accessions with superior P uptake in optimal P conditions also performed well when P availability was reduced.

Discussion

Lettuce response to different phosphorus levels.

Genetic variation for PUE was identified in lettuce grown with different P levels and P sources, as observed by the discrepancies in the percentage of shoot weight reduction between P treatments and the significant differences in PUpE and PUtE among the accessions tested. Applying only 10% of the optimal P recommended concentration led to a decrease in the shoot weight of lettuce. Intraspecific genotypic variation in shoot weight was detected in five cultivars and breeding lines producing similar shoot weight in P-limited conditions. This suggests that lettuce germplasm responded differently to the reduction in P availability in greenhouse, as described in lettuce grown in field (Kreutz et al. 2022). Breeding line 60183 and ‘Little Gem’ produced similar head weight under half-P and standard-P rates in field and greenhouse conditions and are considered P-efficient (Kreutz et al. 2022). ‘Okeechobee’ experienced the greatest reduction in shoot weight when grown in low P in hydroponics, contrasting results from field experiments (Kreutz et al. 2022). These findings indicate that PUE of lettuce in specific accessions varies according to the environment and growing conditions. Likewise, PUE in wheat, sorghum, and maize is environment-dependent (Parentoni et al. 2012).

A significant increase in root weight of lettuce when grown at low P observed in this research is a response of plants to the lower P availability, leading to a greater R–S ratio in lettuce (Bertossi et al. 2013; Neocleous and Savvas 2019). However, the R–S ratio was not correlated to PUpE at low P treatment, suggesting that P uptake of lettuce plants was not improved by the increases in root weight. This likely occurred due to limited amounts of P in the solution, which in turn, precluded the continuous P uptake by roots after all the P was fully depleted from the solution (Lee et al. 2021; van de Wiel et al. 2016). As opposed to these results, the increase of root biomass often contributes to a greater P scavenging capacity of plants, and consequently, greater P uptake in field conditions (van de Wiel et al. 2016).

Some lettuce accessions have the capacity to uptake more P than others. All 12 accessions were in the same NFT system and grown in the same nutrient solution in the experiments, and therefore the differences observed in PUpE can be attributed to the genetic makeup of each accessions. This hypothesis could explain the significantly greater PUpE observed for accessions 60183 and ‘Manatee’ at low P treatment. Nevertheless, 60183 and ‘Manatee’ were considered P-efficient and P-inefficient accessions in previous field evaluations, suggesting that additional biological (morphological and/or physiological traits) and environmental factors may be involved in PUE in lettuce (Kreutz et al. 2022).

Lettuce response to different phosphorus sources.

In an initial experiment, lettuce accessions were subjected to TCP [Ca3(PO4)2] containing an extra 5 mM of Ca to mimic a growing medium where P is present in non-bioavailable forms. The bioavailability of P in the solution depends on the equilibrium of Ca+2 and PO4−3 ions [i.e., solubility product (Ksp)] (Lee et al. 2021). When supplemental Ca is absent or low, sufficient P is mobilized from TCP in the nutrient solution; therefore, the TCP solution had enough P to support lettuce growth in E3. Consequently, the discrimination of P-efficient lettuce accessions was not possible, similarly to studies conducted in wheat, in which the shoot biomass was not reduced when plants were grown under a treatment containing TCP combined with 10 mM of extra Ca (Liu et al. 2007). The method has proven to be efficient at detecting PUE in crops as genotypic variability for PUE was detected in Indian mustard, potato, and wheat grown in solutions containing TCP with the addition of Ca (Aziz et al. 2006; Bera et al. 2020; Lee et al. 2021; Liu et al. 2007). Thus, each species responds differently to different levels of P solubility in the growing medium.

In a follow-up experiment, the concentration of extra Ca added to the TCP treatment was increased to 10 mM. The extra Ca added in E4 likely decreased the solubility of P to a point in which plants were no longer able to achieve adequate shoot growth and favored the precipitation of P. In turn, shoot weight, root weight, shoot TP, and root TP of lettuce accessions substantially decreased, as observed in wheat (Akhtar et al. 2016). In addition to higher P precipitation, the extra 10 mM of Ca could have contributed to a Ca-Mg or Ca-K antagonism (inhibition of Mg or K uptake due to high Ca concentration), as previously seen in Vitis vinifera L. grown hydroponically (Garcia et al. 1999). Consequently, the uptake of Mg and/or K could have been reduced, which would result in lower lettuce yield. In this research, lettuce had different levels of internal P utilization (PUtE) at low P. Interestingly, accessions with the greatest PUtE values experienced the greatest shoot weight reduction. The negative correlations between PUtE and lettuce shoot weight could be an indication of greater P starvation rather than superior P utilization by lettuce plants, as previously reported in rice grown with moderate to extreme low P levels (Rose and Wissuwa 2012; Wissuwa et al. 1998).

Phosphorus levels versus phosphorus sources.

In this study, lettuce accessions were tested for PUE under two P levels (low and high P) and two P sources (MSP and TCP). The former approach has successfully allowed the identification of two lettuce accessions (‘Little Gem’ and 60183) that produced highly similar shoot weight under low and high P. A similar technique has been previously used to evaluate potato and soybean [Glycine max (L.) Merr.] accessions in hydroponics (Lee et al. 2021; Ochigbo and Bello, 2014). A possible disadvantage of testing plants for PUE under low P concentrations is the complete depletion of P in the nutrient solution upon plant uptake, which may inhibit root hair formation as reported in Arabidopsis thaliana L. (Liu et al. 2006). While root hairs were not closely examined in this study, five lettuce accessions produced similar root weight under both P levels, suggesting that their root growth was not inhibited by the low P treatment.

In the second approach, lettuce accessions were tested under different P sources (MSP and TSP combined with Ca). This method has been previously applied to test mustard, wheat, and potato accessions for PUE (Akhtar et al. 2016; Aziz et al. 2006; Lee et al. 2021; Liu et al. 2007). The proper Ca/TSP ratio varies according to the crop species as intra- and interspecific variation exists for traits such as P uptake, P mobilization, and Ca uptake (Akhtar et al. 2016; Lee et al. 2021). For instance, species with greater Ca uptake led to more P release in TCP solutions (Lee et al. 2021). In this study, 5 mM of Ca added to the TSP solution was insufficient to cause yield differences in lettuce. In a second trial, 10 mM of Ca added to the TCP solution led to significant yield reductions in lettuce. Despite the severe P stress, ‘Little Gem’ and 60183 were among the accessions with the least shoot weight reduction in the TCP treatment, confirming the results observed in the low and high P trials. This indicates that the two approaches resulted in similar findings regardless of the magnitude of the P deficient stress caused by the treatments. However, further investigations should be conducted to determine the proper Ca/TCP ratio that will allow the identification of P-efficient lettuce accessions in hydroponics.

Conclusions

Despite previous efforts to investigate the effects of P limitation in hydroponic lettuce, the identification and characterization of lettuce accessions grown with different P concentrations and sources remained unexplored before this study. We identified lettuce accessions with superior PUE in hydroponics that may be used for breeding new elite cultivars adaptive to suboptimum P conditions. In this research, genetic variation for PUE was detected in lettuce accessions grown hydroponically when 10% of P was used in the growing solution. Accessions 60183 and ‘Little Gem’ are considered efficient when grown at 10% of the optimal P concentration in hydroponics. Shoot biomass of lettuce was unaffected when the TCP had an extra 5 mM of Ca. In contrast, drastic reductions in yield were observed when lettuce accessions were grown at TCP accompanied by an extra 10 mM of Ca, hindering the discrimination of P-efficient and P-inefficient accessions. Future research should investigate proper ratios of Ca (between 5 and 10 mM) and P in nutrient solutions that allow the discrimination of P-efficient lettuce accessions under TCP conditions.

In addition, genotypic variation for R–S ratio (an indicative of P-stress response), PUpE, and PUtE was detected across the different P treatments and offers an opportunity to use these parameters for selecting lettuce for PUE breeding. Although, these PUE-related traits require the measurement of additional characteristics such as fresh and dry weight, and P concentration in shoots and roots that might difficult the use of these characteristics for selection. Instead, the detection of characteristics highly associated with PUE-related traits can aid the selection of P-efficient lettuce accessions for hydroponic production. The identification of indirect traits linked to PUE should facilitate and expedite the development of new P-efficient lettuce cultivars.

References Cited

  • Ahmed, ZFR, Alnuaimi, AKH, Askri, A & Tzortzakis, N 2021 Evaluation of lettuce (Lactuca sativa L.) production under hydroponic system: Nutrient solution derived from fish waste vs. inorganic nutrient solution Horticulturae. 7 9 292 https://doi.org/10.3390/horticulturae7090292

    • Search Google Scholar
    • Export Citation
  • Akhtar, MS, Oki, Y, Nakashima, Y, Adachi, T & Nishigaki, M 2016 Phosphorus stress-induced differential growth, and phosphorus acquisition and use efficiency by spring wheat cultivars Commun Soil Sci Plant Anal. 47 Suppl. 15 27 https://doi.org/10.1080/00103624.2016.1232089

    • Search Google Scholar
    • Export Citation
  • Anderson, TS, Villiers, DD & Timmons, MB 2017 Growth and tissue elemental composition response of butterhead lettuce (Lactuca sativa, cv. Flandria) to hydroponic and aquaponic conditions Horticulturae. 3 3 43 https://doi.org/10.3390/horticulturae3030043

    • Search Google Scholar
    • Export Citation
  • Aziz, T, Maqsood, MA, Tahir, MA, Ahmad, I & Cheema, MA 2006 Phosphorus utilization by six brassica cultivars (Brassica juncea L.) from tri-calcium phosphate: A relatively insoluble P compound Pak J Bot. 38 5 1529 1538

    • Search Google Scholar
    • Export Citation
  • Bera, T, McLamore, ES, Wasik, B, Rathinasabapathi, B & Liu, G 2018 Identification of a maize (Zea mays L.) inbred line adapted to low-P conditions via analyses of phosphorus utilization, root acidification, and calcium influx J Plant Nutr Soil Sci. 181 275 286 https://doi.org/10.1002/jpln.201700319

    • Search Google Scholar
    • Export Citation
  • Bera, T, Song, F & Liu, G 2020 Rapid identification of phosphorus-efficient genotypes from commercially grown tomato (Solanum lycopersicum L.) varieties in a simulated soil solution J Hortic Sci Biotechnol. 95 3 395 404 https://www.tandfonline.com/doi/full/10.1080/14620316.2019.1684210

    • Search Google Scholar
    • Export Citation
  • Bertossi, APA, Thomazini, A, Fonseca, AS & Amaral, JFT 2013 Nutritional efficiency of phosphorus in lettuce J Agric Sci. 5 8 125 131 https://doi.org/10.5539/jas.v5n8p125

    • Search Google Scholar
    • Export Citation
  • Choi, B, Lee, SS & Ok, YS 2011 Effects of waste nutrient solution on growth of Chinese cabbage (Brassica campestris L.) in Korea Korean J Environ Agric. 30 2 125 131 https://doi.org/10.5338/KJEA.2011.30.2.125

    • Search Google Scholar
    • Export Citation
  • Delaide, B, Goddek, S, Gott, J, Soyeurt, H & Jijakli, MH 2016 Lettuce (Lactuca sativa L.) growth performance in complemented aquaponic solution outperforms hydroponics Water. 8 467 https://doi.org/10.3390/w8100467

    • Search Google Scholar
    • Export Citation
  • Fageria, NK, He, Z & Baligar, VC 2017 Phosphorus management in crop production Boca Raton, FL CRC Press https://doi.org/10.1201/9781315162096

  • Garcia, M, Daverede, C, Gallego, P & Toumi, M 1999 Effect of various potassium-calcium ratios on cation nutrition of grape grown hydroponically J Plant Nutr. 22 3 417 425 https://doi.org/10.1080/01904169909365639

    • Search Google Scholar
    • Export Citation
  • Hammond, JP, Broadley, MR, White, PJ, King, GJ, Bowen, HC, Hayden, R, Meacham, MC, Mead, A, Overs, T, Spracklen, WP & Greenwood, DJ 2009 Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits J Expt Bot. 60 7 1953 1968 https://doi.org/10.1093/jxb/erp083

    • Search Google Scholar
    • Export Citation
  • Islam, MZ, Lee, Y, Mele, MA, Choi, I & Kang, H 2019 The effect of phosphorus and root zone temperature on anthocyanin of red romaine lettuce Agronomy (Basel). 9 2 47 https://doi.org/10.3390/agronomy9020047

    • Search Google Scholar
    • Export Citation
  • Kreutz, GF, Bhadha, JH & Sandoya, GV 2022 Evaluating phosphorus use efficiency across different lettuce (Lactuca sativa L.) accessions Euphytica. 218 28 https://doi.org/10.1007/s10681-022-02973-6

    • Search Google Scholar
    • Export Citation
  • Lan, P, Li, W & Schmidt, W 2015 ‘Omics’ approaches towards understanding plant phosphorus acquisition and use 65 98 Plaxton, WC & Lambers, H Annual plant reviews volume 48: Phosphorus metabolism in plants. https://doi.org/10.1002/9781118958841

    • Search Google Scholar
    • Export Citation
  • Lee, W, Zotarelli, L, Rowland, DL & Liu, G 2021 Evaluation of potato varieties grown in hydroponics for phosphorus use efficiency Agriculture. 11 668 https://doi.org/10.3390/agriculture11070668

    • Search Google Scholar
    • Export Citation
  • Liu, G, Dunlop, J & Phung, T 2006 Induction of root hair growth in a phosphorus-buffered culture solution Agric Sci China. 5 5 370 376

  • Liu, G, Dunlop, J, Phung, T & Li, Y 2007 Physiological responses of wheat phosphorus-efficient and -inefficient genotypes in field and effects of mixing other nutrients on mobilization of insoluble phosphates in hydroponics Commun Soil Sci Plant Anal. 38 2239 2256 https://doi.org/10.1080/00103620701549249

    • Search Google Scholar
    • Export Citation
  • Neocleous, D & Savvas, D 2019 The effects of phosphorus supply limitation on photosynthesis, biomass production, nutritional quality, and mineral nutrition in lettuce grown in a recirculating nutrient solution Scientia Hortic. 252 379 387 https://doi.org/10.1016/j.scienta. 2019.04.007

    • Search Google Scholar
    • Export Citation
  • Neto, AP, Favarin, JL, Hammond, JP, Tezotto, T & Couto, HTZ 2016 Analysis of phosphorus use efficiency traits in Coffea genotypes reveals Coffea arabica and Coffea canephora have contrasting phosphorus uptake and utilization efficiencies Front Plant Sci. 7 408 https://doi.org/10.3389/fpls.2016.00408

    • Search Google Scholar
    • Export Citation
  • Nirubana, V, Vanniarajan, C, Aananthi, N & Ramalingam, J 2020 Screening tolerance to phosphorus starvation and haplotype analysis using phosphorus uptake (Pup1) QTL linked markers in rice genotypes Physiol Mol Biol Plants. 26 2355 2369 https://doi.org/10.1007/s12298-020-00903-1

    • Search Google Scholar
    • Export Citation
  • Ochigbo, AE & Bello, LL 2014 Screening of soybean varieties for phosphorus use efficiency in nutrient solution Agric Biol J N Am. 5 2 68 77

  • Parentoni, SN, Mendes, FF & Guimarães, LJM 2012 Breeding for phosphorus use efficiency 67 85 Fritsche-Neto, R & Borém, A Plant breeding for abiotic stress tolerance. Berlin, Heidelberg Springer https://doi.org/10.1007/978-3-642-30553-5_5

    • Search Google Scholar
    • Export Citation
  • Raghothama, KG 1999 Phosphate acquisition Annu Rev Plant Physiol Plant Mol Biol. 50 665 693

  • Resh, HM 2022 Hydroponic food production: A definite guidebook for the advanced home gardener and the commercial hydroponic grower Boca Raton, FL CRC Press

    • Search Google Scholar
    • Export Citation
  • Rose, TJ & Wissuwa, M 2012 Rethinking internal phosphorus utilization efficiency: A new approach is needed to improve PUE in grain crops 185 217 Sparks, DL Advances in Agronomy. Academic Press https://doi.org/10.1016/B978-0-12-394277-7.00005-1

    • Search Google Scholar
    • Export Citation
  • Sandaña, P 2016 Phosphorus uptake and utilization efficiency in response to potato genotype and phosphorus availability Eur J Agron. 76 95 106 https://doi.org/10.1016/j.eja.2016.02.003

    • Search Google Scholar
    • Export Citation
  • Sandoya, GV 2019 Advances in lettuce breeding and genetics 459 478 Hochmuth, G Burleigh Dodds series in agricultural science. Burleigh Dodds Science Publishing

    • Search Google Scholar
    • Export Citation
  • Sandoya, GV, Bosques, J, Rivera, F & Campoverde, EV 2021 Growing lettuce in small hydroponic systems: HS 1422 EDIS. 2021 5 https://doi.org/10.32473/edis-hs1422-2021

    • Search Google Scholar
    • Export Citation
  • Sapkota, S, Sapkota, S & Liu, Z 2019 Effects of nutrient composition and lettuce cultivar on crop production in hydroponic culture Horticulturae. 5 72 https://doi.org/10.3390/horticulturae5040072

    • Search Google Scholar
    • Export Citation
  • Sarvajayakesavalu, S, Lu, Y, Withers, PJA, Pavinato, PS, Pan, G & Chareonsudjai, P 2018 Phosphorus recovery: A need for an integrated approach Ecosyst Health Sustain. 4 2 48 57 https://doi.org/10.1080/20964129.2018.1460122

    • Search Google Scholar
    • Export Citation
  • Sharma, N, Acharya, S, Kumar, K, Singh, N & Chaurasia, OP 2018 Hydroponics as an advanced technique for vegetable production: An overview J Soil Water Conserv. 17 4 364 371 https://doi.org/10.5958/2455-7145.2018. 00056.5

    • Search Google Scholar
    • Export Citation
  • van de Wiel, CCM, Linden, CG & Scholten, OE 2016 Improving phosphorus use efficiency in agriculture: Opportunities for breeding Euphytica. 207 1 22 https://doi.org/10.1007/s10681-015-1572-3

    • Search Google Scholar
    • Export Citation
  • Wen, Z, Li, H, Shen, Q, Tang, X, Xiong, C, Li, H, Pang, J, Ryan, MH, Lambers, H & Shen, J 2019 Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species New Phytol. 223 2 882 895 https://doi.org/10.1111/nph.15833

    • Search Google Scholar
    • Export Citation
  • Wissuwa, M, Yano, M & Ae, N 1998 Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.) Theor Appl Genet. 97 777 789 https://doi.org/10.1007/s001220050955

    • Search Google Scholar
    • Export Citation

Supplemental Fig. 1.
Supplemental Fig. 1.

Least square means of shoot and root TP (g·kg−1) with 95% confidence intervals of 12 lettuce accessions grown under low and high P in E1 and E2.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

Supplemental Fig. 2.
Supplemental Fig. 2.

Average least square means of shoot and root weight (g·plant−1) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3 and E4.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

Supplemental Fig. 3.
Supplemental Fig. 3.

Least square means of shoot and root TP (g·kg–1) with 95% confidence intervals of 12 lettuce accessions grown under tri-calcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

Supplemental Fig. 4.
Supplemental Fig. 4.

Least square means of shoot and root total-P (g·kg−1) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E4.

Citation: HortScience 58, 4; 10.21273/HORTSCI17040-22

Supplemental Table 1.

Analysis of variance of shoot and root weight and shoot and root tissue total-P (TP), for the 12 lettuce accessions in E1 and E2.

Supplemental Table 1.
Supplemental Table 2.

Analysis of variance of shoot and root fresh weight, and shoot and root tissue total-P (TP) for the 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3 and E4.

Supplemental Table 2.
  • Fig. 1.

    Least square means of shoot and root weight (g/plant) with 95% confidence intervals of 12 lettuce accessions grown under low and high P in E1 and E2. Shoot weight means with different lowercase letters and root weight means with different uppercase letters within an accession are significantly different at P ≤ 0.05 using the least significant difference test.

  • Fig. 2.

    Least square means of shoot and root weight (g/plant) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3. Shoot weight means with different lowercase letters and root weight means with different uppercase letters within an accession are significantly different at P ≤ 0.05 using the least significant difference test.

  • Fig. 3.

    Least square means of shoot and root weight (g/plant) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E4. Shoot weight means with different lowercase letters and root weight means with different uppercase letters within an accession are significantly different at P ≤ 0.05 using the least significant difference test.

  • Supplemental Fig. 1.

    Least square means of shoot and root TP (g·kg−1) with 95% confidence intervals of 12 lettuce accessions grown under low and high P in E1 and E2.

  • Supplemental Fig. 2.

    Average least square means of shoot and root weight (g·plant−1) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3 and E4.

  • Supplemental Fig. 3.

    Least square means of shoot and root TP (g·kg–1) with 95% confidence intervals of 12 lettuce accessions grown under tri-calcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E3.

  • Supplemental Fig. 4.

    Least square means of shoot and root total-P (g·kg−1) with 95% confidence intervals of 12 lettuce accessions grown under tricalcium phosphate (TCP) and monosodium phosphate (MSP) treatments in E4.

  • Ahmed, ZFR, Alnuaimi, AKH, Askri, A & Tzortzakis, N 2021 Evaluation of lettuce (Lactuca sativa L.) production under hydroponic system: Nutrient solution derived from fish waste vs. inorganic nutrient solution Horticulturae. 7 9 292 https://doi.org/10.3390/horticulturae7090292

    • Search Google Scholar
    • Export Citation
  • Akhtar, MS, Oki, Y, Nakashima, Y, Adachi, T & Nishigaki, M 2016 Phosphorus stress-induced differential growth, and phosphorus acquisition and use efficiency by spring wheat cultivars Commun Soil Sci Plant Anal. 47 Suppl. 15 27 https://doi.org/10.1080/00103624.2016.1232089

    • Search Google Scholar
    • Export Citation
  • Anderson, TS, Villiers, DD & Timmons, MB 2017 Growth and tissue elemental composition response of butterhead lettuce (Lactuca sativa, cv. Flandria) to hydroponic and aquaponic conditions Horticulturae. 3 3 43 https://doi.org/10.3390/horticulturae3030043

    • Search Google Scholar
    • Export Citation
  • Aziz, T, Maqsood, MA, Tahir, MA, Ahmad, I & Cheema, MA 2006 Phosphorus utilization by six brassica cultivars (Brassica juncea L.) from tri-calcium phosphate: A relatively insoluble P compound Pak J Bot. 38 5 1529 1538

    • Search Google Scholar
    • Export Citation
  • Bera, T, McLamore, ES, Wasik, B, Rathinasabapathi, B & Liu, G 2018 Identification of a maize (Zea mays L.) inbred line adapted to low-P conditions via analyses of phosphorus utilization, root acidification, and calcium influx J Plant Nutr Soil Sci. 181 275 286 https://doi.org/10.1002/jpln.201700319

    • Search Google Scholar
    • Export Citation
  • Bera, T, Song, F & Liu, G 2020 Rapid identification of phosphorus-efficient genotypes from commercially grown tomato (Solanum lycopersicum L.) varieties in a simulated soil solution J Hortic Sci Biotechnol. 95 3 395 404 https://www.tandfonline.com/doi/full/10.1080/14620316.2019.1684210

    • Search Google Scholar
    • Export Citation
  • Bertossi, APA, Thomazini, A, Fonseca, AS & Amaral, JFT 2013 Nutritional efficiency of phosphorus in lettuce J Agric Sci. 5 8 125 131 https://doi.org/10.5539/jas.v5n8p125

    • Search Google Scholar
    • Export Citation
  • Choi, B, Lee, SS & Ok, YS 2011 Effects of waste nutrient solution on growth of Chinese cabbage (Brassica campestris L.) in Korea Korean J Environ Agric. 30 2 125 131 https://doi.org/10.5338/KJEA.2011.30.2.125

    • Search Google Scholar
    • Export Citation
  • Delaide, B, Goddek, S, Gott, J, Soyeurt, H & Jijakli, MH 2016 Lettuce (Lactuca sativa L.) growth performance in complemented aquaponic solution outperforms hydroponics Water. 8 467 https://doi.org/10.3390/w8100467

    • Search Google Scholar
    • Export Citation
  • Fageria, NK, He, Z & Baligar, VC 2017 Phosphorus management in crop production Boca Raton, FL CRC Press https://doi.org/10.1201/9781315162096

  • Garcia, M, Daverede, C, Gallego, P & Toumi, M 1999 Effect of various potassium-calcium ratios on cation nutrition of grape grown hydroponically J Plant Nutr. 22 3 417 425 https://doi.org/10.1080/01904169909365639

    • Search Google Scholar
    • Export Citation
  • Hammond, JP, Broadley, MR, White, PJ, King, GJ, Bowen, HC, Hayden, R, Meacham, MC, Mead, A, Overs, T, Spracklen, WP & Greenwood, DJ 2009 Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits J Expt Bot. 60 7 1953 1968 https://doi.org/10.1093/jxb/erp083

    • Search Google Scholar
    • Export Citation
  • Islam, MZ, Lee, Y, Mele, MA, Choi, I & Kang, H 2019 The effect of phosphorus and root zone temperature on anthocyanin of red romaine lettuce Agronomy (Basel). 9 2 47 https://doi.org/10.3390/agronomy9020047

    • Search Google Scholar
    • Export Citation
  • Kreutz, GF, Bhadha, JH & Sandoya, GV 2022 Evaluating phosphorus use efficiency across different lettuce (Lactuca sativa L.) accessions Euphytica. 218 28 https://doi.org/10.1007/s10681-022-02973-6

    • Search Google Scholar
    • Export Citation
  • Lan, P, Li, W & Schmidt, W 2015 ‘Omics’ approaches towards understanding plant phosphorus acquisition and use 65 98 Plaxton, WC & Lambers, H Annual plant reviews volume 48: Phosphorus metabolism in plants. https://doi.org/10.1002/9781118958841

    • Search Google Scholar
    • Export Citation
  • Lee, W, Zotarelli, L, Rowland, DL & Liu, G 2021 Evaluation of potato varieties grown in hydroponics for phosphorus use efficiency Agriculture. 11 668 https://doi.org/10.3390/agriculture11070668

    • Search Google Scholar
    • Export Citation
  • Liu, G, Dunlop, J & Phung, T 2006 Induction of root hair growth in a phosphorus-buffered culture solution Agric Sci China. 5 5 370 376

  • Liu, G, Dunlop, J, Phung, T & Li, Y 2007 Physiological responses of wheat phosphorus-efficient and -inefficient genotypes in field and effects of mixing other nutrients on mobilization of insoluble phosphates in hydroponics Commun Soil Sci Plant Anal. 38 2239 2256 https://doi.org/10.1080/00103620701549249

    • Search Google Scholar
    • Export Citation
  • Neocleous, D & Savvas, D 2019 The effects of phosphorus supply limitation on photosynthesis, biomass production, nutritional quality, and mineral nutrition in lettuce grown in a recirculating nutrient solution Scientia Hortic. 252 379 387 https://doi.org/10.1016/j.scienta. 2019.04.007

    • Search Google Scholar
    • Export Citation
  • Neto, AP, Favarin, JL, Hammond, JP, Tezotto, T & Couto, HTZ 2016 Analysis of phosphorus use efficiency traits in Coffea genotypes reveals Coffea arabica and Coffea canephora have contrasting phosphorus uptake and utilization efficiencies Front Plant Sci. 7 408 https://doi.org/10.3389/fpls.2016.00408

    • Search Google Scholar
    • Export Citation
  • Nirubana, V, Vanniarajan, C, Aananthi, N & Ramalingam, J 2020 Screening tolerance to phosphorus starvation and haplotype analysis using phosphorus uptake (Pup1) QTL linked markers in rice genotypes Physiol Mol Biol Plants. 26 2355 2369 https://doi.org/10.1007/s12298-020-00903-1

    • Search Google Scholar
    • Export Citation
  • Ochigbo, AE & Bello, LL 2014 Screening of soybean varieties for phosphorus use efficiency in nutrient solution Agric Biol J N Am. 5 2 68 77

  • Parentoni, SN, Mendes, FF & Guimarães, LJM 2012 Breeding for phosphorus use efficiency 67 85 Fritsche-Neto, R & Borém, A Plant breeding for abiotic stress tolerance. Berlin, Heidelberg Springer https://doi.org/10.1007/978-3-642-30553-5_5

    • Search Google Scholar
    • Export Citation
  • Raghothama, KG 1999 Phosphate acquisition Annu Rev Plant Physiol Plant Mol Biol. 50 665 693

  • Resh, HM 2022 Hydroponic food production: A definite guidebook for the advanced home gardener and the commercial hydroponic grower Boca Raton, FL CRC Press

    • Search Google Scholar
    • Export Citation
  • Rose, TJ & Wissuwa, M 2012 Rethinking internal phosphorus utilization efficiency: A new approach is needed to improve PUE in grain crops 185 217 Sparks, DL Advances in Agronomy. Academic Press https://doi.org/10.1016/B978-0-12-394277-7.00005-1

    • Search Google Scholar
    • Export Citation
  • Sandaña, P 2016 Phosphorus uptake and utilization efficiency in response to potato genotype and phosphorus availability Eur J Agron. 76 95 106 https://doi.org/10.1016/j.eja.2016.02.003

    • Search Google Scholar
    • Export Citation
  • Sandoya, GV 2019 Advances in lettuce breeding and genetics 459 478 Hochmuth, G Burleigh Dodds series in agricultural science. Burleigh Dodds Science Publishing

    • Search Google Scholar
    • Export Citation
  • Sandoya, GV, Bosques, J, Rivera, F & Campoverde, EV 2021 Growing lettuce in small hydroponic systems: HS 1422 EDIS. 2021 5 https://doi.org/10.32473/edis-hs1422-2021

    • Search Google Scholar
    • Export Citation
  • Sapkota, S, Sapkota, S & Liu, Z 2019 Effects of nutrient composition and lettuce cultivar on crop production in hydroponic culture Horticulturae. 5 72 https://doi.org/10.3390/horticulturae5040072

    • Search Google Scholar
    • Export Citation
  • Sarvajayakesavalu, S, Lu, Y, Withers, PJA, Pavinato, PS, Pan, G & Chareonsudjai, P 2018 Phosphorus recovery: A need for an integrated approach Ecosyst Health Sustain. 4 2 48 57 https://doi.org/10.1080/20964129.2018.1460122

    • Search Google Scholar
    • Export Citation
  • Sharma, N, Acharya, S, Kumar, K, Singh, N & Chaurasia, OP 2018 Hydroponics as an advanced technique for vegetable production: An overview J Soil Water Conserv. 17 4 364 371 https://doi.org/10.5958/2455-7145.2018. 00056.5

    • Search Google Scholar
    • Export Citation
  • van de Wiel, CCM, Linden, CG & Scholten, OE 2016 Improving phosphorus use efficiency in agriculture: Opportunities for breeding Euphytica. 207 1 22 https://doi.org/10.1007/s10681-015-1572-3

    • Search Google Scholar
    • Export Citation
  • Wen, Z, Li, H, Shen, Q, Tang, X, Xiong, C, Li, H, Pang, J, Ryan, MH, Lambers, H & Shen, J 2019 Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species New Phytol. 223 2 882 895 https://doi.org/10.1111/nph.15833

    • Search Google Scholar
    • Export Citation
  • Wissuwa, M, Yano, M & Ae, N 1998 Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.) Theor Appl Genet. 97 777 789 https://doi.org/10.1007/s001220050955

    • Search Google Scholar
    • Export Citation
Gustavo F. Kreutz Horticultural Sciences Department, Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA

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Jehangir H. Bhadha Department of Soil, Water, and Ecosystem Sciences, Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA

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Guodong D. Liu Horticultural Sciences Department, University of Florida, 2550 Hull Road, Gainesville, FL 32611, USA

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Germán V. Sandoya Horticultural Sciences Department, Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA

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Contributor Notes

We acknowledge the hatch project FLA-EREC-005599. The Plant Breeding Graduate Initiative from the Plant Breeding Working Group and the Dean of Research Office of the University of Florida Institute of Food and Agricultural Sciences. We thank Heriberto Trevino for his help conducting the experiments and Dr. Abul Rabbany for technical assistance conducting P analyses in the Soil, Water, and Nutrient Management Lab.

Current affiliation for G.F.K.: Department of Plant Sciences, North Dakota State University, 1360 Albrecht Boulevard, Fargo, ND 58102, USA G.V.S. is the corresponding author. E-mail: gsandoyamiranda@ufl.edu.

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