Lettuce Germplasm in Humid Subtropical Environments Tolerant to Postharvest Development of Pink Rib Disorder

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Catherine E. Belisle Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Gainesville, FL 32611, USA

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Germán V. Sandoya Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Everglades Research and Education Center, Belle Glade, FL 33430, USA

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Steven A. Sargent Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Gainesville, FL 32611, USA

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Gustavo F. Kreutz Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Everglades Research and Education Center, Belle Glade, FL 33430, USA

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Abstract

Pink rib discoloration or pinking in the midribs of lettuce (Lactuca sativa) leaves is a stress-induced disorder that leads to crop loss worldwide. Maintaining recommended field and postharvest conditions reduces its incidence but does not eliminate the issue. During the past decade, research has identified the tolerance of this disorder among lettuce types and cultivars grown in cooler climates. However, tolerance to pink rib among lettuce types grown in humid subtropical climates is unknown; therefore, it is necessary to screen lettuce germplasm under these growing conditions. During this study, diverse lettuce accessions were planted for early-season, mid-season, and late-season harvests over two seasons in Belle Glade, FL, USA. Harvested midribs were wounded to induce pink rib, stored for 6 to 9 days at 5 °C and >95% relative humidity, and rated for severity using a 5-point subjective scale. Genotype × environment interactions were evaluated to understand the environmental factors that favor the development of pink rib during storage and between planting seasons. Pink rib severity increased during storage, with the highest increase observed after 3 to 4 days in both seasons. After 9 days of storage, lettuce accessions with the least pink rib for each leaf type were identified. The lowest pink rib ratings after 9 days of storage were “moderate” (rating of 3) for crisphead, Latin, and romaine, “slight” (rating of 2) for butterhead types, and “none” (rating of 1) for leaf types. Additionally, pink rib severity increased among accessions during the late spring season harvest when field temperatures were higher and daylight hours were extended. The lettuce germplasm with low susceptibility to pink rib is promising to breed lettuce lines for future research.

Lettuce (Lactuca sativa) is primarily produced in the United States in California, Arizona, and Florida, with a production value of $2.7 billion (USDA-NASS 2021). Florida produces an estimated 3% of the total lettuce in the United States (USDA-NASS 2019), primarily in the Everglades Agricultural Area, which is a humid subtropical region in southern Florida (Sandoya and Lu 2020). Despite this relatively low proportion of the industry in the United States, lettuce grown in Florida has significant market demand because it is harvested during winter and spring months.

The approximate shelf life of lettuce is 2 to 3 weeks when promptly cooled and held at 1 °C and 95% to 100% relative humidity (Saltveit 2018). Shelf life is limited by several postharvest factors, including physiological disorders such as russet spotting, brown stain, and pink rib or pinking. The development of these disorders generally can be minimized by storage under recommended conditions (Subbarao et al. 2017). Among these disorders, pink rib causes economic losses throughout the lettuce supply chain. Pink rib appears as a pink-to-red discoloration in the midribs and veins of leafy crops. Pink rib development (preharvest or postharvest) is primarily a consequence of abiotic stresses, including high field temperatures (Jenni 2005), heads harvested past market maturity (Hilton et al. 2009), improper storage and handling (Monaghan et al. 2017), and mechanical damage (Pereyra et al. 2005).

Storage conditions influence the expression of pink rib, although the influence on environmental conditions of multiple lettuce types are not well understood. For instance, leaf edge discoloration development on 25 lettuce cultivars was reduced during 7 d in an active storage atmosphere at 7 °C, despite a wide range of O2 and CO2 levels within the headspace during storage (Tudela et al. 2016). The development of pink rib varies among lettuce types; generally, stem and butterhead types have lower susceptibility, whereas the romaine type is highly susceptible (Atkinson et al. 2013a; Teng et al. 2019). Furthermore, pink rib expression is accession dependent. Teng et al. (2019) evaluated romaine cultivars and found the most pink rib discoloration on Tall Guzmaine and the least on Parris Island Cos.

A comprehensive evaluation of the unique lettuce germplasm at the University of Florida breeding program remains to be conducted to identify tolerance to pink rib discoloration for this subtropical production region. This may be particularly important because stress from high field temperatures may increase pink rib development. Therefore, testing in the subtropical conditions of Florida may identify superior genotypes with tolerance to pink rib. The first objective of this study was to identify genetic variations in lettuce accessions to the development of pink rib during storage. The second objective was to understand the genotype × environment (G × E) interaction that influences pink rib expression between planting seasons and during storage.

Materials and Methods

Plant material.

During the 2019–20 season (season 1), 17 romaine lettuce breeding lines and cultivars and one crisphead cultivar (control) were evaluated for two plantings (Table 1). Because pink rib severity of romaine lettuce was only studied in season 1, an expanded follow-up study was conducted during the 2020–21 season (season 2), which included the previous romaine lines and cultivars plus nine crisphead, five butterhead, eight leaf, and three Latin accessions in three plantings (Table 1). These accessions represented elite breeding lines from the University of Florida Institute of Food and Agriculture Sciences lettuce breeding program, commercial cultivars currently used by growers in the Everglades Agricultural Area in Florida, and commercial and noncommercial cultivars not adapted to Florida. The crisphead cultivar Salinas was used as a control for this study because it consistently develops “moderate” to “moderately severe” pink rib (Artés and Martínez 1996).

Table 1.

Lettuce accessions of five morphological types and seasons planted near Belle Glade, FL, USA, and accessed for susceptibility to pink rib disorder in two planting seasons (2019–20 and 2020–21). Breeder and pedigree information, when available, and zone of adaptation of lettuce accessions used in the study are provided.

Table 1.
Table 1.

Sample preparation and evaluation.

For both growing seasons, all lettuce accessions involved in this research were planted in a commercial field in the Everglades Agricultural Area near Belle Glade, FL, USA, and grown using local commercial practices (Sandoya et al. 2021). There were three 6-m-long plots per accession that were assigned using a completely randomized design. In each plot, lettuce seeds were manually planted in double-row beds, with 0.20-m spacing between rows; plants were thinned to 0.43-m in-row spacing at the three true-leaf stage. During season 1, seeds were planted on 13 Nov and 10 Dec 2019; during season 2, seeds were planted on 8 Oct 2020, 16 Dec 2020, and 3 Mar 2021 (Table 2).

Table 2.

Planting and harvest dates for lettuce accessions accessed for susceptibility to pink rib disorder in five morphological lettuce types grown in the Everglades Agricultural Area in two seasons 2019–20 and 2020–21 and types. Minimum, medium and maximum temperatures averages during the crop cycle on each of the experiments planted during two seasons and the growing degree days calculated from University of Florida, Agroclimate Project (2023).

Table 2.

At harvest, in both seasons, outer leaves not folded into the lettuce heart were discarded and whole heads (n = 3 heads/accession) were placed in commercial waxed, corrugated cartons (60 cm length × 39 cm width × 33 cm height, 24 romaine heads/carton). Lettuce was commercially vacuum-cooled within 2 hours of harvest to an internal (core tissue) temperature of ∼5 °C and then stored in a commercial cold room (5 °C) in Belle Glade, FL. The experimental setup began within 1 h at 5 °C, noted as “day 0”.

Whole lettuce heads (n = 3) were randomly selected; one to two outer leaves with no visual sign of decay or mechanical damage were selected per head (n = five leaves total). The leaves were prepared using a procedure modified from Cantwell (2016). A midrib segment (12.5 cm) was excised from the center of each leaf (n = 5), and excess leaf blade tissue was trimmed parallel to the midrib, leaving 1- to 2-cm-wide midrib tissue. Each midrib was oriented with the abaxial surface (leaf underside) facing upward, and 9 or to 10 perpendicular slices (∼0.8 cm depth) were made at 1.3-cm increments along the midrib, leaving only the midrib cuticle layer attached. Then, the midribs were placed with the surface cuts facing up in an unsealed polyethylene bag and stored at 5 °C.

A subjective scale was used to rate pink rib severity for the cuts on each midrib every 2 d, starting on day 2 during season 1 (total = 6 d) or day 1 during season 2 (total = 9 d), based on a 5-point discoloration scale, where 1 = none, 2 = slight, 3 = moderate and the limit of marketability, 4 = moderately severe, and 5 = severe (Cantwell 2016) (Fig. 1).

Fig. 1.
Fig. 1.

Subjective rating scale for pink rib severity of lettuce midribs. Scores range from 1 (no discoloration) to 5 (severe discoloration); 3 is the limit of acceptability/salability (adapted from Cantwell 2016).

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05295-23

Experimental design and statistical analysis.

Pink rib severity was analyzed using a nonparametric statistical method of the ranked means (Brunner et al. 2002; Shah and Madden 2004). Because pink rib severity was evaluated during a time-point storage period, the data were analyzed as repeated measures; the analysis of variance (ANOVA) was calculated using PROC MIXED in SAS (version 9.4; SAS Institute Inc., Cary, NC, USA) according to Shah and Madden (2004). Replicate, accession (A), storage time (ST), experiment (E), and their interactions (A × ST, A × E, ST × E, and A × ST × E) were considered as the fixed statement, and an “r” and “corr” covariance structure was used as the repeated statement. The macros LD_CI and F1_LD_F1 were used to calculate the relative marginal effects (RMEs) and their confidence interval (CI) at 95% for each accession through the storage periods (Shah and Madden 2004). The RMEs are a transformation of the rating scale used to measure severity. The method transforms the ranked means into a relative value of the ordinal scale used to measure a trait. Differences during storage periods were considered significant when the CI of the RME between a given accession did not overlap with the CI of the control cultivar Salinas. Additionally, linear contrasts were calculated between each accession and the commercial control cultivar (Salinas) during the storage period.

Furthermore, to perform a better assessment of the overall pink rib development for each of the accessions, weighted means and RMEs were calculated for each season. The subjective ratings recorded every other day for 9 d were used to calculate weighted means across the evaluation dates to obtain a single mean value per accession using the following formula (Hills et al. 1980):
WM =Σi=1n(RiWi)Σi=1n(Wi)
where WM is the weighted mean for each accession, n is the number of evaluation dates to be averaged, Ri is the rating value at the ith evaluation date, and Wi is the weight applied to each rating value at the ith evaluation date (1, 2, 3, 4, and 5 correspond to days 1, 3, 5, 7, and 9 of storage, respectively).

During this analysis, an ANOVA-F was calculated as previously described following the methodology of Shah and Madden (2004), except for the use of the LD_CI macro. This analysis was conducted considering the weighted means as a randomized complete block design. Similarly, RMEs and 95% CIs were calculated (Shah and Madden 2004).

Genotype × environment analysis.

For season 2, pink rib severity data of a discriminant temperature (5 °C) were subjected to genotype + genotype × environment (GGE) biplot analysis to identify the winning accessions (accessions with less pink rib severity) in a mega-environment and the most stable lettuce accessions in terms of pink rib across the three harvest dates. The three harvest dates for season 2 are herein referred to the following three environments as proposed by Yan et al. (2000): Expt. 1 = S2H1; Expt. 2 = S2H2; and Expt. 3 = S2H3. For the GGE biplot analysis, values recorded using the pink rib rating severity scale (range, 1–5) were proportionally inverted because higher values of pink rib severity were less desirable (5 = no discoloration to 1 = severe pink rib). A “which-won-where” biplot analysis was used to identify accessions (which) that are the best performers (won) in a specific mega-environment (where) (Yan and Kang 2003). In the “which-won-where” biplots, a polygon is graphed by connecting the most responsive accessions located at the farthest positions from the origin. Perpendicular lines are drawn to divide the polygon into sectors called mega-environments that may group one or more of the actual tested environments (e.g., Expts. 1, 2, and 3). The subjective ratings recorded every other day for 9 d were used to calculate weighted means across the evaluation dates to obtain a single mean value per accession using a previously described formula (Hills et al. 1980).

Then, PBTools software (version 14; International Rice Research Institute, Los Baños, Laguna, Philippines) was used to perform the GGE biplot analysis and generate which-won-where biplots for pink rib severity.

In addition, the average environment coordination (AEC) view of the biplot was graphed to rank accessions based on the mean performance and stability of each accession across environments. The single-arrow line in the graph refers to the AEC abscissa and points to the highest PC2 value, which signifies the least pink rib severity across environments (harvests). The AEC ordinate (y-axis) points to the variability of the trait toward both directions. The accessions, experiments, and their respective codes used in the GGE biplots are listed in Tables 1 and 2.

Results

Pink rib severity.

During both seasons 1 and 2, there were significant differences in pink rib severity (P < 0.001) among accessions.

For season 1, romaine cultivars Hialeah and Holbrook had the lowest rated pink rib severity, as demonstrated by the average RME values (0.07 and 0.15, respectively), and a “slight” rating for the weighted means (rating of 2.3 and 2.5), independent of the harvest and storage period (Fig. 2, Table 3). In contrast, 50098, 60182, 60184, and ‘Tall Guzmaine’ had the highest average RME values (0.85, 0.72, 0.79, and 0.89, respectively) and “moderately severe” ratings for the weighted means (ratings >4). The remaining 11 romaine accessions and one crisphead accession developed “moderate” pink rib severity, as indicated by the RME values (from 0.21 to 0.71) and weighted means (ratings from 2.8 to 4.0) (Fig. 2, Table 3).

Fig. 2.
Fig. 2.

Relative marginal effects and 95% confidence intervals for pink rib of 17 romaine lettuce accessions and one crisphead control (‘Salinas’) stored at 5 °C in season 1.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05295-23

Table 3.

Pink rib severity and the weighted means of 17 romaine and one crisphead (control) lettuce accessions during storage (days 2, 4, and 6) at 5 °C in season 1. Weighted means were calculated using the subjective ratings recorded every other day for 6 d to obtain a single mean value per accession.

Table 3.

For season 2, ‘Holbrook’, ‘Hialeah’, ‘Manatee’, and 50100 had the lowest pink rib severity among romaine types, as demonstrated by the average RME values (0.25, 0.34, 0.47, and 0.48, respectively), and a “slight” rating for the weighted means (ratings of 2.3, 2.3, 2.4, and 2.7, respectively) across the harvest and storage periods (Fig. 3A, Table 4). The romaine accessions Floricos 83, 70096, 60183, and 60182 had the highest RME values (0.67, 0.72, 0.86, 0.68, respectively) and “moderately severe” ratings for the weighted means (ratings >4). ‘Terrapin’, ‘Tall Guzmaine’, and 43007 also had high average RME values (0.72, 0.73, and 0.76, respectively), but the pink rib severity was not severe; therefore, the weighted means were “moderate” (3.5, 3.7, and 3.5, respectively). The remaining six accessions developed “slight” to “moderate” pink rib severity, as shown by the RME values (0.48–0.70) and weighted means (ratings from 2.4 to 3.8).

Fig. 3.
Fig. 3.

Relative marginal effects and 95% confidence intervals for pink rib of romaine (A), crisphead (B), butterhead (C), leaf (D), and Latin (E) lettuce accessions and a control (‘Salinas’) stored at 5 °C in season 2.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05295-23

Table 4.

Pink rib severity and the weighted means of 43 lettuce accessions of five morphological types (romaine, crisphead, butterhead, leaf, and Latin) during storage (days 1, 3, 5, 7, and 9) at 5 °C in season 2. Weighted means were calculated using the subjective ratings recorded every other day for 9 d to obtain a single mean value per accession.

Table 4.

For the crisphead type, H1098 had the lowest pink rib severity, as indicated by the low RME value (0.43), and a “slight” rating for the weighted mean (rating of 2.8) in season 2 (Fig. 3B, Table 4). The accessions ‘Salinas’, 60167, and H1078 had the highest average RME values (0.62, 0.69, and 0.73, respectively) and “moderate” ratings for the weighted means (ratings of 3.2, 3.3, and 3.4, respectively). The remaining six accessions developed “slight” pink rib severity, as shown by the RME values (0.43–0.56) and weighted mean (rating of 2.9).

The butterhead (B1190 and ‘Palmetto’), leaf (‘Cordoba’ and ‘Galactic’), and Latin (45060) accessions developed the lowest pink rib severity within these individual types, as shown by the average RME values (0.35, 0.21, 0.13, 0.38, and 0.34, respectively), and “no” to “slight” ratings for the weighted means (ratings of 1.9, 2.1, 1, 1, and 2.1, respectively) (Fig. 3C–E, Table 4). The remaining eight accessions among the butterhead, leaf, and Latin types developed “slight” pink rib severity, as shown by the RME values (0.17–0.56) and weighted means (ratings from 2.1 to 2.7).

In season 1, there were significant differences for storage period (P < 0.001), accession × storage period interactions (P < 0.001), and accession × harvest (P < 0.001) interactions, but not for harvest (P = 0.089). The susceptible control ‘Salinas’ developed “slight to moderate” (rating of 2.5) pink rib by day 2 of storage, whereas 5 of the 17 accessions had ratings of 1.0 to 1.5 (Table 3). The linear contrasts, which compare lettuce accessions with ‘Salinas’, support this finding with significant differences for pink rib by day 2 for six breeding lines (50100, 60182, 60183, 60184, 70096, and C1145) and seven cultivars (Green Towers, Hialeah, King Henry, Manatee, Okeechobee, PIC, and Tall Guzmaine) (Supplemental Table 1). By day 4, 9 of the 17 accessions were significantly different from ‘Salinas’ (rating of 3.5) (Supplemental Table 1), either because of less pink rib (ratings ≤3.0), as for ‘Hialeah’, ‘Holbrook’, ‘Green Towers’, and C1145, or because of greater pink rib (ratings ≥3.8), as for 50098, 60182, 60183, 60184, and ‘Tall Guzmaine’ (Table 3, Supplemental Table 1). On day 6, only ‘Hialeah’ and ‘Holbrook’ were rated as “slight” to “moderate” (ratings of 2–3), with significantly lower severity than ‘Salinas’, which developed “moderately severe” (rating of 4) pink rib (Table 3, Supplemental Table 1). Accessions 50098, 60182, 60184, and ‘Tall Guzmaine’ developed “severe” (ratings of 4.8–5) pink rib. RME values were low for ‘Hialeah’ (0.07), ‘Hialeah’ (0.25), and ‘Holbrook’ (0.38), and they were high for ‘Salinas’ (0.38), ‘Tall Guzmaine’ (0.88) and ‘Tall Guzmaine’ (0.94) at days 2, 4, and 6, respectively (Supplemental Table 2).

In season 2, linear contrasts between individual accessions and ‘Salinas’ for each storage evaluation estimated these differences (Supplemental Table 3). On day 1, most accessions had no pink rib development; therefore, very few significant contrasts were detected (Table 4, Supplemental Table 3). By day 3 of storage, ‘Salinas’ developed “moderate” (rating of 3) pink rib; 10 of the accessions had significant contrasts with ‘Salinas’, with ratings of 2.5 or less, whereas four had ratings of 3 (Supplemental Table 3). The number of significant contrasts increased to 15 by day 5, with nine accessions significantly lower than ‘Salinas’ (rating of 3), with ratings of 2.5 or less, whereas two accessions (43007 and ‘Tall Guzmaine’) were rated as “moderately severe” (rating of 4) compared with the “moderate” (rating of 3) rating of ‘Salinas’. By day 7, there were 20 significant contrasts, and the findings were similar to those on day 5; eight accessions had significantly lower pink rib ratings of 2 or less, and eight accessions had higher ratings than ‘Salinas’ (rating of 3). By day 9, 22 of the 43 accessions had significant linear contrasts because of less (ratings ≤3) pink rib severity than ‘Salinas’ (rating of 4) for 50113, 60157, 60159, 70882, B1190, C1148, ‘Chosen’, ‘Cordoba’, H1098, H2020, ‘Hialeah’, ‘Manatee’, ‘Palmetto’, ‘RSX743’, ‘Tehama’, and ‘Two Star’. Greater pink rib severity (ratings of 4 or 4.5) was found for 43007, C1145, ‘PIC’, ‘Tall Guzmaine’, ‘Terrapin’, and ‘Floricos 83’ (Supplemental Table 3). RME values were as low for ‘Salinas’ (0.12) and for 16 other accessions at day 1, including ‘Galactic’ (0.30) at day 3, ‘Holbrook’ (0.36) at day 5, ‘Galactic’ (0.32) at day 7, and ‘Cordoba’ (0.33) at day 9. RME values were high for 50098, 60184, and 70202 (0.30) at day 1, 60182 (0.67) at day 3, 60183 (0.83) at day 5, 60183 (0.91) at day 7, and 60183 (0.91) at day 9 (Supplemental Table 4).

Genotype × environment interaction for pink rib severity.

The GGE biplot analysis allowed dissection of the effects of the genotype and G × E interaction on the total phenotypic variation observed for the trait of interest. In addition, the principal component (PC) scores derived from singular value decomposition allowed the construction of “which-won-where” biplots and, consequently, the identification of superior accessions in specific environments (Yan et al. 2000).

During this research, PC1 and PC2 accounted for 75.7% and 16.3%, respectively, of the total variability of the visual ratings that estimated pink rib severity in season 2 (Fig. 4A). Significant correlations were observed between Expt. 1 (S2H1) and Expt. 2 (S2H2) (r = 0.62; n = 170; P < 0.001), Expt. 1 and Expt. 3 (S2H3) (r = 0.53; n = 170; P < 0.001), and Expt. 2 and Expt. 3 (r = 0.52; n = 215; P < 0.001).

Fig. 4.
Fig. 4.

Which-won-where (A) and stability analysis (B) of the genotype + genotype × environment (GGE) biplot analysis of weighted means of pink rib severity from lettuce accessions tested in season 2. G1 to G43 represent accessions listed in Table 1, whereas Expt. 1 (E1) to Expt. 3 (E3) were conducted in season 2 and listed as S2H1, S2H2, and S2H3 in Table 2. The empty dot (B) represents the ideal average environment to identify germplasm with less pink rib, and the full dot represents the ideal genotype or the genotype with consistently less pink rib across the tested experiments.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05295-23

Two mega-environments were identified for the three experiments during this research (Fig. 4A). The first mega-environment comprised only Expt. 3, in which the leaf cultivar Cordoba (G33 in Fig. 4) was considered the “winning accession,” or the accession that consistently had the lowest pink rib severity. Expt. 1 and Expt. 2 were placed within a second mega-environment, and the leaf cultivar Galactic (G34) was the “winning accession,” with the lowest pink rib severity for both environments (Fig. 4A). Although ‘Galactic’ had less pink rib severity when grown in the environmental conditions for Expt. 1 (S2H1) and Expt. 2 (S2H2), the mega-environment was positioned in the negative y-axis, suggesting that selection of accessions with lower pink rib severity during both early-season and mid-season plantings might not be simultaneously possible (Fig. 4A).

According to the AEC view of the GGE biplot, accessions on the right side of the AEC ordinate (double-arrow line) had below-average pink rib severity, whereas those accessions on the left side had above-average pink rib severity ratings. Cordoba (G33) was confirmed to be the accession closest to the ideal genotype; namely, it is the one that developed the least severe pink rib across the three experiments (plantings) during this analysis (Fig. 4B). Germplasm such as Cordoba would be better-suited (i.e., would develop less pink rib) for environments similar to the one in Expt. 1, because the AEA (x-axis) of the “average environment” was positioned closer to that of Expt. 1 (Fig. 4B).

Discussion

Pink rib variation among accessions.

Reducing pink rib severity of whole-head lettuce is a focus for multiple breeding programs; however, there have been no reports of long-term solutions, such as new cultivars or exogenously applied compounds that can reduce or eliminate the development of pink rib (Luna et al. 2016; Saltveit et al. 2005; Tomás-Barberán et al. 1997). Therefore, the identification of accessions with lower susceptibility to pink rib is essential for the long-term mitigation of this disorder. In the current study, lettuce accessions with less susceptibility to pink rib severity were identified from germplasm adapted to a humid subtropical climate. Variations in mid-rib discoloration severity have been reported for numerous lettuce types and accessions (Atkinson et al. 2013a; Cantos et al. 2001; Tudela et al. 2016) that are not adapted to the subtropical climate of Florida.

Atkinson et al. (2013a) reported a distinct rate of discoloration for each lettuce type, with romaine and butterhead types showing the quickest onset of pink rib. Similar findings were reported after 7 d of storage at 5 °C, when the highest a* values of affected tissues, representative of pink to red discoloration, were noted for crisphead cultivars, a butterhead type, a romaine type, and a romaine cultivar (Atkinson et al. 2013a). These findings align with the present study, in which romaine accessions developed the highest pink rib severity, followed by a crisphead type, a butterhead type, a leaf type, and a Latin type, respectively. Similarly, all lettuce accessions developed pink rib after 9 d of storage at 5 °C; the lone exceptions were the two red-leaf cultivars, Cordoba and Galactic. The accessions studied that showed “no” to “slight sensitivity” to pink rib disorder were not previously reported (Atkinson et al. 2013a, 2013b; Cantos et al. 2001; Teng et al. 2019; Tudela et al. 2016). As a consequence, multiple potential parents incorporated into breeding lettuce with tolerance to pink rib for the humid subtropics.

Latin, butterhead, and leaf types had lower susceptibility to pink rib than the other morphological types. Several studies found that the romaine cultivar Green Towers had the least discoloration after 5 d at 7 °C (Teng et al. 2019). Similar findings were presented by Peng et al. (2021), who found that ‘Green Towers’ had little midrib discoloration, whereas ‘King Henry’ and ‘Tall Guzmaine’ developed the most severe discoloration among the 10 accessions evaluated. A similar severity pattern was found during the present study in season 1; pink rib development of ‘Green Towers’ was less severe than that of ‘King Henry’ and ‘Tall Guzmaine’. Three romaine cultivars, Hialeah, Holbrook, and Okeechobee, were the only commercial cultivars with lower pink rib than Green Towers in seasons 1 and 2, and they are commonly planted by Florida growers. However, in season 2, an additional 12 romaine accessions were identified that developed less pink rib than ‘Green Towers’, suggesting that there is wide genetic variation within the lettuce germplasm, and that future studies should evaluate more romaine accessions to identify germplasm with the least pink rib severity.

Salinas, a crisphead lettuce, has been a cultivar of interest for many researchers because of its many positive postharvest characteristics, including relative tolerance to the development of pink rib (Artés and Martínez 1996; López-Gálvez et al. 1996) and longer shelf life. ‘Salinas 88’, a highly related progeny of Salinas (Ryder 1991), was reported to have reported “moderate” to “moderately severe” pink rib severity after 2 weeks at 2 °C Artés and Martínez (1996). Although the value of ‘Salinas’ was confirmed during the present study, seven other crisphead accessions developed less pink rib than ‘Salinas’. Furthermore, leaf lettuce had the least pink rib severity; therefore, further screenings should be conducted with more accessions of this type. For each lettuce type evaluated, there are multiple lettuce accessions that can be used as a source of less pink rib severity in breeding programs.

Pink rib variation during storage.

In the present study, the overall pink rib severity was determined within 5 d of storage. Lettuce accessions with moderate pink rib severity (>3 rating) by storage day 5 either maintained this severity rating or progressed to a higher rating by day 9. Additionally, accessions with less severity (<3 rating) by day 5 maintained less pink rib severity throughout the study. Based on these results, the susceptibility of lettuce germplasm to pink rib appears to be genetically controlled until day 5 of storage at 5 °C; after that time, the accessions differed in their capacity to develop pink rib, which could be attributed to the environment. It was confirmed that this variation in pink rib severity can be attributed to the genetics of lettuce accessions, and not to the environment, because multiple environmental factors, including larger wounds or higher storage temperatures, that normally induce pink rib (Pereyra et al. 2005) were avoided during the present study. In this study, lettuce was not stored under modified atmosphere conditions (low O2 and/or increased CO2 levels) that normally suppresses the development of pink rib (Luna et al. 2016; Singh et al. 1972). Therefore, pink rib development was not masked by modified atmosphere conditions.

Pink rib variation among planting seasons.

The G × E (accession × harvest) interactions for pink rib severity were influenced by the harvest time, as demonstrated in romaine lettuce during season 1 and in multiple lettuce types during season 2. For example, the cultivar Cordoba had the least pink rib severity overall, whereas the cultivar Galactic had the least in the first and second plantings. ‘Cordoba’ was determined to be the most stable germplasm, with less pink rib severity, and the best-suited for environmental conditions similar to those during Expt. 3 (spring season), with increasingly higher temperatures and longer daylengths.

Although pink rib severity has been positively correlated to overly mature heads at harvest (Hilton et al. 2009), it is unlikely that the higher severity of pink rib during Expt. 3 was attributable to lettuce being overly mature because the lettuce was harvested at proper market maturity for the commercial cultivars commonly grown in Florida. There were variations in growing degrees in different seasons and different plantings that may have influenced the differences in pink rib severity across these experiments (Table 2).

The significant positive correlations for pink rib severity among experiments suggested noncrossover G × E interactions. Noncrossover G × E interactions indicate that germplasm selection within a single representative environment should be sufficient for breeders to identify lettuce with less pink rib severity (Jenni 2005; Jenni and Hayes 2010; Jenni and Yan 2009). Previously, pink rib in romaine lettuce accessions were reported to have high broad sense heritability, indicating a small environmental effect (Peng et al. 2021). However, as plant breeders evaluate progeny during multilocation trials for traits with potential G × E crossover interactions, inclusions of ratings of accessions for susceptibility to pink rib would be useful when assessed in a wide range of environments (locations).

This is the first study to identify genetic variation of pink rib severity among diverse lettuce accessions adapted to humid subtropical growing conditions. Although the cultivars Cordoba and Galactic had less pink rib severity across all the tested accessions among all types, accessions with the least pink rib severity were identified within each type. For instance, ‘Hialeah’ and ‘Holbrook’ in romaine, H1098 in crisphead, B1190 in butterhead, and 45060 in Latin types showed less pink rib severity. Developing mapping and breeding populations that combine low susceptibility to pink rib of these accessions with other desirable quality and horticultural characteristics should be a priority for genetics studies and breeding purposes.

References Cited

  • Artés F, Martínez JA. 1996. Influence of packaging treatments on the keeping quality of ‘Salinas’ lettuce. Lebensm Wiss Technol. 29:664668. https://doi.org/10.1006/fstl.1996.0102.

    • Search Google Scholar
    • Export Citation
  • Atkinson LD, Hilton HW, Pink DA. 2013a. A study of variation in the tendency for postharvest discoloration in a lettuce (Lactuca sativa) diversity set. Int J Food Sci Technol. 48:801807. https://doi.org/10.1111/ijfs.12030.

    • Search Google Scholar
    • Export Citation
  • Atkinson LD, McHale LK, Truco MJ, Hilton HW, Lynn J, Schut JW, Michelmore RW, Hand P, Pink DAC. 2013b. An intra-specific linkage map of lettuce (Lactuca sativa) and genetic analysis of postharvest discolouration traits. Theor Appl Genet. 126:27372752. https://doi.org/10.1007/s00122-013-2168-8.

    • Search Google Scholar
    • Export Citation
  • Brunner E, Munzel U, Puri ML. 2002. The multivariate nonparametric Behrens–Fisher problem. J Stat Plan Inference. 108:3753. https://doi.org/10.1016/S0378-3758(02)00269-0.

    • Search Google Scholar
    • Export Citation
  • Cantos E, Espin JC, Tomas-Barberan FA. 2001. Effect of wounding on phenolic enzymes in six minimally processed lettuce cultivars upon storage. J Agr Food Chem. 49:322330. https://doi.org/10.1021/jf000644q.

    • Search Google Scholar
    • Export Citation
  • Cantwell M. 2016. Postharvest physiological disorders: Pinking in romaine hearts. http://calgreens.org/wp-content/uploads/2016/06/Pinking-in-Romaine-Hearts-Cantwell.pdf. [accessed 23 Jul 2021].

  • Hills FJ, Chiarappa L, Geng S. 1980. Powdery mildew of sugar beet: Disease and crop loss assessment. Phytopathology. 70:680682.

  • Hilton HW, Clifford SC, Wurr DCE, Burton KS. 2009. The influence of agronomic factors on the visual quality of field grown, minimally-processed lettuce. J Hortic Sci Biotechnol. 84:193198. https://doi.org/10.1080/14620316.2009.11512503.

    • Search Google Scholar
    • Export Citation
  • Jenni S. 2005. Rib discoloration: A physiological disorder induced by heat stress in crisphead lettuce. HortScience. 40:20312035. https://doi.org/10.21273/HORTSCI.40.7.2031.

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

    • Search Google Scholar
    • Export Citation
  • Jenni S, Yan W. 2009. Genotype by environment interactions of heat stress disorder resistance in crisphead lettuce. Plant Breed. 128:374380. https://doi.org/10.1111/j.1439-0523.2009.01657.x.

    • Search Google Scholar
    • Export Citation
  • Luna MC, Tudela JA, Tomas-Barberan FA, Gil MI. 2016. Modified atmosphere (MA) prevents browning of fresh-cut romaine lettuce through multi-target effects related to phenolic metabolism. Postharvest Biol Technol. 119:8493. https://doi.org/10.1016/j.postharvbio.2016.05.001.

    • Search Google Scholar
    • Export Citation
  • López-Gálvez G, Saltveit M, Cantwell M. 1996. Wound-induced phenylalanine ammonia lyase activity: Factors affecting its induction and correlation with the quality of minimally processed lettuces. Postharvest Biol Technol. 9:223233. https://doi.org/10.1016/S0925-5214(96)00050-6.

    • Search Google Scholar
    • Export Citation
  • Monaghan JM, Vickers LH, Grove IG, Beacham AM. 2017. Deficit irrigation reduces postharvest rib pinking in wholehead Iceberg lettuce, but at the expense of head fresh weight. J Sci Food Agr. 97:15241528. https://doi.org/10.1002/jsfa.7895.

    • Search Google Scholar
    • Export Citation
  • Peng H, Luo Y, Teng Z, Zhou B, Bornhorst ER, Fonseca JM, Simko I. 2021. Phenotypic characterization and inheritance of enzymatic browning on cut surfaces of stems and leaf ribs of romaine lettuce. Postharvest Biol Technol. 181:111653. https://doi.org/10.1016/j.postharvbio.2021.111653.

    • Search Google Scholar
    • Export Citation
  • Pereyra L, Roura SI, del Valle CE. 2005. Phenylalanine ammonia lyase activity in minimally processed romaine lettuce. Lebensm Wiss Technol. 38:6772. https://doi.org/10.1016/j.lwt.2004.05.004.

    • Search Google Scholar
    • Export Citation
  • Ryder EJ. 1991. ‘Salinas 88’ lettuce. HortScience. 26:439440. https://doi.org/10.21273/HORTSCI.26.4.439.

  • Saltveit ME. 2018. Pinking of lettuce. Postharvest Biol Technol. 145:4152. https://doi.org/10.1016/j.postharvbio.2018.06.001.

  • Saltveit ME, Choi YJ, Tomas-Barberan FA. 2005. Involvement of components of the phospholipid-signaling pathway in wound-induced phenylpropanoid metabolism in lettuce (Lactuca sativa) leaf tissue. Physiol Plant. 125:345355. https://doi.org/10.1111/j.1399-3054.2005.00574.x.

    • Search Google Scholar
    • Export Citation
  • Sandoya GV, Lu H. 2020. Evaluation of lettuce cultivars for production on muck soils in southern Florida. Inst Food Agric Sci, Univ Florida HS1225. https://edis.ifas.ufl.edu/hs1225. [accessed 25 Jun 2020].

  • Sandoya GV, Kanissery R, Raid RN, Desaeger J, Beuzelin J. 2021. Leafy vegetable production, p 165–206. In: Paret ML, Dittmar PJ, Agehara S, Smith HA (eds). Vegetable production handbook of Florida, 2021-2022 edition. Inst Food Agric Sci, Univ Florida. Gainesville, FL, USA. https://doi.org/10.32473/edis-cv293-2022.

  • Shah DA, Madden LV. 2004. Nonparametric analysis of ordinal data in designed factorial experiments. Phytopathology. 94:3343. https://doi.org/10.1094/PHYTO.2004.94.1.33.

    • Search Google Scholar
    • Export Citation
  • Singh B, Yang CC, Salunkhe DK. 1972. Controlled atmosphere storage of lettuce. 1. Effects on quality and respiration rate of lettuce heads. J Food Sci. 37:4851.

    • Search Google Scholar
    • Export Citation
  • Subbarao KV, Davis RM, Gilbertson RL, Raid RN. 2017. Postharvest diseases disorders, p 136–140. In: Krishna V, Subbarao, RMD, Gilbertson RL, Raid RN (eds). Compendium of lettuce diseases and pests (2nd ed). American Phytopathological Society, St. Paul, MN, USA.

  • Teng Z, Luo Y, Bornhorst ER, Zhou B, Simko I, Trouth F. 2019. Identification of romaine lettuce (Lactuca sativa var. longifolia) cultivars with reduced browning discoloration for fresh-cut processing. Postharvest Biol Technol. 156:110931. https://doi.org/10.1016/j.postharvbio.2019.110931.

    • Search Google Scholar
    • Export Citation
  • Tomás-Barberán FA, Loaiza-Velarde J, Bonfanti A, Saltveit ME. 1997. Early wound- and ethylene-induced changes in phenylpropanoid metabolism in harvested lettuce. J Am Soc Hortic Sci. 122:399404. https://doi.org/10.21273/JASHS.122.3.399.

    • Search Google Scholar
    • Export Citation
  • Tudela JA, Hernández N, Pérez-Vicente A, Gil MI. 2016. Comprehensive evaluation of different storage conditions for the varietal screening of lettuce for fresh-cut performance. Postharvest Biol Technol. 120:3644. https://doi.org/10.1016/j.postharvbio.2016.05.009.

    • Search Google Scholar
    • Export Citation
  • University of Florida. Agroclimate Project. 2023. Climate indicators for agriculture. http://cloud.agroclimate.org/tools/climate-indicators-monitoring. [accessed 30 May 2023].

  • US Department of Agriculture, National Agricultural Statistics Service. 2019. Quick Stats. https://quickstats.nass.usda.gov/. [accessed 20 Jun 2020].

  • US Department of Agriculture, National Agricultural Statistics Service. 2021. Lettuce production measured in $. https://www.nass.usda.gov/Statistics_by_Subject/result.php?40059755-5467-3494-8DC7-A502F090C847&sector=CROPS&group=VEGETABLES&comm=LETTUCE. [accessed 28 Mar 2022].

  • Wehner TC, Mou B. 2013. Vegetable cultivar descriptions for North America List 27 2013. HortScience. 48:245286. https://doi.org/10.21273/HORTSCI.48.2.245.

    • Search Google Scholar
    • Export Citation
  • Yan W, Kang MS. 2003. GGE biplot analysis: A graphical tool for breeders, geneticists, and agronomists. CRC Press, Boca Raton, FL, USA. https://doi.org/10.1201/9781420040371.

  • Yan W, Hunt LA, Sheng Q, Szlavnics Z. 2000. Cultivar evaluation and mega-environment investigation based on the GGE biplot. Crop Sci. 40:597605. https://doi.org/10.2135/cropsci2000.403597x.

    • Search Google Scholar
    • Export Citation

Supplemental Table 1.

Linear contrasts of pink rib severity between 17 romaine lettuce accessions and ‘Salinas’ in combined harvests conducted in season 1 (2019–20) during storage for 6 d at 5 °C.

Supplemental Table 1.
Supplemental Table 2.

Relative marginal effects (RME) and lower (L) and upper (U) 95% confidence intervals for pink rib severity of lettuce accessions during storage for 6 d at 5 °C in season 1.

Supplemental Table 2.
Supplemental Table 3.

Linear contrasts for pink rib severity between 43 lettuce accessions and ‘Salinas’ in combined harvests conducted in season 2 (2020–21) during storage for 9 d at 5 °C.

Supplemental Table 3.
Supplemental Table 4.

Relative marginal effects (RME) and lower (L) and upper (U) 95% confidence intervals of pink rib severity of lettuce accessions during storage for 9 d at 5 °C in season 2 (2020–21).

Supplemental Table 4.
  • Fig. 1.

    Subjective rating scale for pink rib severity of lettuce midribs. Scores range from 1 (no discoloration) to 5 (severe discoloration); 3 is the limit of acceptability/salability (adapted from Cantwell 2016).

  • Fig. 2.

    Relative marginal effects and 95% confidence intervals for pink rib of 17 romaine lettuce accessions and one crisphead control (‘Salinas’) stored at 5 °C in season 1.

  • Fig. 3.

    Relative marginal effects and 95% confidence intervals for pink rib of romaine (A), crisphead (B), butterhead (C), leaf (D), and Latin (E) lettuce accessions and a control (‘Salinas’) stored at 5 °C in season 2.

  • Fig. 4.

    Which-won-where (A) and stability analysis (B) of the genotype + genotype × environment (GGE) biplot analysis of weighted means of pink rib severity from lettuce accessions tested in season 2. G1 to G43 represent accessions listed in Table 1, whereas Expt. 1 (E1) to Expt. 3 (E3) were conducted in season 2 and listed as S2H1, S2H2, and S2H3 in Table 2. The empty dot (B) represents the ideal average environment to identify germplasm with less pink rib, and the full dot represents the ideal genotype or the genotype with consistently less pink rib across the tested experiments.

  • Artés F, Martínez JA. 1996. Influence of packaging treatments on the keeping quality of ‘Salinas’ lettuce. Lebensm Wiss Technol. 29:664668. https://doi.org/10.1006/fstl.1996.0102.

    • Search Google Scholar
    • Export Citation
  • Atkinson LD, Hilton HW, Pink DA. 2013a. A study of variation in the tendency for postharvest discoloration in a lettuce (Lactuca sativa) diversity set. Int J Food Sci Technol. 48:801807. https://doi.org/10.1111/ijfs.12030.

    • Search Google Scholar
    • Export Citation
  • Atkinson LD, McHale LK, Truco MJ, Hilton HW, Lynn J, Schut JW, Michelmore RW, Hand P, Pink DAC. 2013b. An intra-specific linkage map of lettuce (Lactuca sativa) and genetic analysis of postharvest discolouration traits. Theor Appl Genet. 126:27372752. https://doi.org/10.1007/s00122-013-2168-8.

    • Search Google Scholar
    • Export Citation
  • Brunner E, Munzel U, Puri ML. 2002. The multivariate nonparametric Behrens–Fisher problem. J Stat Plan Inference. 108:3753. https://doi.org/10.1016/S0378-3758(02)00269-0.

    • Search Google Scholar
    • Export Citation
  • Cantos E, Espin JC, Tomas-Barberan FA. 2001. Effect of wounding on phenolic enzymes in six minimally processed lettuce cultivars upon storage. J Agr Food Chem. 49:322330. https://doi.org/10.1021/jf000644q.

    • Search Google Scholar
    • Export Citation
  • Cantwell M. 2016. Postharvest physiological disorders: Pinking in romaine hearts. http://calgreens.org/wp-content/uploads/2016/06/Pinking-in-Romaine-Hearts-Cantwell.pdf. [accessed 23 Jul 2021].

  • Hills FJ, Chiarappa L, Geng S. 1980. Powdery mildew of sugar beet: Disease and crop loss assessment. Phytopathology. 70:680682.

  • Hilton HW, Clifford SC, Wurr DCE, Burton KS. 2009. The influence of agronomic factors on the visual quality of field grown, minimally-processed lettuce. J Hortic Sci Biotechnol. 84:193198. https://doi.org/10.1080/14620316.2009.11512503.

    • Search Google Scholar
    • Export Citation
  • Jenni S. 2005. Rib discoloration: A physiological disorder induced by heat stress in crisphead lettuce. HortScience. 40:20312035. https://doi.org/10.21273/HORTSCI.40.7.2031.

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

    • Search Google Scholar
    • Export Citation
  • Jenni S, Yan W. 2009. Genotype by environment interactions of heat stress disorder resistance in crisphead lettuce. Plant Breed. 128:374380. https://doi.org/10.1111/j.1439-0523.2009.01657.x.

    • Search Google Scholar
    • Export Citation
  • Luna MC, Tudela JA, Tomas-Barberan FA, Gil MI. 2016. Modified atmosphere (MA) prevents browning of fresh-cut romaine lettuce through multi-target effects related to phenolic metabolism. Postharvest Biol Technol. 119:8493. https://doi.org/10.1016/j.postharvbio.2016.05.001.

    • Search Google Scholar
    • Export Citation
  • López-Gálvez G, Saltveit M, Cantwell M. 1996. Wound-induced phenylalanine ammonia lyase activity: Factors affecting its induction and correlation with the quality of minimally processed lettuces. Postharvest Biol Technol. 9:223233. https://doi.org/10.1016/S0925-5214(96)00050-6.

    • Search Google Scholar
    • Export Citation
  • Monaghan JM, Vickers LH, Grove IG, Beacham AM. 2017. Deficit irrigation reduces postharvest rib pinking in wholehead Iceberg lettuce, but at the expense of head fresh weight. J Sci Food Agr. 97:15241528. https://doi.org/10.1002/jsfa.7895.

    • Search Google Scholar
    • Export Citation
  • Peng H, Luo Y, Teng Z, Zhou B, Bornhorst ER, Fonseca JM, Simko I. 2021. Phenotypic characterization and inheritance of enzymatic browning on cut surfaces of stems and leaf ribs of romaine lettuce. Postharvest Biol Technol. 181:111653. https://doi.org/10.1016/j.postharvbio.2021.111653.

    • Search Google Scholar
    • Export Citation
  • Pereyra L, Roura SI, del Valle CE. 2005. Phenylalanine ammonia lyase activity in minimally processed romaine lettuce. Lebensm Wiss Technol. 38:6772. https://doi.org/10.1016/j.lwt.2004.05.004.

    • Search Google Scholar
    • Export Citation
  • Ryder EJ. 1991. ‘Salinas 88’ lettuce. HortScience. 26:439440. https://doi.org/10.21273/HORTSCI.26.4.439.

  • Saltveit ME. 2018. Pinking of lettuce. Postharvest Biol Technol. 145:4152. https://doi.org/10.1016/j.postharvbio.2018.06.001.

  • Saltveit ME, Choi YJ, Tomas-Barberan FA. 2005. Involvement of components of the phospholipid-signaling pathway in wound-induced phenylpropanoid metabolism in lettuce (Lactuca sativa) leaf tissue. Physiol Plant. 125:345355. https://doi.org/10.1111/j.1399-3054.2005.00574.x.

    • Search Google Scholar
    • Export Citation
  • Sandoya GV, Lu H. 2020. Evaluation of lettuce cultivars for production on muck soils in southern Florida. Inst Food Agric Sci, Univ Florida HS1225. https://edis.ifas.ufl.edu/hs1225. [accessed 25 Jun 2020].

  • Sandoya GV, Kanissery R, Raid RN, Desaeger J, Beuzelin J. 2021. Leafy vegetable production, p 165–206. In: Paret ML, Dittmar PJ, Agehara S, Smith HA (eds). Vegetable production handbook of Florida, 2021-2022 edition. Inst Food Agric Sci, Univ Florida. Gainesville, FL, USA. https://doi.org/10.32473/edis-cv293-2022.

  • Shah DA, Madden LV. 2004. Nonparametric analysis of ordinal data in designed factorial experiments. Phytopathology. 94:3343. https://doi.org/10.1094/PHYTO.2004.94.1.33.

    • Search Google Scholar
    • Export Citation
  • Singh B, Yang CC, Salunkhe DK. 1972. Controlled atmosphere storage of lettuce. 1. Effects on quality and respiration rate of lettuce heads. J Food Sci. 37:4851.

    • Search Google Scholar
    • Export Citation
  • Subbarao KV, Davis RM, Gilbertson RL, Raid RN. 2017. Postharvest diseases disorders, p 136–140. In: Krishna V, Subbarao, RMD, Gilbertson RL, Raid RN (eds). Compendium of lettuce diseases and pests (2nd ed). American Phytopathological Society, St. Paul, MN, USA.

  • Teng Z, Luo Y, Bornhorst ER, Zhou B, Simko I, Trouth F. 2019. Identification of romaine lettuce (Lactuca sativa var. longifolia) cultivars with reduced browning discoloration for fresh-cut processing. Postharvest Biol Technol. 156:110931. https://doi.org/10.1016/j.postharvbio.2019.110931.

    • Search Google Scholar
    • Export Citation
  • Tomás-Barberán FA, Loaiza-Velarde J, Bonfanti A, Saltveit ME. 1997. Early wound- and ethylene-induced changes in phenylpropanoid metabolism in harvested lettuce. J Am Soc Hortic Sci. 122:399404. https://doi.org/10.21273/JASHS.122.3.399.

    • Search Google Scholar
    • Export Citation
  • Tudela JA, Hernández N, Pérez-Vicente A, Gil MI. 2016. Comprehensive evaluation of different storage conditions for the varietal screening of lettuce for fresh-cut performance. Postharvest Biol Technol. 120:3644. https://doi.org/10.1016/j.postharvbio.2016.05.009.

    • Search Google Scholar
    • Export Citation
  • University of Florida. Agroclimate Project. 2023. Climate indicators for agriculture. http://cloud.agroclimate.org/tools/climate-indicators-monitoring. [accessed 30 May 2023].

  • US Department of Agriculture, National Agricultural Statistics Service. 2019. Quick Stats. https://quickstats.nass.usda.gov/. [accessed 20 Jun 2020].

  • US Department of Agriculture, National Agricultural Statistics Service. 2021. Lettuce production measured in $. https://www.nass.usda.gov/Statistics_by_Subject/result.php?40059755-5467-3494-8DC7-A502F090C847&sector=CROPS&group=VEGETABLES&comm=LETTUCE. [accessed 28 Mar 2022].

  • Wehner TC, Mou B. 2013. Vegetable cultivar descriptions for North America List 27 2013. HortScience. 48:245286. https://doi.org/10.21273/HORTSCI.48.2.245.

    • Search Google Scholar
    • Export Citation
  • Yan W, Kang MS. 2003. GGE biplot analysis: A graphical tool for breeders, geneticists, and agronomists. CRC Press, Boca Raton, FL, USA. https://doi.org/10.1201/9781420040371.

  • Yan W, Hunt LA, Sheng Q, Szlavnics Z. 2000. Cultivar evaluation and mega-environment investigation based on the GGE biplot. Crop Sci. 40:597605. https://doi.org/10.2135/cropsci2000.403597x.

    • Search Google Scholar
    • Export Citation
Catherine E. Belisle Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Gainesville, FL 32611, USA

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Germán V. Sandoya Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Everglades Research and Education Center, Belle Glade, FL 33430, USA

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Steven A. Sargent Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Gainesville, FL 32611, USA

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Gustavo F. Kreutz Horticultural Sciences Department, University of Florida, Institute of Food and Agriculture Sciences, Everglades Research and Education Center, Belle Glade, FL 33430, USA

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Contributor Notes

This research was partially funded through a subrecipient grant awarded by the US Department of Agriculture’s (USDA) Agricultural Marketing Service through the Florida Department of Agriculture and Consumer Services (award no. 266097) and the Hatch projects (FLA-ERC-006174 and FLA-HOS-005972). The contents do not necessarily reflect the views or policies of USDA, nor does mention of trade names, commercial productions, services, or organization imply endorsement by the US Government. We thank the Horticultural Sciences Department at the University of Florida (UF) for funding provided to Catherine Belisle and the Florida Vegetable Exchange for assistance with this project. We thank Jesse Murray, Lis Natali Rodrigues Porto, Heriberto Treviño, and Amanda Carroll for help with planting and harvesting, Roth Farms and TKM-Bengard Farms for cooling and storage, and Adrian Berry for assistance with experimental planning and setup. We thank Dr. Clyde W. Fraisse from the Agricultural and Biological Engineering Department at UF for valuable help with calculating precise growing degree days.

G.V.S. is the corresponding author. E-mail: gsandoyamiranda@ufl.edu.

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  • Fig. 1.

    Subjective rating scale for pink rib severity of lettuce midribs. Scores range from 1 (no discoloration) to 5 (severe discoloration); 3 is the limit of acceptability/salability (adapted from Cantwell 2016).

  • Fig. 2.

    Relative marginal effects and 95% confidence intervals for pink rib of 17 romaine lettuce accessions and one crisphead control (‘Salinas’) stored at 5 °C in season 1.

  • Fig. 3.

    Relative marginal effects and 95% confidence intervals for pink rib of romaine (A), crisphead (B), butterhead (C), leaf (D), and Latin (E) lettuce accessions and a control (‘Salinas’) stored at 5 °C in season 2.

  • Fig. 4.

    Which-won-where (A) and stability analysis (B) of the genotype + genotype × environment (GGE) biplot analysis of weighted means of pink rib severity from lettuce accessions tested in season 2. G1 to G43 represent accessions listed in Table 1, whereas Expt. 1 (E1) to Expt. 3 (E3) were conducted in season 2 and listed as S2H1, S2H2, and S2H3 in Table 2. The empty dot (B) represents the ideal average environment to identify germplasm with less pink rib, and the full dot represents the ideal genotype or the genotype with consistently less pink rib across the tested experiments.

 

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