In the present study, chromatic coordinates, phenolic acids, flavonoids and antioxidant capacity assessed by 1,1-diphenyl-2-picrylhydrazyl (DPPH), 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonate (ABTS) and lipid peroxidation inhibition capacity (LPIC) essays and their relative IC50 were investigated in 25 fig cultivars growing in Morocco. The aims of this study were to determine (i) the variation in these compounds among light and dark-colored cultivars, (ii) their partitioning between fruit peel and pulp and (iii) to display network connections among these variables. Twelve phenolic compounds (PCs) were isolated in peel extract versus eight in pulp samples. Anthocyanins, mainly cyanidin-3,5-diglucoside and cyanidin-3-O-rutinoside, were the predominant compounds in peels, where the mean concentrations were 75.90 ± 18.76 and 77.97 ± 18.95 µg/g dw, respectively. On the other hand, (−)-epicatechin and cyanidin-3-O-rutinoside were the major compounds in the pulp extracts, where the mean values were 5.23 ± 4.03 and 9.01 ± 5.67 µg/g dw, respectively. A two-dimensional hierarchically clustered heatmap was applied to the dataset to explore correlations in the dataset and similarities between cultivars, without dimensionality reduction. Results showed that anthocyanins, particularly pelargonidin-3-O-rutinoside, cyanidin-3,5-diglucoside and cyanidin-3-O-rutinoside, were the main contributors to the peels' free radical scavenging capacity. This capacity was particularly higher in the peel of dark-colored figs compared to the fruit pulp. The local cultivar "INRA 1301" showed the most promising phenolic profile due to its very high levels of almost all detected PCs, especially (−)-epicatechin, quercetin-3-O-rutinoside, quercetin-3-O-glucoside, cyanidine-3,5-diglucoside, cyanidine-3-O-rutinoside and pelargonidin-3-O-rutinoside (54.66, 141.08, 35.48, 494.08, 478.66, 12.56 µg/g dw, respectively). Having the darkest figs in the collection (L* = 25.72, c* = 22.09 and h° = 20.99), this cultivar has also combined promising IC50 values, which were of 19.85, 40.58 and 124.78 µg/mL for DPPH, ABTS and LPIC essays, respectively.
Keywords: phenolic acids; flavonoids; antioxidant activity; Ficus carica L.; chemometric; heatmap
The ever-growing interest in functional foods, particularly underutilized fruits, is based on their uniqueness of the natural biological resources necessary to enhance human health and well-being. Worldwide, large species are not fully assessed for their nutritional values and biologically active compounds involved in the consumer health promotion, so far. Although the naturally occurring phenotypic, chemotypic and ecotypic diversity of most of these species is still scarcely studied, it is evident that they present an invaluable potential source of bioactive compounds directly associated to the prevention of coronary diseases. Particular attention should be devoted to the investigation of secondary metabolites of these species, since they not only present the main quality indicators of new cultivars but are also important in chemotaxonomy [[
According to the United States Department of Agriculture database (USDA), figs (Ficus carica L.), emblematic food in the Mediterranean diet [[
The fig peels and pulps color showed significant differences among cultivars at p < 0.001, with the exception of the pulp lightness coordinate (L*) (Table 1). Therefore, peels' chromatic coordinates present more accurate discrimination between cultivars than pulp color coordinates. Overall, peel color varied from bright yellow color (high and positive values of L* and c*) to atypical dark and blue purple color (negative L* and c* and high values of the hue). While in pulp, the color varied from pale pink (high values of L*, positive values of a* and b*) to dark red (low L* and c* and high positive a*). The cultivar "Trojana" had the brightest peels with the coordinates L* and c* recorded the highest values (73.15 and 50.94, respectively), whereas "INRA 1301" had the darkest colored figs (L* = 25.72 and c* = 22.09). Regarding pulp samples, the cultivars "Fassi" and "Breval Blanca" had the darkest color, where L* recorded the lowest values (18.6 and 19.05, respectively). All cultivars were classified based on their fruits' peels and pulps characterization using principal component analysis (Figure 1). Inspection of scatterplots showed that peels color displayed outlying subsets more than the pulp. Hence, the total variance obtained with peels data was of 91.51%, while pulps characterization accounted about 78.54%. In fact, the principal component analysis (PCA) scatterplot for peels' chromatic coordinates splits the samples into two main groups describing blue-purple and light-colored cultivars. Having the lowest chroma value, the local cultivar "Fassi" was largely distinguished from the other subsets. However, a pulp samples scatterplot showed low discrimination resolution. Therefore, peel and pulp color evaluation using these coordinates is of great importance in fruits quality assessment. Several studies highlighted the importance of these descriptors to explore potential correlations between them and some antioxidant compounds, mainly phenols (anthocanins, tanins, catechins, etc.) and carotenoids (lycopene, beta-carotene, etc.) [[
Total phenols (TPC), total flavonoids (TFC), total anthocyanins (TAC) and total proanthcyanidins content (TPAC) showed highly significant differences among cultivars, depending on their fruit parts (p < 0.001) (Table 1). These compounds were more than two times higher in fruits peels compared to their pulps, as observed in other fruits such as quince [[
In peels, TPC varied between 370 and 3162.86 mg GAE/100 g dw, while TFC were in the range of 188.57 and 2013.57 mg CE/100 g dw. TAC was highly abundant in dark samples and ranged between 4.14 and 192.5 mg cyanidin-3-rutinoside/100 g dw. In pulps extracts, TPC, TFC and TAC were in the range of 105.71–1255.71 mg GAE/100 g dw, 13.57–331.43 mg CE/100 g dw and 2.27–19.44 mg cyanidin/100 g dw, respectively. For both fruit parts, TPAC varied within a narrow interval of 0.2–3.09 and 0.2–1.06 mg cyanidin/100 g dw. Generally, they were present in high amounts in purple pulps when compared to light-colored ones. It is noteworthy that proanthocyanidins are quantified in all pulps samples as the same as the peels, which is probably due to the fact that they are the key determinant for red color in pulp and purple and blue colors skin fruits as well as anthocyanins [[
The local cultivar "INRA 1301" combined the highest levels of TPC, TFC, TAC and TPCA in its peels, where the mean values were of 2860.48 mg GAE/100 g dw, 1944.52 mg CE/100 g dw, 192.23 mg cyanidin-3-rutinoside/100 g dw and 2.59 mg cyanidin/100 g dw, respectively (Table 2; Table 3). Regarding the pulps, the local cultivar "Ghoudan" combined the highest amounts of TPC and TFC, where the mean concentrations were of 1186.67 mg GAE/100 g dw and 271.90 mg CE/100 g dw (Table 2 and Table 3). It is noteworthy that these compounds were found to be more abundant in dark-colored peels compared to light-colored ones, which is not always in the same sense regarding the fig pulps.
These results are consistent with those of Çalişkan and Polat. [[
In the industrial processing of figs, the pulp is used, whilst the peel is usually discarded [[
Results of the free-radical-scavenging effect of figs' peel and pulp extracts on DPPH• and ABTS•+ radicals and lipid peroxidation inhibition are summarized in Table 1, Table 2 and Table 3. They are expressed as Trolox equivalent per g of dry weight and by the antioxidant concentration required for a 50% of radical reduction (IC50), so that a lower value of IC50 indicated a higher antioxidant activity and vice versa. These methods were combined to obtain an overview of figs antioxidant capacity, since no single assay can fully characterize the profile of each sample [[
The ABTS assay showed a wide range of variation for both peel and pulp antiradical capacity (7.57–563.53 and 6.59–207.49 mMol TE/g dw, respectively) (Table 2). Peels of the cultivars "Chaari" and "Fassi" showed the highest AA (527.25 and 493.69 mMol TE/g, respectively), while "Cuello Dama Blanca" and "Snowden" fig pulps exhibited the highest AA, where the values were 204.68 and 160.43 mMol TE/g, respectively (Table 2 and Table 3).
The lipid peroxidation inhibitory effects of both fig parts were significantly different among cultivars and, generally, showed a narrow interval of variation compared to the other assays. Hence, in peels, the lipid peroxidation inhibition capacity (LPIC) was in the range of 139.17 and 353.11 mMol TE/g dw, whereas in pulps, it ranged between 42.89 and 226.88 mMol TE/g dw, respectively (Table 2). Peels of "Kadota" and "Ghoudan" exhibited the highest LPIC (301.76 and 289.63 mMol TE/g dw, respectively), while "Bioudie" and "White Adriatic" had the lowest values (154.84 and 156.27 mMol TE/g dw, respectively). Similarly, pulps extracts displayed low LPIC compared to the peels, where "INRA 1305" and "Bioudie" showed the highest values (189.08 and 147.81 mMol TE/g dw, respectively), while "Sarilop" and "Ournaksi" recorded the lowest ones (57.85 and 67.12 mMol TE/g dw, respectively) (Table 2 and Table 3). To conclude, among all assays, figs' peels seem to be the main contributors to the antioxidant capacity comparing to their pulps. In addition, dark-colored peels exhibited the highest antioxidant capacity compared to the light-colored ones. These results were similar to those reported by Solomon et al. [[
The IC50 is a variable that reflects the quality of radical scavenging for each of the antioxidant tests. The antioxidant potency, inversely proportional to the IC50 value, is more important when very small concentrations are required to scavenge half of the radicals [[
Even consumers usually prefer fruits with attractive appearance, especially the peels' color, they tend, while eating the fruit, to remove the peel; however, this fruit part is evidently the major source of phenolic compounds that highly contribute to the antioxidant capacity and systematically protect against diseases related to oxidative stress. The consumption of the whole figs is clearly an important habit for promoting the health promoting diet in Mediterranean society [[
High-performance liquid chromatography (HPLC) with a diode-array detector (DAD) analyses showed the presence of several phenolic compounds belonging to phenolic acids (hydroxycinnamic acid and hydroxybenzoic acid derivatives) and flavonoids (flavonols, flavones and anthocyanidins). Indeed, eight phenolic compounds, including: (+)-catechin, (−)-epicatechin, chlorogenic acid, quercetin-3-O-rutinoside, quercetin-3-O-glucoside, luteolin-7-O-glucoside, cyanidin-3,5-diglucoside and cyanidin-3-O-rutinoside, were detected in the pulp. While in peel extract, twelve compounds were isolated (gallic acid, (+)-catechin, (−)-epicatechin, chlorogenic acid, quercetin-3-O-rutinoside, quercetin-3-O-glucoside, luteolin-7-O-glucoside, quercetin, apigenin, cyanidin-3,5-diglucoside, cyanidin-3-O-rutinoside and pelargonidine-3-O-rutinoside) (Figure 2 and Figure 3). These compounds showed significant differences among cultivars and fruits parts (p < 0.001) (Table 1). These results were similar to those reported by Vallejo et al. [[
Among all cultivars, the PCs' concentrations were higher in peels compare to pulps extracts. Anthocyanins, particularly cyanidin-3,5-diglucoside and cyanidin-3-O-rutinoside, were the predominant compounds in peels, where the mean concentrations were 75.902 ± 18.76 and 77.972 ± 18.95 µg/g dw, respectively. For flavonols, only (−)-epicatechin, quercetin-3-O-rutinoside and quercetin-3-O-glucoside were detected. Gallic acid and pelargonidin-3-O-rutinoside were only detected in the local cultivars "Chetoui" and "Nabout", with the respective levels of 8.363 ± 1.88 and 6.731 ± 2.019 µg/g dw (Table 4). These results agree with those reported for peels of the Portuguese variety "Pingo de Mel" by Palmeira et al. [[
In pulps extracts, (−)-epicatechin and cyanidin-3-O-rutinoside were the major compounds. They were detected in all cultivars at high levels (5.23 ± 4.03 and 9.01 ± 5.67 µg/g dw, respectively). Cyanidin-3,5-diglucoside were the third predominant compound, that ranged from 0.81 to 28.45 µg/g dw, with a mean of 6.06 ± 6.71 µg/g dw, followed by (+)-catechin and chlorogenic acid (1.93 ± 1.29 and 1.01 ± 1.16 µg/g dw, respectively). However, luteolin-7-O-glucoside was detected in only two cultivars, "Chetoui" and "Palmeras", with respective concentrations of 0.75 ± 0.35 and 4.47 ± 0.04 µg/g dw (Table 5). These results are generally in agreement with those of Del Caro and Piga. [[
In the study of Palmeira et al. [[
Data visualization is an essential tool for biochemical data analysis, and dimensionality reduction methods, such as principal component analysis (PCA), are usually used to draw high dimensional data onto two- or three-dimensional space so it can be visualized. However, this transition is costly, often resulting in loss of the total variance. A hierarchically clustered heatmap is one of numerous analyses that does not need a dimensionality reduction to visualize data. It is a widely used technique to analyze complex biological data by displaying network connections in a symmetric adjacency matrix [[
Color-coded two-dimensional heatmaps for both fruit parts are formed with two clusters using Euclidean distance following Ward method; one is sample-oriented while the other is variable-oriented (Figure 4). In this figure, weak correlations between studied variables are displayed in low color intensity, while stronger ones are shown with high color intensity. Cultivars and variables clustering as well as the correlations among dataset were quite different between fig peel and pulp. In pulp samples, the chromatic coordinates (L*, c*, h°) were clustered with LPIC and the IC50 of DPPH and ABTS assays, which are correlated to quercetin and apigenin. These compounds seem to have a large effect on the peel antioxidant potency (Figure S1). These variables tend to be higher in the cultivars "Trojana", "Breval Blnaca", "Ournaksi", "Bioudie" and "Nabout" that constitute, among others, a distinctive cluster. On the other hand, catechin, luteolin-7-O-glucoside, quercetin-3-O-rutinoside, epicatechin and chlorogenic acid were clustered together and correlated to TPC, TFC and IC50 (LPIC). These compounds showed similar tendencies to be accumulated by the local cultivars "Chetoui", "Noukali", "INRA 2305′, "Ghoudan" and "Chaari", which constitute a homogenous cluster. It is noteworthy that these cultivars are characterized by dark-colored figs, which are known to hold abundant amounts of these compounds. Pelargonidin-3-O-rutinoside, canidin-3,5-diglucoside and cyanidin-3-O-rutinoside are anthocyanins that were clustered together with total proanthocyanins and revealed a strong correlation to the free radical scavenging capacity of peel extracts (Figure S2). The pigments belong to the flavonoid class and seem to be the major contributors to the free radical scavenging process of fig peels. The local cultivar "INRA 1301" is clustered as a single branch and therefore largely distinguished from the other clusters. It combined the highest levels of flavonoids compounds and consequently showed high level of DPPH• and ABTS•+ radical scavenging capacity. This cultivar has dark-colored fruits, which is in accordance with several studies, which showed that fig skins have much higher amounts of phytochemical compounds, mainly flavonoids, which strongly contribute to the antioxidant capacity [[
The pulp heatmap showed a different spatial distribution of individuals and variables, where catechin, epicatechin, chlorogenic acid, cyanidine-3.5-diglucoside and cyanidine-3-O-rutinoside were the highly correlated variables, which were related to the free radical scavenging capacity. The cluster composed of the cultivars "INRA 2105", "INRA 1302" and "White Adriatic" showed similar tendencies to accumulate these variables. "Chetoui", the nearest neighbor to this cluster, combined the highest level of quercetin-3-O-rutinoside, quercetin-3-O-glucoside and TPAC. The other cultivars were essentially clustered based on their pulp chromatic coordinates that seemed moderately correlated to TAC and the antioxidant potential.
Figs of an ex-situ collection were randomly harvested at their full maturity (August–September of 2018). The collection is composed of 16 local and 9 introduced varieties and was planted in complete randomized block in the experimental station on the National Institute for Agricultural Research of Meknes (INRA) in the northern Morocco (Table 6). Figs were considered fully ripened when they were easily separated from the twig and when the receptacle turned to reddish-purple coloration. They were picked randomly at different positions around the canopy at height of 160 cm.
The cultivars were planted in the same orchard characterized with ferritic soil. During the harvest time, the average air temperature was about 27 °C with important rainfall (26.4 mm) during the last decade of August. Intense solar radiation was observed during the second decade of August and the first decade of September. The ripening process was generally rapid, lasting several days from August to early September, with significant differences among cultivars (Table 6).
The figs' peels and pulps color were measured using a colorimeter (NH310 colorimeter (Shenzhen 3NH Technology, Shenzhen, China), standardized with white and black calibration. Peel color measurements were obtained from two randomized spots located on opposite sides of the equatorial region of the fruit, while pulp color was measured at two random spots of both half of the fruit. The mean of the two measurements was considered as one replicate. Fifteen replications per sample were considered.
The color was studied in the CIEL*a*b* color space using a Minolta CM-700 (Minolta Camera Co., Osaka, Japan), with illuminant D65, SCI mode and an observer angle of 10°. Low reflectance glass (Minolta CR-A51/1829-752) was placed between the samples and the equipment. The CIEL*a*b* coordinates determined were lightness (L*), redness (a*, coordinate red/green), and yellowness (b*, coordinate yellow-blue) and the psychophysical parameters hab (hue) and Cab∗ (chroma), which were calculated as follows:
The present study focused particularly on L*, c* and h° indices, since a* and b* are merely coordinates that indirectly reflect hue and Chroma.
For each cultivar, figs randomly chosen were manually peeled and each part was frozen at −80 °C for 48 h and then lyophilized (CHRIST ALPHA 1-2 LDplus). Hereto, triplicate lots of fig peels and pulps of each cultivar were grounded to a powder using an IKA A11 Basic Grinder (St. Louis, MO, USA) at room temperature.
Phenolic extraction was performed on the powder of lyophilized peels and pulps as described by Xie and Bolling [[
TFC was measured using the colorimetric method with aluminum chloride [[
TAC was measured with the pH differential absorbance method, as described by Cheng and Breen. [[
TPAC was determined based on acid hydrolysis and color formation method as reported by Porter et al. [[
The antioxidant activity was assessed as the free radical scavenging activity using two assays DPPH and ABTS in methanolic solution [MeOH/water; 80/20%; v:v; +1% HCl] and the inhibition of lipid peroxidation in linoleic acid system.
The DPPH (radical 2,2-diphenyl-1-picrylhydrazyl) method was performed as described by Brand-Williams et al. [[
For the three assays above, the analyses were performed in triplicate, and the results were expressed as mMol Trolox equivalent/g dw (mMol TE/g dw) using the following formula:
(
where, I(%) represents the percentage inhibition of samples, and a and b correspond, respectively, to the slope and the constant of the linear equation related to the standard curve of each assay.
The half-maximal inhibitory concentration (IC50) was estimated by linear regression using the fitted line as follows:
(
(
where, y represents radical scavenging percentage, and x represents samples extracts concentrations.
Fig samples (1 g) were mixed with 10 mL of methanol: water (80:20, v/v). The mixture was sonicated and then macerated for 60 min at 4 °C. The samples were centrifuged for 10 min, 8000 g at 4 °C, and the supernatants were collected, and the pellets were mixed with 10 mL of acetone: water (70:30, v/v). The same steps (sonication, maceration and centrifugation) were repeated three times, and the supernatants were combined and evaporated using a rotary evaporator R-205 under reduced pressure, at 40 °C. Five milliliters of methanol were added to the residue, and the mixture was well shaken in a Vortex for 2 min. The samples were filtered through a Sep-Pak (c-18) to remove the sugar content and then were stored at −20 °C until further use.
Polyphenolic profiles of both peel and pulp fruits were determined by high-performance liquid chromatography (HPLC) following the methodology described by Genskowsky et al. [[
Statistical analysis of the data was performed using SPSS v22. Multivariate analysis of variance (MANOVA), with Wilks Lambda used as the test statistic, was performed in the data treatment to test significant differences among cultivars and their fruits' peels and pulps in addition to their interaction. The differences in the results were estimated with Duncan new multiple range (DMRT) test for pairwise comparison at a level of 5%. A two-dimensional CHA heatmap was applied to the dataset using R software 3.0.2. Prior to this analysis, data were standardized to a comparable scale (µ = 0 and σ = 1). In this presentation of data, the effect size measure is represented by the color intensity. The heatmap groups similar rows and similar columns together, with their similarity represented by a dendrogram. This method is of importance to achieve a better understanding of complex biological systems where one-way direction is assumed [[
Understanding the partitioning of phenolic compounds, antioxidant capacity and chromatic coordinates between fig peels and pulps and investigating the relationship between these factors are necessary, since the potential benefits to the consumer health of regular fig intake is to be exploited. In this study, fig samples showed highly significant differences among cultivars and between the fruit parts. The antioxidant potency of these samples was particularly important in peels, where the phenolic compounds are mainly concentrated. All antioxidant test showed a strong correlation with those compounds especially anthocyanins (cyanidine-3.5-diglucoside, cyanidine-3-O-rutinoside), that were the predominant compounds in the peel extracts. In pulps samples, (−)-epicatechin and cyanidin-3-O-rutinoside were the major compounds. The dark-colored cultivar "INRA 1301" presented the most promising phenolic profile due to its very high levels of almost all detected PCs, especially (−)-epicatechin, quercetin-3-O-rutinoside, quercetin-3-O-glucoside, cyanidine-3,5-diglucoside and cyanidine-3-O-rutinoside. However, it is evident from this study that it is difficult to attribute the antioxidant capacity to one or a specific group of compounds, and that another multifactorial approach is required. Chemometric approaches such as color-coded visualization of the clustered data via dendrograms and heatmaps are of great use to understand the partitioning of studied variables between both cultivars and their fruit parts. The findings herein reported confirm that the figs peels are largely superior to the corresponding pulps, as it relates to phenolic compounds as well as antioxidant potency, endorsing the insistence to further investigate and valorize this unexploited discarded agro-industrial byproduct. They also confirmed the importance of consuming the whole figs as an important habit for the health promoting diet.
Graph: Figure 1 Principal component analysis (PCA) two-dimensional scatter plots based on the first two principal components (PC1 and PC2) generated for 25 cultivars based chromatic coordinates color of figs' peels and pulps.
Graph: Figure 2 HPLC-DAD profile, chemical structures of the main phenolic compounds identified in the fig pulp. Example of the cultivar INRA 2015.
Graph: Figure 3 Chemical structures of the main phenolic compounds identified in the fig peels (A) and pulp (B).
Graph: Figure 4 Hierarchically clustered heatmap based on the correlation matrix of studied variables in both peel (red map) and pulp (blue map). The low color intensity means the lower value and vice versa. Chr.A: chlorogenic acid; Q.3.O.r: quercetin-3-O-rutinoside; Q.3.O.g: quercetin-3-O-glucoside; Lu.7.O.g: luteolin-7-O-glucoside; Quercetin: quercetin; Apigenin: apigenin; Cya.3,5.d: cyanidin-3,5-diglucoside; Cya.3.O.r: cyanidin-3-O-rutinoside; Pel.3.O.r: pelargonidin-3-O-rutinoside. White A.: "White Adriatic"; Cuello B.D: "Cuello Dama Blanca"; Breval B.: "Breval Blanca"; Breba B.: "Breba Blanca"; El Quoti L.: "El Quoti Lbied".
Graph: molecules-26-02574-g004b.tif
Table 1 Descriptive analysis and multivariate analysis of variance of all studied variables over figs' peels and pulps.
Variables Fruit Part Mini Max Mean Std. Deviation ANOVA Gallic acid * Peel 0 11.29 0.54 2.24 <0.001 (+)-Catechin * 0 24.06 5.89 5.95 <0.001 (−)-Epicatechin * 2.61 55.44 17.31 12.89 <0.001 Chlorogenic acid * 0 10.67 3.03 2.94 <0.001 Quercetin-3- 5.3 147.42 58.46 38.66 <0.001 Quercetin-3- 2.52 35.58 11.48 7.76 <0.001 Luteolin-7- 0 18.24 6.75 4.87 <0.001 Quercetin * 0 59.61 4.49 12.48 <0.001 Apigenin * 0 4.91 0.41 1.04 <0.001 Cyanidin-3,5-diglucoside * 0 495.76 48.58 109.91 <0.001 Cyanidin-3- 0 478.9 46.78 105.29 <0.001 Pelargonidin-3- 0 12.67 0.67 2.58 <0.001 TPC (mg GAE/100 g dw) 370 3162.86 1368.67 671.01 <0.001 TFC (mg CE/100 g dw) 188.57 2013.57 690.19 371.47 <0.001 TPAC (mg Cyan /100 g dw) 0.2 3.09 0.83 0.83 <0.001 TAC (mg cy-3-r /100 g dw) 4.14 192.5 37.17 41.9 <0.001 DPPH (mMol TE/g dw) 21.23 367.26 156.76 21.53 <0.001 ABTS (mMol TE/g dw) 7.57 563.53 231.52 19.59 <0.001 LPIC (mMol TE/g dw) 139.17 353.11 226.26 10.44 <0.001 L* 19.81 73.51 49.51 15.54 <0.001 c* 0.89 62.76 37.42 16.36 <0.001 h* -3.41 360.95 78.58 57.02 <0.001 Gallic acid Pulp nd nd nd nd <0.001 (+)-Catechin 0 6.65 1.47 1.4 <0.001 (−)-Epicatechin 1.25 19.06 5.23 4.03 <0.001 Chlorogenic acid 0 4.84 0.77 1.09 <0.001 Quercetin-3- 0 26.85 1.89 5.16 <0.001 Quercetin-3- 0 4.05 0.44 0.95 <0.001 Luteolin-7- 0 4.5 0.21 0.89 <0.001 Quercetin nd nd nd nd <0.001 Apigenin nd nd nd nd <0.001 Cyanidin-3,5-diglucoside 0 28.45 5.82 6.68 <0.001 Cyanidin-3- 0.94 34.43 9.01 8.67 <0.001 Pelargonidin-3- nd nd nd nd <0.001 TPC 105.71 1255.71 426.38 234.32 <0.001 TFC 13.57 331.43 157.57 79.96 <0.001 TPAC 0.2 1.06 0.37 0.13 <0.001 TAC 2.27 19.44 7.71 4.49 <0.001 DPPH 13.92 151.24 73.99 7.05 <0.001 ABTS 6.59 207.49 76.19 7.35 <0.001 LPIC 42.89 226.88 121.25 7.7 <0.001 L* 12.17 34645 493.3 6.81 0.622 c* 12.35 59.85 28.02 13.64 <0.001 h* 4.87 74.8 32.33 16.59 <0.001 Variety 0 477.23 560 1376.367 0 Fruit part 0 496,075.72 20 79 0 Variety * Fruit part 0 464.37 440 1242.807 0
Table 2 Total phenols, flavonoids, anthocyanins, proanthocyanidins, antioxidant activity and chromatic coordinates of fig peels.
Cultivars TPC TFC TPAC TAC DPPH ABTS LPIC IC50 (DPPH) IC50 (ABTS) IC50 (LPIC) L* c* h° Bioudie 1346.19 602.86 0.90 10.82 332.96 452.52 154.84 172.38 292.70 114.83 55.46 45.97 91.43 Breba Blanca 1093.81 590.95 0.43 14.27 100.19 192.06 278.94 125.46 185.47 83.56 59.81 47.67 85.01 Breval Blanca 796.19 669.52 0.51 15.78 254.75 364.80 231.87 306.04 285.62 24.45 62.62 54.83 90.86 Chaari 696.19 388.57 0.39 9.93 299.74 527.25 169.11 129.47 112.22 51.81 44.85 39.14 90.87 Chetoui 1100.95 708.81 2.20 18.13 329.04 336.61 160.55 27.42 119.33 124.80 65.56 50.4 96.1 Cuello Dama Blanco 1391.43 1177.86 0.33 34.88 333.99 491.90 155.56 80.47 163.46 86.35 63.32 51.12 92.73 El Quoti Lbied 1241.43 493.33 0.50 11.65 68.83 175.95 255.40 156.99 154.30 99.83 48.8 37.29 95.72 Fassi 2020.00 935.00 0.58 47.90 332.13 493.69 232.58 0.28 97.35 216.92 31.78 10.28 215.93 Ghoudan 927.14 602.86 0.46 19.16 133.21 210.85 289.63 76.47 225.29 81.13 28.13 28.96 42.36 Herida 389.05 214.76 0.33 21.50 56.86 77.49 240.43 234.03 230.18 125.68 51.25 44.53 90.85 INRA 1302 1627.14 807.62 1.97 53.00 37.87 77.49 191.22 3.97 56.49 76.19 31.36 18.39 18.33 INRA 1305 912.86 417.14 1.04 22.33 40.76 157.60 216.89 92.67 114.38 136.79 36.42 19.02 36.25 INRA 2105 2070.00 1282.62 1.67 51.97 79.97 137.01 251.84 3.88 73.70 101.26 34.61 13.85 19.96 INRA 2201 1865.24 689.76 1.13 126.41 54.38 147.31 295.34 109.17 68.01 263.49 36.79 24.53 25.41 INRA 2304 2396.19 385.00 0.76 63.75 16.62 91.81 238.29 2.12 21.84 124.04 24.52 38.88 23.35 INRA1301 2860.48 1944.52 2.59 192.23 152.40 190.72 198.35 19.85 40.58 124.78 25.72 22.09 20.99 Kadata 1208.10 492.14 0.54 17.16 29.41 126.27 301.76 201.52 174.22 98.09 59.62 48.67 98.26 Nabout 810.48 699.29 1.21 82.29 121.45 459.23 239.00 16.98 177.38 132.85 52.86 55.04 89.07 Noukali 822.38 677.86 0.50 21.23 128.26 212.64 203.34 25.04 202.71 55.03 28.7 41.67 53.68 Ouarraksi 1384.29 763.57 0.48 4.82 218.02 293.65 278.94 161.00 297.22 88.32 59.26 38.39 103.53 Palmeras 2855.71 1070.71 0.33 18.06 29.21 157.15 199.06 106.34 179.49 87.90 65.15 36.95 93.99 Sarilop 1155.71 263.57 0.38 17.16 21.78 12.82 278.22 175.77 200.03 78.28 59.21 48.26 90.94 Snowden 1700.95 598.10 0.42 15.58 69.45 440.43 248.98 123.15 190.12 80.01 72.62 54.57 94.84 Trojana 415.24 317.14 0.56 11.10 5.27 12.01 189.79 170.40 495.99 295.07 73.16 50.95 90.38 White Adriatic 1129.52 461.19 0.44 28.05 22.66 0.07 156.27 162.94 299.49 103.07 59.7 37.58 99.14
Table 3 Total phenols, flavonoids, anthocyanins, proanthocyanidins, antioxidant activity and chromatic coordinates of fig pulps.
Cultivar TPC TFC TPAC TAC DPPH ABTS LPIC IC50 (DPPH) IC50 (ABTS) IC50 (LPIC) L* c* h° Bioudie 339.05 95.71 0.40 3.58 22.21 24.37 40.48 275.08 418.35 152.16 20.67 44.04 7.83 Breba Blanca 255.71 170.71 0.36 5.86 19.43 24.32 35.86 206.83 226.64 231.46 34.91 17.05 36.51 Breval Blanca 731.90 257.62 0.45 6.75 35.01 16.42 23.51 163.29 455.25 169.11 19.05 55.05 16.46 Chaari 284.29 250.48 0.26 3.03 25.41 23.44 24.85 202.38 220.80 241.85 34.10 29.50 32.35 Chetoui 491.43 257.62 0.64 8.27 39.50 25.03 38.99 168.57 204.48 231.55 25.18 15.33 27.07 Cuello Dama Dlanco 439.05 93.33 0.25 3.45 33.75 40.83 21.13 199.52 221.21 238.04 19.95 46.79 6.52 El Quoti Lbied 422.38 162.38 0.41 3.24 32.69 33.51 21.43 139.85 198.06 201.63 44.51 16.53 42.33 Fassi 234.29 93.33 0.38 11.37 27.66 22.73 31.40 245.24 201.32 130.18 18.62 44.07 36.60 Ghoudan 1186.67 271.90 0.29 12.48 33.60 33.95 32.59 201.06 241.50 85.47 33.24 14.72 54.88 Herida 174.76 107.62 0.29 7.72 18.70 17.67 35.86 151.47 233.68 148.96 34.18 15.14 62.97 INRA 1302 520.00 250.48 0.47 7.31 34.06 35.82 26.79 167.29 316.70 392.39 35.10 22.29 36.35 INRA 1305 262.86 131.43 0.22 16.89 15.35 14.43 43.45 269.32 665.58 138.37 40.04 17.22 55.95 INRA 2105 753.33 160.00 0.56 9.58 38.78 32.85 33.33 117.46 138.88 164.76 34.31 17.98 38.18 INRA 2201 374.76 106.43 0.43 3.24 25.75 33.20 35.12 160.10 186.17 145.74 45.91 18.83 42.91 INRA 2304 465.24 229.05 0.31 5.17 30.21 23.26 24.55 273.64 299.00 138.24 41.24 27.78 40.09 INRA1301 398.57 186.19 0.41 14.06 31.43 22.99 35.42 124.58 309.90 149.39 36.55 19.90 39.46 Kadata 331.90 146.90 0.43 10.68 29.18 26.01 24.55 152.18 225.52 187.61 33.31 14.83 33.58 Nabut 662.86 285.00 0.42 3.10 25.22 31.69 28.27 202.18 292.24 241.83 27.72 40.87 24.90 Noukali 329.52 21.90 0.30 5.03 30.51 28.81 23.96 290.33 242.72 212.67 20.45 46.30 23.42 Ouarraksi 255.71 137.38 0.55 3.58 26.48 22.50 18.01 173.75 288.42 306.69 37.63 31.32 35.36 Palmeras 450.95 199.29 0.22 11.85 32.38 29.69 30.36 187.54 138.48 185.15 19.22 49.20 13.68 Sarilop 408.10 110.00 0.26 5.44 24.23 20.86 16.07 308.37 353.84 300.35 41.90 22.04 57.91 Snowden 274.76 20.71 0.39 10.34 27.01 35.86 26.49 152.55 359.54 138.24 36.62 15.71 44.56 Trojana 205.71 133.81 0.31 3.86 19.54 15.85 28.57 563.91 892.67 231.46 24.06 34.28 15.21 White Adriatic 405.71 60.00 0.35 16.82 42.63 24.01 31.40 166.52 415.02 125.67 38.22 20.90 46.45
Table 4 Contents of individual phenolic compounds (µg/g dw) among cultivars figs peels.
Cultivars Gallic Acid (+)-Catechin (−)-Epicatechin Chlorogenic Acid Quercetin-3- Quercetin-3- Luteolin-7- Quercetin Apigenin Cyanidin-3,5-Diglucoside Cyanidin-3- Pelargonidin-3- Total (µg/g) Biondie - 3.38 14.05 3.34 55.39 11.66 7.19 0.86 - - 95.86 Breba Blanca - 1.74 6.37 0.56 10.98 6.16 - - - 0.86 1.06 - 27.74 Breval Blanca - 5.14 19.01 1.66 65.05 7.29 12.43 - - 0.76 0.84 - 112.18 Chaari - 1.30 9.84 0.59 44.18 10.07 5.83 - - 3.76 6.31 - 81.88 Chetoui 11.25 2.86 10.21 2.93 125.68 18.66 8.96 - - 0.86 1.08 - 182.49 Cuello Dama Blanco - 16.54 42.35 8.77 46.49 5.32 17.91 59.52 4.84 - - - 201.73 El Quoti Lbied - 2.81 16.24 0.49 28.94 6.92 - 1.01 1.13 7.03 - - 64.57 Fassi - 7.76 19.01 4.12 147.33 21.06 15.21 1.00 - 81.08 83.91 - 380.49 Ghoudan - 2.35 16.67 1.16 85.87 21.91 11.86 1.40 - 21.06 20.17 - 182.46 Herida - 0.99 5.12 0.46 17.88 3.39 2.58 - - 30.42 INRA 1302 - 4.02 12.23 4.28 53.78 10.34 5.69 4.45 - 97.69 100.32 - 292.81 INRA 1305 - 3.82 18.96 8.71 70.98 14.67 1.17 21.14 21.61 - 161.05 INRA 2105 - 23.87 13.18 0.67 38.35 8.63 3.82 5.52 1.70 43.03 40.55 - 179.31 INRA 2201 - 4.67 24.83 5.49 54.77 13.46 5.82 1.20 275.20 246.86 4.16 632.31 INRA 2304 - 7.45 11.07 0.86 64.49 14.19 7.26 3.87 130.12 131.23 - 370.54 INRA1301 - 14.36 54.66 7.81 141.08 35.48 11.50 2.17 494.08 478.66 12.56 1239.80 Kadata - 0.92 6.21 1.40 20.23 2.56 3.34 0.91 1.11 - 36.69 Nabout 2.22 7.01 9.86 0.90 33.78 6.03 6.71 1.46 - 1.04 1.15 - 70.15 Noukali - 6.28 31.98 8.39 112.91 21.47 1.86 - - 35.89 34.88 - 253.66 Ouarraksi - 3.19 12.42 3.71 92.49 11.22 8.61 - - 0.83 0.94 - 133.41 Palmeras - 18.25 44.22 4.48 23.15 18.31 15.03 - 1.40 - - - 151.77 Sarilop - 3.60 14.91 2.30 41.88 4.64 4.30 - - - - - 71.63 Snowden - 2.83 11.52 2.24 49.46 6.86 5.33 - - - - - 78.23 Trojana - 2.67 16.47 3.25 2.39 - - - - - 24.78 White Adriatic - 2.24 5.09 0.57 19.79 3.53 5.17 0.91 - - - - 37.30
Table 5 Contents of individual phenolic compounds (µg/g dw) among cultivars' fig pulps.
Cultivars (Pulp) (+)-Catechin (−)-Epicatechin Chlorogenic Acid Quercetine-3- Quercetine-3- Luteoline-7- Cyanidine-3.5-Diglucoside Cyanidine-3- Total (µg/g) Biondie - 2.15 - - - - 0.82 1.31 1.43 Breba Blanca 1.12 3.38 0.46 - - - 3.86 1.85 2.13 Breval Blanca 1.71 4.79 0.33 0.92 - - 5.53 8.05 3.56 Chaari 1.43 4.09 - 1.23 - - 2.59 3.8 2.63 Chetoui 1 7.99 1.3 26.8 4.03 0.75 ± 0.35 6.87 11.87 8.55 Cuello Dama Blanca - 3.85 3.14 1.23 0.98 - 4.74 11.05 4.17 El Quoti Lbied - 1.75 0.38 - - - 3.91 7.93 3.49 Fassi 2.63 9.08 0.68 1.23 - - 11.93 16.94 7.08 Ghoudan 1.92 2.47 0.31 1.51 1.31 - 2.41 5.42 2.19 Herida 0.67 2.03 - - - - 0.9 1.04 1.16 INRA 1302 2.96 9.91 1.22 1.06 - - 14.74 20.37 8.38 INRA 1305 2.11 7.83 1.04 - - - - 1.52 3.13 INRA 2105 6.63 19.05 4.83 2.21 1.45 - 20.38 28.78 11.90 INRA 2201 1.34 1.75 0.4 - - - 4.73 10.44 3.73 INRA 2304 - 1.27 - 0.81 - - 2.83 5.12 2.51 INRA 1301 0.73 1.3 - - - - 0.83 1.39 1.06 Kadota 1.2 8.37 0.44 1.02 - - 8.98 16.6 6.10 Nabout 1.5 2.52 0.36 1.03 1.05 - 1.11 3.03 1.51 Noukali 1.67 4.28 0.33 1.48 - - 6.15 11.1 4.17 Ouarraksi 1.39 1.65 0.47 1.42 - - 4.11 9.68 3.12 Palmeras 3.06 7.23 2.07 1.92 2.19 4.47 ± 0.04 6.88 8.81 4.59 Sarilop 1.82 10.88 0.49 0.89 - - 0.93 2.25 2.88 Snowden - 5.08 0.37 - - - 0.89 1.57 1.98 Trojana - 4.15 - 1.2 - - 0.84 0.96 1.79 White Adriatic 1.83 3.91 0.58 1.22 - - 28.43 34.42 11.73
Table 6 Cultivars geographical origins, harvest time and monthly meteorological data from August to early September 2018 in Northern Morocco, Meknes (Ain-Taoujdate experimental station—INRA).
Cultivars Geographical Origin August September (1–5) (6–10) (11–15) (16–20) (21–25) (26–30) (31–4) (5–9) Local El Quoti Lbied Morocco Nabout Fassi Noukali Ghoudan Chetoui Bioudie Chaari Ournaksi INRA 1305 INRA 2105 INRA 1302 INRA 2201 INRA 2304 INRA 1301 Introduced Snowden USA White Adriatic Italy Kadota Italy Triana Italy Cuello Dama Blanca Spain Breval Blanca Spain Palmeras Spain Herida Spain Breba Blanca Spain Total rainfall (mm) 0 0 0 0 0 26.4 0 0 Average temperature (°C) 25.84 28.5 27.56 29.24 29.44 23.64 25.6 25.42 Average solar radiation (W/m²) 169.29 208.74 243.83 238.28 185.35 123.5 270.21 271.38 Soil type Sandy clay loam with an average organic matter of 1% [0–30 cm soil layer] Soil pH 7.2
L.H.: supervision, conceptualization, methodology, investigation, data curation, software, resources, validation, review and editing, in vitro assays methodology and experiments, and writing—original draft. M.V.-M. and F.H.: formal analysis. H.H., S.E., M.L.F., and D.E.: visualization. R.R. and J.C.: visualization. R.O., K.H. and I.H.: data curation. All authors have read and agreed to the published version of the manuscript.
This research received no external funding.
Not Avaliability.
The authors declare no conflict of interest.
The following are available online, Figure S1: Heatmap correlation between all studied variables in fig pulp samples. Figure S2: Heatmap correlation between all studied variables in fig peel samples. Blue color refers to the positive correlations, while red one indicates low correlations between variables. For both, the low color intensity means the lower value and vice versa.
By Lahcen Hssaini; Francisca Hernandez; Manuel Viuda-Martos; Jamal Charafi; Rachid Razouk; Karim Houmanat; Rachida Ouaabou; Said Ennahli; Driss Elothmani; Ilham Hmid; Marie Laure Fauconnier; Hafida Hanine and Encarna Gómez-Plaza
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