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Article

Comparative Study on the Total Phenolics, Total Flavonoids, and Biological Activities of Papaver rhoeas L. Extracts from Different Geographical Regions of Morocco

by
Anouar Hmamou
1,*,
Mohammed Kara
1,2,*,
Mostafa El Khomsi
3,
Asmaa Saleh
4,
Omkulthom Al Kamaly
4,
Ahmed Bendaoud
1,
Faiçal El Ouadrhiri
1,
Abderrazzak Adachi
1,
Sara Tlemcani
1,
Noureddine Eloutassi
1 and
Amal Lahkimi
1
1
Laboratory of Engineering, Electrochemistry, Modeling and Environment, Faculty of Sciences Dhar El Mahraz, Sidi Mohamed Ben Abdellah University, B.P. 1796 Atlas, Fez 30000, Morocco
2
Laboratory of Biotechnology, Conservation and Valorisation of Natural Resources (LBCVNR), Department of Biology, Faculty of Science Dhar El Mahraz, Sidi Mohamed Ben Abdellah University, B.P. 1796 Atlas, Fez 30000, Morocco
3
Natural Resources and Sustainable Development Laboratory, Department of Biology, Faculty of Sciences, Ibn Tofail University, B.P. 133, Kenitra 14000, Morocco
4
Department of Pharmaceutical Sciences, College of Pharmacy, Princess Nourah Bint Abdulrahman University, P.O. Box 84428, Riyadh 11671, Saudi Arabia
*
Authors to whom correspondence should be addressed.
Appl. Sci. 2023, 13(4), 2695; https://doi.org/10.3390/app13042695
Submission received: 7 January 2023 / Revised: 9 February 2023 / Accepted: 17 February 2023 / Published: 19 February 2023
(This article belongs to the Section Food Science and Technology)
Browse Figures
Versions Notes

Abstract

:
In this research, a comparative analysis was carried out to characterize the content of phenolics and biological activities of the whole plant of Papaver rhoeas L. (P. rhoeas) from different geographical regions of Morocco, as well as to determine the synergistic antimicrobial and antioxidant effects of all parts of P. rhoeas. The determination of total polyphenol content (TPC), total flavonoid content (TFC), and total anthocyanin content (TA) in extracts of whole plants of P. rhoeas from three different geographical regions: Taounate (P1E), Fez (P2E), and Sefrou (P3E) were estimated by the Folin–Ciocalteu reaction, the aluminum trichloride method and the differential pH absorption technique, respectively. Two tests were used to evaluate the antioxidant power of our samples: the DPPH test and the TAC test. Using two methods, disk diffusion and microdilution, antimicrobial activity was studied against four pathogenic bacteria and one yeast. The results of TPC, TFC, and TA show that the P3E sample is the richest in polyphenols, flavonoids, and anthocyanins, with values 37.33 ± 1.307 mg GAE/g, 4.72 ± 0.346 QE/g, and 1.77 ± 0.026 CGE/g, respectively. In addition, P3E showed the best antioxidant activity with an IC50 = 0.27 ± 0.001 mg/mL and TAC = 9.99 ± 0.768 mg AAE/g, respectively. The results of antimicrobial activity showed significant activity on almost all the tested strains. The lowest MIC was recorded for P3E against E. coli ATCC 25922 and E. coli CIP 53126 strains at 0.78 and 0.78 mg/mL, respectively. These results show that the geographical region can influence the plant’s phytochemistry and then these biological activities.

1. Introduction

Medicinal and aromatic plants are traditionally employed in phytotherapy. Medicinal plant knowledge has been passed down over the centuries within and between human cultures [1,2,3]. Plants produce bioactive chemicals that have pharmacological effects such as anti-inflammatory, antidiabetic, anticancer, antilithiasic, antioxidant, and antibacterial properties [4,5,6,7,8,9]. Many infectious illnesses are caused by bacteria, fungi, and viruses [10]. Despite the fact that many current antimicrobial medications have been designed to treat communicable illnesses, antimicrobial resistance has been observed over time. Several pathologies, such as cancer, cardiovascular diseases, chronic kidney diseases, diabetes, and neurological diseases, are among the chronic diseases that are related to oxidative stress [11].
The plant P. rhoeas belongs to the family Papaveraceae. It is found in Western Asia, Africa, and Northern Europe [12]. It is used as a medicinal plant in traditional phytotherapy to treat a variety of pathologies [13,14]. Several phytochemical studies show that P. rhoeas contains several bioactive molecules such as carbohydrates, vitamins, fatty acids, amino acids, phenolic compounds, alkaloids, flavonoids, organic acids, and coumarins [15,16,17,18,19]. Recent research has also proven the antioxidant, antidepressant, cytoprotective, antibacterial, antimutagenic, anti-analgesic, anti-inflammatory, and antiulcerogenic properties of P. rhoeas extracts [12,14,20,21,22,23,24,25,26,27].
Furthermore, plant metabolites are influenced by many factors, such as crop management, genotypes, and environmental conditions [28], whereas there are no studies regarding the variation of P. rhoeas phenolic content obtained from different geographical regions and their effect on biological activities. In addition, there are no studies on the antimicrobial and antioxidant synergies of all parts of P. rhoeas. Therefore, the present study aimed to examine comparatively the total polyphenol, flavonoid, and anthocyanin content as well as the antimicrobial and antioxidant activities of the whole plant of P. rhoeas from three geographical regions of Morocco: Taounate, Fez, and Sefrou for the first time. In addition, we evaluated the antimicrobial and antioxidant synergies of all parts of P. rhoeas. In addition, correlations between phenolic content and antimicrobial and antioxidant activities were determined.

2. Materials and Methods

2.1. Plant Material

The P. rhoeas plants were collected in late April 2021 from three different provinces in the Fez Meknes region, Morocco: Taounate (34°32′09″ N, 4°38′24″ W), Fez (34°03′00″ N, 4°58′59″ W), and Sefrou (33°49′50″ N, 4°50′15″ W). The selection of selected geographical areas is based on the difference in geographical and ecological factors between the provinces of the Fez Meknes region [29]. In this study, we used the whole plant to prepare our extracts. To determine the mass of each organ in the whole plant of P. rhoeas, we took 20 dried plants, separated the four organs, and weighed them. After simple calculations, we found that the percentage of the mass of each organ (roots, stems, leaves, and flowers) in the whole plant is 8.26%, 46.44%, 29.32%, and 15.96%, respectively.

2.2. Preparation of Extracts and Extraction Yield

Thirty g of the whole plant of P. rhoeas powder (2.48 g of root, 13.93 g of stem, 8.8 g of leaf, and 4.79 g of flower) from each geographical region was macerated by ethanol 70% and distilled water 30% (v/v) for 48 h at room temperature. Until use, the finished product was stored at 4 °C. Several studies show that extracts of 70% ethanol are very rich in bioactive molecules and have remarkable biological activities [30,31]. The yield was determined after extraction using the formula proposed by Falleh et al. [32]:
Y (%) = (M1/M0) × 100
Y: yield in percentage; M1: mass of dry extract in gram; M0: mass of the initial dry plant material in gram.

2.3. Determination of Phenolic, Flavonoid, and Anthocyanin Content

The TPC and TFC of P. rhoeas extracts were assessed using the methods described in our previous publication [33]. The pH differential absorbance technique was used to estimate the total anthocyanin content (TA) [34]. The values for TA, TFC, and TPC were given as cyanidin-3-glucoside chloride equivalents (CGE), quercetin equivalents (QE), and gallic acid equivalents (GAE), in grams of each P. rhoeas sample, respectively.

2.4. Antioxidant Activity of P. rhoeas Extracts

The antioxidant potential of P. rhoeas plant was assessed in vitro using two distinct tests: DPPH inhibition and total antioxidant capacity (TAC).

2.4.1. DPPH Free Radical Scavenging Test

The DPPH technique was used to determine the antioxidant activity, according to the methods used in these studies [35,36]. The same test was performed with BHT, ascorbic acid and quercetin as reference antioxidants. Each test was performed three times. The percentage of DPPH inhibition by P. rhoeas extracts was measured according to the equation below. The results are presented as IC50 in mg/mL:
DPPH inhibition (%) = [1 − (A1/A0)] × 100
A0 is the absorbance of a negative control, and A1 is the absorbance of the extract.

2.4.2. Total Antioxidant Capacity Test (TAC)

To evaluate the total antioxidant capacity of our extracts, we used the same method used in our recently published article [33]. The TAC was measured using an ascorbic acid calibration curve and expressed in mg ascorbic acid equivalents (AAE/g). The experiment was then repeated three times.

2.5. Antimicrobial Activity of P. rhoeas Extracts

The antibacterial potential of the P. rhoeas extracts studied in this paper was determined against a pathogenic yeast: C. albicans ATCC 10231 and against four pathogenic bacterial strains (E. coli ATCC 25922, E. coli CIP 53126, K. pneumoniae, and S. aureus). Microbial cultures on Mueller–Hinton (MH) agar were stored at 4 °C in the refrigerator.

2.5.1. Disc Diffusion Technique

In this investigation, the antimicrobial effect of P. rhoeas extracts was assessed using the disk diffusion method [37]. Positive controls included the antibiotics fluconazole (5 mg/disc), streptomycin (0.02 mg/disc), and tetracycline (0.02 mg/disc). The infected Petri plates were then incubated for both the bacterial and fungal strains at 37 °C in the dark; 24 h after incubation, the diameter of the inhibitory zones (DIZ), measured in millimeters, was determined. To get the mean value of the inhibition zones, which was used to compute the standard deviation, all experiments were conducted three times [38].

2.5.2. Determination of the Minimum Inhibitory Concentration (MIC)

To determine the MIC of P. rhoeas extracts against microbial strains, we used the microdilution method that was published in our recent article [33].

2.6. Statistical Analysis

The data’s mean and SD were calculated. The results were evaluated using one-way ANOVA, with a p < 0.050. Multiple correspondence analysis was used to evaluate homogeneous clustering. Utilizing the Minitab 19 program, principal component analyses were used to separate the three samples according to the parameters examined. We chose the first two main components with eigenvalues larger than one using the Kaiser criteria.

3. Results and Discussion

3.1. Extract Yields

The yield of the P1E, P2E, and P3E are 14.37 ± 0.80, 8.90 ± 1.02, and 11.81% ± 0.92, respectively. The difference in extraction yield between the three samples studied is statistically significant (p < 0.05). A recent study shows that the extraction yield of four plant parts studied (root, stem, leaf, and flower) is 12.30%, 11.77%, 18.77%, and 18.60%, respectively [33]. In addition, according to Marsoul et al. [39], the yield of the methanolic flower extract is 21%. The difference in yield can be explained by the difference in the solvent used [40], the organ of the plant used [33], and the extraction technique [39].

3.2. Determination of Total Polyphenol Content (TPC)

The TPC results were given in milligrams of gallic acid equivalent per gram of extract. Figure 1 shows that TPC in the P1E, P2E, and P3E is 29.38 ± 1.570, 26.15 ± 0.823, and 37.33 ± 1.307 mg GAE/g, respectively. The TPC value in the P3E sample is high compared to the P1E and P12 samples, and this difference between the values is significant (p < 0.05). Comparing our values obtained of TPC from three studied samples with the results of previous researches, the obtained values of TPC in the three extracts are higher than those of the fresh petals’ hydroethanolic extract and the basal leaves’ methanolic extract, at 14.30 mg GAE/g of fresh petals and 25.86 mg GAE/g of extract, respectively [41,42]. Additionally, our obtained TPC values in whole plant extracts of three samples are higher than those obtained in hydroethanolic extracts of four organs of P. rhoeas: flower, leaf, stem, and root, at 22.10, 24.24, 10.58, and 10.22 mg GAE/g, respectively [33]. In addition, the TPC in the dried pollen extract of our study plant is approximately similar to our values obtained at 34.8 mg GAE/g [43]. The most abundant metabolites detected in the Papaveraceae family are alkaloids. (+)-rhoeadine was found to be the most abundant alkaloid isolated from the aerial portions of P. rhoeas. Allocryptopine, berberine, protopine, coptisine, coulteropine, (−)-sinactine, (+)-isocorydine, sanguinarine, (+)-rhoeagenine, and (+)-roemerine were the minor alkaloids [44]. These alkaloids, particularly those of the isoquinoline type, are the most significant in terms of pharmacology [45,46]. The antioxidant [47,48,49] and antimicrobial [50] properties of Papaver alkaloids are well established.

3.3. Determination of Total Flavonoid (TFC) and Total Anthocyanin Content (TA)

The TFC in P1E, P2E, and P3E was determined at 430 nm using the reagent aluminum trichloride (AlCl3) technique, and the findings were calculated in mg of quercetin equivalent per one gram of extract (mg QE/g). Figure 2 shows that the TFC in P1E, P2E, and P3E is as follows 4.47 ± 0.30, 4.44 ± 0.286, 4.72 ± 0.346 mg QE/g of dry extract, respectively. The variation in total flavonoid between the three samples is not significant (p > 0.05). Comparing our obtained TFC values with previous literature, in Morocco, Marsoul et al. found that the TFC in methanolic flowers extract is 8.67 mg QE/g [39]. The TFC in the extract of fresh petals of P. rhoeas is 9.07 mg QE/g [41], while in the P. rhoeas basal leaves’ extract is 12 QE mg/g [42]. The total flavonoid content in these works are relatively higher than our obtained values. Moreover, the values obtained of TFC in the three studied extracts of the whole plant are relatively similar to those obtained in the extracts of four organs (flower, leaf, stem, and root) of P. rhoeas: 4.50, 4.39, 4.49, and 4.38 mg QE/g, respectively [33]. In this regard, a research from 2004 found that the methanolic extracts included the kaempferol flavonoids, luteolin, hypolaetin, and quercetin as well as the glycosides, flavonoid, hyperoside, astragalin, and isoquercitrin [18]. Further research revealed that the hydro-alcoholic extracts included vitexin, rutin, coumarin, malvidin, and luteolinidin [14].
The TA in the studied extracts PE1, PE2, and PE3 was highly unified 1.71 ± 0.008, 1.66 ± 0.070, 1.77 ± 0.026 mg CGE/g extract, respectively (Figure 3). The difference in TA values in the three samples was statistically not significant (p > 0.05). Comparing our TA values with previous studies, a Serbian study showed that the total content of monomeric anthocyanins in all studied extracts ranged from 4.72 to 5.3 mg CGE/g of fresh petals. The values of total monomeric anthocyanin content do not differ significantly in ethanolic, aqueous, and methanolic extracts [41].
Variability in plant metabolites may be caused by environmental factors (geographical location, cultivar genotype, soil type, etc.) and experimental variables (period of harvest of the plant studied, the part of the plant used, the polarity of the solvent used, and the extraction method used) [51,52].

3.4. Antioxidant Activity

3.4.1. Scavenging of the Free Radical DPPH

The antioxidant properties of three P. rhoeas extracts were evaluated using the DPPH method. Figure 4 illustrates the IC50 data achieved in this test. The IC50 values for P1E, P2E, and P3E are 0.30 ± 0.006, 0.37 ± 0.003, and 0.27 ± 0.001 mg/mL, respectively. The difference in IC50 values between the three samples studied is significant (p < 0.05). The IC50 values for reference molecules: butylated hydroxytoluene (BHT), ascorbic acid, and quercetin are 0.20 ± 0.004, 0.062 ± 0.004, and 0.054 ± 0.004 mg/mL, respectively. The IC50 values obtained for the three samples studied are relatively higher than those for standard molecules. The difference in IC50 between the three samples studied and these reference molecules is statistically significant (p < 0.05). Comparing the IC50 values obtained with previous literature, the IC50 of Moroccan P. rhoeas flower extract (Soxhlet and maceration) is 3.81 and 4.97 mg/mL, respectively [39]. Furthermore, in a recent Moroccan study, the IC50 of the four organs (flower, leaf, stem, and root) of P. rhoeas were 0.52, 0.50, 1.56, and 2.12 mg/mL, respectively [33]. In addition, the acetone, ethanolic, and aqueous P. rhoeas leaves extracts had IC50 values of 5.49, 3.11, and 1.39 mg/mL, respectively [12].

3.4.2. Total Antioxidant Capacity

The total antioxidant capacity values is calculated in mg of AAE per one gram of extract. Figure 5 illustrates the TAC results obtained of the samples examined. The TAC of our samples, P1E, P2E, and P3E, is 7.53 ± 1.675, 6.99 ± 1.248, and 9.99 ± 0.768 mg AAE/g, respectively. The difference in total antioxidant capacity values between the three P. rhoeas samples was not significant (p > 0.05). Comparing the obtained TAC results of three studied samples with the former studies, the TAC values of four organs (flower, leaf, stem, and root) of P. rhoeas were 5.53, 6.60, 5.45, and 3.22 AAE mg/g, respectively [33]. Our obtained TAC values for the whole plant are higher than those obtained in this study.

3.5. Antimicrobial Activity

3.5.1. Disc Diffusion Test

The disc inhibition assay was used to examine the antimicrobial potential of P1E, P2E, and P3E against five pathogenic microorganisms. Table 1 shows the DIZ values of our three extracts. The DIZ results varied from 15.00 ± 1.00 mm for E. coli CIP 53126 to 10.00 ± 2.00 mm for C. albicans. The K. pneumoniae strain is resistant to P3E and the C. albicans strain is resistant to P1E and P3E samples. The difference between the DIZ values of the three samples against the strains E. coli ATCC 25922, S. aureus, and K. pneumoniae is not significant (p > 0.05), whereas against the E. coli CIP 53126 strain, this difference is significant between P2E and P3E with the P1E. The antibiotic tetracycline shows higher DIZ values against all bacterial strains compared to our extracts, whereas streptomycin shows a lower DIZ of 09.61 ± 0.20 mm against the S. aureus strain compared to our samples. Fluconazole causes a DIZ of 21.20 ± 04.20 mm against C. albicans. The difference in DIZ values between extracts and antibiotics is significant (p < 0.05). In comparing the DIZ results obtained from the three samples with previous studies, in a recent Moroccan study, the majority of the strains studied (C. albicans, E. coli ATCC, K. pneumoniae, E. coli CIP, and S. aureus) were sensitive to extracts of four organs of P. rhoeas. The DIZ values ranged from 8.33 mm against K. pneumoniae to 13.66 mm against S. aureus [33].

3.5.2. Determination of the Minimum Inhibitory Concentration (MIC) of P. rhoeas Extracts

The MIC results of the P. rhoeas samples were determined against most of the microbes studied. The MIC results of three samples and antibiotics are presented in Table 2. The MIC results of our samples against the studied bacteria range from 0.78 mg/mL for sample P3E against E. coli ATCC and E. coli CIP and 50 mg/mL for sample P2E against the same strains, while the MIC values of P1E and P2E samples against yeast C. albicans are 50 and 25 mg/mL, respectively. Our values of MIC are also consistent with the literature when compared to the MIC values from previous research. A study in Turkey, the ethanolic extract of P. rhoeas showed antibacterial effect against S. aureus at 0.150 mg/mL but no action against C. albicans, E. coli, and K. pneumoniae. In addition, the MIC of diethyl ether, acetone, and chloroform extracts against S. aureus was 39.06 g/mL [27]. In Morocco, the MICs of flower P. rhoeas extract against S. aureus, K. pneumoniae, and E. coli were 60, 30, and 60 mg/mL, respectively [39]. In another Moroccan research, the antimicrobial effect of the four organs (flower, leaf, stem, and root) of P. rhoeas was determined. The MIC ranged from 0.78 mg/mL to 50 mg/mL [33].
In this regard, study [53] suggested that the presence of hydroxyl groups in phenolic substances may be related to their increased antimicrobial activity [54,55]. Çoban et al., on the other hand, discovered a link between the content of alkaloids (particularly roemerine) in P. rhoeas extracts and their antibacterial potential [20].
In this context of the effect of the geographic region on plant metabolites and biological activities, recent studies confirm our results. A Chinese study on P. ostii stamen extracts collected from eight different locations in China was conducted to demonstrate the distinction of bioactive molecules and biological capacities between P. ostii stamen extracts from different geographical locations [28]. Another Moroccan study showed that the geographical region influences the metabolites, antimicrobial potential, and yield of rosemary essential oil [56].

3.6. Relationships between Studied Parameters of P. rhoeas Extracts

Table 3 represents the Pearson correlation coefficients between the different parameters in this work. Some parameters are positively correlated while others are negatively correlated. Starting with the positively correlated parameters namely: TPC with TFC, TA, and TAC (r = 0.984, 0.983, and 0.993, respectively), TFC with TA and TAC (r = 0.934, 0.998, respectively), TA with TAC (r = 0.954), E. coli CIP with E. coli ATCC (r = 1.00), and finally K. pneumoniae with S. aureus (r = 1.00). Other parameters are negatively correlated, namely: IC50 with TAC (r = −0.824), yield with IC50 (r = −0.723), TPC with IC50 and MIC E. coli ATCC, E. coli CIP (r = −0.884, −0.969, and −0.971, respectively), TFC with IC50 and MIC E. coli ATCC, E. coli CIP (r= −0.787, −0.911, and −0.914, respectively), TA with IC50 and MIC E. coli ATCC, E. coli CIP (r = −0.955, −0.998, and −0.999, respectively) and lastly IC50 with TAC (r = −0.824). Our correlation results show that the antioxidant activity of three samples studied is positively correlated with TPC, TFC, and TA. In this context, several studies show the linear correlation between antioxidant activity and phenolic substances [57,58,59].
Principal component analysis (PCA) is a powerful method for extracting data from multivariate matrices because it portrays the data as a set of a few orthogonal variables [60]. The parameters are displayed in blue, while the samples are plotted in red (Figure 6). The first component represents (PC1) 83% of the variation in the data, while the second component (PC2) represents 16%. PC1 is positively correlated with TPC, TFC, TA, TAC, MIC Kp, and MIC Sa. Therefore, a negative correlation can be observed between the same principal component and IC50, MIC E. coli ATCC, and MIC E. coli CIP. In addition, the PC2 is positively correlated with IC50 and MIC E. coli ATCC and MIC E. coli CIP, so it is negatively correlated with MIC Ca, TA, and yield.
Given the similarities of the samples, PCA was able to distinguish between the three samples studied. There was a large difference between the three samples. The P3E sample presented a high content of TPC, TFC, and TA and, consequently, the highest antioxidant activity (high TAC and low IC50) and better antibacterial activity (MIC) against E. coli ATCC and E. coli CIP strains compared to the other samples. In addition, P2E and P1E samples showed very high antimicrobial activity against K. pneumoniae, S. aureus, and C. albicans strains compared to the P3E sample.

4. Conclusions

In this study, the whole plant of P. rhoeas, collected from three geographical regions of Morocco, was studied to characterize the content of phenolic and some biological activities (antimicrobial and antioxidant activities). The whole plant of P. rhoeas from the three regions studied is rich in polyphenols, flavonoids, and anthocyanins, which may be involved in the antioxidant and antimicrobial properties studied in this work. The results showed distinct differences in phenolics content and biological activities between the whole plant of P. rhoeas from the three regions studied. In short, the information presented here could serve as a valuable database for further research aimed at exploiting novel natural substances present in the whole plant of P. rhoeas to combat free radical damage and microbial infections. In this context, further studies are needed to determine the factors responsible for the difference in phenolics content and biological activities, as well as to identify the bioactive molecules of P. rhoeas responsible for the antimicrobial and antioxidant activities.

Author Contributions

Conceptualization, A.H., M.K. and A.L.; Data curation, O.A.K.; Formal analysis, O.A.K.; Investigation, A.H., M.K. and M.E.K.; Methodology, A.H., M.K., S.T. and N.E.; Software, A.H., M.K. and A.S.; Supervision, N.E. and A.L.; Visualization, A.A. and A.B.; Writing—original draft, A.H. and A.L.; Writing—review and editing, A.H., M.K., A.S. and F.E.O. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2023R141), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors extend their appreciation to Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2023R141), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 13 02695 g001 550
Figure 1. Polyphenol content in the P1E, PE2, and PE3; GAE: gallic acid equivalents; a and b—values with a significant difference (p < 0.05).
Figure 1. Polyphenol content in the P1E, PE2, and PE3; GAE: gallic acid equivalents; a and b—values with a significant difference (p < 0.05).
Applsci 13 02695 g001
Applsci 13 02695 g002 550
Figure 2. Flavonoid content in PE1, PE2, and PE3; QE: quercetin equivalents; a: the difference between the three samples was not significant (p > 0.05).
Figure 2. Flavonoid content in PE1, PE2, and PE3; QE: quercetin equivalents; a: the difference between the three samples was not significant (p > 0.05).
Applsci 13 02695 g002
Applsci 13 02695 g003 550
Figure 3. Anthocyanin content in the P. rhoeas extracts; CGE: cyanidin-3-glucoside chloride equivalents; a: the difference between the three samples was not significant (p > 0.05).
Figure 3. Anthocyanin content in the P. rhoeas extracts; CGE: cyanidin-3-glucoside chloride equivalents; a: the difference between the three samples was not significant (p > 0.05).
Applsci 13 02695 g003
Applsci 13 02695 g004 550
Figure 4. The IC50 values of P. rhoeas extracts, Butylated hydroxytoluene (BHT), ascorbic acid, and quercetin; a, b, c, d and e—values with a significant difference (p < 0.05).
Figure 4. The IC50 values of P. rhoeas extracts, Butylated hydroxytoluene (BHT), ascorbic acid, and quercetin; a, b, c, d and e—values with a significant difference (p < 0.05).
Applsci 13 02695 g004
Applsci 13 02695 g005 550
Figure 5. TAC values of PE1, PE2, and PE3; AAE: ascorbic acid equivalents; a: the difference between the three samples was not significant (p > 0.05).
Figure 5. TAC values of PE1, PE2, and PE3; AAE: ascorbic acid equivalents; a: the difference between the three samples was not significant (p > 0.05).
Applsci 13 02695 g005
Applsci 13 02695 g006 550
Figure 6. Biplot overlays the score plot and the loading plot. MIC: minimal inhibitory concentration; TPC: total polyphenol content; TFC: total flavonoid content; TA: total anthocyanin content; TAC: total antioxidant activity; E.c ATCC: E. coli ATCC 25922; E.c CIP: E. coli CIP 53126; Kp: K. pneumoniae; Sa: S. aureus; Ca: C. albicans.
Figure 6. Biplot overlays the score plot and the loading plot. MIC: minimal inhibitory concentration; TPC: total polyphenol content; TFC: total flavonoid content; TA: total anthocyanin content; TAC: total antioxidant activity; E.c ATCC: E. coli ATCC 25922; E.c CIP: E. coli CIP 53126; Kp: K. pneumoniae; Sa: S. aureus; Ca: C. albicans.
Applsci 13 02695 g006
Table
Table 1. Diameter of inhibition zones of P1E, P2E, P3E, tetracycline, streptomycin, and fluconazole in millimeters.
Table 1. Diameter of inhibition zones of P1E, P2E, P3E, tetracycline, streptomycin, and fluconazole in millimeters.
SampleGram − BacteriaGram + BacteriaYeast
Escherichia coli
ATCC		Escherichia coli
CIP		Klebsiella
pneumoniae		Staphylococcus aureusCandida albicans
P1E12.66 ± 0.57 b15.00 ± 1.00 b13.33 ± 1.52 ab13.66 ± 0.57 bR
P2E13.00 ± 0.00 b12.33 ± 0.57 c10.66 ± 1.15 b14.00 ± 1.00 b10.00 ± 2.00 b
P3E13.00 ± 0.00 b11.66 ± 0.57 cR12.33 ± 0.57 bR
Tetracycline19.00 ± 1.00 a18.10 ± 0.70 a14.90 ± 0.60 a16.70 ± 0.90 a—
StreptomycinRRR09.61 ± 0.200 c—
Fluconazole————21.20 ± 04.20 a
R—resistant; “—“—antibiotic is not compatible with this strain; a, b, and c—DIZ values of extracts with a significant difference against the same strain (p < 0.05).
Table
Table 2. Minimal inhibitory concentration of P. rhoeas extracts and antibiotics in mg/mL.
Table 2. Minimal inhibitory concentration of P. rhoeas extracts and antibiotics in mg/mL.
SampleGram − BacteriaGram + BacteriaYeast
Escherichia coli
ATCC		Escherichia coli
CIP		Klebsiella
pneumoniae		Staphylococcus
aureus		Candida
albicans
P1E2525252550
P2E5050252525
P3E0.780.78ND50ND
Streptomycin0.250.500.0030.062—
Tetracycline0.250.250.0620.003—
Fluconazole————0.40
ND—none detected; R—resistant; “—“—antibiotic does not match this strain.
Table
Table 3. Correlation between studied parameters of P. rhoeas extracts.
Table 3. Correlation between studied parameters of P. rhoeas extracts.
YieldTPCTFCTAIC50TACMIC E. coli ATCCMIC
E. coli CIP		MIC
K. pneumoniae		MIC
S. aureus
TPC0.315
TFC0.1430.984
TA0.4870.9830.934
IC50−0.723−0.884−0.787−0.955
TAC0.2030.9930.9980.954−0.824
MIC E. coli ATCC−0.539−0.969−0.911−0.9980.972−0.934
MIC E. coli CIP−0.532−0.971−0.914−0.9990.970−0.9371.000
MIC K. pneumoniae0.0370.9600.9940.891−0.7170.986−0.861−0.866
MIC S. aureus0.0370.9600.9940.891−0.7170.986−0.861−0.8661.000
MIC C. albicans0.8840.7230.5890.839−0.9620.638−0.871−0.8660.5000.500
MIC: minimal inhibitory concentration; TPC: total polyphenol content; TFC: total flavonoid content; TA: total anthocyanin content; TAC: total antioxidant activity.
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Hmamou, A.; Kara, M.; Khomsi, M.E.; Saleh, A.; Al Kamaly, O.; Bendaoud, A.; El Ouadrhiri, F.; Adachi, A.; Tlemcani, S.; Eloutassi, N.; et al. Comparative Study on the Total Phenolics, Total Flavonoids, and Biological Activities of Papaver rhoeas L. Extracts from Different Geographical Regions of Morocco. Appl. Sci. 2023, 13, 2695. https://doi.org/10.3390/app13042695

AMA Style

Hmamou A, Kara M, Khomsi ME, Saleh A, Al Kamaly O, Bendaoud A, El Ouadrhiri F, Adachi A, Tlemcani S, Eloutassi N, et al. Comparative Study on the Total Phenolics, Total Flavonoids, and Biological Activities of Papaver rhoeas L. Extracts from Different Geographical Regions of Morocco. Applied Sciences. 2023; 13(4):2695. https://doi.org/10.3390/app13042695

Chicago/Turabian Style

Hmamou, Anouar, Mohammed Kara, Mostafa El Khomsi, Asmaa Saleh, Omkulthom Al Kamaly, Ahmed Bendaoud, Faiçal El Ouadrhiri, Abderrazzak Adachi, Sara Tlemcani, Noureddine Eloutassi, and et al. 2023. "Comparative Study on the Total Phenolics, Total Flavonoids, and Biological Activities of Papaver rhoeas L. Extracts from Different Geographical Regions of Morocco" Applied Sciences 13, no. 4: 2695. https://doi.org/10.3390/app13042695

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