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BY 4.0 license Open Access Published by De Gruyter Open Access May 23, 2023

Black mulberry (Morus nigra L.) fruits: As a medicinal plant rich in human health-promoting compounds

  • Ebru Sakar , Sezai Ercisli , Romina Alina Marc , Hatice Gulen , Amine Assouguem EMAIL logo , Riaz Ullah , Abdelaaty A. Shahat , Ahmed Bari and Abdellah Farah
From the journal Open Chemistry

Abstract

Morus nigra, black mulberry, is the most attractive among mulberry species. The study aimed to determine human health-promoting content and antifungal activity in fruits of seven black mulberry genotypes grown in the Tortum district of Turkey. The genotypes exhibited significant differences in most of the human health-promoting content. Among individual sugars and organic acids, glucose (6.98–8.03 g/100 g fresh weight base) and malic acid (6.33–10.45 g/100 g fresh weight base) were predominant. The ascorbic acid content of genotypes was found between 18.13 and 26.77 mg/100 g fresh weight base, indicating that black mulberry fruits had moderate ascorbic acid content. Total phenolic content, total antioxidant capacity, and total anthocyanin contents in fruit extracts of seven black mulberry genotypes were also investigated. The results showed that the levels of the aforementioned parameters changed depending on genotypes. The total phenolic and total anthocyanin contents were in the range of 1,656–2,348 μg gallic acid equivalent (GAE)/g and 623–804 μg C3GE (cyanidin-3-glucoside equivalent)/g, respectively. The genotypes had antioxidant capacity between 17.41 and 3.86 μg/mL and between 10.08 and 14.11 μmol TE/g measured by the 2,2-diphenyl-1-picrylhydrazyl and ferric reducing antioxidant power assay, respectively. Some of the genotypes (TOR-1 and TOR-2) had high antifungal activity particularly against C. albicans. It was determined that the people living in the region traditionally use mulberries as blood enhancer, immune system booster, and mouth lesion treatments to protect themselves against different types of cancers and against inflammation. The present results confirm that attractive fruits of black mulberry are a rich natural source of phenolic antioxidants and can contribute to the dietary intake of antioxidants, depending on genotypes.

1 Introduction

The genus Morus is extensively distributed around the world, and it is estimated that almost 90 species have been identified under different climatic conditions. The most common fruit-producing species are Morus alba, Morus nigra, and Morus rubra [1,2,3].

The origin of the mulberry plant is Asia and widely distributed between latitudes 50° north and 10° south of southeast Asia and Japan, some parts of Indonesia, the islands of Java and Sumatra, North African countries, the temperate zone and humid regions of the southeast Caucasus, Iran, and Western Asia. It is also found in North-South America. Mulberry can grow naturally in places with 600–2,500 mm of annual precipitation. Rather than the total precipitation, the distribution of precipitation throughout the year, particularly in the vegetation period, is important. About 65–80% air relative humidity is an ideal environment for the growth of mulberries. Mulberry trees can be found up to 1,500 m of altitude. Even though it can reach an altitude of 1,735 m in Japan, the ideal altitude is accepted as 700 m [2,3].

Mulberry trees have high adaptive capacity and grow in different climatic and soil conditions worldwide. Anatolia is the homeland of mulberry trees and one of the oldest cultivation areas of this unique fruit. In most agricultural regions of Turkey, mulberries grow well, and high-quality mulberry fruit is obtained [4,5,6].

M. nigra, black mulberry, has the most attractive fruits among mulberry species. M. nigra has very attractive big dark red fruits with a slightly sour-sweet unique taste. The fruits have traditionally been used as medicine in Türkiye for centuries to treat various ailments due to their higher biological activities [5,7,8]. In Türkiye, 2,500,000 fruit-bearing mulberry trees produce 70,000 tons of fruits per year. Turkey’s Mideast, Northeast, Midnorth, and Black Sea regions share 70% of the total production (equally 17.5% each) [9].

Black mulberry trees are grown in agricultural regions of Turkey in different climates and soil characteristics. Considering the regions, the Aegean and Mediterranean regions are in first place in terms of black mulberry existence, and there are black mulberry trees in the other agricultural regions as well. Each agricultural region in the country has numerous unnamed black mulberry trees.

Among different mulberry species grown in main mulberry producer countries including Türkiye, black mulberry (M. nigra) is the most distinct species due to its attractive colourful fruits, and these fruits are very rich for human health-promoting components [10,11,12,13,14,15]. In addition to vitamins A, B, C, E, and K, ascorbic acid, riboflavin, niacin, and thiamine, useful minerals such as sodium and potassium are abundant in black mulberry fruits. Since all these beneficial substances are found in considerable amounts, black mulberry fruits can provide many benefits to human body. It is one of the biggest and most natural aids in dealing with bad cholesterol, especially thanks to potassium it contains [16]. The fruit is also a rich source of carbohydrates, proteins, lipids, and their precursors [17,18,19,20,21,22].

In Türkiye, black mulberry fruits are accepted as medicinal food and have been consumed for centuries and traditionally used to treat several ailments including antipyretic, diuretic, and blood sugar regulator. It is especially useful for tonsillitis and used in the treatment of mouth and tooth wound. It is also used especially in the healing of infections caused by Candida microorganisms known as thrush in children [6,23,24,25].

Previous studies showed that mulberries, in particular M. nigra, have high therapeutic potentials including improving vision, acting as a hepatoprotective immune stimulator, and showing anti-microbial, anti-cancer, and anti-stress activity [6,12,26,27,28]. Black mulberry fruits were traditionally used for a mouth lesion treatment in Anatolia for centuries [24]. The fruits also have atherosclerosis, neuroprotective functions, and anti-obesity action [22,29,30,31,32,33,34,35]. Black mulberry fruits are a good source of polyphenolics including a diverse group of phenolic acids, flavonoids, etc. [13,26,34,36,37,38,39,40,41].

Hundreds of years old black mulberry trees exist in Türkiye that have adapted to the climatic and soil conditions of different agroclimatic regions. The long culture period has led to the emergence of genotypes with different fruit characteristics due to natural mutations. In addition, the emergence of new promising genotypes from seeds and their establishment by farmer selection have also increased diversity.

The fruit characteristics of different genotypes are quite variable [2,40]. In Türkiye, black mulberry is consumed fresh and processed into black mulberry juices, black mulberry jam, black mulberry marmalade, black mulberry yogurt, black mulberry wine, black mulberry galette, and fresh fruit cakes [4,8].

Genotypes are a main factor affecting the sensory, nutraceutical, and nutritional qualities of black mulberry fruits [7,10,40]. In Türkiye, black mulberries are harvested from different unnamed genotypes at dark red stages when their flavour is most desirable. Therefore, the effect of genotypes on antioxidant and quality is a major issue. Most of the current literature focuses on antioxidant and photochemical properties of mature dark red a single black mulberry genotype. The aim of this study was to search the effects of genotypes on the sensory, nutraceutical, and nutritional qualities of black mulberries naturally grown in the Tortum district of Erzurum province of Turkey.

2 Materials and methods

2.1 Plant material and research area

Tortum district belongs to Erzurum province and has very old black mulberry cultivation. Black mulberry trees exist in the form of a single tree in the field of region. In the present study, a total of seven black mulberry (M. nigra) genotypes (TOR-1 to TOR-7) were used (Table 1). Around 1 kg of fruits was sampled from seven black mulberry genotypes in mid-July 2021 under the same climatic condition.

Table 1

Characteristics of seven M. nigra genotypes

Genotypes Location Altitude (m) Estimated tree age (year) Fruit mass (g) Fruit shape index Traditional medicinal use
TOR-1 Serdarlı 1,418 85 5.12 ± 0.20ab 0.84 ± 0.09a
  1. Blood enhancer

  2. Immune system booster

  3. Mouth lesion treatments

  4. To protect against different types of cancers

  5. Against inflammation

TOR-2 Serdarlı 1,430 80 5.04 ± 0.22b 0.75 ± 0.06ab
TOR-3 Bağbaşı 1,235 85 5.22 ± 0.24a 0.78 ± 0.07ab
TOR-4 Bağbaşı 1,220 90 4.70 ± 0.18 cd 0.82 ± 0.09ab
TOR-5 Bağbaşı 1,267 70 4.88 ± 0.20c 0.72 ± 0.04ab
TOR-6 Bağbaşı 1,245 105 5.10 ± 0.19ab 0.70 ± 0.08b
TOR-7 Bağbaşı 1,240 90 5.15 ± 0.20ab 0.79 ± 0.05ab

In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05.

Fresh black mulberry fruits (thawed form after deep freezing −80°C) were processed using a food blender (Heidolph Crusher M, Germany). For each analysis, four replicates were used.

Through a conversation with tree’s owner, tree ages were estimated. Using 30 fruits with four replications, the fruit mass was calculated using an electronic balance (Mettler Toledo ME-T, Switzerland). The fruit shape index was obtained by fruit width/length. The use of traditional medicine was determined by a questionnaire.

2.2 Individual sugar analysis

Melgarejo et al. [42] performed an individual sugar analysis. To carry out this experiment, 5 g of fruit samples were homogenized in distilled water and centrifuged at 6,000 rpm for 5 min. The resulting supernatants were filtered, and individual sugars were determined by the PerkinElmer HPLC system. The results are expressed as g/100 g fresh weight (FW). The Roussos et al. [43] method was used to determine the sweetness index (SI). It is given in the following equation:

(1) SI = 1.00 × Glucose + 2.3 × Fructose + 1.35 × Saccharose .

2.3 Organic acid analysis

The Bevilacqua and Califano [44] method was used to determine organic acid in black mulberry fruits. For analysis, approximately 10 g of fruit samples were homogeneously dissolved in 10 mL of 0.009 N H2SO4. The thawed fruit samples were centrifuged at 14,000 rpm for 15 min. The supernatants were then filtered, and organic acids were detected using high-performance liquid chromatography (Agilent 1100 series HPLC G 1322A, Germany). Organic acid results are expressed as g/100 g FW.

2.4 Ascorbic acid (vitamin C), total phenolic, and total anthocyanin

Ascorbic acid (vitamin C) in black mulberry fruits was determined by titrating 5 g of fruit with 2,6-dichlorophenolindophenol sodium salt.

The total phenolic content of fruits was determined using a spectrophotometer (Shimadzu, Japan) by using the Folin–Ciocalteu method [45,46]. Results are expressed as μg gallic acid equivalent (GAE)/g FW.

The bisulphite bleaching method [26] was used for the total anthocyanin content of fruits. Anthocyanins were extracted from 2 g of fruits with 0.1% hydrochloric acid (HCl, 2 mL) in 96% ethanol and 2% HCl (40 mL). The mixture was centrifuged at 5,500 rpm for 10 min. Results were expressed as μg of C3GE/g of FW.

2.5 Determination of antioxidant activity

Benzie and Strain [47] conducted the ferric reducing antioxidant power (FRAP) assay. Homogenized fruits (5 g) were extracted with methanol, and after filtration (using filtration paper), they were used for the FRAP test. Results are expressed as Trolox equivalents, μmol TE/g FW, against standard Trolox (TE, 6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid).

Brand-Williams et al. [48] conducted a 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay. Homogenized fruits (5 g) were extracted with methanol. The results were then expressed as μg/mL.

2.6 Determination of antifungal activity

Methanol extracts were obtained after the black mulberry fruits were ground into powder. It was weighed and extracted in 200 cc methanol in reflux for 5 h. The extracts were filtered and lyophilized by evaporating methanol at 40°C under pressure in the evaporator. In the study, the anticandidal activity of the extracts was determined using the disc diffusion method. A concentration of 30 mg/mL was prepared by dissolving with methanol, and the solvents were removed by absorbing on sterile paper discs of 6 mm diameter. Sabouraud dextrose agar cultures for the strains of Candida species used in the study. Suspensions equivalent to McFarland 0.5 turbidity were prepared. After 24 and 48 h of incubation, it was checked whether the inhibition zone diameter was formed, and the formed zone diameters were measured and recorded as a positive control. Commercial discs containing amphotericin B were used as negative controls. Minimum inhibition concentration (MIC) was used in the study. MIC values were determined by the microdilution method [23].

2.7 Statistical analysis

SPSS statistical program was used in the analysis. The least significant difference at p ≤ 0.05 was used to analyse the variance tables.

3 Results and discussion

3.1 Characteristics of seven M. nigra genotypes

The location, altitude, estimated tree age, fruit mass, fruit shape index, and traditional medicinal use are shown in Table 1. The genotypes are found between 1,220 and 1,430 m altitude. Estimated tree ages were in the range of between 80 and 105, indicating old cultivation of black mulberries in the region. Significant differences (p ≤ 0.05) were found among genotypes on fruit mass and fruit shape index, which were between 4.70 and 5.22 g and between 0.70 and 0.84, respectively (Table 1). The people living in the region traditionally use mulberries as blood enhancer, immune system booster, against inflammation, mouth lesions treatments, and to protect themselves against different types of cancers.

Due to some plant characteristics, black mulberries are not widely found in the region as commercial orchards. Propagation difficulties, slow growth nature, and harvest difficulties are critical problems to establishing commercial orchards. Gurcan [8] investigated monument black mulberry trees in different parts of Türkiye and found that most of the trees are over 100 years old. The author also found that black mulberry fruits are used for mouth lesion treatments in different regions of Türkiye. Koyuncu et al. [15] reported fruit mass between 3.74 and 5.67 g and fruit shape index between 0.65 and 0.73 among a large number of black mulberry genotypes sampled from lake region in Türkiye. Erkaleli and Dalkilic [49] reported fruit mass and fruit shape index of 2.87–4.30 g and 0.71–0.78, respectively. They also found 95 years old black mulberry trees in the Aegean region in Türkiye. Uzun and Bayir [50], in their study in the Antalya province of Türkiye, determined that the fruit weight of black mulberries was 2.5–5.4 g and the fruit shape index was between 0.65 and 0.77, respectively.

3.2 Sugars

The results of the analysis of individual sugars (glucose, fructose, and saccharose) are given in Table 2. Significant statistical differences among all three individual sugars (p ≤ 0.05) among the black mulberry genotypes were found. The individual sugar content was in descending order: glucose > fructose > saccharose (Table 2).

Table 2

Glucose, fructose, saccharose, and SI in fruits of M. nigra genotypes

Genotype Glucose (g/100 g FW) Fructose (g/100 g FW) Saccharose (g/100 g FW) SI
TOR-1 7.95 ± 0.3b 7.60 ± 0.3ab 1.95 ± 0.01ab 28.06 ± 1.3ab
TOR-2 8.03 ± 0.4a 7.76 ± 0.3a 2.04 ± 0.02a 28.63 ± 1.0a
TOR-3 7.11 ± 0.4f 6.89 ± 0.2cd 1.62 ± 0.01cd 25.15 ± 1.1de
TOR-4 6.98 ± 0.3g 6.72 ± 0.2d 1.54 ± 0.03d 24.52 ± 1.0e
TOR-5 7.84 ± 0.3c 7.48 ± 0.1b 1.90 ± 0.04b 27.61 ± 0.8b
TOR-6 7.67 ± 0.4d 7.23 ± 0.2bc 1.78 ± 0.02bc 26.70 ± 0.8c
TOR-7 7.35 ± 0.3e 7.04 ± 0.3c 1.70 ± 0.02c 25.84 ± 1.0d

In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05.

The highest glucose content was recorded in the TOR-2 genotype as 8.03 g/100 g, followed by TOR-1 genotype as 7.95 g/100 g, while the lowest glucose value was observed in the TOR-4 genotype as 6.98 g/100 g (Table 2). The fructose content of all genotypes was found a little bit lower than the glucose content of the genotypes and was in the range between 15.46 g/100 g (TOR-4) and 17.85 g/100 g (TOR-2) (Table 2). Overall, saccharose content was found to be the lowest value in fruits of black mulberry genotypes compared to glucose and fructose content. Saccharose content was between 2.19 g/100 g (TOR-3) and 2.75 g/100 g (TOR-2). For fruit flavour, glucose/fructose is very important. Yaman [51] used a number of black mulberry genotypes for sugar analysis of fruits and reported fructose and glucose between 5.80–10.53 g/100 g and 4.70–8.19 g/100 g fresh fruit base. Ozgen et al. [11] used 14 black mulberry genotypes in sugar analysis and found that glucose was the main sugar in black mulberry fruits and changed between 5.50 and 7.12 g/100 g, followed by fructose (4.86–6.41 g/100 g), which shows similarities with our present study.

Sugars in fruits are affected by many factors, including cultivars/genotypes, growing conditions, harvest period, cultural treatments, etc. [52,53,54]. In Syria, Makhoul et al. [55] used 11 black mulberry phenotypes and reported glucose and fructose content with an average 6.32 g/100 g and 4.91%, respectively.

However, Roussos et al. [43] reported lower values of glucose (1.83–5.85 g/100 g FW) and fructose content (1.88–6.25 g/100 g FW) among a number of black mulberries grown in Greece. Makhoul et al. [55] also determined the lowest levels of sugars were saccharose (0.03–1.47 g/100 g FW), and Roussos et al. [43] also found lower values of saccharose in black mulberries (0.03–0.16 g/100 g FW).

In the present study, SIs were calculated as between 24.52 and 28.63 among seven black mulberry genotypes. Higher SI values indicate higher levels of fructose analysed in black mulberry fruits. Roussos et al. [43] reported lower SI (between 6.86 and 22.31) in Greece than our results, probably due to the genotypic or environmental effects on fruit composition.

3.3 Organic acids

Depending on the species, cultivars, and genotypes, fruits contain different types and amounts of organic acids (0.1–35 g/kg). A high sugar-to-acid ratio in fruits indicates a sweet taste, and a low ratio indicates a sour taste. With the help of different acids in the composition of fruits, it can be determined whether the fruit juices are cheated or not. During storage, fruits made respiration. They can use organic acids during storage; therefore, a decrease in organic acid can be seen in stored fruits. The main organic acids in fruits are malic and citric acid [56].

Table 3 shows the organic acid distribution in fruits of seven black mulberry genotypes. Significant statistical differences are evident among genotypes for malic, citric, oxalic, and tartaric acid content (p ≤ 0.05). As indicated in Table 3, black mulberry fruits dominantly included malic acid. The genotypes exhibited malic acid content between 6.33 and 10.45 g/100 g FW. Malic acid followed by citric acid (2.55–4.10 g/100 g), oxalic acid (2.90–4.11 g/100 g), and tartaric acid (0.56–1.04 g/100 g). Li et al. [57] indicated that apple’s organic acid content is genotype and altitude dependent. They indicated that higher altitudes increase malic acid content in apple fruits. We also obtained higher malic acid content in higher altitude, which is in agreement with the above study. Previous studies also indicated that black mulberry fruits are rich in particularly malic acid and citric acid content. Can et al. [7] found that malic acid was dominant in black mulberry fruits and changed between 2.233 and 7.452 g/100 g FW. Okatan [58] also reported that malic acid was the major organic acid in black mulberry fruits (between 6.65 and 13.65 g/100 g FW). Ercisli and Orhan [4] found similar citric acid content in black mulberry fruits (2.12–7.02 g/100 g FW). Okatan [58] found oxalic and tartaric acid concentrations in black mulberry fruits between 0.45–1.25 g/100 g FW and 0.22–0.86 g/100 g FW, respectively. Compared to the aforementioned studies, we can say that our results are in agreement with them. Black mulberry fruits have distinct tastes (better balance of sweet and sour taste, namely perfect sugar/acid ratio) compared to white and red mulberries, and this could be regarded as one of their most significant sensory properties [11].

Table 3

Organic acid distribution in fruits of M. nigra genotypes

Genotype Malic acid (g/100 g FW) Citric acid (g/100 g FW) Oxalic acid (g/100 g FW) Tartaric acid (g/100 g FW)
TOR-1 9.87 ± 0.4b 4.10 ± 0.08a 3.75 ± 0.03ab 1.04 ± 0.02a
TOR-2 10.45 ± 0.2a 3.95 ± 0.12b 4.11 ± 0.04a 0.86 ± 0.01ab
TOR-3 7.74 ± 0.2d 4.02 ± 0.10ab 3.60 ± 0.03b 0.60 ± 0.02ab
TOR-4 8.56 ± 0.3c 3.45 ± 0.09d 3.25 ± 0.02bc 0.55 ± 0.02ab
TOR-5 6.33 ± 0.4f 2.55 ± 0.06f 2.90 ± 0.02c 0.48 ± 0.01b
TOR-6 7.68 ± 0.4e 3.02 ± 0.11e 2.98 ± 0.04bc 0.70 ± 0.01ab
TOR-7 8.20 ± 0.3d 3.77 ± 0.10c 3.47 ± 0.02bc 0.75 ± 0.02ab

In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05.

Previous studies showed that fruit acids are an important component of human health. Among organic acids, malic acid is found dominantly in most of the fruits that have health-promoting factor in humans [59,60].

3.4 Ascorbic acid (vitamin C), total phenolic, total anthocyanin and antioxidant activity

As can be seen from Figures 15, the fruits of black mulberry genotypes contain a significant amount of vitamin C, total phenolics, ascorbic acid, and finally, those produce high antioxidant activity as determined by DPPH and FRAP assays. In addition, results indicated statistically significant differences among genotypes for vitamin C, total phenolics, ascorbic acid, and antioxidant activity (p < 0.05).

Figure 1 
                  Ascorbic acid content of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).
Figure 1

Ascorbic acid content of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).

Figure 2 
                  Total phenolic content of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).
Figure 2

Total phenolic content of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).

Figure 3 
                  Total anthocyanin content of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).
Figure 3

Total anthocyanin content of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).

Figure 4 
                  DPPH values of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).
Figure 4

DPPH values of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).

Figure 5 
                  FRAP values of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).
Figure 5

FRAP values of genotypes. (In the same column, statistically significant differences among genotypes are presented by different letters at p ≤ 0.05).

Ascorbic acid is an important component of berry fruits, in particular, black mulberries [11]. Among seven mulberry genotypes, TOR-1 and TOR-2 showed the highest ascorbic acid values with 27.6 and 26.2 mg/100 g of fresh weight base. The TOR-5 genotype had the lowest value overall at 20.4 g/100 g FW. TOR-3, TOR-6, and TOR-7 were grouped together statistically with 21.8, 22.8, and 22.0 mg/100 g FW ascorbic acid content (Figure 1).

Mulberries are widely studied species for their ascorbic acid content. Previous studies indicated that variable vitamin C content indicates genotype dependence. For example, Makhoul et al. [55] used a large number of black mulberry fruits belonging to diverse genotypes and reported a great variation ranging from 3 to 42 mg/100 g FW. They also indicated that the average Vitamin C content of black mulberries was 21.27 mg/100 g, which indicates similarities with our present findings. In Türkiye, several researchers from different agroclimatic regions also reported variable vitamin C content among black mulberries. Okatan et al. [61] used a number of black mulberry samples from the western part of Türkiye and found vitamin C levels between 18.40 and 23.67 mg/100 g FW also indicating high similarity with our findings. However, Eyduran et al. [3] and Erkaleli and Dalkilic [49] reported lower vitamin C content among black mulberries between 10.12 and 16.29 mg/100 g from the eastern part of Türkiye and between 15.37 and 16.70 mg/100 mL among 15 black mulberry genotypes in the Aegean region of Türkiye, respectively. Ascorbic acid is, in particular, abundant in horticultural plant cells and well known for its numerous biological functions. It is one of the important components of antioxidants in plants. Ascorbic acid has a protective effect on plants from both internal (respiration, photosynthesis) and external factors (environmental pollution). As a biochemical parameter, it is widely affected by cultivars/genotypes, altitude, growth conditions, such as light and heat [61,62,63].

Total phenolics differ in accordance with the genotypes (p < 0.05) (Figure 2). Total phenolic content was the lowest in genotype TOR-5 (1,656 μg GAE/g FW), whereas it was the highest in TOR-1 genotype (2,348 μg GAE/g FW) (Figure 2). In the present study, total phenolic content was also the highest in higher altitude (Figure 2). Martinez et al. [64] found that total phenolic content was the highest at higher altitude in chestnut fruits in Spain. Erkaleli and Dalkilic [49] used 14 diverse black mulberry genotypes in total phenolic content analysis and reported 1,320–1,470 μg GAE/g FW. Yaman [51] conducted total phenolic content analysis on six black mulberry genotypes in Türkiye and found total phenolic content between 958 and 3,573 mg/kg GAEs. Okatan [58] also reported 1,874–2,977 μg GAE/g FW total phenolic content among 13 black mulberry genotypes sampled from the Aegean region in Türkiye. Okatan et al. [61] also reported total phenolic content between 1,920 and 2,575 μg GAE/g FW among eight black mulberry genotypes in Türkiye. Ozgen et al. [11] found out that 14 black mulberry genotypes had average 2,737 μg GAE/g FW. Kostic et al. [17] found total phenol content between 902 and 1,188 μg GAE/g FW in Serbia. Our results are comparable with the above results from different parts of Türkiye and abroad. It is well reported in the literature that total phenolics accumulated in plants as a response to stress conditions, including drought, extreme temperatures, pollution, etc. [65].

Total anthocyanin content significantly varied among genotypes and was found between 623 μg C3GE/g FW and 804 μg C3GE/g FW (Figure 3).

TOR-2 genotype, specifically, had the highest total anthocyanin content, followed by TOR-1 and TOR-7 (771 and 745 μg C3GE/g FW, respectively), TOR-4 genotype (735 μg C3GE/g FW), and TOR-5 (720 μg C3GE/g FW), respectively. TOR-3 (686 μg C3GE/g FW) and TOR-6 (623 μg C3GE/g FW) genotypes were to found to have the lowest values. Yaman [51] reported between 177 and 2,221 mg/kg FW total anthocyanin contents between six genotypes. Ozgen et al. [11] and Okatan et al. [61] reported total anthocyanin in black mulberry fruits to range from 253 to 830 μg C3GE/g FW. Kostic et al. [17] reported higher total anthocyanin content ranging from 1,148 to 1,286 μg of C3GE/g FW. Colourful berry fruits are very rich in anthocyanins. Black mulberry is one of the richest sources in this regard. Anthocyanins are one of the most important contributors to the antioxidant properties of fruits. Black mulberry draws attention with its rich anthocyanin content [66]. Kim and Lee [67] obtained similar results in their study. On the other hand, the anthocyanin content of the black mulberry varies depending on cultivar/genotype, but environmental conditions, harvest time, etc., affect this property.

Berries are rich source of natural antioxidants. There are different methods used to determine the antioxidant activities. In this study, the antioxidant capacity of the different black mulberry genotypes was determined using two methods, namely DPPH and FRAP assays. DPPH and FRAP methods are simple and rapid. Figures 4 and 5 show the antioxidant capacity values of black mulberry fruits using the DPPH and FRAP methods. Genotypes varied statistically from one another in both antioxidant measurement methods (p < 0.05). In the literature, black mulberry fruits have been shown to have more antioxidant capacity than the other mulberry species [24]. DPPH and FRAP assays exhibited variation in the antioxidant capacity of fruits among black mulberry genotypes. The DPPH values in fruits of black mulberry genotypes under study varied from 17.41 (TOR-2) to 23.86 μg/mL (TOR-5), indicating that TOR-2 had the highest antioxidant capacity (Figure 4). In the FRAP assay, total antioxidant activity ranged from 10.08 (TOR-6) to 14.11 μmol TE/g FW (TOR-2) (Figure 5).

The same genotypes showed high antioxidant capacities in both DPPH and FRAP assays. Among genotypes, TOR-2 showed the highest values in both assays. Overall, TOR-5 had the lowest antioxidant capacity at 23.86 μg/mL FW (Figure 4).

The antioxidant activity of several black mulberry genotypes has previously been assessed using several methods. Yaman [51] found a significant variation among six black mulberry genotypes using the DPPH antioxidant measurement method. Okatan [58] used 13 black mulberry genotypes from the western Turkey and reported DPPH values between 16.87 and 26.80 μg/mL.

Okatan et al. [61] conducted a study on the antioxidant activity of black mulberry genotypes in Türkiye and presented DPPH values ranging from 18.24 to 23.18 μg/mL. Our finding confirmed the antioxidants activities by FRAP assay of Seven black mulberry genotypes from 10.08 to 14.11 μmol TE/g FW. Previously kiwi, lemon, apple, and plum fruits (2.9 μmol TE/g) and orange fruits (11.4 μmol TE/g) showed lower FRAP values. Many factors, such as species, cultivars, altitude, soil, harvest period, etc., affect the antioxidant capacity of horticultural crops [63,64].

3.5 Antifungal activity

Table 4 shows the antifungal activity of black mulberry genotypes. In addition to antioxidant properties, fruits also have antimicrobial properties against fungi, bacteria, and viruses that may be easily detected in laboratory conditions. Depending on the cultivars used, the type and load of the microorganisms, the composition of the food, and processing and storage conditions, antimicrobial activity of fruits varies among fruit species. The antimicrobial properties of phenolic substances are governed by proteins, lipids, salts, pH, and temperature.

Table 4

Antifungal properties of black mulberry genotypes

Genotype Candida species Methanol Inhibition zone (mm) MIC (mg/mL)
TOR-1 C. albicans 28 1.25
C. parapsilosis 22 2.50
C. tropicalis 20 1.25
TOR-2 C. albicans 29 1.25
C. parapsilosis 19 1.25
C. tropicalis 22 1.25
TOR-3 C. albicans 23 2.50
C. parapsilosis 19 2.50
C. tropicalis 23 2.50
TOR-4 C. albicans 25 2.50
C. parapsilosis 20 2.50
C. tropicalis 20 2.50
TOR-5 C. albicans 24 1.25
C. parapsilosis 21 2.50
C. tropicalis 22 2.50
TOR-6 C. albicans 22 2.50
C. parapsilosis 20 2.50
C. tropicalis 19 2.50
TOR-7 C. albicans 25 1.25
C. parapsilosis 19 2.50
C. tropicalis 24 2.50

All the genotypes of black mulberry fruits that were tested showed antifungal activity, especially against C. albicans. TOR-2 and TOR-1 genotypes were found to be the most active on fungus and completely inhibit the fungal growth. The rest of the five genotypes showed relatively less inhibition. The most active TO-2 and TO-1 genotypes were also found with the highest phenolic content. Thus, it could be correlated with antifungal activity. In fact, many fruit species and their cultivars/genotypes have been previously reported to have reached certain levels of human health components, and these components vary among cultivars/genotypes and also have high antimicrobial activity [68,69,70,71,72,73,74].

4 Conclusions

The present work indicated that the fruits of M. nigra have high antioxidant content and potent antimicrobial properties. These results also support its use in traditional medicine for centuries. Fruits of black mulberry genotypes are found to be very rich in human health-promoting compounds, including ascorbic acid, phenolic, and anthocyanin, and have a strong antioxidant activity. TOR-2 and TOR-1 genotypes exhibited higher amount of human health-promoting compounds. According to the results of the study, including black mulberry fruits to a balanced diet can create a protective shield for the human body against harmful free radicals. In addition, there is a very clear correlation between the high phenolic content of black mulberry fruits and their antifungal activity. Thus, developing countries should support the cultivation of these unique plants.

Acknowledgement

The authors extend their appreciation to researchers Supporting Project Number (RSP2023R110) at King Saud University Riyadh Saudi Arabia for financial support.

  1. Funding information: This research work was supported by researchers Supporting Project Number (RSP2023R110) at King Saud University Riyadh Saudi Arabia.

  2. Author contributions: Conceptualization, E.S.; S.E. and H.G.; formal analysis, S.E.; H.G. and E.S.; writing – original draft preparation, R.A.M.; A.A.; R.U. and A.B.; writing – review and editing, S.E.; H.G. and E.S.; supervision, E.S. and S.E. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: The data presented in this study are available on request from the authors.

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Received: 2023-03-05
Revised: 2023-05-01
Accepted: 2023-05-05
Published Online: 2023-05-23

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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