Food Applications of Berberis Plants

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This entry is adapted from the peer-reviewed paper 10.3390/foods8100522

The genus Berberis includes about 500 different species and commonly grown in Europe, the United States, South Asia, and some northern areas of Iran and Pakistan. Leaves and fruits can be prepared as food flavorings, juices, and teas. Phytochemical analysis of these species has reported alkaloids, tannins, phenolic compounds and oleanolic acid, among others. Moreover, p-cymene, limonene and ocimene as major compounds in essential oils were found by gas chromatography. Berberis is an important group of the plants having enormous potential in the food and pharmaceutical industry, since they possess several properties, including antioxidant, antimicrobial, anticancer activities.

Berberis food preservative alkaloid antioxidant human health

1. Introduction

Berberis species. are shrubs in the family Berberidaceae, native to central and southern Europe, western Asia, as well as northwest Africa ^[1]. About 500 species of these plants are found in most areas of central and southern Europe, the north-eastern region of United States, and Asia (including the northern area of Pakistan ^[2] and Iran ^[3]). The genus Berberis consists of spiny deciduous evergreen shrubs which are characterized by yellow wood and flowers ^[2], dimorphic long and short shoots (1–2 mm). Some Berberis fruits are small oblong berries 7–10 mm long and 3–5 mm broad and turn blue or red upon ripening during the late summer or autumn ^[1].

Berberis spp. are mainly consumed fresh, dried or used in juice production ^[4]. The fruits are very popular, known as zereshk in Iran where they are commonly used for cooking and in jam production, thus, encouraging the production of fresh edible seedless barberries fruits reaching about 22,000 tons per annum ^[5]. The fruits are also processed into beverages, drinks, syrups, candy and other confectionary products which are popular Iran. Furthermore, the leaves and fruits have also found applications in the production of food flavorings and teas. Berberis are popular due to their nutritional importance; however, they have found most usefulness in folk and traditional medicine where various parts, including roots, bark, leaves and fruits serve as major ingredients of herbal remedies in Ayurvedic, Iranian and Chinese medicine dating back at least 3000 years ^[6]. Currently, this species flower is popularly used amongst Tibetan speaking population in areas, such as Litang, China ^[7].

The effect of cold-pressed filtered oil of Berberis spp. seeds in delaying soybean oil oxidation in comparison to commercial antioxidants were carried out, and the study reported that Berberis oil contributed to oxidative stability of soybean oil comparably to commercial antioxidants ^[8]. Antioxidant and antibacterial activity of water extract of barberry has suggested their possible application as preservatives in food industries ^[9].

Isoquinoline alkaloids are the major bioactive constituents in Berberis ^[10]. Protoberberines and bisbenzyl-isoquinoline alkaloids, such as berbamine, tetrandrine and chondocurine, which have been known for their anti-inflammatory and immunosuppressive properties, have been detected by phytochemical analysis of the root and stem back extracts of B. vulgaris. Berberine (an isoquinoline alkaloid) and berbamine are the most abundant phytochemicals of Berberis species ^[2]. The fruits contain a high amount of alkaloids, tannins, phenolic compounds and oleanolic acid ^[3]^[11], gum, pectin, oleoresins, organic acids, anthocyanins and carotenoids. In addition, palmitine ^[10], stigmasterol and its glycoside ^[12] have all been detected in various species of the Berberis plant.

Some Berberis fruits have been employed in the treatment of guts ^[13] kidney stones ^[14] and liver ^[15] and gall bladder ^[10] conditions. The root bark and stem of the Berberis have found usage as a diuretic, febrifuge, cathartic and antiseptic. Furthermore, preparations of the stem and root bark have been used to treat mouth and stomach ulcers ^[16]. Several parts of the plant have been reported to possess astringent and antiseptic properties, while the stem bark and flowers were found to be anti-rheumatic ^[17]. The alkaloid rich root bark of the plant has also been used as purgative and treatment for both diarrhea and rheumatism ^[18]. The berberine-rich rhizomes of Berberis species possess marked antibacterial and antitumor properties, with reported efficacies in treatment of various eye conditions ^[10]^[19]. Furthermore, the anti-inflammatory activity of berberine has been extensively studied amongst other pharmacological actions ^[10]^[20].

Berberine sulphate which is an alkaloid extracted from the roots and bark of various Berberis spp. Have been reported to possess antibacterial, antifungal and antiprotozoal activities. Reported the bacteriostatic activity of berberine against streptococci, and that the sub-minimum inhibitory concentrations (MICs) of the compound blocked the adherence of streptococci to host cells, immobilized fibronectin, and hexadecane in epithelial cells ^[21]. Furthermore, blood glucose and lipid regulatory properties of Berberis have been demonstrated ^[3]^[22]^[23]^[24]; and this was due to berberine-induced improvement in insulin sensitivity through regulation of adipokine secretion ^[25]^[26]^[27]. Effectiveness of Berberis species in the maintenance of heart health has been demonstrated in their ability to improve hypertension, ischemic heart disease, cardiac arrhythmias and cardiomyopathy ^[2]^[28].

The health-promoting effect of Berberis spp. cannot be overemphasized, as well as its popularity; however, this is restricted to central and southern Europe, western Asia, as well as northwest Africa. Hence, efforts should be geared towards making the Berberis plant also available to other regions of the world. Furthermore, most studies on Berberis spp. have been on berberine; therefore, efforts should be made towards researching possible therapeutic benefits of all other important phytoconstituents of the plant. Furthermore, the synergistic or additive effect of these phytoconstituents should be studied so as to elucidate the complex molecular interaction amongst various phytochemicals leading to the observed therapeutic properties. In addition, the modulatory effect of the plant/plant materials on gene expression should be prioritized.

2. Berberis Plants Essential Oils and Phytochemical Composition

Essential oils (EO) are volatile, complex natural compounds, which formed in aromatic plants as secondary metabolites. They are used in pharmaceutical, agricultural, and food industries, as well as are associated with antibacterial, anti-inflammatory, antioxidant, and insecticidal potential ^[29]^[30]^[31].

The gas chromatography coupled to mass spectrometry (GC-MS) analysis of various parts of B. vulgaris revealed that benzaldehyde, benzyl alcohol, 1-hexanol and I-2-hexenal ^[32] were major compounds of the EOs from fruit, while p-cymene, limonene and ocimene were identified as major compounds of the EOs (Figure 1) from leaves and flowers ^[33].

Figure 1. Major compounds of the essential oils (EOs) of Berberis vulgaris leaves and flowers. (a) p-cymene; (b) limonene; (c) ocimene.

Turkish B. crataegina fruit berry has 22 volatile compounds which are aldehydes had the highest concentration (5382 μg/kg), followed by alcohols (2487 μg/kg) and lactone (2422 μg/kg).

Major volatile compounds of the B. crataegina fruit are γ-butyrolactone, 3-hexanal and 2,6-dimethylphenol. Moreover, the olfactometric analysis of dry B. crataegina resulted eight aroma active compounds ^[34].

EOs of the roots of B. integerrima were analyzed by using modified microwave-assisted hydrodistillation (MAHD). Chemical diversity of 10 and 18 compounds were obtained from MAHD, MAHD with modified anyl, and with modified phenyl magnetic nanoparticles, the yields of the EOs were 0.16, 0.61 and 0.71 w/w %, respectively. Hexadecanoic acid was identified as a major compound for MAHD and modified MAHD methods ^[35].

Moreover, the GC/MS study on hexane extracts of the B. aetnensis and B. libanotica roots was showed that B. aetnensis have twenty-six and B. libanotica have thirty-seven non-polar compounds. Stigmasterol (Figure 2) is the major compound of both species ^[36].

Figure 2. Stigmasterol.

On the other hand, alkaloids (Table 1) represent the main compounds in Berberis species, and many of them have been identified by different spectroscopic techniques previously mentioned. The most known are berberine, berbamine, palmitine, jatrorrhizine, and isotetrandrine. They are located mainly in the cortical tissues of the roots and stems and have important biological activities. In fact, in vitro and in vivo anti-proliferative and anti-metastatic effects on various types of cancers have been reported for different alkaloids. These compounds, such as vinblastine, have already used as anticancer drugs ^[3].

Table 1. Alkaloids from Berberis species.

Chemical structure	Name	Plant
	palmatine	B. vulgaris
	berberine	B. vulgaris
	oxyberberine	B. vulgaris
	isocoridine	B. vulgaris
	lambertine	B. vulgaris
	magniflorine	B. vulgaris
	oxycanthine	B. vulgaris
	berbamine	B. aristata
	(+)-N-methylcoclaurine	B. montana
	(−)-pronuciferine	B. montana
	(+)-9-hydroxynuciferine	B. montana
	(+)-orientine	B. montana
	2-norberbamunine	B. stoloniferais
	berbamunine	B. stoloniferais
	aromoline	B. stoloniferais
	isotetrandrine	B. stoloniferais
	jatrorrhizine	B. umbellate

3. Food Preservative Applications of Berberis Plants

Food preservation is the most vital issue in food industries to ensure food safety for a longer period. Basically, the process of food preservation depends on the growth inhibition of undesirable microorganisms. Use of chemical agents with antimicrobial activity is commonly used a traditional method for food preservation ^[37]. However, antimicrobial agents also gain momentum, due to their fewer side effects and compatibility with the human body. Further, synthetic antimicrobials and their toxicological safety as food additives needed to be ensured by regulatory authorities. Moreover, processed foods with natural preservatives have great demand and considered safer and beneficial for public health ^[38]. The naturally occurring compounds demonstrated antimicrobial activity in foods as natural ingredients and can be used as additives to other foods.

Berberis is an important plants having enormous potential in the food industry. However, only a few reports are available on the direct application of these plants in food products. For example, seed oil and fruit extracts of B. crataegina were supplementing into chitosan matrix for preparation of a chitosan-based edible film. The films produced have been analyzed for the physiochemical and biological activities. Results showed that chitosan-fruit extract film exhibited higher thermal stability, antimicrobial, antioxidant, and anti-quorum sensing activity as compared to other films. Furthermore, the addition of B. crataegina seed oil and fruit extract into the chitosan film create a mark reduction in the UV-vis transmittance but improve the tensile strength. Likewise, hydrophobicity of the chitosan-seed oil film was found to be higher than chitosan-control film, while chitosan-fruit extract film displayed slightly lower hydrophobicity than chitosan film. These results indicated that chitosan-fruit extract film of B. crataegina fruit extract could be used as an effective ingredient for the production of the edible film with increased physicochemical and biological properties ^[39].

A list of the antimicrobial potential of the Berberis species evaluated across the globe is provided which support the use of Berberis species in food preservation (Table 2).

Table 2. A list of the antimicrobial potential of the Berberis species evaluated across the globe is provided which support the use of Berberis species in food preservation.

S. No.	Species	Part	Country	Extract/Model/Compound	Tested Micro-Organism	Results	Reference
1	B. aristata	Stem and leaves	Nepal	Hexane, Ethyl acetate, Methanol	Staphylococcus aureus, Kleibsella pneumoniae, Salmonella typhimurium	Against S. aureus: methanol significant zone of inhibition (21 mm), ethyl acetate extracts moderate activity, hexane extract of stem slightly active.	^[40]
2	B. aristata, and B. ligulata	Bark stem Leaves	Nepal	Ethanol	Bacillus subtilis, Escherichia coli, Pseudomona aeruginosa, Salmonella. typhi, Salmonella dyjenteriae, Salmonella cholerae	Ethanol extract of B. aristata: largest zone of inhibition (21 mm) against B. subtilis and the smallest MBC value (90 mg/mL) for S. aureus. Gram positive bacteria more susceptible to the ethanol extract. B. aristata relatively broad-spectrum antibacterial activity.	^[41]
3	B. vulgaris	Stem	Iran	Ethanol	P. aeruginosa, Acinetobacter baumannii, E. coli and Salmonella enteritidis	MIC determination: stem extracts inhibit the growth of all the studied bacteria (3900 to 37,500 μg/mL) by synergistic effects with ciprofloxacin.	^[42]
4	B. asiatica	Leaves	Uttarakhand, India	Methanol	E. coli, Enterobacter aerogenes, Proteus vulgaris, P. aeruginosa, K. pneumoniae, B. subtilis, S. aureus	Methanol extracts of leaves: high inhibitory potential on S. aureus, K. pneumoniae, E. coli, B. subtilis and P. vulgaris in all concentration.	^[43]
5	B. aristata, B. asiatica, B. lycium	Stem	Bangalore, India	Methanol	Nocardia sp., S. aureus, S. pneumonia, P. aeruginosa, Streptococcus viridians, E. coli	Sensitivity to Nocardia sp., S. pneumonia and E. coli.	^[44]
6	B. glaucocarpa	Root wood	Pakistan	Ethanol	SMRSA, EMRSA, Mycobacterium marinum, E. coli, Trypanosoma brucei	Berberine (MIC = 12.5 and 25 μg/mL), berberine chloroform (MIC = 25 and 12.5 μg/mL) and syringaresinol (12.5 μg/mL): very active against SMRSA, M. marinum and T. brucei.	^[45]
7	B. vulgaris	Stem bark	Romania	Ethanol	Botrytis cinerea	B. vulgaris bark extract, berberine, and fluconazole significantly inhibited growth of B. cinerea.	^[46]
8	B. vulgaris			Ethanol	S. aureus, Staphylococcus epidermidis, K. pneumoniae, B. subtilis, E. coli, Aspergillus niger, Trichoderma, Alternaria solanai	20 mm zone of inhibition against E. coli. Good activity against B. Subtilis, moderate against Trichoderma, insignificant against other stains.	^[47]
9	B. vulgaris and its active constituent, berberine	Root	Egypt	Ethanolic extract	Candida albicans, E. coli	Berberis ethanolic extract and berberine standard can inhibit C. albicans and E. coli growth.	^[48]
10	B. vulgaris	Fruit	Pakistan	Distilled water	S. aureus, Proteus, S. typhi, Salmonella paratyphi A, Salmonella paratyphi B, K. pneumoniae, E. coli, P. aeruginosa	Antibacterial activity against all tested pathogens.	^[49]
11	B. thunbergii	Fruit	Hungary	Juice; water extract and -methanol extract	B. subtilis, Bacillus cereus var. mycoides, E. coli, Serratia marcescens	Juice, water extract and methanol extract showed activity against all bacteria.	^[50]
12	B. calliobotrys	Stems and branches	Pakistan	Methanol	B. subtilis, P. aeruginosa, S. aureus fungal strains namely C. albicans, Penicillium notatum	The methanol extract, ethyl acetate and n-butanol fractions: maximum zone of inhibition against all bacterial strains especially S. aureus and antifungal effects.	^[51]
13	B. lycium	Roots	Libya	Distilled water, ethanol, isopropanol and methanol	Pseudomonas sp., E. coli, Streptococcus sp., Staphylococcus sp.	Methanolic displayed maximum inhibitory zone (16 mm), isopropanol extract (13 mm) and ethanol extract (12 mm). The aqueous extract exhibited the least inhibitory zone (10 mm). The methanolic extract: maximum inhibitory zone (12 mm), Pseudomonas (11 mm) and Staphylococcus (10 mm).	^[52]
14	B. hispanica	Root Bark	Marocco	Ethanolic extract	Mycobactérium smegmatis, Mycobacterium aurum	The ethanolic extract from root bark displayed an important antimycobacterial activity. The inhibition zones for M. aurum A+ were significantly larger than those for M. smegmatis MC2.	^[53]
15	B. ruscifolia	-	Argentina	Acetone, chloroform-methanol (1:1) and methanol	E. coli, P. aeruginosa, Listeria monocytogenes, S. aureus	All extracts exhibited antibacterial activity with MIC varying from 16 to 2 mg/mL. The highest inhibition with acetonic and chloroform-methanolic extracts of species against S. aureus (MIC = 2 mg/mL). Methanolic extracts B. ruscifolia showed no antibacterial activity against all tested bacteria.	^[54]
16	B. aristata	Stem bark	India	Ethanol and aqueous extracts	Shigella flexneri, Shigella sonnei, Shigella dysenteriae, Shigella boydii	Extracts of B. aristata: antibacterial activity against four strains of Shigella (8 and 23 mm).	^[55]
17	B. aristata, B. asiatica, B. chitria and B. lycium	Root and stem	India	Ethanol	Micrococcus luteus, B. subtilis, B. cereus, Enterobacter aerogenus, E. coli, K. pneumoniae, Proteus mirabilis, P. aeruginosa, S. aureus, S. typhimurium, Streptococcus pneumonia, Fungal strains Aspergillus nidulans, C. albicans, Aspergillus terreus, Trichophyton rubrum, Cistus albidus, Aspergillus flavus, A. niger	B. lycium, B. aristata and B. asiatica root extract showed significant antifungal activity against A. terreus and A. flavus. B. aristata root and B. lycium (stem) extracts gave very low MIC values (0.31 μg/mL) as compared to other tested species.	^[56]
18	B. Lycium	Root	Pakistan	Ethanol, petroleum ether	S. aureus, S. epidermidis, B. subtilis, S. typhi, E. coli, C. albicans	The ethanolic and aqueous crud root extract: most effective antifungal and antibacterial agents.	^[57]
19	B. integerrima Syn: B. densiflora	Roots	Iran	Methanol	Brucella abortus	MIC and MBC results, jatrorhizine exhibited higher antibacterial activity with MIC (0.78 μg/mL) and MBC (1.56 μg/mL) compared with the standard (streptomycin, 10 μg/mL).	^[58]
20	B. lycium	Roots	Pakistan	Hydric extract	E. coli, Pseudomonas, Staphylococcus, Proteus	Significant activity against E. coli and Proteus (80 to 100%), while it demonstrated a good activity against Pseudomonas and Staphylococcus (60 to 70%).	^[59]
21	B. aristata	Bark and leaves	India	Methanol, ethanol and hexane	B. subtilis, Agrobacterium tumefaciens, E. coli, Xanthomonas. Phaseoli, Erwinia chrysanthemi	All the extracts of tested plants showed variable activity against all the tested bacterial strains. Methanol extract revealed highest antibacterial activity (11 mm) recorded against E. chrysanthemi. Hexane extract: totally inactive against all the tested strains.	^[60]
22	B. aristata	Roots	India	Aqueous and alcohol extracts	S. aureus, B. subtilis, E. coli, S. typhimurium	Alcoholic and aqueous extract showed antimicrobial activity against four tested bacteria. B. aristata exhibited highest zone of inhibition for B. subtilis followed by S. aureus, E. coli and S. typhimurium.	^[61]
23	B. microphylla	Leaves, stems and roots	Chile	Methanol	E. coli, S. typhimurium, L. monocytogenes, E. aerogenes, S. aureus, B. cereus, S. epidermidis and B. subtilis	All extract possesses significant antibacterial activity against Gram-positive bacteria but not against Gram-negative bacteria.	^[62]
24	B. lycium	Root bark	Pakistan		E. coli, K. pneumoniae, P. aeruginosa, S. aureus, B. subtilis	Silver nanoparticles were very active against Gram-negative and Gram-positive bacteria Aqueous bark extract (10 μg/mL) possess highest activity against E. coli and P. aeruginosa.	^[63]
25	B. vulgaris	Fruit	Iran		L. monocytogenes	Average diagonal of growing area in disk diffusion test for species: 12 mm and MIC was 125 μg/mL and MBC of B. vulgaris was 500 μg/mL.	^[64]
26	B. aristata	Stem bark	Alcohol	In vivo in an animal model using Sprague Dawley rats	Carbapenem-resistant E. coli	An aquo-alcoholic extract of the species: effectively manage peritonitis induced by Carbapenem-resistant E. coli in a rat model at a single post-exposure prophylactic dose of 0.5 mg/kg body weight.	^[65]
27	B. aristata	Roots	India	Aqueous and alcoholic extract of fresh roots, as well as aqueous extract of dried roots	S. aureus, S. epidermidis, Streptococcus pyogenes, Streptococcus viridans, Enterococcus faecalis, B. subtilis, B. cereus, E. coli, K. pneumoniae, P. aeruginosa, P. vulgaris, P. mirabilis, S. typhi, S. paratyphi A, S. typhimurium, S. dysenteriae type 1, Vibrio cholerae	All three extracts displayed wide antibacterial activity against Gram-positive bacteria. Among the Gram-negative bacteria tested, the antibacterial activity was limited to E. coli, S. typhimurium, S. dysenteriae type 1 and V. cholerae. All extracts also possess antifungal activity against the fungal species tested, except Candida krusei.	^[66]
28	B. aristata	Root Stem Leaf	Pakistan		E. coli, S. typhi, S. aureus, Shigella, Citrobacter, P. vulgaris,Enterobacter, Streptococcus pyrogenes, V. cholera, Klebsiella spp., A. niger, Cladosporium, Rhizoctonia, Alternaria, Trichoderma, Penicillium, Curvularia, Paecilomyces and Rhizopus	The extracts significantly inhibited the growth of the studied microbes, except A. niger, Curvularia, Paecilomyces and Rhizopus.	^[67]
29	B. aristata		India		V. cholerae, S. aureus	All the strains of V. cholerae are susceptible. All the Salmonella sp., Pseudomonas sp., and some of the E. coli strains are highly resistant, except some strains of E. coli as AL26, and Shigella sp. are susceptible. All Xanthomonas sp. were highly susceptible. Berberine sulfate showed antifungal action against C. albicans, Candida tropicalis, Trichophyton mentagrophytes, Microsporum gypseum, Cryptococcus neoformans and Sporothrix schenkii, Mycobacterium tuberculosis var. hominis H₃₇RV and Entamoeba histolytica.	^[68]
30	B. heterophylla	Leaves, stems and roots berberine	Argentina		S. aureus, E. faecali, P.aeruginosa, E. coli, C. albicans, Candida glabrata, Candida haemulonii, Candida lusitaniae, C. krusei, Candida parapsilosis	The aqueous extracts of B. heterophylla do not possess significant antimicrobial activity. Berberine displayed a significant antibacterial and antifungal activity against S. aureus and different Candida spp., some of them obtained from the clinical isolated.	^[69]
31	B. amurensis	Branches and leaves	Korea		Bacillus atrophaeus, Kocuria rhizophila, M. luteus, S. epidermidis, B. subtilis subsp. Spizizenii, K. pneumoniae, Enterobacter cloacae, Salmonella enterica subsp. enterica, P. aeruginosa	No significant activity against gram-negative bacteria.	^[70]
32	B. croatica and B. vulgaris	Roots, leaves, and twigs	Croatia	Ethanol	B. subtilis, S. aureus, E. coli, P. aeruginosa, C. albicans	Extracts of both species: significant antibacterial activity against the Gram-positive bacteria. Root extracts of B. croatica: activity against P. aeruginosa, and leaf extracts against B. subtilis. Neither species possessed antifungal activity. Leaf extracts of B. croatica: antibacterial activity against B. subtilis. Likewise, neither of the species extracts showed activity against E. coli and C. albicans, except when were diluted. Ethanolic extracts of twigs of both species: inactive against B. subtilis and against S. aureus, with the exception of B. croatica twig from Kiza locality.	^[71]
33	B. lycium	Roots	India	Hexane extract, Methanolic extract, aqueous extract and berberine	K. pneumonia, E. coli, P. aeuroginosa, S. aureus, B. subtilis, C. albicans, A. niger, Aspergillus fumigates	Methanolic extract of species was highly effective against E. coli, S. aureus, B. subtilis, C. albicans, A. fumigates. Pure berberine was effective against E. coli and C. albicans.	^[72]
34	B. aetnensis	Roots	Italy	Ethanol ether and chloroform	S. aureus, B. subtilis, E. faecalis, E. coli, P. aeruginosa, Stenotrophomonas maltophilia, against 14 strains of nosocomial origin: two strains of S. aureus (1 Met-S, 1 Met-R); four strains of S. epidermidis (2 Met-S, 2 Met-R); three strains of E. coli; four strains of P. aeruginosa, Hafnia alvei and C. albicans, C. parapsilosis, C. krusei	The root and leaf extracts showed a greater activity against Gram-positive bacteria and yeasts than against Gram-negative bacteria, except for P. aeruginosa. The chloroform extract of leaves was more active than the ethanol.	^[73]
35	B. thunbergii, B. vulgaris	Roots	USA		E. coli, P. aeruginosa, S. aureus, S. mutans, and S. pyogenes	Ethanolic extracts more active against studied bacteria, strongest activity against S. pyogenes and S. aureus.	^[74]
36	B. vulgaris	Root bark	Algeria	Methanol and water	S. aureus, E. faecalis, E. coli, E. cloacae, K. pneumoniae, P. aeruginosa	The extracts of species root barks presented a strong activity against S. aureus (23.0 mm), a weak activity against E. faecalis (13.0 mm) and no activity toward other strains.	^[75]

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1. Introduction

2. Berberis Plants Essential Oils and Phytochemical Composition

3. Food Preservative Applications of Berberis Plants

References