Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Phytochemical and antioxidant studies of Cleome heratensis (Capparaceae) plant extracts

Phytochemical and antioxidant studies of Cleome heratensis (Capparaceae) plant extracts Background: In this research, different active phytochemical constituents present in Cleome heratensis (C. heratensis) from Capparaceae family were investigated. Moreover, the fatty acids present in the seed and aerial parts of the plant were identified by gas chromatography (GC) after esterification of the oil. Antioxidant activity of the aerial parts and seed of C. heratensis methanolic extract over 2,2′-diphenylpicryl-1-hydrazyl (DPPH) was investigated using ultraviolet– visible (UV–Vis) spectrophotometer. Methods: To study total phenolic compounds and flavonoids, the plant was extracted from ethanol by ultrasonic method, then further extracted with other solvents. Amounts of anthocyanins and tannins/condensed tannins were determined by their corresponding ethanolic and acetone extracts. Antioxidant activity of the plant species was stud- ied by a spectrophotometric method using 80% methanolic extract. Results: The high content of phenolics as 16.915 mg tannic acid equivalents per gram of dry matter ( TAE/g DM), tan- nins (12.231 mg TA/gr DM) and condensed tannins (4.086 mg TA/g DM) was obtained for the C. heratensis extract. The most flavonoids content was found 4.444 rutin equivalents (in mg) per gram of dry matter (mg RE/g DM) in plant’s aerial extract. The most amount of anthocyanin (0.48 mmol/gr WM) was observed in flowering stage. Antioxidant activity of the aerial parts and seed of C. heratensis methanolic extract were 11.92 and 63.54 mg/mL IC , respectively. Conclusion: High level of phenolic components including flavonoids, proanthocyanidins and tannins was detected in the extract of aerial parts of the plant. The oil of seed of this plant is a rich source of saturated and unsaturated fatty acids. Finally, C. heratensis aerial part extract was found as an excellent natural antioxidant. Keywords: Cleome heratensis, Plant extract, Phytochemicals, Fatty acid, Antioxidant not only helps for the quality control analysis of the plant Background but also manifests nature of the drug or formulation (Jain Natural products contain different valuable chemical et al. 2011). components such as phenolic compounds, phthalides, Phenolic compounds are one of the important groups phenylpropanoids, terpenoids, essential oils, aromatic of secondary metabolites of natural products that have compounds, alkaloids, alkynes, sterols, polysaccharides, a large diversity of structures and functions includ- fatty acids, anthocyanin, tannins, etc. (Oksman-Calden- ing water-soluble (flavonoids, phenolic acids, quinones, tey and Inze 2004; Picot et  al. 2017; Mollica et  al. 2015). phenyl propanoids) and water-insoluble compounds They also have significant antioxidant activity (Embus - (tannins, lignins condensed, cell-wall bound hydroxy- cado 2015). Knowledge of these components in a plant cinnamic acids) (Alu’datt et  al. 2017; Mocan et  al. 2016;  Quispe et  al. 2012;  Nile et  al. 2017). In this way, *Correspondence: miladkazemnejadi@birjand.ac.ir; various biological effects have been found for phenolic miladkazemnejad@yahoo.com compounds; they are known as antioxidants that could Department of Chemistry, Faculty of Sciences, University of Birjand, Birjand, Iran © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 2 of 10 be served as free radical scavengers and protect oxida- species include spider flowers, spider plants, spider tive damages (Zhu et al. 2017; Sreelatha and Padma 2009; weeds or bee plants (Pakdaman et  al. 2013). The germi - Rauter et al. 2012; Haminiuk et al. 2012). Anti-inflamma - nating, flowering and fruiting stage of this plant are in tory (Ambriz-Pérez et  al. 2016) and antidiabetic (Ghor- May, September and October, respectively (Ghaderian bani 2017) effects are another biological activities of and Baker 2007). Various biological activities have been phenolic compounds. known for different species of Cleome (Singh et al. 2018), Tannins are one of the most important classes of poly- such as anti-microbial and insecticidal activities (Wil- phenols that are found in fruits and plants (Rauter et  al. liams et  al. 2003), anti-inflammatory (Puchchakayala 2012). They are mostly present as phenolic polymers. et  al. 2008), antioxidant (Narendhirakannan et  al. 2007), Two main types of tannins are condensed and hydrolys- hepatoprotective (Gupta and Dixit 2009). The aim of this able. Gallotannin or tannic acid is a type of hydrolysable research is focused on comprehensive assessment of phy- tannin in fruits (Maia et al. 2017; Ma et al. 2017). tochemical and fatty acid composition as well as antioxi- Anthocyanins are another class of flavonoids and the dant activity of different extracts from roots and aerial largest group of water-soluble natural pigments belong- parts in different phenological periods of C. heratensis. ing to the polyphenolic family. They are responsible for the colors red, violet, and blue for many fruits, vegeta- Methods bles, and cereal grains (Hosseinian and Beta 2007). The - Plant and chemicals ses bioactive molecules are widely spread in plant food. Aerial part, root, and seed (Fig.  2) of C. heratensis were They show useful health effects, radical scavenging, collected in late September and October 2014 from South chelation of heavy metals such as copper, zinc, and iron Khozestan, Birjand, Iran at four stages of growth includ- (Prior and Wu 2006; Ma et al. 2018). The chemical struc - ing: vegetative (S ), pre-flowering (S ), flowering (S ) and 1 2 3 ture of the major compounds in a natural plant is shown fruiting stage (S ) in May, early September, late Septem- in Fig. 1a–d. ber and October 2014, respectively. They were identified Fatty acids (FAs) are another class of bioactive com- in the Herbarium of Agriculture Institute, Mashhad, Iran pounds that make up an important part of the human (Herbarium number: 5413). All the chemicals were of diet (de Koning et al. 2001). They could be classified into analytical reagent grade purchased from Sigma Aldrich unsaturated and saturated fatty acids, which both play and used as received without further purification. an inevitable role in human health and nutrition (Smith Folin–Ciocalteu’s (FC) phenol reagent, sodium carbon- et al. 2013; Xiao et al. 2012). Also, poly-unsaturated fatty ate anhydrous, sodium hydroxide, polyvinyl pyrrolidone acids (PUFAs), as a health-supporting nutrients, have (PVP), hydrochloric acid, acetate sodium, aluminum the unique medicinal and preventing properties toward chloride hexahydrate, tannic acid, rutin and 2,2′-diphe- inflammatory, heart diseases, atherosclerosis, autoim - nylpicryl-1-hydrazyl were purchased from Sigma and mune disorder, diabetes, eczema, dermatitis, asthma, Merck companies. Gallic acid was purchased from Fluka rheumatoid arthritis, atherosclerosis, diabetes, obesity— supplier. even cancer and other diseases (Belch and Hill 2000; Lev- enthal et  al. 1993; Sierra-Cantor and Guerrero-Fajardo Instrumentation 2017; Kaurinovic et  al. 2011; Xiao et  al. 2012; Ramadan Analysis of the fatty acids was performed on a YL 6100 gas et  al. 2006). From this viewpoint, identification of total chromatograph system with a CBP5 column (Shimadzu fatty acids and lipids in plant seems to be essential. 30 m × 0.32 mm × 0.25 mm) equipped with an FID detec- So, isolation and identification of these bioactive com - tor. Compounds were separated on a CP-Sil 88 Fused- pounds in a plant are of utmost importance leading to silica capillary column (100  m × 0.25  mm × 0.2  μm). further biological and pharmacologic investigations. UV–Vis spectra were recorded on Shimadzu UV-Win These study might be served for developing the herbal X-ma 2000 spectrophotometer at span 20–800 nm. drug that requires the isolate novel bioactive compounds from the medicinal plants, which may open a new route to cure various irremediable diseases such as diabetes Fatty acid composition and hepatitis (Azmir et al. 2013). Extraction of seed oil Cleome heratensis (C. heratensis) belongs to Cleo- To obtain the fatty acid components in C. heraten- maceae family that includes more than 170 species of sis seed, the dried ground seed of the plant (Fig.  2b) shrubs, herbaceous annual and perennial plants (Ase- was extracted with n-hexane using a Soxhlet apparatus maneh et al. 2006). The genus C. heratensis is a flowering (70  °C, 8  h, 5% extraction yield). After removing n-hex- annual herbaceous plant which is typical of warm tem- ane using a rotary evaporator, the obtained oily mixture perate areas during summer and autumn. Its well-known Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 3 of 10 ab cd Fig. 1 Basic structures of a anthocyanins, b proanthocyanidins, c tannins, d flavonoids Fig. 2 a Aerial parts and b seed of C. heratensis was treated with sodium methoxide, according to the and then, sodium methoxide (50 μg) and water (100 μL) Standard ISO 5509:2000 (ISO2000) to produce the cor- were added to the mixture. The tube was centrifuged responding methyl esters by the trans-esterification reac - at 4500  rpm for 10  min and the lower aqueous phase tion (de Souza Schneider et  al. 2004). Briefly, a drop of was separated after addition of HCl (50 μL, 1.0  mol the obtained oil was dissolved in n-heptane (1.0  mL) with methyl orange). Next, 20  mg of sodium hydrogen Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 4 of 10 sulphate was added to the solution and the mixture was extract, was read simultaneously. Rutin solution was pre- centrifuged at 4500 rpm for 10 min. The resultant organic pared with addition of 10  mL of 50% ethanol to 0.005  g phase was transferred to a vial and injected to GC to of dried rutin. Quantitative determination of flavonoids identify its fatty acid composition. contents was performed using standard calibration curves using various rutin concentrations of 25, 50, 100 and 250 mg/L. Finally, the flavonoids concentrations were Determination of amounts of phenolic compounds reported as rutin equivalents in milligrams per gram of Preparation of extracts dry plant material weight (mg RE/gr DW). Aerial parts (Fig.  1a) and stem of C. heratensis were rinsed with deionized water, air-dried at room tem- Analysis of anthocyanins perature, then finely meshed and grinded with mortar Analysis of anthocyanins was conducted according to the and pestle, individually. Each plant powder (3.5  g) was method described by Hara et  al. (2003). The fresh parts extracted with ethanol (80%) into an ultrasonic bath for of C. heratensis (0.2  g) were extracted by rubbing with 7  min. The extracts were filtered, and the solvent was 3.0 mL of acidified methanol (MeOH: HCl; 99:1, v/v). The evaporated at reduced pressure. The yield of extractions crude extract was centrifuged at 6000  rpm for 30  min was found 6% and 4% for the aerial and stem of the plant, and set it aside in dark (covered with an aluminum foil) respectively. The ethanolic extract was successively fur - overnight (yield of extraction: 1.1%). The absorbance ther extracted with four solvents with increasing polarity of the supernatant was recorded at 550  nm to detect (EtO, CHCl , EtOAc and n-BuOH). All five extracts were 2 3 anthocyanins. evaporated to dryness and then dissolved in 50% ethanol to make 1% (w/v) solutions. Analysis of tannin content The total tannins were determined using the three steps Quantification of total phenolics content method reported by Makkar et  al. (1993). Firstly, pow- The amount of total phenolic content of the extracts dered samples (200  mg) were extracted with 70% ace- was determined using the Folin–Ciocalteu colorimetric tone. The yield of extractions was found 5%, 4% and 6% method according to the previously reported protocol for aerial, root and seed of the plant, respectively. The (Chandra et al. 2014). Briefly, the method was performed extract was centrifuged at 3000  rpm for 5  min and then by addition of 0.6  mL distilled water and 0.2  mL Folin– filtered. The first step involves the preparation of calibra - Ciocalteu reagent (0.5  M) to an aliquot of plant extracts tion curves of the standard samples with concentrations as well as standards. The mixture was stirred vigorously ranging from 20, 40, 50, 80 and 100 mg/L of tannic acid for 15  min and then, a solution of sodium carbonate in 50% ethanol. In the second step, the mixture of extract (1.0 mL, 8% w/v) was added to the mixture. The mixture (1.0  mL), distilled water (1.0  mL) and PVP (0.1  g) was was further diluted to 3.0 mL and set it aside for 30 min; shaken for 5 min, incubated for 10 min at 4 °C, and then then, the absorbance of the resulting blue-colored solu- centrifuged. The total phenolic compounds without tan - tion was measured at 760 nm. nins were also determined by standard calibration curves Quantitative determination of phenolic contents was of tannic acid. At last, tannins were determined by the performed based on the calibration curves of the stand- difference between total phenolic compounds before and ard samples with concentrations ranging from 20, 40, 50, after the addition of PVP. 80 and 100 mg/L of gallic acid in 50% ethanol. The results were expressed as gallic acid equivalents (GAE) in milli- grams per gram of dry plant material weight (mg/g). Determination of condensed tannins (Proanthocyanidins) 200  mg of powdered samples (aerial, root, seed) was Total flavonoids content extracted with 70% acetone followed by ultra-sonication The total content of flavonoids was measured quan - at 3000  rpm for 20  min at room temperature. Then, the titatively using rutin as a reference, according to the extract was centrifuged for 10  min at 3000  rpm. The described procedure by Bousselsela et  al. with a little supernatant was collected and kept on ice. The yield of modification (Brand-Williams et  al. 1995). Briefly, in a extractions was found 5%, 4% and 6% for aerial, root and dry tube, 1.0 mL of aluminum trichloride solution in 50% seed of the plant, respectively. ethanol along with 3.0 mL sodium acetate (10% w/v) was The amount of proanthocyanidins in extracts was added to the plant extract (1.0  mL). Then, the absorb - measured according to the method described by Porter ance was recorded at 415 nm after 40 min of the mixing. et  al. (1985). Briefly, in first, acidified butanol reagent Also, the absorbance of a reference solution, which was (butanol–HCI (37%) 95:5 v/v) was prepared by mix- prepared by 1  mL of rutin solution instead of the plant ing 950  mL of n–butanol with 50  mL concentrated HCl Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 5 of 10 (37%). Ferric reagent was prepared by dissolving 2.0 g of measured by a spectrophotometric assay (Brand-Wil- ferric ammonium sulfate in 2 N HCl. In a glass test tube, liams et al. 1995). Different concentrations of the extract 3  mL of the butanol–HCl reagent along with 0.1  mL were prepared and for each experiment, 75 μL plant of the ferric reagent was added to 0.5  mL of the tannin extract was added to 3.9  mL of 0.00463  g/L DPPH solu- extract diluted with 70% acetone. This amount of acetone tion. The final solution was protected with an aluminum was used to prevent exceeding the absorbance from 0.6 foil to prevent from light. After vigorous shaking of the (Porter et  al. 1985). The tubes were capped with a glass solution, it was left for 30  min (incubation period) at marble, then shaken using a Vortex and placed in a boil- ambient temperature; then the absorbance was read at ing water bath for 1  h. After cooling the tubes, their 517 nm. The percent of the remaining radicals at 30 min absorbance was recorded at 550  nm. The absorbance of was calculated using the following equation: the unheated mixture (considered as a suitable blank) A − A c s was subtracted from the absorbance of heated mixture. Antiradical activity(%) = × 100, The absorption band at 550 nm was used for calculation of the condensed tannins. If the development of pink where A and A are the absorbance of the control (con- c s color without heating happened, one heated blank will sist of solvent and DPPH) and the sample extract, respec- be used for each sample containing 0.5 mL of the extract, tively. Methanol and ascorbic acid were used as blank 3 mL of butanol and 0.1 mL of the ferric reagent (Seabra and positive control, respectively. All of the experiments et  al. 2018). The condensed tannins (% in dry matter) as were repeated for three times and their average was leucocyanidin equivalent were calculated using the fol- reported. The IC values were calculated by plotting the lowing equation (Ben Ahmed et al. 2017): inhibition percentage against the concentration of the extract (Muthukrishnan and Manogaran 2018). Differ - A (550 nm) × Dillution factor Condensed tannins = ent concentrations (1/10, 1/20, 1/30, 1/40) of the aqueous % Dry matter extract of C. heratensis were prepared by boiling 1  g of Given that the extract was prepared from 70% acetone, aerial parts of the plant in 10, 20, 30, 40 mL of deionized the dilution factor is calculated by the following formula water for 5  min. IC is the required initial concentra- (Ben Ahmed et al. 2017): tion of a selected antioxidant sample (plant extract in this study) to quench 50% of the free radicals in the reaction 0.5 mL mixture. Dilution factor = Volume of extract taken Results and discussion The dry matter was determined according to the fol - Fatty acid composition lowing procedure: Sample (5  g) was placed into an oven The fatty acid composition of oil is a major indicator of adjusted at 100–105  °C to complete drying and to reach oil quality; oils with high percentages of unsaturated fatty a constant weight. After cooling to room temperature, acids, mainly oleic and linoleic, are of high quality (Jokić weight of the dried sample was recorded and then,  % dry et al. 2013). The fatty acid composition of the C. heraten - matter was calculated by the following formula: Dry mat- sis seed extract was determined by GC analysis (Fig.  3). ter (%) = W /W × 100, where W and W are mass (g) of 2 1 2 1 The oil content of seeds can be varying from around 1% the sample before and after drying. in rice to more than 55% in Myristicaceae; the oil con- tent in C. heratensis seed extract was found 27.47%. The Antioxidant capacity analysis of fatty acid obtained from seed extract of C. Extraction heratensis revealed the presence of over 8 different com - Approximately, 0.15 g of dried parts of C. heratensis with pounds as shown in Fig.  3 and Table  1. The major com - 3  mL of 80% methanol was extracted at ambient tem- ponents were linoleic acid (67.8%), oleic acid (17.8%) and perature for 45  min under an ultrasonic wave. Then, the palmitic acid (8.7%). extracts were kept in the dark for 15  min and were cen- The results demonstrated that the amount of unsatu - trifuged for 15 min at 5000 rpm. After centrifugation, the rated fatty acids (87.8%) was higher than saturated fatty supernatants were collected. The extracts were kept at acids (12.2%). The ratio of unsaturated to saturated fatty 4 °C in dark until further analysis (yield of extraction: 7%). acids (U:S) was 7.20 in this oil. The fatty acid composition of C. heratensis seed with other edible vegetable oils was DPPH radical scavenging activity compared (Table  2). According to Table  2, the U/S ratio The ability of the C. heratensis extracts towards hydro - which is obtained for our plant was higher than olive and gen atom- or an electron donation was determined using corn oil. Therefore, considering that the higher ratio of the bleaching of the DPPH methanol solution as a rea- gent; then the antioxidant capacity of the extracts was Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 6 of 10 Phenolic composition Total phenolics content The results obtained from the determination of the total phenolic content of C. heratensis extracts are summa- rized in Table  3. As shown in Table  3, the total phenols content of the C. heratensis extract depends on harvest- ing time in various solvents. The concentration of total phenols of C. heratensis extracts was measured as gallic acid equivalents in mil- ligrams per gram of dry plant material weight (mg GAE/g DW). The results showed that in most cases, the quanti - ties of phenolic compounds of the plant were increased in different solvents during various developmental stages. The higher content was detected in acetone extract of Fig. 3 Chromatogram of fatty acids in C. heratensis seed extract. (YL aerial part (16.915  mg TAE/g DM) in S (fruiting stage) 6100 gas chromatograph system with a CBP5 column (Shimadzu 30 m × 0.32 mm × 0.25 mm) equipped with an FID detector) and the lowest total phenolic level was seen in ether extract of the root (0.048  mg GAE/g DM) in S (Pre- flowering stage). Also, the highest amount (19.0377  mg U:S for oil is safer for the heart and blood vessels, it pro- TAE/g DM) was observed in the acetone extract of the poses that these seeds are examined for feed intake. seed. In general, the highest total phenolic content was More importantly, the amount of linolenic acid, as an detected in aerial parts and extraction by acetone has a essential fatty acid in human food nutrition, was found maximum output. 67.8%, which is higher than the most vegetable oils (Table 2). Table 1 Fatty acid composition of seed oil of the C. heratensis seed Entry Fatty acid Type Retention time (min) Content (%) 1 Myristic acid ( C ) Saturated 2.383 0.2 14:0 2 Palmitic acid (C ) Saturated 2.867 8.7 16:0 3 Stearic acid (C ) Saturated 3.717 3.1 18:0 4 Arachidic acid (C ) Saturated 5.117 0.2 20:0 5 Palmitoleic acid (C ) Unsaturated (ω − 7) 3.140 0.2 16:1 cis 6 Oleic acid (C ) Unsaturated (ω − 9) 4.113 17.8 18:1 7 Linoleic acid ( C ) Unsaturated (ω − 6) 4.867 67.8 18:2 8 α-Linoleic acid (C ) Unsaturated (ω − 3) 5.737 2.0 18:3 Saturated carbon: unsaturated carbon Table 2 Comparison of  fatty acids composition of  C. heratensis seed with  the  various vegetable oils (Katragadda et  al. 2010) Type Saturated Mono unsaturated Total poly unsaturated U/S Linoleic acid (%) Coconut 91.00 6.00 3.00 0.1 2 Corn 12.95 27.58 54.68 6.35 59 Cottonseed 25.90 17.80 51.90 2.69 54 Olive 14 72 14 6.14 3.5–21 Soybean 15.65 22.78 57.74 5.14 51 Sunflower (60% linoleic) 10.1 45.4 40.1 8.46 10 Sunflower (70% Oleic) 9.86 83.69 3.80 8.87 – Seed of C. heratensis 12.2 18 69.8 7.20 67.8 Unsaturated/saturated fatty acids Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 7 of 10 Table 3 The amounts of phenolic compounds in the tissues extracts of the C. heratensis (mg GAE/g DM ) Sample Harvesting time H O n-BuOH EtOAc Chloroform Ether Acetone Aerial parts S 0.730 1.605 0.455 0.405 0.270 10.5426 S 0.866 4.596 0.445 0.199 0.316 7.1247 S 2.934 7.558 0.528 0.139 0.425 16.9146 Root S 3.394 0.165 0.282 0.057 0.048 1.8299 S 1.159 0.272 0.207 0.080 0.079 1.6642 S 1.046 0.355 0.369 0.218 1.009 2.7589 Seed – 1.054 0.758 0.435 0.190 0.452 19.0377 mg gallic acid equivalents per gram of dry matter As tannic acid equivalents (TAEs) Table 4 The amounts of flavonoids compounds in the tissues extracts of the C. heratensis (mg RE/g DM ) Sample Harvesting time H O n-BuOH EtOAc Chloroform Ether Aerial parts S 0.405 2.256 0.514 0.193 0.350 S 0.389 2.956 0.504 0.136 0.399 S 1.417 4.444 0.541 0.113 0.387 Root S 0.476 0.517 0.156 0.020 0.003 S 0.477 0.221 0.483 0.103 0.023 S 0.786 0.324 0.280 0.152 0.158 Seed – 0.134 0.098 0.074 0.073 0.244 Rutin equivalents in milligrams per gram of dry plant material weight results showed that the amount of flavonoid compounds of the plant was increased in different solvents at differ - ent stages of growth (Table 4). The highest flavonoids content was detected in n-BuOH extract of the aerial part (4.444  mg RE/g DM) in S (fruiting stage) and the lowest content was seen in ether extract of the root (0.003  mg RE/gr DM) in S (Pre flowering stage) (Table  4). In general, similar to phe- nolic compounds, the highest content of flavonoids was detected in the aerial part at fruiting stage. Also, extrac- tion by n-BuOH and acetone provides a maximum out- put, respectively. Anthocyanin content As shown in Fig.  4, concentration of anthocyanin of C. heratensis extract was measured as millimole per gram of wet plant material weight (mmol/g WM). The Fig. 4 The amounts of anthocyanin compounds in the extracts of results showed that in the primary stages, the anthocya- tissues (mmol/g WM). *mmol anthocyanin per gram of wet plant nin amount increased and at the flowering stage (S ), it material weight reached to 0.48  mmol/g WM, and then decreased. In general, these results showed that extraction at flowering stage has maximum output due to flowers. Also, seed of Flavonoids content the plant demonstrated 0.39  mmol/g WM anthocyanin The concentrations of flavonoids of C. heratensis extract which is higher than aerial parts of the plant. were determined as rutin equivalents in milligrams per gram of dry plant material weight (mg RE/g DW). The Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 8 of 10 of aerial part in S (fruiting stage) including total tan- nins (12.2312  mg TAE/g DM) and proanthocyanidin (4.0856 mg TAE/g DM). The lowest amount was seen in the extract of root in S equal to 0.9757, 0.0226 mg TAE/g DM for total and condensed tannin, respectively. In gen- eral, similar to other identified compounds, the highest contents were detected in the seed. The differential accumulation of phenolic compounds in C. heratensis extracts at the different stages could be related to physiological changes during growth in response to environmental stress. The season, sunlight duration, UV radiation, and temperature are known parameters that affect the plant metabolism, since some compounds may be accumulated at a particular period to respond to environmental changes (Generalić et al. 2011; Negrão et al. 2017; Lu et al. 2017). Determination of antioxidant capacities Antioxidant activity of the C. heratensis extracts was determined using DPPH radical scavenging assay. This assay is based on hydrogen/electron transfer from a given antioxidant to DPPH. The DPPH has a strong absorption band at λ = 517  nm with deep purple max color, whereas the redacted product is yellowish with- out any absorption band (Lu et  al. 2017). Although Fig. 5 The amounts of tannin (blue columns) and proanthocyanidin DPPH-H is the final product, other complexes could (yellow curves) and seed (yellow column) compounds in the tissues acetone extracts of the C. heratensis (mg TAE/g DM).*Tannin/ be formed by reacting DPPH and oxidized intermedi- proanthocyanidin ates in the extract and generate high molecular weight polymers (Pedan et  al. 2016). The results from anti - oxidant property of the extract revealed the radical scavenging of the aerial and root extract of C. herat- ensis. Figure  6 shows the curve of inhibition percent- age of the extract versus extract concentration as I C (mg/mL). As shown in the figure, the extract of aerial parts (11.92 mg/mL) exhibited higher scavenging activ- ity than the roots extract (63.44 mg/mL). According to the definition of IC , the lower IC value refers to a 50 50 stronger antioxidant activity in a testing sample. Thus, aerial parts of the plant have higher antioxidant activity. Figure  7 shows the UV–Vis spectra of DPPH solution before and after the addition of the aerial C. heratensis extract. The spectra clearly demonstrated the antioxidant Fig. 6 Linear relationship between inhibition percentage of the extract and extract concentration activity of the extract with the complete elimination of the absorption band at λ = 517 nm for DPPH (Fig. 7a). max Figure 7b shows UV–Vis spectra recorded for aerial parts of C. heratensis extract. Electronic spectra of the extract Tannin and proanthocyanidin contents showed one absorption band at ~305 nm (Fig. 7b). The concentrations of total and condensed tannins (proanthocyanidins) in the extracts of C. heratensis (mg TAE/g DM) are shown in Fig. 5. The results showed that Conclusions the amount of tannins in aerial parts of the plant was The C. heratensis from Capparaceae family is found increased during various developmental stages from mainly in the eastern region (Birjand) of Iran. The seed S to S . The highest content was detected in extract oil of this plant (27.47%) is a rich source of unsaturated 1 4 Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 9 of 10 Fig. 7 a Antiradical activity of the aerial extract of C. heratensis (0.1 g/mL) over quenching 2,2′-diphenylpicryl-1-hydrazyl (DPPH) radicals at room temperature. b UV–visible spectra of aerial part of C. heratensis extract Ethics approval and consent to participate fatty acids (87.8%), especially linoleic acid (67.8%) and All the authors have read and agreed the ethics for publishing the manuscript. oleic acid (17.8%). The highest total amounts of phenolic (16.915 mg TAE/g DM), flavonoids (4.444 mg RE/g DM), Funding No funding was received for this article. total tannins (12.231  mg TA/gr DM) and proanthocya- nidins (4.086  mg TA/g DM) components were detected Publisher’s Note in extract of aerial parts in fruiting stage and seed of the Springer Nature remains neutral with regard to jurisdictional claims in pub- plant. Also, the most amount of anthocyanin (0.48 mmol/ lished maps and institutional affiliations. gr WM) was observed in flowering stage. Harvesting C. Received: 13 November 2018 Accepted: 25 January 2019 heratensis at the fruiting stage and extracting of aerial parts of plant or seeds by acetone give the most amounts of bioactive compounds. C. heratensis extract is a good natural antioxidant that could be added as a chemical References basis in food and therapeutics. Alu’datt MH, Rababah T, Alhamad MN, Al-Mahasneh MA, Almajwal A, Gammoh S, Ereifej K, Johargy A, Alli I (2017) A review of phenolic compounds in oil-bearing plants: distribution, identification and occurrence of phenolic Abbreviations compounds. Food Chem 218:99–106 Cleome heratensis: C. heratensis; GC: gas chromatography; FA: fatty acids; PUFA: Ambriz-Pérez DL, Leyva-López N, Gutierrez-Grijalva EP, Heredia JB (2016) poly unsaturated fatty acid; FC: folin–ciocalteau’s; PVP: polyvinyl pyrrolidone; Phenolic compounds: natural alternative in inflammation treatment. a DPPH: 2,2′-diphenylpicryl-1-hydrazyl; DM: dry matter; RE: rutin equivalents; review. Cogent Food Agric 2:1131412 TAE: tannic acid equivalents; GAE: gallic acid equivalents. Asemaneh T, Ghaderian SM, Crawford SA, Marshall AT, Baker AJM (2006) Cel- lular and subcellular compartmentation of Ni in the Eurasian serpentine Authors’ contributions plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome MAN and AA design the study. SB and MK performed the research experi- heratensis (Capparaceae). Planta 225:193–202 ments, acquired the data and wrote the manuscript. All authors were involved Azmir J, Zaidul ISM, Rahman MM, Sharif KM, Mohamed A, Sahena F, Jahurul in the analysis and approved the final manuscript of publication. MAN and SB MHA, Ghafoor K, Norulaini NAN, Omar AKM (2013) Techniques for extrac- interpreted the results. All authors read and approved the final manuscript. tion of bioactive compounds from plant materials: a review. J Food Eng 117:426–436 Belch JJ, Hill A (2000) Evening primrose oil and borage oil in rheumatologic Acknowledgements conditions. Am J Clin Nutr 71:352s–356s The authors are thankful to Research Council of University of Birjand for pro- Ben Ahmed Z, Yousfi M, Viaene J, Dejaegher B, Demeyer K, Mangelings D, viding all the necessary facilities to carry out the research work. Vander Heyden Y (2017) Seasonal, gender and regional variations in total phenolic, flavonoid, and condensed tannins contents and in antioxidant Competing interests properties from Pistacia atlantica ssp. leaves. Pharm Biol 55:1185–1194 The authors declare that they have no competing interests. Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30 Availability of data and materials Chandra S, Khan S, Avula B, Lata H, Yang MH, ElSohly MA, Khan IA (2014) All data that are relevant to the study are reported within the article. Assessment of total phenolic and flavonoid content, antioxidant properties, and yield of aeroponically and conventionally grown leafy Consent for publication vegetables and fruit crops: a comparative study. Evid Based Complement The authors approved the consent for publishing the manuscript. Altern Med 2014:1–9 Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 10 of 10 de Koning S, van der Meer B, Alkema G, Janssen HG, Udo A (2001) Automated Narendhirakannan RT, Subramanian S, Kandaswamy M (2007) Evaluation of determination of fatty acid methyl ester and cis/trans methyl ester com- antioxidant potential of Cleome gynandra L. leaf extract on the compo- position of fats and oils. J Chromatogr A 922:391–397 nents of the lymphoid organs in adjuvant induced arthritis in rats. Int J de Souza Schneider RC, Baldissarelli VZ, Trombetta F, Martinelli M, Caramão EB Biol Chem 1:1–10 (2004) Optimization of gas chromatographic–mass spectrometric analy- Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses sis for fatty acids in hydrogenated castor oil obtained by catalytic transfer of plants to salinity stress. Ann Bot 119:1–11 hydrogenation. Anal Chim Acta 505:223–226 Nile SH, Nile AS, Keum YS (2017) Total phenolics, antioxidant, antitumor, and Embuscado ME (2015) Spices and herbs: natural sources of antioxidants–a enzyme inhibitory activity of Indian medicinal and aromatic plants mini review. J Funct Foods 18:811–819 extracted with different extraction methods. 3 Biotech 7:76 Generalić I, Skroza D, Ljubenkov I, Katalinić A, Burčul F, Katalinić V (2011) Influ- Oksman-Caldentey KM, Inze D (2004) Plant cell factories in the post-genomic ence of the phenophase on the phenolic profile and antioxidant proper - era: new ways to produce designer secondary metabolites. Trends Plant ties of Dalmatian sage. Food Chem 127:427–433 Sci 9:433–444 Ghaderian SM, Baker AJM (2007) Geobotanical and biogeochemical reconnais- Pakdaman N, Ghaderian SM, Ghasemi R, Asemaneh T (2013) Eec ff ts of calcium/ sance of the ultramafics of Central Iran. J Geochem Explor 92:34–42 magnesium quotients and nickel in the growth medium on growth and Ghorbani A (2017) Mechanisms of antidiabetic effects of flavonoid rutin. nickel accumulation in Pistacia atlantica. J Plant Nutr 36:1708–1718 Biomed Pharmacother 96:305–312 Pedan V, Fischer N, Rohn S (2016) An online NP-HPLC-DPPH method for the Gupta NK, Dixit VK (2009) Evaluation of hepatoprotective activity of Cleome determination of the antioxidant activity of condensed polyphenols in viscosa Linn. extract. Indian J Pharmacol 41:36–40 cocoa. Food Res Int 89:890–900 Haminiuk CW, Maciel GM, Plata-Oviedo MS, Peralta RM (2012) Phenolic com- Picot MC, Zengin G, Mollica A, Stefanucci A, Carradori S, Mahomoodally M pounds in fruits–an overview. Int J Food Sci Technol 47:2023–2044 (2017) In vitro and in silico studies of mangiferin from Aphloia theiformis Hara M, Oki K, Hoshino K, Kuboi T (2003) Enhancement of anthocyanin on key enzymes linked to diabetes type 2 and associated complications. biosynthesis by sugar in radish (Raphanus sativus) hypocotyl. Plant Sci Med Chem 13:633–640 164:259–265 Porter LJ, Hrstich LN, Chan BG (1985) The conversion of procyanidins and Hosseinian FS, Beta T (2007) Saskatoon and wild blueberries have higher prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230 anthocyanin contents than other Manitoba berries. J Agric Food Chem Prior RL, Wu X (2006) Anthocyanins: structural characteristics that result in 55:10832–10838 unique metabolic patterns and biological activities. Free Radical Res Jain V, Murugananthan G, Deepak M, Viswanatha GL, Manohar D (2011) Isolation 40:1014–1028 and standardization of various phytochemical constituents from metha- Puchchakayala G, Podili L, Bobbala D, Thirupathi K, Boini K, Yellu N, Bobbala R, nolic extracts of fruit rinds of Punica granatum. Chin J Nat Med 9:414–420 Gottemukkala K, Pragada R (2008) Antinociceptive and anti-inflammatory Jokić S, Sudar R, Svilović S, Vidović S, Bilić M, Velić D, Jurković V (2013) Fatty acid effects of Cleome chelidonni linn. roots in experimental animals. Pharma- composition of oil obtained from soybeans by extraction with supercriti- cogn Mag 4:32–36 cal carbon dioxide. Czech J Food Sci 31:116–125 Quispe C, Viveros-Valdez E, Schmeda-Hirschmann G (2012) Phenolic constitu- Katragadda HR, Fullana A, Sidhu S, Carbonell-Barrachina ÁA (2010) Emissions ents of the Chilean herbal tea Fabiana imbricata R. et P. Plant Foods Hum of volatile aldehydes from heated cooking oils. Food Chem 120:59–65 Nutr 67:242–246 Kaurinovic B, Popovic M, Vlaisavljevic S, Trivic S (2011) Antioxidant capacity Ramadan MF, Sharanabasappa G, Seetharam YN, Seshagiri M, Moersel JT of Ocimum basilicum L. and Origanum vulgare L. extracts. Molecules (2006) Characterisation of fatty acids and bioactive compounds of kach- 16:7401–7414 nar (Bauhinia purpurea L.) seed oil. Food Chem 98:359–365 Leventhal LJ, Boyce EG, Zurier RB (1993) Treatment of rheumatoid arthritis with Rauter AP, Dias C, Martins A, Branco I, Neng NR, Nogueira JM, Goulart M, Silva gammalinolenic acid. Ann Intern Med 119:867–873 FV, Justino J, Trevitt C, Waltho JP (2012) Non-toxic Salvia sclareoides Brot. Lu Y, Wu N, Fang Y, Shaheen N, Wei Y (2017) An automatic on-line 2, 2-diphe- extracts as a source of functional food ingredients: phenolic profile, anti- nyl-1-picrylhydrazyl-high performance liquid chromatography method oxidant activity and prion binding properties. Food Chem 132:1930–1935 for high-throughput screening of antioxidants from natural products. J Seabra IJ, Chim RB, Salgueiro P, Braga ME, de Sousa HC (2018) Influence Chromatogr A 1521:100–109 of solvent additives on the aqueous extraction of tannins from pine Ma H, Xu J, DaSilva NA, Wang L, Wei Z, Guo L, Johnson SL, Lu W, Xu J, Gu Q, bark: potential extracts for leather tanning. J Chem Technol Biotechnol Seeram NP (2017) Cosmetic applications of glucitol-core containing gal- 93:1169–1182 lotannins from a proprietary phenolic-enriched red maple (Acer rubrum) Sierra-Cantor JF, Guerrero-Fajardo CA (2017) Methods for improving the cold leaves extract: inhibition of melanogenesis via down-regulation of flow properties of biodiesel with high saturated fatty acids content: a tyrosinase and melanogenic gene expression in B16F10 melanoma cells. review. Renew Sustain Energy Rev 72:774–790 Arch Dermatol Res 309:265–274 Singh H, Mishra A, Mishra AK (2018) The chemistry and pharmacology of Ma H, Johnson SL, Liu W, DaSilva NA, Meschwitz S, Dain JA, Seeram NP (2018) Cleome genus: a review. Biomed Pharmacother 101:37–48 Evaluation of polyphenol anthocyanin-enriched extracts of blackberry, black Smith MA, Dauk M, Ramadan H, Yang H, Seamons LE, Haslam RP, Beaudoin F, raspberry, blueberry, cranberry, red raspberry, and strawberry for free radical Ramirez-Erosa I, Forseille L (2013) Involvement of Arabidopsis ACYL- scavenging, reactive carbonyl species trapping, anti-glycation, anti-β-amyloid COENZYME A DESATURASE-LIKE2 (At2g31360) in the biosynthesis of the aggregation, and microglial neuroprotective effects. Int J Mol Sci 19:461–480 very-long-chain monounsaturated fatty acid components of membrane Maia IRDO, Trevisan MTS, Silva MGDV, Breuer A, Owen RW (2017) Content of lipids. Plant Physiol 161:81–96 total phenolic compounds, flavonoids and tannins in methanol extracts Sreelatha S, Padma PR (2009) Antioxidant activity and total phenolic content of the genus Senna Mill. from the northeast of Brazil and evaluation of of Moringa oleifera leaves in two stages of maturity. Plant Foods Hum antioxidant capacity. J Pharmacogn Phytochem 6:1321–1325 Nutr 64:303 Makkar HP, Blümmel M, Borowy NK, Becker K (1993) Gravimetric determination Williams LAD, Vasques E, Reid W, Porter R, Kraus W (2003) Biological activities of tannins and their correlations with chemical and protein precipitation of an extract from Cleome viscosa L. (Capparaceae). Naturwissenschaften methods. J Sci Food Agric 61:161–165 90:468–472 Mocan A, Zengin G, Crişan G, Mollica A (2016) Enzymatic assays and molecular Xiao L, Mjøs SA, Haugsgjerd BO (2012) Efficiencies of three common lipid modeling studies of Schisandra chinensis lignans and phenolics from fruit extraction methods evaluated by calculating mass balances of the fatty and leaf extracts. J Enzyme Inhib Med Chem 31:200–210 acids. J Food Compos Anal 25:198–207 Mollica A, Costante R, Akdemir A, Carradori S, Stefanucci A, Macedonio G, Zhu L, Chen J, Tan J, Liu X, Wang B (2017) Flavonoids from Agrimonia pilosa Ceruso M, Supuran CT (2015) Exploring new Probenecid-based carbonic Ledeb: free radical scavenging and DNA oxidative damage protection anhydrase inhibitors: synthesis, biological evaluation and docking stud- activities and analysis of bioactivity-structure relationship based on ies. Bioorg Med Chem 23:5311–5318 molecular and electronic structures. Molecules 22:195–206 Muthukrishnan S, Manogaran P (2018) Phytochemical analysis and free radical scavenging potential activity of Vetiveria zizanioides Linn. J Pharmacogn Phytochem 7:1955–1960 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png "Bioresources and Bioprocessing" Springer Journals

Phytochemical and antioxidant studies of Cleome heratensis (Capparaceae) plant extracts

Download PDF
10 pages

Loading next page...
 
/lp/springer-journals/phytochemical-and-antioxidant-studies-of-cleome-heratensis-capparaceae-YgcANreTmY

References (56)

Publisher
Springer Journals
Copyright
2019 The Author(s)
eISSN
2197-4365
DOI
10.1186/s40643-019-0240-1
Publisher site
See Article on Publisher Site

Abstract

Background: In this research, different active phytochemical constituents present in Cleome heratensis (C. heratensis) from Capparaceae family were investigated. Moreover, the fatty acids present in the seed and aerial parts of the plant were identified by gas chromatography (GC) after esterification of the oil. Antioxidant activity of the aerial parts and seed of C. heratensis methanolic extract over 2,2′-diphenylpicryl-1-hydrazyl (DPPH) was investigated using ultraviolet– visible (UV–Vis) spectrophotometer. Methods: To study total phenolic compounds and flavonoids, the plant was extracted from ethanol by ultrasonic method, then further extracted with other solvents. Amounts of anthocyanins and tannins/condensed tannins were determined by their corresponding ethanolic and acetone extracts. Antioxidant activity of the plant species was stud- ied by a spectrophotometric method using 80% methanolic extract. Results: The high content of phenolics as 16.915 mg tannic acid equivalents per gram of dry matter ( TAE/g DM), tan- nins (12.231 mg TA/gr DM) and condensed tannins (4.086 mg TA/g DM) was obtained for the C. heratensis extract. The most flavonoids content was found 4.444 rutin equivalents (in mg) per gram of dry matter (mg RE/g DM) in plant’s aerial extract. The most amount of anthocyanin (0.48 mmol/gr WM) was observed in flowering stage. Antioxidant activity of the aerial parts and seed of C. heratensis methanolic extract were 11.92 and 63.54 mg/mL IC , respectively. Conclusion: High level of phenolic components including flavonoids, proanthocyanidins and tannins was detected in the extract of aerial parts of the plant. The oil of seed of this plant is a rich source of saturated and unsaturated fatty acids. Finally, C. heratensis aerial part extract was found as an excellent natural antioxidant. Keywords: Cleome heratensis, Plant extract, Phytochemicals, Fatty acid, Antioxidant not only helps for the quality control analysis of the plant Background but also manifests nature of the drug or formulation (Jain Natural products contain different valuable chemical et al. 2011). components such as phenolic compounds, phthalides, Phenolic compounds are one of the important groups phenylpropanoids, terpenoids, essential oils, aromatic of secondary metabolites of natural products that have compounds, alkaloids, alkynes, sterols, polysaccharides, a large diversity of structures and functions includ- fatty acids, anthocyanin, tannins, etc. (Oksman-Calden- ing water-soluble (flavonoids, phenolic acids, quinones, tey and Inze 2004; Picot et  al. 2017; Mollica et  al. 2015). phenyl propanoids) and water-insoluble compounds They also have significant antioxidant activity (Embus - (tannins, lignins condensed, cell-wall bound hydroxy- cado 2015). Knowledge of these components in a plant cinnamic acids) (Alu’datt et  al. 2017; Mocan et  al. 2016;  Quispe et  al. 2012;  Nile et  al. 2017). In this way, *Correspondence: miladkazemnejadi@birjand.ac.ir; various biological effects have been found for phenolic miladkazemnejad@yahoo.com compounds; they are known as antioxidants that could Department of Chemistry, Faculty of Sciences, University of Birjand, Birjand, Iran © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 2 of 10 be served as free radical scavengers and protect oxida- species include spider flowers, spider plants, spider tive damages (Zhu et al. 2017; Sreelatha and Padma 2009; weeds or bee plants (Pakdaman et  al. 2013). The germi - Rauter et al. 2012; Haminiuk et al. 2012). Anti-inflamma - nating, flowering and fruiting stage of this plant are in tory (Ambriz-Pérez et  al. 2016) and antidiabetic (Ghor- May, September and October, respectively (Ghaderian bani 2017) effects are another biological activities of and Baker 2007). Various biological activities have been phenolic compounds. known for different species of Cleome (Singh et al. 2018), Tannins are one of the most important classes of poly- such as anti-microbial and insecticidal activities (Wil- phenols that are found in fruits and plants (Rauter et  al. liams et  al. 2003), anti-inflammatory (Puchchakayala 2012). They are mostly present as phenolic polymers. et  al. 2008), antioxidant (Narendhirakannan et  al. 2007), Two main types of tannins are condensed and hydrolys- hepatoprotective (Gupta and Dixit 2009). The aim of this able. Gallotannin or tannic acid is a type of hydrolysable research is focused on comprehensive assessment of phy- tannin in fruits (Maia et al. 2017; Ma et al. 2017). tochemical and fatty acid composition as well as antioxi- Anthocyanins are another class of flavonoids and the dant activity of different extracts from roots and aerial largest group of water-soluble natural pigments belong- parts in different phenological periods of C. heratensis. ing to the polyphenolic family. They are responsible for the colors red, violet, and blue for many fruits, vegeta- Methods bles, and cereal grains (Hosseinian and Beta 2007). The - Plant and chemicals ses bioactive molecules are widely spread in plant food. Aerial part, root, and seed (Fig.  2) of C. heratensis were They show useful health effects, radical scavenging, collected in late September and October 2014 from South chelation of heavy metals such as copper, zinc, and iron Khozestan, Birjand, Iran at four stages of growth includ- (Prior and Wu 2006; Ma et al. 2018). The chemical struc - ing: vegetative (S ), pre-flowering (S ), flowering (S ) and 1 2 3 ture of the major compounds in a natural plant is shown fruiting stage (S ) in May, early September, late Septem- in Fig. 1a–d. ber and October 2014, respectively. They were identified Fatty acids (FAs) are another class of bioactive com- in the Herbarium of Agriculture Institute, Mashhad, Iran pounds that make up an important part of the human (Herbarium number: 5413). All the chemicals were of diet (de Koning et al. 2001). They could be classified into analytical reagent grade purchased from Sigma Aldrich unsaturated and saturated fatty acids, which both play and used as received without further purification. an inevitable role in human health and nutrition (Smith Folin–Ciocalteu’s (FC) phenol reagent, sodium carbon- et al. 2013; Xiao et al. 2012). Also, poly-unsaturated fatty ate anhydrous, sodium hydroxide, polyvinyl pyrrolidone acids (PUFAs), as a health-supporting nutrients, have (PVP), hydrochloric acid, acetate sodium, aluminum the unique medicinal and preventing properties toward chloride hexahydrate, tannic acid, rutin and 2,2′-diphe- inflammatory, heart diseases, atherosclerosis, autoim - nylpicryl-1-hydrazyl were purchased from Sigma and mune disorder, diabetes, eczema, dermatitis, asthma, Merck companies. Gallic acid was purchased from Fluka rheumatoid arthritis, atherosclerosis, diabetes, obesity— supplier. even cancer and other diseases (Belch and Hill 2000; Lev- enthal et  al. 1993; Sierra-Cantor and Guerrero-Fajardo Instrumentation 2017; Kaurinovic et  al. 2011; Xiao et  al. 2012; Ramadan Analysis of the fatty acids was performed on a YL 6100 gas et  al. 2006). From this viewpoint, identification of total chromatograph system with a CBP5 column (Shimadzu fatty acids and lipids in plant seems to be essential. 30 m × 0.32 mm × 0.25 mm) equipped with an FID detec- So, isolation and identification of these bioactive com - tor. Compounds were separated on a CP-Sil 88 Fused- pounds in a plant are of utmost importance leading to silica capillary column (100  m × 0.25  mm × 0.2  μm). further biological and pharmacologic investigations. UV–Vis spectra were recorded on Shimadzu UV-Win These study might be served for developing the herbal X-ma 2000 spectrophotometer at span 20–800 nm. drug that requires the isolate novel bioactive compounds from the medicinal plants, which may open a new route to cure various irremediable diseases such as diabetes Fatty acid composition and hepatitis (Azmir et al. 2013). Extraction of seed oil Cleome heratensis (C. heratensis) belongs to Cleo- To obtain the fatty acid components in C. heraten- maceae family that includes more than 170 species of sis seed, the dried ground seed of the plant (Fig.  2b) shrubs, herbaceous annual and perennial plants (Ase- was extracted with n-hexane using a Soxhlet apparatus maneh et al. 2006). The genus C. heratensis is a flowering (70  °C, 8  h, 5% extraction yield). After removing n-hex- annual herbaceous plant which is typical of warm tem- ane using a rotary evaporator, the obtained oily mixture perate areas during summer and autumn. Its well-known Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 3 of 10 ab cd Fig. 1 Basic structures of a anthocyanins, b proanthocyanidins, c tannins, d flavonoids Fig. 2 a Aerial parts and b seed of C. heratensis was treated with sodium methoxide, according to the and then, sodium methoxide (50 μg) and water (100 μL) Standard ISO 5509:2000 (ISO2000) to produce the cor- were added to the mixture. The tube was centrifuged responding methyl esters by the trans-esterification reac - at 4500  rpm for 10  min and the lower aqueous phase tion (de Souza Schneider et  al. 2004). Briefly, a drop of was separated after addition of HCl (50 μL, 1.0  mol the obtained oil was dissolved in n-heptane (1.0  mL) with methyl orange). Next, 20  mg of sodium hydrogen Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 4 of 10 sulphate was added to the solution and the mixture was extract, was read simultaneously. Rutin solution was pre- centrifuged at 4500 rpm for 10 min. The resultant organic pared with addition of 10  mL of 50% ethanol to 0.005  g phase was transferred to a vial and injected to GC to of dried rutin. Quantitative determination of flavonoids identify its fatty acid composition. contents was performed using standard calibration curves using various rutin concentrations of 25, 50, 100 and 250 mg/L. Finally, the flavonoids concentrations were Determination of amounts of phenolic compounds reported as rutin equivalents in milligrams per gram of Preparation of extracts dry plant material weight (mg RE/gr DW). Aerial parts (Fig.  1a) and stem of C. heratensis were rinsed with deionized water, air-dried at room tem- Analysis of anthocyanins perature, then finely meshed and grinded with mortar Analysis of anthocyanins was conducted according to the and pestle, individually. Each plant powder (3.5  g) was method described by Hara et  al. (2003). The fresh parts extracted with ethanol (80%) into an ultrasonic bath for of C. heratensis (0.2  g) were extracted by rubbing with 7  min. The extracts were filtered, and the solvent was 3.0 mL of acidified methanol (MeOH: HCl; 99:1, v/v). The evaporated at reduced pressure. The yield of extractions crude extract was centrifuged at 6000  rpm for 30  min was found 6% and 4% for the aerial and stem of the plant, and set it aside in dark (covered with an aluminum foil) respectively. The ethanolic extract was successively fur - overnight (yield of extraction: 1.1%). The absorbance ther extracted with four solvents with increasing polarity of the supernatant was recorded at 550  nm to detect (EtO, CHCl , EtOAc and n-BuOH). All five extracts were 2 3 anthocyanins. evaporated to dryness and then dissolved in 50% ethanol to make 1% (w/v) solutions. Analysis of tannin content The total tannins were determined using the three steps Quantification of total phenolics content method reported by Makkar et  al. (1993). Firstly, pow- The amount of total phenolic content of the extracts dered samples (200  mg) were extracted with 70% ace- was determined using the Folin–Ciocalteu colorimetric tone. The yield of extractions was found 5%, 4% and 6% method according to the previously reported protocol for aerial, root and seed of the plant, respectively. The (Chandra et al. 2014). Briefly, the method was performed extract was centrifuged at 3000  rpm for 5  min and then by addition of 0.6  mL distilled water and 0.2  mL Folin– filtered. The first step involves the preparation of calibra - Ciocalteu reagent (0.5  M) to an aliquot of plant extracts tion curves of the standard samples with concentrations as well as standards. The mixture was stirred vigorously ranging from 20, 40, 50, 80 and 100 mg/L of tannic acid for 15  min and then, a solution of sodium carbonate in 50% ethanol. In the second step, the mixture of extract (1.0 mL, 8% w/v) was added to the mixture. The mixture (1.0  mL), distilled water (1.0  mL) and PVP (0.1  g) was was further diluted to 3.0 mL and set it aside for 30 min; shaken for 5 min, incubated for 10 min at 4 °C, and then then, the absorbance of the resulting blue-colored solu- centrifuged. The total phenolic compounds without tan - tion was measured at 760 nm. nins were also determined by standard calibration curves Quantitative determination of phenolic contents was of tannic acid. At last, tannins were determined by the performed based on the calibration curves of the stand- difference between total phenolic compounds before and ard samples with concentrations ranging from 20, 40, 50, after the addition of PVP. 80 and 100 mg/L of gallic acid in 50% ethanol. The results were expressed as gallic acid equivalents (GAE) in milli- grams per gram of dry plant material weight (mg/g). Determination of condensed tannins (Proanthocyanidins) 200  mg of powdered samples (aerial, root, seed) was Total flavonoids content extracted with 70% acetone followed by ultra-sonication The total content of flavonoids was measured quan - at 3000  rpm for 20  min at room temperature. Then, the titatively using rutin as a reference, according to the extract was centrifuged for 10  min at 3000  rpm. The described procedure by Bousselsela et  al. with a little supernatant was collected and kept on ice. The yield of modification (Brand-Williams et  al. 1995). Briefly, in a extractions was found 5%, 4% and 6% for aerial, root and dry tube, 1.0 mL of aluminum trichloride solution in 50% seed of the plant, respectively. ethanol along with 3.0 mL sodium acetate (10% w/v) was The amount of proanthocyanidins in extracts was added to the plant extract (1.0  mL). Then, the absorb - measured according to the method described by Porter ance was recorded at 415 nm after 40 min of the mixing. et  al. (1985). Briefly, in first, acidified butanol reagent Also, the absorbance of a reference solution, which was (butanol–HCI (37%) 95:5 v/v) was prepared by mix- prepared by 1  mL of rutin solution instead of the plant ing 950  mL of n–butanol with 50  mL concentrated HCl Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 5 of 10 (37%). Ferric reagent was prepared by dissolving 2.0 g of measured by a spectrophotometric assay (Brand-Wil- ferric ammonium sulfate in 2 N HCl. In a glass test tube, liams et al. 1995). Different concentrations of the extract 3  mL of the butanol–HCl reagent along with 0.1  mL were prepared and for each experiment, 75 μL plant of the ferric reagent was added to 0.5  mL of the tannin extract was added to 3.9  mL of 0.00463  g/L DPPH solu- extract diluted with 70% acetone. This amount of acetone tion. The final solution was protected with an aluminum was used to prevent exceeding the absorbance from 0.6 foil to prevent from light. After vigorous shaking of the (Porter et  al. 1985). The tubes were capped with a glass solution, it was left for 30  min (incubation period) at marble, then shaken using a Vortex and placed in a boil- ambient temperature; then the absorbance was read at ing water bath for 1  h. After cooling the tubes, their 517 nm. The percent of the remaining radicals at 30 min absorbance was recorded at 550  nm. The absorbance of was calculated using the following equation: the unheated mixture (considered as a suitable blank) A − A c s was subtracted from the absorbance of heated mixture. Antiradical activity(%) = × 100, The absorption band at 550 nm was used for calculation of the condensed tannins. If the development of pink where A and A are the absorbance of the control (con- c s color without heating happened, one heated blank will sist of solvent and DPPH) and the sample extract, respec- be used for each sample containing 0.5 mL of the extract, tively. Methanol and ascorbic acid were used as blank 3 mL of butanol and 0.1 mL of the ferric reagent (Seabra and positive control, respectively. All of the experiments et  al. 2018). The condensed tannins (% in dry matter) as were repeated for three times and their average was leucocyanidin equivalent were calculated using the fol- reported. The IC values were calculated by plotting the lowing equation (Ben Ahmed et al. 2017): inhibition percentage against the concentration of the extract (Muthukrishnan and Manogaran 2018). Differ - A (550 nm) × Dillution factor Condensed tannins = ent concentrations (1/10, 1/20, 1/30, 1/40) of the aqueous % Dry matter extract of C. heratensis were prepared by boiling 1  g of Given that the extract was prepared from 70% acetone, aerial parts of the plant in 10, 20, 30, 40 mL of deionized the dilution factor is calculated by the following formula water for 5  min. IC is the required initial concentra- (Ben Ahmed et al. 2017): tion of a selected antioxidant sample (plant extract in this study) to quench 50% of the free radicals in the reaction 0.5 mL mixture. Dilution factor = Volume of extract taken Results and discussion The dry matter was determined according to the fol - Fatty acid composition lowing procedure: Sample (5  g) was placed into an oven The fatty acid composition of oil is a major indicator of adjusted at 100–105  °C to complete drying and to reach oil quality; oils with high percentages of unsaturated fatty a constant weight. After cooling to room temperature, acids, mainly oleic and linoleic, are of high quality (Jokić weight of the dried sample was recorded and then,  % dry et al. 2013). The fatty acid composition of the C. heraten - matter was calculated by the following formula: Dry mat- sis seed extract was determined by GC analysis (Fig.  3). ter (%) = W /W × 100, where W and W are mass (g) of 2 1 2 1 The oil content of seeds can be varying from around 1% the sample before and after drying. in rice to more than 55% in Myristicaceae; the oil con- tent in C. heratensis seed extract was found 27.47%. The Antioxidant capacity analysis of fatty acid obtained from seed extract of C. Extraction heratensis revealed the presence of over 8 different com - Approximately, 0.15 g of dried parts of C. heratensis with pounds as shown in Fig.  3 and Table  1. The major com - 3  mL of 80% methanol was extracted at ambient tem- ponents were linoleic acid (67.8%), oleic acid (17.8%) and perature for 45  min under an ultrasonic wave. Then, the palmitic acid (8.7%). extracts were kept in the dark for 15  min and were cen- The results demonstrated that the amount of unsatu - trifuged for 15 min at 5000 rpm. After centrifugation, the rated fatty acids (87.8%) was higher than saturated fatty supernatants were collected. The extracts were kept at acids (12.2%). The ratio of unsaturated to saturated fatty 4 °C in dark until further analysis (yield of extraction: 7%). acids (U:S) was 7.20 in this oil. The fatty acid composition of C. heratensis seed with other edible vegetable oils was DPPH radical scavenging activity compared (Table  2). According to Table  2, the U/S ratio The ability of the C. heratensis extracts towards hydro - which is obtained for our plant was higher than olive and gen atom- or an electron donation was determined using corn oil. Therefore, considering that the higher ratio of the bleaching of the DPPH methanol solution as a rea- gent; then the antioxidant capacity of the extracts was Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 6 of 10 Phenolic composition Total phenolics content The results obtained from the determination of the total phenolic content of C. heratensis extracts are summa- rized in Table  3. As shown in Table  3, the total phenols content of the C. heratensis extract depends on harvest- ing time in various solvents. The concentration of total phenols of C. heratensis extracts was measured as gallic acid equivalents in mil- ligrams per gram of dry plant material weight (mg GAE/g DW). The results showed that in most cases, the quanti - ties of phenolic compounds of the plant were increased in different solvents during various developmental stages. The higher content was detected in acetone extract of Fig. 3 Chromatogram of fatty acids in C. heratensis seed extract. (YL aerial part (16.915  mg TAE/g DM) in S (fruiting stage) 6100 gas chromatograph system with a CBP5 column (Shimadzu 30 m × 0.32 mm × 0.25 mm) equipped with an FID detector) and the lowest total phenolic level was seen in ether extract of the root (0.048  mg GAE/g DM) in S (Pre- flowering stage). Also, the highest amount (19.0377  mg U:S for oil is safer for the heart and blood vessels, it pro- TAE/g DM) was observed in the acetone extract of the poses that these seeds are examined for feed intake. seed. In general, the highest total phenolic content was More importantly, the amount of linolenic acid, as an detected in aerial parts and extraction by acetone has a essential fatty acid in human food nutrition, was found maximum output. 67.8%, which is higher than the most vegetable oils (Table 2). Table 1 Fatty acid composition of seed oil of the C. heratensis seed Entry Fatty acid Type Retention time (min) Content (%) 1 Myristic acid ( C ) Saturated 2.383 0.2 14:0 2 Palmitic acid (C ) Saturated 2.867 8.7 16:0 3 Stearic acid (C ) Saturated 3.717 3.1 18:0 4 Arachidic acid (C ) Saturated 5.117 0.2 20:0 5 Palmitoleic acid (C ) Unsaturated (ω − 7) 3.140 0.2 16:1 cis 6 Oleic acid (C ) Unsaturated (ω − 9) 4.113 17.8 18:1 7 Linoleic acid ( C ) Unsaturated (ω − 6) 4.867 67.8 18:2 8 α-Linoleic acid (C ) Unsaturated (ω − 3) 5.737 2.0 18:3 Saturated carbon: unsaturated carbon Table 2 Comparison of  fatty acids composition of  C. heratensis seed with  the  various vegetable oils (Katragadda et  al. 2010) Type Saturated Mono unsaturated Total poly unsaturated U/S Linoleic acid (%) Coconut 91.00 6.00 3.00 0.1 2 Corn 12.95 27.58 54.68 6.35 59 Cottonseed 25.90 17.80 51.90 2.69 54 Olive 14 72 14 6.14 3.5–21 Soybean 15.65 22.78 57.74 5.14 51 Sunflower (60% linoleic) 10.1 45.4 40.1 8.46 10 Sunflower (70% Oleic) 9.86 83.69 3.80 8.87 – Seed of C. heratensis 12.2 18 69.8 7.20 67.8 Unsaturated/saturated fatty acids Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 7 of 10 Table 3 The amounts of phenolic compounds in the tissues extracts of the C. heratensis (mg GAE/g DM ) Sample Harvesting time H O n-BuOH EtOAc Chloroform Ether Acetone Aerial parts S 0.730 1.605 0.455 0.405 0.270 10.5426 S 0.866 4.596 0.445 0.199 0.316 7.1247 S 2.934 7.558 0.528 0.139 0.425 16.9146 Root S 3.394 0.165 0.282 0.057 0.048 1.8299 S 1.159 0.272 0.207 0.080 0.079 1.6642 S 1.046 0.355 0.369 0.218 1.009 2.7589 Seed – 1.054 0.758 0.435 0.190 0.452 19.0377 mg gallic acid equivalents per gram of dry matter As tannic acid equivalents (TAEs) Table 4 The amounts of flavonoids compounds in the tissues extracts of the C. heratensis (mg RE/g DM ) Sample Harvesting time H O n-BuOH EtOAc Chloroform Ether Aerial parts S 0.405 2.256 0.514 0.193 0.350 S 0.389 2.956 0.504 0.136 0.399 S 1.417 4.444 0.541 0.113 0.387 Root S 0.476 0.517 0.156 0.020 0.003 S 0.477 0.221 0.483 0.103 0.023 S 0.786 0.324 0.280 0.152 0.158 Seed – 0.134 0.098 0.074 0.073 0.244 Rutin equivalents in milligrams per gram of dry plant material weight results showed that the amount of flavonoid compounds of the plant was increased in different solvents at differ - ent stages of growth (Table 4). The highest flavonoids content was detected in n-BuOH extract of the aerial part (4.444  mg RE/g DM) in S (fruiting stage) and the lowest content was seen in ether extract of the root (0.003  mg RE/gr DM) in S (Pre flowering stage) (Table  4). In general, similar to phe- nolic compounds, the highest content of flavonoids was detected in the aerial part at fruiting stage. Also, extrac- tion by n-BuOH and acetone provides a maximum out- put, respectively. Anthocyanin content As shown in Fig.  4, concentration of anthocyanin of C. heratensis extract was measured as millimole per gram of wet plant material weight (mmol/g WM). The Fig. 4 The amounts of anthocyanin compounds in the extracts of results showed that in the primary stages, the anthocya- tissues (mmol/g WM). *mmol anthocyanin per gram of wet plant nin amount increased and at the flowering stage (S ), it material weight reached to 0.48  mmol/g WM, and then decreased. In general, these results showed that extraction at flowering stage has maximum output due to flowers. Also, seed of Flavonoids content the plant demonstrated 0.39  mmol/g WM anthocyanin The concentrations of flavonoids of C. heratensis extract which is higher than aerial parts of the plant. were determined as rutin equivalents in milligrams per gram of dry plant material weight (mg RE/g DW). The Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 8 of 10 of aerial part in S (fruiting stage) including total tan- nins (12.2312  mg TAE/g DM) and proanthocyanidin (4.0856 mg TAE/g DM). The lowest amount was seen in the extract of root in S equal to 0.9757, 0.0226 mg TAE/g DM for total and condensed tannin, respectively. In gen- eral, similar to other identified compounds, the highest contents were detected in the seed. The differential accumulation of phenolic compounds in C. heratensis extracts at the different stages could be related to physiological changes during growth in response to environmental stress. The season, sunlight duration, UV radiation, and temperature are known parameters that affect the plant metabolism, since some compounds may be accumulated at a particular period to respond to environmental changes (Generalić et al. 2011; Negrão et al. 2017; Lu et al. 2017). Determination of antioxidant capacities Antioxidant activity of the C. heratensis extracts was determined using DPPH radical scavenging assay. This assay is based on hydrogen/electron transfer from a given antioxidant to DPPH. The DPPH has a strong absorption band at λ = 517  nm with deep purple max color, whereas the redacted product is yellowish with- out any absorption band (Lu et  al. 2017). Although Fig. 5 The amounts of tannin (blue columns) and proanthocyanidin DPPH-H is the final product, other complexes could (yellow curves) and seed (yellow column) compounds in the tissues acetone extracts of the C. heratensis (mg TAE/g DM).*Tannin/ be formed by reacting DPPH and oxidized intermedi- proanthocyanidin ates in the extract and generate high molecular weight polymers (Pedan et  al. 2016). The results from anti - oxidant property of the extract revealed the radical scavenging of the aerial and root extract of C. herat- ensis. Figure  6 shows the curve of inhibition percent- age of the extract versus extract concentration as I C (mg/mL). As shown in the figure, the extract of aerial parts (11.92 mg/mL) exhibited higher scavenging activ- ity than the roots extract (63.44 mg/mL). According to the definition of IC , the lower IC value refers to a 50 50 stronger antioxidant activity in a testing sample. Thus, aerial parts of the plant have higher antioxidant activity. Figure  7 shows the UV–Vis spectra of DPPH solution before and after the addition of the aerial C. heratensis extract. The spectra clearly demonstrated the antioxidant Fig. 6 Linear relationship between inhibition percentage of the extract and extract concentration activity of the extract with the complete elimination of the absorption band at λ = 517 nm for DPPH (Fig. 7a). max Figure 7b shows UV–Vis spectra recorded for aerial parts of C. heratensis extract. Electronic spectra of the extract Tannin and proanthocyanidin contents showed one absorption band at ~305 nm (Fig. 7b). The concentrations of total and condensed tannins (proanthocyanidins) in the extracts of C. heratensis (mg TAE/g DM) are shown in Fig. 5. The results showed that Conclusions the amount of tannins in aerial parts of the plant was The C. heratensis from Capparaceae family is found increased during various developmental stages from mainly in the eastern region (Birjand) of Iran. The seed S to S . The highest content was detected in extract oil of this plant (27.47%) is a rich source of unsaturated 1 4 Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 9 of 10 Fig. 7 a Antiradical activity of the aerial extract of C. heratensis (0.1 g/mL) over quenching 2,2′-diphenylpicryl-1-hydrazyl (DPPH) radicals at room temperature. b UV–visible spectra of aerial part of C. heratensis extract Ethics approval and consent to participate fatty acids (87.8%), especially linoleic acid (67.8%) and All the authors have read and agreed the ethics for publishing the manuscript. oleic acid (17.8%). The highest total amounts of phenolic (16.915 mg TAE/g DM), flavonoids (4.444 mg RE/g DM), Funding No funding was received for this article. total tannins (12.231  mg TA/gr DM) and proanthocya- nidins (4.086  mg TA/g DM) components were detected Publisher’s Note in extract of aerial parts in fruiting stage and seed of the Springer Nature remains neutral with regard to jurisdictional claims in pub- plant. Also, the most amount of anthocyanin (0.48 mmol/ lished maps and institutional affiliations. gr WM) was observed in flowering stage. Harvesting C. Received: 13 November 2018 Accepted: 25 January 2019 heratensis at the fruiting stage and extracting of aerial parts of plant or seeds by acetone give the most amounts of bioactive compounds. C. heratensis extract is a good natural antioxidant that could be added as a chemical References basis in food and therapeutics. Alu’datt MH, Rababah T, Alhamad MN, Al-Mahasneh MA, Almajwal A, Gammoh S, Ereifej K, Johargy A, Alli I (2017) A review of phenolic compounds in oil-bearing plants: distribution, identification and occurrence of phenolic Abbreviations compounds. Food Chem 218:99–106 Cleome heratensis: C. heratensis; GC: gas chromatography; FA: fatty acids; PUFA: Ambriz-Pérez DL, Leyva-López N, Gutierrez-Grijalva EP, Heredia JB (2016) poly unsaturated fatty acid; FC: folin–ciocalteau’s; PVP: polyvinyl pyrrolidone; Phenolic compounds: natural alternative in inflammation treatment. a DPPH: 2,2′-diphenylpicryl-1-hydrazyl; DM: dry matter; RE: rutin equivalents; review. Cogent Food Agric 2:1131412 TAE: tannic acid equivalents; GAE: gallic acid equivalents. Asemaneh T, Ghaderian SM, Crawford SA, Marshall AT, Baker AJM (2006) Cel- lular and subcellular compartmentation of Ni in the Eurasian serpentine Authors’ contributions plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome MAN and AA design the study. SB and MK performed the research experi- heratensis (Capparaceae). Planta 225:193–202 ments, acquired the data and wrote the manuscript. All authors were involved Azmir J, Zaidul ISM, Rahman MM, Sharif KM, Mohamed A, Sahena F, Jahurul in the analysis and approved the final manuscript of publication. MAN and SB MHA, Ghafoor K, Norulaini NAN, Omar AKM (2013) Techniques for extrac- interpreted the results. All authors read and approved the final manuscript. tion of bioactive compounds from plant materials: a review. J Food Eng 117:426–436 Belch JJ, Hill A (2000) Evening primrose oil and borage oil in rheumatologic Acknowledgements conditions. Am J Clin Nutr 71:352s–356s The authors are thankful to Research Council of University of Birjand for pro- Ben Ahmed Z, Yousfi M, Viaene J, Dejaegher B, Demeyer K, Mangelings D, viding all the necessary facilities to carry out the research work. Vander Heyden Y (2017) Seasonal, gender and regional variations in total phenolic, flavonoid, and condensed tannins contents and in antioxidant Competing interests properties from Pistacia atlantica ssp. leaves. Pharm Biol 55:1185–1194 The authors declare that they have no competing interests. Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30 Availability of data and materials Chandra S, Khan S, Avula B, Lata H, Yang MH, ElSohly MA, Khan IA (2014) All data that are relevant to the study are reported within the article. Assessment of total phenolic and flavonoid content, antioxidant properties, and yield of aeroponically and conventionally grown leafy Consent for publication vegetables and fruit crops: a comparative study. Evid Based Complement The authors approved the consent for publishing the manuscript. Altern Med 2014:1–9 Nasseri et al. Bioresour. Bioprocess. (2019) 6:5 Page 10 of 10 de Koning S, van der Meer B, Alkema G, Janssen HG, Udo A (2001) Automated Narendhirakannan RT, Subramanian S, Kandaswamy M (2007) Evaluation of determination of fatty acid methyl ester and cis/trans methyl ester com- antioxidant potential of Cleome gynandra L. leaf extract on the compo- position of fats and oils. J Chromatogr A 922:391–397 nents of the lymphoid organs in adjuvant induced arthritis in rats. Int J de Souza Schneider RC, Baldissarelli VZ, Trombetta F, Martinelli M, Caramão EB Biol Chem 1:1–10 (2004) Optimization of gas chromatographic–mass spectrometric analy- Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses sis for fatty acids in hydrogenated castor oil obtained by catalytic transfer of plants to salinity stress. Ann Bot 119:1–11 hydrogenation. Anal Chim Acta 505:223–226 Nile SH, Nile AS, Keum YS (2017) Total phenolics, antioxidant, antitumor, and Embuscado ME (2015) Spices and herbs: natural sources of antioxidants–a enzyme inhibitory activity of Indian medicinal and aromatic plants mini review. J Funct Foods 18:811–819 extracted with different extraction methods. 3 Biotech 7:76 Generalić I, Skroza D, Ljubenkov I, Katalinić A, Burčul F, Katalinić V (2011) Influ- Oksman-Caldentey KM, Inze D (2004) Plant cell factories in the post-genomic ence of the phenophase on the phenolic profile and antioxidant proper - era: new ways to produce designer secondary metabolites. Trends Plant ties of Dalmatian sage. Food Chem 127:427–433 Sci 9:433–444 Ghaderian SM, Baker AJM (2007) Geobotanical and biogeochemical reconnais- Pakdaman N, Ghaderian SM, Ghasemi R, Asemaneh T (2013) Eec ff ts of calcium/ sance of the ultramafics of Central Iran. J Geochem Explor 92:34–42 magnesium quotients and nickel in the growth medium on growth and Ghorbani A (2017) Mechanisms of antidiabetic effects of flavonoid rutin. nickel accumulation in Pistacia atlantica. J Plant Nutr 36:1708–1718 Biomed Pharmacother 96:305–312 Pedan V, Fischer N, Rohn S (2016) An online NP-HPLC-DPPH method for the Gupta NK, Dixit VK (2009) Evaluation of hepatoprotective activity of Cleome determination of the antioxidant activity of condensed polyphenols in viscosa Linn. extract. Indian J Pharmacol 41:36–40 cocoa. Food Res Int 89:890–900 Haminiuk CW, Maciel GM, Plata-Oviedo MS, Peralta RM (2012) Phenolic com- Picot MC, Zengin G, Mollica A, Stefanucci A, Carradori S, Mahomoodally M pounds in fruits–an overview. Int J Food Sci Technol 47:2023–2044 (2017) In vitro and in silico studies of mangiferin from Aphloia theiformis Hara M, Oki K, Hoshino K, Kuboi T (2003) Enhancement of anthocyanin on key enzymes linked to diabetes type 2 and associated complications. biosynthesis by sugar in radish (Raphanus sativus) hypocotyl. Plant Sci Med Chem 13:633–640 164:259–265 Porter LJ, Hrstich LN, Chan BG (1985) The conversion of procyanidins and Hosseinian FS, Beta T (2007) Saskatoon and wild blueberries have higher prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230 anthocyanin contents than other Manitoba berries. J Agric Food Chem Prior RL, Wu X (2006) Anthocyanins: structural characteristics that result in 55:10832–10838 unique metabolic patterns and biological activities. Free Radical Res Jain V, Murugananthan G, Deepak M, Viswanatha GL, Manohar D (2011) Isolation 40:1014–1028 and standardization of various phytochemical constituents from metha- Puchchakayala G, Podili L, Bobbala D, Thirupathi K, Boini K, Yellu N, Bobbala R, nolic extracts of fruit rinds of Punica granatum. Chin J Nat Med 9:414–420 Gottemukkala K, Pragada R (2008) Antinociceptive and anti-inflammatory Jokić S, Sudar R, Svilović S, Vidović S, Bilić M, Velić D, Jurković V (2013) Fatty acid effects of Cleome chelidonni linn. roots in experimental animals. Pharma- composition of oil obtained from soybeans by extraction with supercriti- cogn Mag 4:32–36 cal carbon dioxide. Czech J Food Sci 31:116–125 Quispe C, Viveros-Valdez E, Schmeda-Hirschmann G (2012) Phenolic constitu- Katragadda HR, Fullana A, Sidhu S, Carbonell-Barrachina ÁA (2010) Emissions ents of the Chilean herbal tea Fabiana imbricata R. et P. Plant Foods Hum of volatile aldehydes from heated cooking oils. Food Chem 120:59–65 Nutr 67:242–246 Kaurinovic B, Popovic M, Vlaisavljevic S, Trivic S (2011) Antioxidant capacity Ramadan MF, Sharanabasappa G, Seetharam YN, Seshagiri M, Moersel JT of Ocimum basilicum L. and Origanum vulgare L. extracts. Molecules (2006) Characterisation of fatty acids and bioactive compounds of kach- 16:7401–7414 nar (Bauhinia purpurea L.) seed oil. Food Chem 98:359–365 Leventhal LJ, Boyce EG, Zurier RB (1993) Treatment of rheumatoid arthritis with Rauter AP, Dias C, Martins A, Branco I, Neng NR, Nogueira JM, Goulart M, Silva gammalinolenic acid. Ann Intern Med 119:867–873 FV, Justino J, Trevitt C, Waltho JP (2012) Non-toxic Salvia sclareoides Brot. Lu Y, Wu N, Fang Y, Shaheen N, Wei Y (2017) An automatic on-line 2, 2-diphe- extracts as a source of functional food ingredients: phenolic profile, anti- nyl-1-picrylhydrazyl-high performance liquid chromatography method oxidant activity and prion binding properties. Food Chem 132:1930–1935 for high-throughput screening of antioxidants from natural products. J Seabra IJ, Chim RB, Salgueiro P, Braga ME, de Sousa HC (2018) Influence Chromatogr A 1521:100–109 of solvent additives on the aqueous extraction of tannins from pine Ma H, Xu J, DaSilva NA, Wang L, Wei Z, Guo L, Johnson SL, Lu W, Xu J, Gu Q, bark: potential extracts for leather tanning. J Chem Technol Biotechnol Seeram NP (2017) Cosmetic applications of glucitol-core containing gal- 93:1169–1182 lotannins from a proprietary phenolic-enriched red maple (Acer rubrum) Sierra-Cantor JF, Guerrero-Fajardo CA (2017) Methods for improving the cold leaves extract: inhibition of melanogenesis via down-regulation of flow properties of biodiesel with high saturated fatty acids content: a tyrosinase and melanogenic gene expression in B16F10 melanoma cells. review. Renew Sustain Energy Rev 72:774–790 Arch Dermatol Res 309:265–274 Singh H, Mishra A, Mishra AK (2018) The chemistry and pharmacology of Ma H, Johnson SL, Liu W, DaSilva NA, Meschwitz S, Dain JA, Seeram NP (2018) Cleome genus: a review. Biomed Pharmacother 101:37–48 Evaluation of polyphenol anthocyanin-enriched extracts of blackberry, black Smith MA, Dauk M, Ramadan H, Yang H, Seamons LE, Haslam RP, Beaudoin F, raspberry, blueberry, cranberry, red raspberry, and strawberry for free radical Ramirez-Erosa I, Forseille L (2013) Involvement of Arabidopsis ACYL- scavenging, reactive carbonyl species trapping, anti-glycation, anti-β-amyloid COENZYME A DESATURASE-LIKE2 (At2g31360) in the biosynthesis of the aggregation, and microglial neuroprotective effects. Int J Mol Sci 19:461–480 very-long-chain monounsaturated fatty acid components of membrane Maia IRDO, Trevisan MTS, Silva MGDV, Breuer A, Owen RW (2017) Content of lipids. Plant Physiol 161:81–96 total phenolic compounds, flavonoids and tannins in methanol extracts Sreelatha S, Padma PR (2009) Antioxidant activity and total phenolic content of the genus Senna Mill. from the northeast of Brazil and evaluation of of Moringa oleifera leaves in two stages of maturity. Plant Foods Hum antioxidant capacity. J Pharmacogn Phytochem 6:1321–1325 Nutr 64:303 Makkar HP, Blümmel M, Borowy NK, Becker K (1993) Gravimetric determination Williams LAD, Vasques E, Reid W, Porter R, Kraus W (2003) Biological activities of tannins and their correlations with chemical and protein precipitation of an extract from Cleome viscosa L. (Capparaceae). Naturwissenschaften methods. J Sci Food Agric 61:161–165 90:468–472 Mocan A, Zengin G, Crişan G, Mollica A (2016) Enzymatic assays and molecular Xiao L, Mjøs SA, Haugsgjerd BO (2012) Efficiencies of three common lipid modeling studies of Schisandra chinensis lignans and phenolics from fruit extraction methods evaluated by calculating mass balances of the fatty and leaf extracts. J Enzyme Inhib Med Chem 31:200–210 acids. J Food Compos Anal 25:198–207 Mollica A, Costante R, Akdemir A, Carradori S, Stefanucci A, Macedonio G, Zhu L, Chen J, Tan J, Liu X, Wang B (2017) Flavonoids from Agrimonia pilosa Ceruso M, Supuran CT (2015) Exploring new Probenecid-based carbonic Ledeb: free radical scavenging and DNA oxidative damage protection anhydrase inhibitors: synthesis, biological evaluation and docking stud- activities and analysis of bioactivity-structure relationship based on ies. Bioorg Med Chem 23:5311–5318 molecular and electronic structures. Molecules 22:195–206 Muthukrishnan S, Manogaran P (2018) Phytochemical analysis and free radical scavenging potential activity of Vetiveria zizanioides Linn. J Pharmacogn Phytochem 7:1955–1960

Journal

"Bioresources and Bioprocessing" – Springer Journals

Published: Dec 1, 2019

Keywords: Biochemical Engineering; Environmental Engineering/Biotechnology; Industrial and Production Engineering

There are no references for this article.