The number of plant species considered edible in the world is about 30,000; however, very few of them are used to fulfil human food requirements (Shaheen et al., 2017). To this aim, the rich biodiversity and abundance of wild edible plants represent a precious resource still underutilized, and that can be used as food sources (Shaheen et al., 2017; Ceccanti et al., 2018; Brito et al., 2021). In this framework, there are numerous plant species with edible flowers and studies ongoing to explore their potential in the human diet as food, supplements or additives (Loizzo et al., 2016; Fernandes et al., 2017; Mulík and Ozuna, 2020). Eating flowers is a legacy of many cultures that have been using flowers in their food traditions during centuries, but nowadays edible flowers can also represent a source of nutrients and phytochemicals with health benefits. Despite this, only a small portion of species has been explored to date with this aim, such as
The positive health effects of edible flowers are ascribed to their chemical composition, which are rich in phytochemicals with bioactive properties, such as vitamins (Fernandes et al., 2017; Scariot et al., 2018; Pires et al., 2019; Zhao et al., 2019; Mulík and Ozuna, 2020; Takahashi et al., 2020; Zheng et al., 2021). Vitamin C is a strong antioxidant that scavenges radicals, thus neutralizing oxidative stress and plays an important role in human metabolism, representing a fundamental supplement in the diet (Fascella et al., 2019; Caritá et al., 2020). Interesting results on the vitamin C content in flowers have been recorded in plants of Zingiberaceae (Rachkeeree et al., 2018),
Polyphenols in foodstuffs are frequently evaluated as a whole group with colorimetric assays; however, the individual quantification of phenolic compounds is essential to understand the bioactivity potential and properties of food (Fernandes et al., 2017; Peìrez-Jimeìnez et al., 2010; Skrajda-Brdak et al., 2020), especially when studying unexplored or underutilized edible flowers. So far, wide variability in terms of total polyphenols and antioxidant activity has been recorded in edible flowers from Asian countries, where flowers are commonly consumed as food or medicine, for example,
The high species richness of European biogeographic regions gives interesting perspectives in the use of wild edible flowers as human foodstuff. Particularly, North-Western Italy, characterized by a wide variety of habitats and vegetation communities, harbours a total of 4,020 taxa (Bartolucci et al., 2018).
In this study, we explored flowers from wild plants that grow spontaneously in self-maintaining populations in semi-natural habitats of North-Western Italy. A total of 26 species (including 22 wild and four commonly cultivated species) were analysed to evaluate their potential as sources of bioactive compounds, through the assessment of total polyphenol content (TPC), antioxidant activity, phenolic profiles and vitamin C content.
An extended area in North-Western Italy was explored (including Aosta Valley and Piedmont administrative regions), collecting flowers from 22 wild species (Table 1). Wild species were selected to explore all altitudinal belts in the studied area, including plain, colline, montane and alpine belts, and to investigate many vegetation communities. Aiming at this, each species was associated with the corresponding phytosociological optimum (at class level, according to Aeschimann et al., 2004), which were then pooled in eight different vegetation communities characterized by homogeneous ecological features: (i) nutrient-rich grasslands (including
List of the 22 wild and 4 cultivated species collected and analysed in the study, with references on their botanical family, vegetation community, food and/or medicinal uses, month, site (WGS84/32N system) and soil (USDA soil taxonomy; the bedrock type is provided in brackets: C, calcareous; S, siliceous)* of sampling in 2017.
Species | Botanical family | Vegetation community | Reference of flower use |
Flower sampling |
Soil type | ||||
---|---|---|---|---|---|---|---|---|---|
Food | Medicinal | Month | Longitude | Latitude | |||||
Amaryllidaceae | Woodlands | Lim (2014a) | Sobolewska et al. (2015) | April | 7.878 | 45.490 | Eutrudept (S) | ||
Asteraceae | Nutrient rich grasslands | Lim (2014a) | Lim (2014a) | March | 7.592 | 45.065 | Hapludalf (S) | ||
Asteraceae | Ruderal communities | Lim (2014a) | Lim (2014a) | May | 7.896 | 45.475 | Eutrudept (S) | ||
Asteraceae | Ruderal communities | Lim (2014a) | Street et al. (2013) | June | 7.843 | 45.192 | Dystrudept (S) | ||
Caryophyllaceae | Dry grasslands | - | Palma (1964) | June | 7.219 | 45.301 | Udifluvent (S) | ||
Caryophyllaceae | Nutrient poor grasslands | - | - | July | 7.122 | 44.391 | Eutrocryept (C) | ||
Liliaceae | Woodlands | - | - | March | 7.371 | 45.157 | Dystrudept (C) | ||
Geraniaceae | Edges | - | - | June | 7.186 | 45.300 | Dystrudept (S) | ||
Lamiaceae | Dry grasslands | Lim (2014b) | Lim (2014b) | June† | -† | -† | -† | ||
Asteraceae | Nutrient rich grasslands | Lim (2014a) | Prinsloo et al. (2018) | April | 7.592 | 45.065 | Hapludalf (S) | ||
Lamiaceae | Wetlands | Lim (2014b) | Alvarado (2018) | September | 7.485 | 45.120 | Hapludalf (S) | ||
Paeoniaceae | Edges | Lim (2014b) | - | April | 7.344 | 45.097 | Udorthent (S) | ||
Primulaceae | Woodlands | Lim (2014b) | Apel et al. (2017) | May | 6.802 | 44.968 | Eutrudept (C) | ||
Primulaceae | Woodlands | Lim (2014b) | Tuttolomondo et al. (2014) | March | 7.379 | 45.145 | Dystrudept (C) | ||
Fabaceae | Woodlands | Lim (2014a) | Jarić et al. (2015) | May | 7.593 | 45.065 | Hapludalf (S) | ||
Rosaceae | Shrublands | Lim (2014b) | Nemati et al. (2015) | May | 7.677 | 45.715 | Udorthent (S) | ||
Rosaceae | Woodlands | - | - | June | 7.192 | 45.301 | Dystrudept (S) | ||
Lamiaceae | Dry grasslands | Kucekova et al. (2013) | Kucekova et al. (2013) | May | 7.603 | 45.036 | Udifluvent (S) | ||
Adoxaceae | Shrublands | Lim (2014a) | Młynarczyk et al. (2018) | May | 7.593 | 45.064 | Hapludalf (S) | ||
Asteraceae | Nutrient rich grasslands | Lim (2014a) | Lim (2014a) | March | 7.593 | 45.064 | Hapludalf (S) | ||
Fabaceae | Nutrient poor grasslands | Abbet et al. (2014) | Agelet and Vallès (2001) | July | 7.122 | 44.390 | Eutrocryept (C) | ||
Violaceae | Ruderal communities | Lim (2014b) | Lim (2014b) | March | 7.591 | 45.065 | Hapludalf (S) | ||
Boraginaceae | Cultivated | Lim (2014a) | Gupta and Singh (2010) | May | -§ | -§ | -§ | ||
Asteraceae | Cultivated | Lim (2014a) | Lim (2014a) | May | -§ | § | -§ | ||
Asteraceae | Cultivated | Lim (2014a) | Lim (2014a) | July | -§ | § | -§ | ||
Tropaeolaceae | Cultivated | Lim (2014b) | Lim (2014b) | May | -§ | § | -§ |
I.P.L.A., Regione Piemonte (2007); Regione Autonoma Valle d’Aosta (2018).
Species already evaluated under the European Novel Food Regulation (Regulation EU 2015/2283), not considered novel food.
Flowers sampled from cultivated plants in the nursery F.lli Gramaglia.
Fresh flower sample was grinded in a mortar using liquid nitrogen and then stored at −80°C until the preparation of the extracts that was performed with ultrasound-assisted extraction, a high reproducible, efficient, simple, time- and solvent-saving methodology. The solid–liquid extraction using organic solvents and water mixture is among the most common methodologies to extract polyphenols (Pires et al., 2019; Takahashi et al., 2020); thus flower powder (1 g) was extracted with 50 mL of a water:methanol solution (1:1) at room temperature with an ultrasound extractor (Sarl Reus, Drap, France) at 23 kHz for 15 min (Demasi et al., 2020). First, the solution was filtered with one layer of filter paper (Whatman No. 1, Maidstone, UK) and afterwards using a 0.45 μm PVDF syringe filter (CPS Analitica, Milano, Italy). The extracts were stored at −20°C until the performance of colorimetric and chromatographic analyses.
The TPC in flower extracts and the evaluation of their antioxidant activity were performed using colorimetric methods, reading the absorbance with the spectrophotometer Cary 60 UV-Vis (Agilent, Santa Clara, CA, USA). In particular, the TPC was analysed using the Folin–Ciocalteu method (Slinkard and Singleton, 1977; Sánchez-Rangel et al., 2013; Demasi et al., 2020). An amount of 200 μL of flower extract were mixed with 1,000 μL of diluted (1:10) Folin–Ciocalteu reagent. The samples were left in the dark at room temperature for 10 min, then adding 800 μL of Na2CO3 (7.5%). After 30 min in the dark at room temperature, absorbance was read at 765 nm, expressing results as mg of gallic acid equivalents (GAE) per 100 g of FW (mg GAE · 100 g−1). The antioxidant activity was evaluated through three different assays: the ferric reducing antioxidant power (FRAP) method (Benzie and Strain, 1998; Demasi et al., 2020), the 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay (Wong et al., 2006) and the 2,2′-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid (ABTS) assay (Tawaha et al., 2007; Dudonneì et al., 2009). In the FRAP method, 30 μL of flower extract were mixed with 90 μL of deionized water and 900 μL of FRAP reagent. This was constituted of a buffer solution at pH 3.6 (C2H3NaO2 + C2H4O2 in water), 2,4,6-tripyridyltriazine (TPTZ, 10 mM in HCl 40 mM) and FeCl3·6H2O (20 mM). The samples were placed at 37°C for 30 min and absorbance was read at 595 nm. The results were expressed as mill moles of ferrous iron (Fe2+) equivalents per kilogram of FW (mmol Fe2+ · kg−1). In the DPPH assay, 40 μL of flower extract was mixed with 3 mL of DPPH radical solution. The samples were left in the dark at room temperature for 30 min and absorbance was read at 515 nm. In the ABTS assays, 30 μL of flower extract was mixed with 2 mL of ABTS radical solution. The samples were left in the dark at room temperature for 10 min and absorbance was read at 734 nm. Both DPPH and ABTS results were expressed as micro moles of Trolox Equivalents (TE) per 1 g of FW (μmol TE · g−1).
The bioactive compounds present in the extracts of edible flowers were determined using High-Performance Liquid Chromatography (HPLC) with Diode Array Detection (DAD) (Agilent 1200, Agilent Technologies, Santa Clara, CA, USA). The separation of compounds was obtained with a Kinetex C18 column (4.6 × 150 mm, 5 μm, Phenomenex, Torrance, CA, USA) and different mobile phases, according to previous validated methodology (Table 2; Caser et al., 2019; Donno et al., 2019). The identification of compounds was made by comparison with retention times and UV spectra of analytical standards and the quantification was achieved using calibration curves at the same chromatographic conditions. The following bioactive compounds were determined: phenolic acids (cinnamic acids: caffeic, chlorogenic, coumaric and ferulic acid; benzoic acids: ellagic and gallic acid); flavonols (hyperoside, isoquercitrin, quercetin, quercitrin and rutin); flavanols (catechin and epicatechin) and vitamin C. The results are expressed as mg · 100 g−1 of fresh flower.
Mobile phases, elution conditions and wavelength used to detect the five classes of compounds with HPLC analysis.
Class of compounds | Mobile phase | Elution conditions | Wavelength (nm) |
---|---|---|---|
Cinnamic acids and flavonols | A: 10 mM KH2PO4/H3PO4, pH = 2.8 |
5%B to 21%B in 17 min + 21%B in 3 min (2 min conditioning time); flow: 1.5 mL min−1 | 330 |
Benzoic acids and flavanols | A: H2O/CH3OH/HCOOH |
3%B to 85%B in 22 min + 85%B in 1 min (2 min conditioning time); flow: 0.6 mL min−1 | 280 |
Vitamin C | A: 5 mM C16H33N(CH3)3Br/50 mM |
Isocratic, ratio of phase A and B: 95:5 in 10 min (5 min conditioning time); flow: 0.9 mL min−1 | 261, 348 |
HPLC, High-Performance Liquid Chromatography.
Raw data of TPC, FRAP, DPPH, and ABTS, were transformed in standard scores and averaged to obtain the Relative Antioxidant Capacity Index (RACI) (Sun and Tanumihardjo, 2007). Then, mean differences between species concerning dry matter content, spectrophotometric data (TPC, FRAP, DPPH, ABTS, RACI) and chromatographic data (class of compounds and single compounds) were analysed using generalized linear models (GLMs) with Gaussian or gamma distribution according to the distribution of data. Tukey’s post hoc-test with Bonferroni’s adjustment was used to identify homogeneous groups of means when
The flowers of the selected species showed highly significant differences in each of the recorded parameters (Table 3), including the content of dry matter, which ranged from 8.9% in
Dry matter, TPC and antioxidant activity (FRAP, DPPH and ABTS assays) in the 26 edible flowers.
Species | Dry matter (%) | TPC (mg GAE · 100 g−1) | Antioxidant activity | ||
---|---|---|---|---|---|
FRAP (mmol Fe2+ · kg−1) | DPPH (mmol TE · g−1) | ABTS (mmol TE · g−1) | |||
10.2 jk | 184.4 k | 4.2 j | 7.6 kl | 0.7 m | |
16.9 ef | 396.3 gi | 81.6 cf | 24.3 i | 13.4 hj | |
26.4 b | 378.5 hi | 68.3 df | 23.6 i | 17.8 fh | |
17.3 ef | 618.4 df | 138.4 ad | 69.2 f | 26.9 d | |
27.8 ab | 936.3 bd | 222.2 ab | 81.1 ef | 33.6 c | |
21.2 cd | 752.8 ce | 176.1 ac | 106.5 c | 24.3 de | |
15.1 fh | 364.3 hi | 53.5 eg | 20.4 ik | 14.4 hj | |
12.8 i | 1,267.8 ab | 267.0 ab | 152.9 b | 55.2 a | |
31.2 a | 396.0 gi | 89.5 ce | 14.8 il | 14.0 hj | |
17.0 ef | 448.8 fi | 44.3 eh | 20.9 ik | 10.8 ij | |
22.3 c | 1,061.7 bc | 256.0 ab | 86.7 de | 42.5 b | |
13.9 gi | 1,930.5 a | 303.8 a | 226.2 a | 55.3 a | |
18.8 de | 1,044.9 bc | 230.1 ab | 97.1 cd | 38.5 bc | |
9.8 jk | 602.9 dg | 127.4 bd | 41.7 gh | 21.5 df | |
12.9 i | 203.8 jk | 15.7 i | 4.5 l | 2.4 m | |
16.7 ef | 1,396.6 ab | 257.5 ab | 146.2 b | 55.6 a | |
21.6 cd | 1,773.7 a | 253.8 ab | 154.3 b | 55.7 a | |
17.7 ef | 314.7 ij | 38.9 fh | 8.9 jl | 9.0 jl | |
16.8 ef | 508.7 eh | 78.8 cf | 28.5 hi | 18.3 fh | |
16.5 ef | 159.4 k | 13.0 i | 7.7 kl | 3.3 lm | |
10.0 jk | 464.6 fi | 91.5 ce | 50.3 gh | 20.3 eg | |
13.0 hi | 428.4 fi | 66.1 dg | 22.6 ij | 15.6 gi | |
15.3 fg | 163.4 k | 29.7 gi | 22.8 i | 3.7 km | |
13.7 gi | 189.6 k | 22.6 hi | 3.6 l | 9.2 jk | |
10.7 j | 470.8 fi | 143.9 ad | 44.1 gh | 23.0 df | |
8.9 k | 355.8 hi | 45.3 eh | 14.8 il | 12.8 hj | |
*** | *** | *** | *** | *** |
Data are expressed on a fresh-weight basis, except for dry matter. The level of statistical significance is given (***
ABTS, 2,2′-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid; DPPH, 2,2-diphenyl-1-picrylhydrazyl; FRAP, ferric reducing antioxidant power; GAE, gallic acid equivalents; TPC, total polyphenol content; TE, trolox equivalents.
Flowers sampled from cultivated plants.
The highest amounts of TPC (Table 3) were detected in
Despite showing slight differences in antioxidant activity ranking, depending on the assay used (Table 3), the results showed that
Different analytical assays are necessary to explain the antioxidant potential of matrices, including TPC, FRAP, DPPH and ABTS, and comparison with other studies can be difficult due to differences in sample processing and extraction techniques (Santos-Buelga et al., 2012). To rank the flower species within our study according to their antioxidant potential, RACI was calculated, being a numerical scale that integrates different analytical methods (Sun and Tanumihardjo, 2007). The ranking of species antioxidant potential based on the calculated RACI is displayed in Figure 1, from the highest values of
The intake of polyphenols and antioxidants in the diet was associated with decreased inflammatory biomarkers (Maleki et al., 2019) and has been positively linked to a reduction of cardiovascular diseases and an improvement in microvascular function in hypertensive patients (Durazzo et al., 2019). High polyphenol intake has been also related to a reduced incidence of diabetes and a chemopreventive efficacy against experimental tumours, despite clinical results not providing univocal results (Li et al., 2013; Durazzo et al., 2019; Kumar and Goel, 2019; Lapuente et al., 2019). Phenolic compounds could also affect the gut microbiota composition, resulting in a greater abundance of beneficial microbes (Rinninella et al., 2019). Our screening of the TPC and antioxidant activity of 26 different flower species allowed to identify interesting wild plants with edible flowers, that is,
Phenolics, with more than 8,000 compounds, are among the most numerous class of secondary metabolites, leading to a complex classification. However, they can be divided into flavonoids (including flavanols and flavonols, among the others) and non-flavonoid polyphenols (including phenolic acids) (Del Rio et al., 2013; Durazzo et al., 2019). HPLC analysis was performed to determine the phenolic compounds that mainly contributed to the antioxidant capacity of edible flowers, by evaluating the amount of six phenolic acids (four cinnamic and two benzoic acids), five flavonols and two flavanols (catechins), being among the most important compounds due to their biological and antioxidant activities (Durazzo et al., 2019; Takahashi et al., 2020). The results highlighted that each flower has a peculiar phenolic composition and the sum of detected polyphenols varied to a wide extent (Figure 2).
The flowers with the highest RACI, that is,
Considering each class of polyphenols, flavonols were on average 346 mg · 100 g−1, cinnamic acids 183 mg · 100 g−1, benzoic acid 133 mg · 100 g−1 and catechins 114 mg · 100 g−1, confirming that flavonols are the main phenolics in edible flowers (Pires et al., 2019). Interestingly, analysing the Phenol-Explorer Database on 452 foods and beverages, Peìrez-Jimeìnez et al. (2010) found a mean content of flavonols, benzoic acids and cinnamic acids equal to 11, 29, and 35 mg · 100 g−1 of FW, respectively, values considerably lower in comparison with edible flowers.
The detailed results on each class of polyphenols are reported in the following sections.
The evaluated flavonols (Figure 2 and Table 4; Figure A1 in Appendix) were present in 23 species, lacking in
Flavonols and flavanols content (mg · 100 g−1) in the flowers of the 26 studied species.
Species | Flavonols | Flavanols | |||||
---|---|---|---|---|---|---|---|
Hyperoside | Isoquercitrin | Quercetin | Quercitrin | Rutin | Catechin | Epicatechin | |
38.7 b | 0.0 - | 0.0 - | 0.9 c | 19.7 b | 0.0 - | 20.8 g | |
0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.4 d | 421.0 a | |
0.0 - | 0.0 - | 0.0 - | 0.9 c | 0.0 - | 0.0 - | 65.2 c | |
23.5 bc | 16.1 c | 0.0 - | 0.0 - | 13.7 b | 19.1 bc | 533.3 a | |
262.4 a | 163.6 b | 0.0 - | 8.0 c | 17.8 b | 0.0 - | 0.1 h | |
0.0 - | 2,072.0 a | 0.0 - | 163.6 c | 34.1 b | 11.7 c | 26.3 dg | |
9.0 cd | 0.0 - | 0.0 - | 108.5 c | 0.5 c | 0.4 d | 29.9 cg | |
0.6 e | 12.5 c | 189.0 a | 34.5 c | 17.1 b | 20.7 bc | 37.7 cg | |
17.3 bd | 0.0 - | 207.3 a | 0.0 - | 0.0 - | 375.6 a | 306.6 ab | |
0.0 - | 0.0 - | 328.1 a | 0.0 - | 0.0 - | 0.0 - | 0.1 h | |
0.0 - | 12.0 c | 227.2 a | 0.0 - | 16.8 b | 24.0 bc | 59.2 cd | |
0.0 - | 0.0 - | 216.3 a | 16.4 c | 0.0 - | 28.6 b | 30.7 cg | |
14.7 bd | 10.8 c | 0.0 - | 82.3 c | 18.1 b | 0.4 d | 52.0 ce | |
9.4 cd | 100.1 b | 0.0 - | 109.6 c | 107.7 a | 0.0 - | 23.9 eg | |
0.0 - | 0.0 - | 0.0 - | 547.3 b | 0.0 - | 0.0 - | 22.0 fg | |
38.5 b | 130.2 b | 205.7 a | 35.9 c | 0.0 - | 26.0 b | 158.1 b | |
15.3 bd | 184.5 b | 0.0 - | 1,353.4 a | 12.9 b | 0.4 d | 388.4 b | |
0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 25.0 eg | |
0.0 - | 0.0 - | 0.0 - | 23.4 c | 0.0 - | 0.0 - | 48.3 cf | |
0.6 e | 0.0 - | 0.7 b | 0.0 - | 0.5 c | 0.0 - | 0.1 h | |
7.4 d | 7.9 c | 0.0 - | 13.5 c | 0.5 c | 0.0 - | 0.1 h | |
16.3 bd | 15.7 c | 0.0 - | 10.8 c | 14.4 b | 0.0 - | 21.9 fg | |
0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
0.0 - | 0.0 - | 0.0 - | 1.7 c | 0.0 - | 0.4 d | 0.1 h | |
0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.5 c | 0.0 - | 29.3 cg | |
0.0 - | 0.0 - | 0.0 - | 619.6 b | 0.0 - | 0.0 - | 49.1 cf |
Different lower case letters in a column indicate significant differences between species according to Tukey’s post-hoc test (
-, compound not detected.
Flowers sampled from cultivated plants.
Considering single compounds (Table 4; Figure A1 in Appendix), hyperoside was detected in 13 out of 26 species, ranging from 0.6 mg · 100 g−1 (
Considering each species,
Flavonols seem to be the main phenolics exerting anti-cancer activity
Flavanols (Figure 2 and Table 4; Figure A2 in Appendix) were present in the flowers of all the studied species, except for
Catechin (Table 4; Figure A2 in Appendix) occurred in 12 species, from 0.4 mg · 100 g−1 (
The flavanols content was generally below 100 mg · 100 g−1 in most of the species, while interesting results are shown by five flowers, in which epicatechin always prevailed on catechin.
Catechin and epicatechin belong to the subgroup of monomeric flavanols and are known to help in decreasing the body mass index and waist circumference (Durazzo et al., 2019); moreover, they help in preventing metabolic and cardiovascular diseases by improving the blood flow and exert antimicrobial, anti-inflammatory and antidiabetic properties (Ananingsih et al., 2013). Thus
Phenolic acids are commonly divided into benzoic and cinnamic acids, wide groups of polyphenols with at least 30 compounds reported in the past 10 years. Phenolic acids are recognized for their radical scavenging activity and their role in food preservation, as well as their therapeutic application, as reducing blood pressure and triglycerides (Kim et al., 2003; Ou and Kwok, 2004; Durazzo et al., 2019).
Benzoic acids (Figure 2 and Table 5; Figure A3 in Appendix) were present in every species ranging from 15.2 mg · 100 g−1 (
Benzoic acids and cinnamic acids content (mg · 100 g−1) in 26 flower species.
Species | Benzoic acids | Cinnamic acids | ||||
---|---|---|---|---|---|---|
Ellagic acid | Gallic acid | Caffeic acid | Chlorogenic acid | Coumaric acid | Ferulic acid | |
15.2 h | 0.1 c | 0.0 - | 0.0 - | 0.5 c | 357.3 a | |
212.9 ad | 0.0 - | 15.6 ab | 0.0 - | 158.5 a | 0.0 - | |
180.1 ad | 0.0 - | 0.1 d | 0.0 - | 0.0 - | 0.0 - | |
23.7 fh | 27.5 b | 0.0 - | 230.0 b | 148.5 a | 0.0 - | |
278.5 ac | 27.6 b | 14.6 ab | 0.0 - | 0.0 - | 0.0 - | |
214.4 ad | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
20.4 gh | 0.0 - | 16.2 a | 275.5 a | 110.7 a | 20.9 bc | |
121.4 be | 0.0 - | 0.0 - | 244.1 b | 16.4 b | 0.0 - | |
122.8 be | 0.0 - | 11.7 c | 0.2 c | 0.0 - | 0.0 - | |
63.2 dg | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
153.8 bd | 0.0 - | 15.9 ab | 270.6 a | 113.8 a | 0.0 - | |
589.2 a | 244.2 a | 13.9 b | 0.0 - | 0.0 - | 32.6 bc | |
27.9 fh | 0.1 c | 15.2 ab | 0.0 - | 0.0 - | 43.9 b | |
16.3 h | 0.0 - | 16.3 a | 0.0 - | 0.0 - | 29.3 bc | |
79.5 cf | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
72.5 dg | 0.1 c | 0.0 - | 232.0 b | 0.0 - | 0.0 - | |
410.7 ab | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
20.4 gh | 0.1 c | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
27.1 fh | 0.1 c | 15.3 ab | 0.0 - | 112.0 a | 0.0 - | |
28.2 fh | 0.0 - | 15.7 ab | 273.3 a | 0.0 - | 0.0 - | |
34.6 eh | 0.0 - | 0.0 - | 0.0 - | 0.5 c | 0.2 c | |
26.2 fh | 0.0 - | 1.9 d | 0.0 - | 113.4 a | 0.2 c | |
0.1 i | 27.9 b | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
15.2 h | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
150.1 bd | 0.0 - | 0.0 - | 0.0 - | 0.0 - | 0.0 - | |
214.3 ad | 0.0 - | 14.1 b | 241.2 b | 109.6 a | 0.0 - |
Different lower-case letters in a column indicate significant differences between species according to Tukey’s post-hoc test (
-, compound not detected.
Flowers sampled from cultivated plants.
Ellagic acid was detected in all the species (Table 5; Figure A3 in Appendix), ranging from 0.1 mg · 100 g−1 (
Gallic acid is mainly known for its antioxidant activity, while ellagic acid has anti-inflammatory properties and both exert anticancer and anti-HIV replication activities (Landete, 2011). Ellagic acid is also important in reducing the risk of cardiovascular diseases and obesity, since it decreases blood pressure and high blood cholesterol (Durazzo et al., 2019). Flowers of
Cinnamic acids (Figure 2 and Table 5; Figure A4 in Appendix) were detected in the flowers of 18 species, ranging from 0.1 mg · 100 g−1 (
Caffeic acid (Table 5; Figure A4 in Appendix) was present in 13 species and ranged from 0.1 mg · 100 g−1 (
Table 5 shows that eight species lacked in cinnamic acids (
Together with the other bioactive properties of phenolic acids, chlorogenic and ferulic acids are also characterized by working as antidiabetic agents (Kumar and Goel, 2019). Ferulic acid also counteracts the enzymes that catalyze the production of free radicals, while it enhances enzymes with free radical scavenging activity (Ou and Kwok, 2004). Our results showed the potentiality of 11 flowers (
Vitamin C (Table 6) was detected in all the flowers, except for
Vitamin C content (mg · 100 g−1) in the flowers of the 26 studied species.
Species | Vitamin C |
---|---|
0.0 - | |
4.4 fi | |
3.3 gi | |
4.0 gi | |
5.5 di | |
16.4 bc | |
6.7 ch | |
7.9 bg | |
2.8 hi | |
5.9 di | |
2.6 i | |
11.3 be | |
44.9 a | |
3.8 gi | |
4.0 gi | |
12.3 bd | |
7.2 bg | |
4.0 gi | |
11.0 bf | |
3.5 gi | |
15.5 bc | |
4.6 ei | |
0.0 - | |
11.8 bd | |
7.2 bg | |
17.7 b |
Different lower case letters in a column indicate significant differences between species according to Tukey’s post-hoc test (
-, compound not detected.
Flowers sampled from cultivated plants.
Most of the flowers had a content of vitamin C up to 8 mg · 100 g−1, whereas eight species were significantly higher (
Vitamin C is one of the plant food components which contribute to lower the risk of cancer, chronic and cardiovascular diseases and premature mortality, together with antioxidants and other compounds (Barros et al., 2011; Aune, 2019). Moreover, vitamin C is essential as an enzymatic cofactor and in response to environmental stimuli. European Food Safety Authority established a Population Reference Intake of 95–110 mg per day for vitamin C (Fenech et al., 2019), easily satisfied by kiwifruit, which has an average content of vitamin C of 93 mg · 100 g−1 FW. In oranges the content is about 53 mg · 100 g−1 FW and in apple 5 mg · 100 g−1 FW (Cruz-Rus et al., 2012). Thus, most of the flowers have an interesting concentration of vitamin C, comparable to apples, and
The correlation analysis (Table 7) highlighted that the TPC of the 26 edible flowers was positively correlated with the antioxidant activity measured with the three assays (FRAP, DPPH and ABTS). These three methods of analysis also positively correlated with each other, confirming previous results on the positive link between TPC and antioxidant activity in edible flowers (Ji et al., 2012; Kaisoon et al., 2012; Xiong et al., 2014; Lu et al., 2016; Petrova et al., 2016). The abovementioned parameters also correlated with the content of flavonols, ellagic acid, both catechins and vitamin C, but they did not correlate with the content of the four cinnamic acids and ellagic acid, probably being the reason for the different ranking of the species evaluated through RACI and chromatographic analysis.
Spearman’s correlation indexes between TPC, antioxidant activity (FRAP, DPPH and ABTS assays) and phenolic compounds recorded in the 26 edible flowers.
FRAP | DPPH | ABTS | Caffeic acid | Chlorogenic acid | Coumaric acid | Ferulic acid | Hyperoside | Isoquercitrin | Quercetin | Quercitrin | Rutin | Ellagic Acid | Gallic Acid | Catechin | Epicatechin | Vitamin C | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
TPC | 0.94** | 0.93** | 0.95** | 0.07 | 0.06 | 0.05 | 0.09 | 0.26* | 0.68** | 0.43** | 0.36** | 0.43** | 0.47** | 0.18 | 0.50** | 0.43** | 0.44** |
FRAP | 1 | 0.93** | 0.96** | 0.09 | 0.09 | 0.06 | 0.04 | 0.23* | 0.65** | 0.40** | 0.26* | 0.40** | 0.49** | 0.21 | 0.56** | 0.49** | 0.37** |
DPPH | 1 | 0.93** | 0.01 | 0.07 | 0.01 | 0.09 | 0.22 | 0.68** | 0.33** | 0.30** | 0.42** | 0.40** | 0.31** | 0.49** | 0.37** | 0.41** | |
ABTS | 1 | 0.07 | 0.15 | 0.07 | 0.05 | 0.25* | 0.67** | 0.36** | 0.29** | 0.38** | 0.47** | 0.19 | 0.52** | 0.47** | 0.44** | ||
Caffeic acid | 1 | 0.30** | 0.44** | 0.35** | 0.04 | −0.01 | −0.03 | 0.08 | 0.12 | 0.02 | −0.03 | −0.07 | 0.11 | −0.05 | |||
Chlorogenic acid | 1 | 0.49** | −0.07 | −0.03 | 0.04 | 0.22* | 0.06 | 0.01 | −0.04 | −0.06 | 0.35** | 0.21 | −0.01 | ||||
Coumaric acid | 1 | −0.12 | −0.08 | −0.07 | −0.04 | 0.02 | 0.05 | −0.05 | −0.06 | 0.09 | 0.40** | −0.02 | |||||
Ferulic acid | 1 | 0.30** | −0.03 | −0.03 | 0.17 | 0.32** | −0.22* | 0.08 | −0.08 | −0.05 | 0.00 | ||||||
Hyperoside | 1 | 0.48** | −0.06 | 0.03 | 0.44** | −0.17 | 0.14 | 0.11 | 0.13 | −0.05 | |||||||
Isoquercitrin | 1 | 0.03 | 0.38** | 0.69** | 0.17 | 0.01 | 0.27* | 0.14 | 0.30** | ||||||||
Quercetin | 1 | −0.09 | −0.08 | 0.29* | 0.06 | 0.70** | 0.20 | 0.02 | |||||||||
Quercitrin | 1 | 0.23 | 0.20 | −0.23* | 0.01 | 0.26* | 0.50** | ||||||||||
Rutin | 1 | −0.04 | 0.04 | 0.14 | 0.07 | −0.05 | |||||||||||
Ellagic acid | 1 | 0.06 | 0.27* | 0.34** | 0.28* | ||||||||||||
Gallic acid | 1 | 0.23* | −0.09 | −0.12 | |||||||||||||
Catechin | 1 | 0.49** | 0.05 | ||||||||||||||
Epicatechin | 1 | 0.04 |
The level of statistical significance is given (**
ABTS, 2,2′-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid; DPPH, 2,2-diphenyl-1-picrylhydrazyl; FRAP, ferric reducing antioxidant power; TPC, total polyphenol content.
The hierarchical cluster analysis performed on TPC and antioxidant activity data identified five main groups (Figure 3), reflecting the ranking of the 26 species based on RACI (Figure 1). A first group (A) is composed of
The results of the cluster analysis performed on phenolic profiles and vitamin C (Figure 4) show that four species should be considered not related to the others due to their peculiar characteristics (
A limited number of species resulted in the same groups in both dendrograms, namely: (i)
This investigation on 22 wild edible flowers compared with four cultivated plants showed wide variability in their phenolic and vitamin C content, as well as in their antioxidant activity, disclosing valuable sources of bioactive compounds. Generally, these traits appeared more species-dependent rather than taxonomic- or habitat-dependent. However, it has to be considered that the phytochemical profile of flowers and their bioactive compounds content are susceptible to variation, depending also on environmental conditions and stresses. The results showed that flowers of