Exploring wild edible flowers as a source of bioactive compounds: New perspectives in horticulture

Demasi, Sonia; Caser, Matteo; Donno, Dario; Enri, Simone Ravetto; Lonati, Michele; Scariot, Valentina

doi:10.2478/fhort-2021-0004

Figures & Tables

RACI calculated for the 26 studied flower species. Different lower case letters indicate significant differences between species according to Kruskal–Wallis’ stepwise comparison (p < 0.05). RACI, relative antioxidant capacity index. §Flowers sampled from cultivated plants.

Total polyphenols and polyphenol classes (flavonols, flavanols, benzoic acids and cinnamic acids) content (mg · 100 g−1) in the flowers of the 26 studied species. Different lower case letters in a row indicate significant differences between species according to Tukey’s post-hoc test (p < 0.05). -, compound not detected. §Flowers sampled from cultivated plants.

Hierarchical cluster analysis of the selected species according to their TPC and antioxidant activity (FRAP, DPPH and ABTS). The respective botanical family and vegetation community is provided for every species. §Flowers sampled from cultivated plants. 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.

Figure 4

Hierarchical cluster analysis of the selected species according to their polyphenolic profile and vitamin C content. The respective botanical family and vegetation community is provided for every species. §Flowers sampled from cultivated plants.

Flavonols (hyperoside, isoquercitrin, quercetin, quercitrin and rutin) content (mg · 100 g−1) in the flowers of the 26 studied species. Different lower case letters in a row indicate significant differences between species according to Tukey’s post-hoc test (p < 0.05). Data are means of three biological replicates. -, compound not detected. §Flowers sampled from cultivated plants.

Flavanols (catechin and epicatechin) content (mg · 100 g−1) in the flowers of the 26 studied species. Different lower case letters in a row indicate significant differences between species according to Tukey’s post-hoc test (p < 0.05). Data are means of three biological replicates. -, compound not detected. §Flowers sampled from cultivated plants.

Benzoic acids (ellagic and gallic acid) content (mg · 100 g−1) in the flowers of the 26 studied species. Different lower case letters in a row indicate significant differences between species according to Tukey’s post-hoc test (p < 0.05). Data are means of three biological replicates. -, compound not detected. §Flowers sampled from cultivated plants.

Cinnamic acids (caffeic, chlorogenic, coumaric and ferulic acid) content (mg · 100 g−1) in the flowers of the 26 studied species. Different lower case letters in a row indicate significant differences between species according to Tukey’s post-hoc test (p < 0.05). Data are means of three biological replicates. -, compound not detected. §Flowers sampled from cultivated plants.

Vitamin C content (mg · 100 g−1) in the flowers of the 26 studied species_

Species	Vitamin C
Allium ursinum	0.0 -
Bellis perennis	4.4 fi
Centaurea cyanus	3.3 gi
Cichorium intybus	4.0 gi
Dianthus carthusianorum	5.5 di
Dianthus pavonius	16.4 bc
Erythronium dens-canis	6.7 ch
Geranium sylvaticum	7.9 bg
Lavandula angustifolia	2.8 hi
Leucanthemum vulgare	5.9 di
Mentha aquatica	2.6 i
Paeonia officinalis	11.3 be
Primula veris	44.9 a
Primula vulgaris	3.8 gi
Robinia pseudoacacia	4.0 gi
Rosa canina	12.3 bd
Rosa pendulina	7.2 bg
Salvia pratensis	4.0 gi
Sambucus nigra	11.0 bf
Taraxacum officinale	3.5 gi
Trifolium alpinum	15.5 bc
Viola odorata	4.6 ei
Borago officinalis^§	0.0 -
Calendula officinalis^§	11.8 bd
Tagetes patula^§	7.2 bg
Tropaeolum majus^§	17.7 b

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
Species	Botanical family	Vegetation community	Food	Medicinal	Month	Longitude	Latitude	Soil type
Allium ursinum L.	Amaryllidaceae	Woodlands	Lim (2014a)	Sobolewska et al. (2015)	April	7.878	45.490	Eutrudept (S)
Bellis perennis L.	Asteraceae	Nutrient rich grasslands	Lim (2014a)	Lim (2014a)	March	7.592	45.065	Hapludalf (S)
Centaurea cyanus L.**	Asteraceae	Ruderal communities	Lim (2014a)	Lim (2014a)	May	7.896	45.475	Eutrudept (S)
Cichorium intybus L.	Asteraceae	Ruderal communities	Lim (2014a)	Street et al. (2013)	June	7.843	45.192	Dystrudept (S)
Dianthus carthusianorum L.	Caryophyllaceae	Dry grasslands	-	Palma (1964)	June	7.219	45.301	Udifluvent (S)
Dianthus pavonius Tausch	Caryophyllaceae	Nutrient poor grasslands	-	-	July	7.122	44.391	Eutrocryept (C)
Erythronium dens-canis L.	Liliaceae	Woodlands	-	-	March	7.371	45.157	Dystrudept (C)
Geranium sylvaticum L.	Geraniaceae	Edges	-	-	June	7.186	45.300	Dystrudept (S)
Lavandula angustifolia Mill.**	Lamiaceae	Dry grasslands	Lim (2014b)	Lim (2014b)	June^†	-^†	-^†	-^†
Leucanthemum vulgare Lam.	Asteraceae	Nutrient rich grasslands	Lim (2014a)	Prinsloo et al. (2018)	April	7.592	45.065	Hapludalf (S)
Mentha aquatica L.	Lamiaceae	Wetlands	Lim (2014b)	Alvarado (2018)	September	7.485	45.120	Hapludalf (S)
Paeonia officinalis L.**	Paeoniaceae	Edges	Lim (2014b)	-	April	7.344	45.097	Udorthent (S)
Primula veris L.	Primulaceae	Woodlands	Lim (2014b)	Apel et al. (2017)	May	6.802	44.968	Eutrudept (C)
Primula vulgaris Huds.	Primulaceae	Woodlands	Lim (2014b)	Tuttolomondo et al. (2014)	March	7.379	45.145	Dystrudept (C)
Robinia pseudoacacia L.	Fabaceae	Woodlands	Lim (2014a)	Jarić et al. (2015)	May	7.593	45.065	Hapludalf (S)
Rosa canina L. **	Rosaceae	Shrublands	Lim (2014b)	Nemati et al. (2015)	May	7.677	45.715	Udorthent (S)
Rosa pendulina L.	Rosaceae	Woodlands	-	-	June	7.192	45.301	Dystrudept (S)
Salvia pratensis L.	Lamiaceae	Dry grasslands	Kucekova et al. (2013)	Kucekova et al. (2013)	May	7.603	45.036	Udifluvent (S)
Sambucus nigra L.	Adoxaceae	Shrublands	Lim (2014a)	Młynarczyk et al. (2018)	May	7.593	45.064	Hapludalf (S)
Taraxacum officinale Weber**	Asteraceae	Nutrient rich grasslands	Lim (2014a)	Lim (2014a)	March	7.593	45.064	Hapludalf (S)
Trifolium alpinum L.	Fabaceae	Nutrient poor grasslands	Abbet et al. (2014)	Agelet and Vallès (2001)	July	7.122	44.390	Eutrocryept (C)
Viola odorata L.	Violaceae	Ruderal communities	Lim (2014b)	Lim (2014b)	March	7.591	45.065	Hapludalf (S)

Borago officinalis L.	Boraginaceae	Cultivated	Lim (2014a)	Gupta and Singh (2010)	May	-^§	-^§	-^§
Calendula officinalis L.	Asteraceae	Cultivated	Lim (2014a)	Lim (2014a)	May	-^§	^§	-^§
Tagetes patula L.	Asteraceae	Cultivated	Lim (2014a)	Lim (2014a)	July	-^§	^§	-^§
Tropaeolum majus L.	Tropaeolaceae	Cultivated	Lim (2014b)	Lim (2014b)	May	-^§	^§	-^§

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
Allium ursinum	38.7 b	0.0 -	0.0 -	0.9 c	19.7 b	0.0 -	20.8 g
Bellis perennis	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -	0.4 d	421.0 a
Centaurea cyanus	0.0 -	0.0 -	0.0 -	0.9 c	0.0 -	0.0 -	65.2 c
Cichorium intybus	23.5 bc	16.1 c	0.0 -	0.0 -	13.7 b	19.1 bc	533.3 a
Dianthus carthusianorum	262.4 a	163.6 b	0.0 -	8.0 c	17.8 b	0.0 -	0.1 h
Dianthus pavonius	0.0 -	2,072.0 a	0.0 -	163.6 c	34.1 b	11.7 c	26.3 dg
Erythronium dens-canis	9.0 cd	0.0 -	0.0 -	108.5 c	0.5 c	0.4 d	29.9 cg
Geranium sylvaticum	0.6 e	12.5 c	189.0 a	34.5 c	17.1 b	20.7 bc	37.7 cg
Lavandula angustifolia	17.3 bd	0.0 -	207.3 a	0.0 -	0.0 -	375.6 a	306.6 ab
Leucanthemum vulgare	0.0 -	0.0 -	328.1 a	0.0 -	0.0 -	0.0 -	0.1 h
Mentha aquatica	0.0 -	12.0 c	227.2 a	0.0 -	16.8 b	24.0 bc	59.2 cd
Paeonia officinalis	0.0 -	0.0 -	216.3 a	16.4 c	0.0 -	28.6 b	30.7 cg
Primula veris	14.7 bd	10.8 c	0.0 -	82.3 c	18.1 b	0.4 d	52.0 ce
Primula vulgaris	9.4 cd	100.1 b	0.0 -	109.6 c	107.7 a	0.0 -	23.9 eg
Robinia pseudoacacia	0.0 -	0.0 -	0.0 -	547.3 b	0.0 -	0.0 -	22.0 fg
Rosa canina	38.5 b	130.2 b	205.7 a	35.9 c	0.0 -	26.0 b	158.1 b
Rosa pendulina	15.3 bd	184.5 b	0.0 -	1,353.4 a	12.9 b	0.4 d	388.4 b
Salvia pratensis	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -	25.0 eg
Sambucus nigra	0.0 -	0.0 -	0.0 -	23.4 c	0.0 -	0.0 -	48.3 cf
Taraxacum officinale	0.6 e	0.0 -	0.7 b	0.0 -	0.5 c	0.0 -	0.1 h
Trifolium alpinum	7.4 d	7.9 c	0.0 -	13.5 c	0.5 c	0.0 -	0.1 h
Viola odorata	16.3 bd	15.7 c	0.0 -	10.8 c	14.4 b	0.0 -	21.9 fg
Borago officinalis^§	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Calendula officinalis^§	0.0 -	0.0 -	0.0 -	1.7 c	0.0 -	0.4 d	0.1 h
Tagetes patula^§	0.0 -	0.0 -	0.0 -	0.0 -	0.5 c	0.0 -	29.3 cg
Tropaeolum majus^§	0.0 -	0.0 -	0.0 -	619.6 b	0.0 -	0.0 -	49.1 cf

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 = 2.8B: CH₃CN	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(5:95:0.1 v/v/v), pH = 2.5B: CH₃OH/HCOOH (100:0.1 v/v)	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 mMKH₂PO₄, pH = 2.5B: CH₃OH	Isocratic, ratio of phase A and B: 95:5 in 10 min (5 min conditioning time); flow: 0.9 mL min⁻¹	261, 348

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)
Allium ursinum	10.2 jk	184.4 k	4.2 j	7.6 kl	0.7 m
Bellis perennis	16.9 ef	396.3 gi	81.6 cf	24.3 i	13.4 hj
Centaurea cyanus	26.4 b	378.5 hi	68.3 df	23.6 i	17.8 fh
Cichorium intybus	17.3 ef	618.4 df	138.4 ad	69.2 f	26.9 d
Dianthus carthusianorum	27.8 ab	936.3 bd	222.2 ab	81.1 ef	33.6 c
Dianthus pavonius	21.2 cd	752.8 ce	176.1 ac	106.5 c	24.3 de
Erythronium dens-canis	15.1 fh	364.3 hi	53.5 eg	20.4 ik	14.4 hj
Geranium sylvaticum	12.8 i	1,267.8 ab	267.0 ab	152.9 b	55.2 a
Lavandula angustifolia	31.2 a	396.0 gi	89.5 ce	14.8 il	14.0 hj
Leucanthemum vulgare	17.0 ef	448.8 fi	44.3 eh	20.9 ik	10.8 ij
Mentha aquatica	22.3 c	1,061.7 bc	256.0 ab	86.7 de	42.5 b
Paeonia officinalis	13.9 gi	1,930.5 a	303.8 a	226.2 a	55.3 a
Primula veris	18.8 de	1,044.9 bc	230.1 ab	97.1 cd	38.5 bc
Primula vulgaris	9.8 jk	602.9 dg	127.4 bd	41.7 gh	21.5 df
Robinia pseudoacacia	12.9 i	203.8 jk	15.7 i	4.5 l	2.4 m
Rosa canina	16.7 ef	1,396.6 ab	257.5 ab	146.2 b	55.6 a
Rosa pendulina	21.6 cd	1,773.7 a	253.8 ab	154.3 b	55.7 a
Salvia pratensis	17.7 ef	314.7 ij	38.9 fh	8.9 jl	9.0 jl
Sambucus nigra	16.8 ef	508.7 eh	78.8 cf	28.5 hi	18.3 fh
Taraxacum officinale	16.5 ef	159.4 k	13.0 i	7.7 kl	3.3 lm
Trifolium alpinum	10.0 jk	464.6 fi	91.5 ce	50.3 gh	20.3 eg
Viola odorata	13.0 hi	428.4 fi	66.1 dg	22.6 ij	15.6 gi
Borago officinalis^§	15.3 fg	163.4 k	29.7 gi	22.8 i	3.7 km
Calendula officinalis^§	13.7 gi	189.6 k	22.6 hi	3.6 l	9.2 jk
Tagetes patula^§	10.7 j	470.8 fi	143.9 ad	44.1 gh	23.0 df
Tropaeolum majus^§	8.9 k	355.8 hi	45.3 eh	14.8 il	12.8 hj
p	***	***	***	***	***

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
Allium ursinum	15.2 h	0.1 c	0.0 -	0.0 -	0.5 c	357.3 a
Bellis perennis	212.9 ad	0.0 -	15.6 ab	0.0 -	158.5 a	0.0 -
Centaurea cyanus	180.1 ad	0.0 -	0.1 d	0.0 -	0.0 -	0.0 -
Cichorium intybus	23.7 fh	27.5 b	0.0 -	230.0 b	148.5 a	0.0 -
Dianthus carthusianorum	278.5 ac	27.6 b	14.6 ab	0.0 -	0.0 -	0.0 -
Dianthus pavonius	214.4 ad	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Erythronium dens-canis	20.4 gh	0.0 -	16.2 a	275.5 a	110.7 a	20.9 bc
Geranium sylvaticum	121.4 be	0.0 -	0.0 -	244.1 b	16.4 b	0.0 -
Lavandula angustifolia	122.8 be	0.0 -	11.7 c	0.2 c	0.0 -	0.0 -
Leucanthemum vulgare	63.2 dg	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Mentha aquatica	153.8 bd	0.0 -	15.9 ab	270.6 a	113.8 a	0.0 -
Paeonia officinalis	589.2 a	244.2 a	13.9 b	0.0 -	0.0 -	32.6 bc
Primula veris	27.9 fh	0.1 c	15.2 ab	0.0 -	0.0 -	43.9 b
Primula vulgaris	16.3 h	0.0 -	16.3 a	0.0 -	0.0 -	29.3 bc
Robinia pseudoacacia	79.5 cf	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Rosa canina	72.5 dg	0.1 c	0.0 -	232.0 b	0.0 -	0.0 -
Rosa pendulina	410.7 ab	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Salvia pratensis	20.4 gh	0.1 c	0.0 -	0.0 -	0.0 -	0.0 -
Sambucus nigra	27.1 fh	0.1 c	15.3 ab	0.0 -	112.0 a	0.0 -
Taraxacum officinale	28.2 fh	0.0 -	15.7 ab	273.3 a	0.0 -	0.0 -
Trifolium alpinum	34.6 eh	0.0 -	0.0 -	0.0 -	0.5 c	0.2 c
Viola odorata	26.2 fh	0.0 -	1.9 d	0.0 -	113.4 a	0.2 c
Borago officinalis^§	0.1 i	27.9 b	0.0 -	0.0 -	0.0 -	0.0 -
Calendula officinalis^§	15.2 h	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Tagetes patula^§	150.1 bd	0.0 -	0.0 -	0.0 -	0.0 -	0.0 -
Tropaeolum majus^§	214.3 ad	0.0 -	14.1 b	241.2 b	109.6 a	0.0 -

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

Exploring wild edible flowers as a source of bioactive compounds: New perspectives in horticulture

Figures & Tables

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