Bioactive compounds, minerals and antioxidants of edible flowers of peach and apple

ABSTRACT

Peach and apple flowers were evaluated for their human nutritional value by obtaining baseline information on their contents of bioactive compounds, minerals and antioxidant capacity. We used simple random sampling and nested statistical analysis to examine flowers of three peach cultivars (“July Flame,” “Cary Mac” and “Fair Time”) and two crab apple cultivars (“Manchurian” and “John Downie”). Flowers of “John Downie” stood out for their high contents of ash, protein and crude fat. Carbohydrate contents were highest for “Fair Time” and “Cary Mac.” Peach and apple differed in their contents of total phenols (73.23 ± 1.94 mg GAE/g peach and 86.65 ± 1.18 mg GAE/g, apple) and total flavonoids (TFl) (5.29 ± 0.10 mg QE/100 g peach and 7.99 ± 0.3 mg QE/100 g apple). The peach cultivar “Fair Time” and the crab apple cultivars “Manchurian” and “John Downie” showed the highest values of K⁺ and Mg²⁺. Micronutrient concentrations differed between species, however, Zn²⁺ and Na⁺ values were similar among species but differed between cultivars. Antioxidant capacity showed inter-species variations with the methods ABTS and FRAP. The results indicate a good potential for both peach and apple flowers to be incorporated in the human diet, for fresh consumption as functional foods.

KEYWORDS:

• Floriphagia
• functional food
• Malus sp.
• nutrients
• proximate analysis
• Prunus persica
• total flavonoids

Introduction

Since the beginning, most human civilizations and cultures have used plants as their primary food source. They have also used plant-derived products in other ways including in their medicines and cosmetics and, their flowers and foliage in particular, have been used for aesthetic and religious purposes.^[1] A plant’s various organs – fruits, leaves, stems, roots, seeds and flowers – each contains its own unique profile of nutritional compounds (including sugars, essential oils, carotenoids and vitamins), of bioactive compounds (including flavonoids, phenols and anthocyanins) and of minerals (including N, P, K⁺, Ca²⁺, Mg²⁺, Fe²⁺, Cu²⁺, Mn²⁺ and Zn²⁺).^[2] However, our consumption of foods of low nutritional value but high energy has contributed to an increase in the occurrence of obesity and so the intensity of cardiovascular and neurodegenerative diseases and also of chronic diseases such as diabetes and some types of cancer.^[3]

In many parts of the world, the consumption of flowers and inflorescences (floriphagia), both wild and cultivated, is considered a part of the gastronomic cultural heritage. The flowers of some 180 species are consumed, many of which are also known for their horticultural, ornamental, medicinal or religious associations.^[4] The better-known species with edible flowers include the Italian pumpkin (Cucurbita pepo L.), begonia (Begonia tuberhybrida), bougainvillea (Bougainvillea spectabilis Willd.), dahlia (Dahlia sp), colorin (Erythrina coralloides DC.), izote (Yucca gigantea Lem.), cempasuchil (Tagetes erecta L.), chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura), geranium (Geranium macrorrhizum L.) and rose (Rosa hybrida L.).^[5–7] In the face of today’s high incidence of chronic and degenerative diseases, recent decades have seen a trend for dietary change (e.g., vegetarianism and veganism), especially in those sectors of the population (higher socioeconomic) where a slightly higher food cost presents less of a problem. In parallel, there has also been a growing interest in so-called “functional foods” which in addition to promising health benefits also offer new taste experiences.^[8] It is in this context that the consumption of flowers is being rediscovered, particularly their use in novel salads, juices, soups and stews. Such gastronomic changes have found particular uptake in restaurants, where food presentation has a more special focus. Flowers also offer bright new colors, interesting new tastes and distinct new textures, so lending them to such innovation.^[9]

Another reason for the increase in flower consumption is their high content of certain bioactive compounds, which offer beneficial effects to human health.^[10,11] Such compounds include phenolic acids, flavonoids and anthocyanins, whose antioxidant properties inhibit or regulate the synthesis and accumulation of free radicals that induce oxidative stress. Among the most abundant secondary metabolites are the phenolic compounds and flavonoids that particularly relate to color, taste and astringency, nutritional characteristics and antioxidant properties.^[5,12] Moreover, the presence of variable amounts of other compounds has also been reported, including of fats, proteins, vitamins, sugars, minerals, which makes these plant organs even more attractive as components of salads or as edible decorations of gourmet dishes.^[3,7]

Human health benefits from an increase in intake of certain functional foods, including the edible flowers of some deciduous fruit trees. Thus, arises the possibility of consumption of the inflorescences of some temperate fruit trees, including those of apple (Malus sylvestris (L.) Mill var. domestica (Borkh) Mansf.) and peach (Prunus persica (L.) Batsch), which are potent sources of K⁺ and amino acids, including leucine, phenylalanine + tyrosine, lysine. They are also an excellent source of bioactive compounds associated with the lowering of blood lipids and glucose, along with antioxidant and antimicrobial activities, due to their high content of ascorbic acid, flavonoids, anthocyanidins, carotenoids and phenolic compounds.^[1,13] Peach flowers contain vitamins A and C and some minerals including Ca²⁺, P and Fe^2+.[2,14] All these compounds are valued by consumers seeking a healthier diet. The aim of our study was to examine the nutritional value of the flowers of peach and apple, and their contents of bioactive compounds, minerals and antioxidant capacity. In this way we set out to generate baseline information on the flowers of these species and with a view to increasing their consumption as human foods.

Materials and methods

Experimental site, plant material and sampling

This study was conducted in the spring-summer cycle of 2022 at the Autonomous University of Chihuahua (UACH), Mexico. The experiment began with the collection (25 March) of ≈ 60 inflorescences from eight-year-old peach trees (Prunus persica) cvs. “July Flame,” “Cary Mac” and “Fair Time” established on native rootstocks with 6 × 6 m spacing (277 trees ha⁻¹) and located in Casas Grandes, Chihuahua, Mexico (30°20’03.7 “N;108°07’13.5 “W; 1569 masl). Likewise, inflorescences were also collected from crab apple trees (5 April) with (cvs. “Manchurian crab apple” Malus baccata and “John Downie crab apple” Malus domestica) established in “Campo C,” Cuauhtemoc, Chihuahua, Mexico (28°38’0’“N;106°59’53”‘W; 2050 masl). Collections were made early in the day between 06:00 and 09:00 h to reducing mechanical damage.

Throughout the experiment, the peach and apple orchards were managed according to standard commercial practice for phytosanitary control (weeds, pests and diseases), mineral nutrition and irrigation scheduling. All inflorescences were quickly transported in paper bags in a container of dry ice to the Chemistry Laboratory of the Faculty of Agrotechnological Sciences (UACH), where they were separated into individual flowers which were then freeze-dried in a BK-F10PT freeze dryer (BIOBASE®, USA). Briefly, 50 g of petals were placed in trays (180 mm x 20 mm) for freeze-drying with a capacity of 0.9 L for 72 h (constant weight) in the equipment previously stabilized at - 56°C and 0.1 mBar. Sampling was random with three replicates per peach cv. and five per apple cv. Trees were chosen to be of similar size (peach 40 ± 1 cm diam. And 2.5 m height, apple 30 ± 1 cm diam. And 3 m height).

Proximate composition

To determine moisture, dry matter, crude protein and raw fat we used the method indicated by Tomasik.^[15] The extract free nitrogen (EFN), also known as total carbohydrate, represents sugars and starches, and was calculated by difference. The results are expressed as percentages. The total energy of one serving (100 g fresh weight) was calculated according to the equation: Total energy = (energy content of 1 g protein × g protein of sample) + (energy content of 1 g fat × g fat of sample) + energy content of 1 g carbohydrate × g carbohydrate of sample).^[16]

The titratable acidity was determined according to Tomasik.^[15] Briefly, a 0.5 g sample was homogenized with 10 mL of distilled water in an Ultra Turrax T25 homogenizer (IKA®, USA) for 2 min, then filtered and titrated with NaOH (0.1N) in which 2% phenolphthalein was added as indicator. The results are expressed as % citric acid. The total soluble solids (TSS) content was determined by placing a drop of the filtrate on the prism of a portable digital refractometer PAL-1 (ATAGO®, Japan). The results are expressed in °Brix. The color coordinates (L = brilliance, C = chrome and h = hue angle) of the flowers were also determined using a portable SP62 sphere colorimeter (X-Rite®, USA).

Bioactive compounds

The determination of the total anthocyanin (Tan) content was carried out according to the method described by Lee et al.^[17] with slight modifications. Briefly, two buffer solutions, pH 1.0 and 4.5, were prepared. Then, 0.1 g of lyophilized tissue was taken, homogenized with 10 mL of water + ethanol (v:v) and centrifuged at 10,000 rpm for 10 min at 4°C. Last, 1 mL of the supernatant was taken to obtain absorbance readings at 520 and 700 nm in the buffer solutions, pH 1.0 and 4.5, respectively. The results are expressed in mg cyanidin-3-glucoside 100 g⁻¹. The determination of total phenols (TP) was carried out according to the Folin-Ciocalteu method described by Waterman & Mole,^[18] for which 0.1 g of tissue was taken and homogenized in 400 µL of distilled water from which an aliquot of 500 µL was taken to form a mixture with 2.5 mL of Folin-Ciocalteu reagent (2N) and 2.0 mL of 20% Na₂CO₃ (w:v) which was left to stand for 2 h at room temperature (22 ± 1°C) in the dark. After this, the absorbance was determined at 760 nm and a standard curve for gallic acid was constructed for different concentrations (10–100 mg L⁻¹). The results are expressed as mg GAE g⁻¹ DW (dry weight). We determined total flavonoids by using the methodology by Arvouet-Grand et al.^[19] Briefly, 0.2 g of tissue was homogenized with 1.8 mL of methanol in an Ultra Turrax (IKA®, USA) and centrifuged for 15 min at 10,000 g at 4°C; 2 mL of sample were taken from the supernatant, that reacted with 2 mL of 2% p/v AlCl₃, left to rest for 15 min in the dark and the absorbance was determined at 415 nm. Results are expressed in mg QE 100 g⁻¹.

Antioxidant capacity

The ABTS assay was carried out as described by Re et al.,^[20] for which the ABTS solution was prepared by mixing equal volumes of 7 mM of the ABTS reagent [(2,2’-azino-bis(3-ethylbenzothiazoline)-6-sulfonic acid)] and potassium persulfate (K₂S₂O₈) at 2.45 mM (w:v), which was left to stand for 116 h at room temperature. Subsequently, 20% ethanol was diluted to obtain an absorbance value between 0.24 and 0.67 at 734 nm and then 10 µL of the sample diluted in ethanol +90 µL of distilled water +3 mL of ABTS applied every 30 s were added and left to react for 15 min. The absorbance at 734 nm was obtained and the results are expressed as µmol TE (Trolox equivalents) g⁻¹. The FRAP (Ferric Reducing Antioxidant Power Assay) method was used to determine the antioxidant capacity (AC) as described by Benzie et al.^[21] Briefly, 0.5 g of tissue was homogenized in 15 mL of deionized water and placed in a flat-bottomed tube. This mixture was then filtered with Whatman® 40 qualitative filter paper (Sigma-Aldrich, USA) and centrifuged at 11,500 rpm for 20 min. Subsequently, 10 µL of the sample +90 µL of distilled water +1900 μL of FRAP reagent were mixed and placed in a Heratherm VCA 230® (Thermo Scientific, USA) oven for 30 min at 37°C. The absorbance value was obtained at 593 nm and the results are expressed as µmol Fe²⁺ g⁻¹. The DPPH (2, 2- diphenyl-1-picrylhydrazyl) assay was carried out according to Brand-Williams et al.^[22] with modifications. Briefly, 0.1 g of sample was homogenized in 90 μL of distilled water. Next 3 mL of DPPH reagent was added and the mixture allowed to stand for 15 min at room temperature before obtaining the absorbance value at 517 nm, where 20% (v:v) methanol was used as a blank. The results are expressed as % inhibition of DPPH.

Statistical analyses

Data were analyzed using a nested model with the upper hierarchy factor being the species and the lower hierarchy factor being the cultivar or crab apples. To validate the analysis of variance (ANOVA), Levene’s test (homogeneity of variances) and Shapiro-Wilk’s test (normality) were applied.^[23] The multiple separation of means for peach and apple employed a Tukey’s test and a t-test (p ≤ .05), respectively. A Pearson’s correlation matrix was also constructed between the nutritional and petal quality variables. In all procedures, SAS version 9.0 (SAS Institute, 2002) software was used.

Results

The values obtained from the proximate analysis are shown in Table 1. Significant differences (p ≤ .05) were found between species and cultivars. The values found for moisture fluctuated between 83.9 ± 0.08 and 88.6 ± 0.03%, where the extreme values, i.e. the lowest or highest values corresponded to apple pollinators. In the case of ash (5.1 ± 0.06 and 6.3 ± 0.03%), protein (16.2 ± 0.01 and 16.9 ± 0.05%) and crude fat (1.7 ± 0.10 and 1.9 ± 0.02%), the highest values were found in the apple pollinator “John Downie.” The total carbohydrate content was higher for the peach varieties “Fair Time” and “Cary Mac” with values of 65.7 ± 0.05 and 64.5 ± 0.13%, respectively. In general, peach and apple flowers offer nutritional benefits as fresh foods, due to their significant mineral, protein and carbohydrate contents but low calorific content.

Table 1. Nutritional value of edible flowers of peach and apple.

P-C	%					(kcal/100 g)	Calories from fat
	M	A	p	CF	CT	TEOS
JF	87.1 ± 0.02^c	4.8 ± 0.02ª	15.7 ± 0.02ª	1.2 ± 0.03^b	55.1 ± 0.04^c	294.2 ± 1.3^a	10.9 ± 0.02^b
CM	87.4 ± 0.03^b	4.4 ± 0.02^c	12.0 ± 0.03^b	1.9 ± 0.03ª	64.4 ± 0.13^b	316.7 ± 1.6^a	15.1 ± 0.01^a
FTime	88.1 ± 0.02^a	4.6 ± 0.03^b	10.8 ± 0.09^c	1.8 ± 0.10ª	65.7 ± 0.05ª	322.2 ± 2.1^a	16.2 ± 0.02^a
C-A
Mn	88.6 ± 0.03ª	5.1 ± 0.06^b	16.2 ± 0.01^b	1.7 ± 0.10^b	58.4 ± 0.32^b	313.9 ± 2.1^b	15.3 ± 0.39^b
JD	83.8 ± 0.08^b	6.3 ± 0.03^a	16.9 ± 0.05^a	1.9 ± 0.02ª	59.8 ± 0.14ª	323.7 ± 1.7^a	16.9 ± 0.41^a
Species (S)	**	**	**	**	**	**	**
S (C or C-A)	**	**	**	**	**	**	**

Mean values ± standard deviation (n = 3 and 5, respectively); values with the same letter within each column for peach cultivars and crab apples do not differ significantly (P ≤ .05; Tukey’s test and t-test, respectively). ns – not significant; *, ** significant at 5 and 1%, respectively. Data are expressed on a dry weight basis. P-C; peach cultivars; C-A; crab apples; M: Moisture; A: Ash; P: protein; FC: Fat crude; TC: total carbohydrates; TEOS; total energy per 100 g fresh weight portion; JF; “July Flame;” CM; “Cary Mac;” Ftime; “Fair Time;” Mn; “Manchurian;” JD; “John Downie;” C – Cultivars

Flowers and inflorescences have brightly colored petals that are very attractive (chrome and hue angle) to pollinating organisms, and also to the eye of the human consumer. Both components were significant (p ≤ .05) only for fruit trees, however, chromaticity also showed variation between peach and apple varieties or pollinators, respectively (Table 2). Likewise, peach and apple blossoms did not show statistical variation with respect to TSS (0.61 ± 0.01 and 0.62 ± 0.02 °Brix) and TA (2.97 ± 0.18 and 3.27 ± 0.04% citric acid) values, where the lowest value was observed for “John Downie.”

Table 2. Colour, total soluble solids and titratable acidity in edible flowers of some peach varieties and apple pollinators.

Peach-cultivars	Colour			TSS (°Bx)	TA (% citric acid)
	L	Chrome	h°
July flame	62.36 ± 1.78^a	13.49 ± 1.04^a	65.38 ± 0.63^a	0.61 ± 0.01^a	3.27 ± 0.04^a
Cary Mac	61.84 ± 1.56^a	13.63 ± 0.87^a	66.13 ± 1.65^a	0.62 ± 0.01^a	3.12 ± 0.03^a
Fair time	62.51 ± 1.86^a	13.51 ± 0.60^a	64.32 ± 0.95^a	0.62 ± 0.02^a	3.11 ± 0.1^a
Crab apples
Manchurian	52.51 ± 3.20^a	26.60 ± 1.23^b	74.65 ± 1.67^a	0.61 ± 0.01^a	3.21 ± 0.11^a
John Downie	56.78 ± 2.28^a	34.72 ± 1.50^a	74.80 ± 0.58^a	0.61 ± 0.01^a	2.97 ± 0.18^a
Species (S)	*	**	**	ns	ns
S (C ó C-A)	ns	**	ns	ns	ns

Mean values ± standard deviation (n = 3 and 5, respectively); values with the same letter within each column for peach varieties and apple pollinators do not differ statistically (P ≤ .05; Tukey’s test and t-test, respectively). ns – not significant; *, ** significant at 5 and 1%, respectively. Data are expressed on a dry weight basis. TSS – Total soluble solids; TA – titratable acidity; C; Cultivars; C-A; crab apples

The bioactive compounds total anthocyanins (TA), total phenols (TP) and total flavonoids (TFl) showed significant differences between peach and apple flowers, respectively (Table 3), where values were: TP 73.23 ± 1.94 and 86.65 ± 1.18 mg GAE/g and TFl 5.29 ± 0.10 and 7.99 ± 0.3 mg QE/100 g. Also, TFl was significant among the cultivars and crab apples analyzed.

Table 3. Bioactive compounds in edible flowers of some peach varieties and apple pollinators.

Peach-cultivars	TA (mg cyanidin-3-glucoside/100 g)	TP (mg GAE/g)	TFl(mg QE/100 g)
July Flame	10.001 ± 0.0001^a	86.65 ± 1.18^a	5.67 ± 0.24^a
Cary Mac	10.001 ± 0.0001^a	85.09 ± 2.73^ab	5.29 ± 0.10^a
Fair Time	10.001 ± 0.0001^a	81.31 ± 1.12^b	5.31 ± 0.38^a
Crab apples
Manchurian	10.0002 ± 0.00005^a	74.87 ± 1.33^a	7.99 ± 0.3^a
John Downie	10.001 ± 0.00005^a	73.23 ± 1.94^a	7.93 ± 0.4^a
Species (S)	ns	**	**
S (C ó C-A)	ns	ns	**

Mean values ± standard deviation (n = 3 and 5, respectively); values with the same letter within each column for peach varieties and apple pollinators do not differ statistically (P ≤ .05; Tukey’s test and t-test, respectively). ns – not significant; *, ** significant at 5 and 1%, respectively. Data are expressed on a dry weight basis. TA: total anthocyanins; TP: total phenols; TFl: total flavonoids; C-A; Crab apples; C; Cultivars

Table 4 shows the mineral composition results for peach and apple flowers. Among the macronutrients, significant variation between peach and apple was found only for K⁺ (11.2 ± 0.01 and 22.0 ± 0.12 g/kg) and Mg²⁺ (2.9 ± 0.05 and 6.5 ± 0.04 g/kg) in which the flowers of “Fair Time” (peach), and “Manchurian” and “John Downie” (apple), stand out. The significantly different micronutrients concentrations (mg/kg) of peach and apple were, respectively: Fe²⁺ (83.70 ± 2.33 and 182.66 ± 3.05), Cu²⁺ (11.16 ± 1.04 and 14.50 ± 0.61), Mn²⁺ (36.0 ± 0.05 and 93.40 ± 1.85), Zn²⁺ (24. 50 ± 1.0 and 45.40 ± 0.54) and Na⁺ (10.00 ± 0.01 and 30.00 ± 0.01). However, the Zn²⁺ and Na⁺ concentrations were not significantly different (P > .05). With the exception of Fe²⁺, apple flowers had high concentrations of Cu²⁺, Mn²⁺, Zn²⁺ and Na⁺.

Table 4. Mineral composition in edible flowers of peach and apple.

Peach-cultivars	Macronutrients (g/kg)
	N-total	P	K^+	Ca^2+	Mg^2+
July Flame	23.7 ± 0.3^a	2.7 ± 0.1^a	11.2 ± 0.01^a	5.4 ± 0.02^a	2.9 ± 0.05^a
Cary Mac	23.5 ± 0.2^a	3.3 ± 0.2^a	11.3 ± 0.03^a	5.6 ± 0.02^a	4.3 ± 0.02^a
Fair Time	22.6 ± 0.3^a	2.8 ± 0.2^a	11.2 ± 0.01^a	6.2 ± 0.02^a	4.5 ± 0.05^a
Crab apples
Manchurian	22.3 ± 1.4^a	3.5 ± 0.02^a	21.5 ± 0.06^a	5.4 ± 0.04^a	6.6 ± 0.02^a
John Downie	23.2 ± 0.8^a	2.9 ± 0.03^a	22.0 ± 0.12^a	5.8 ± 0.05^a	6.5 ± 0.04^a
	Micronutrients (mg/kg)
Peach- cultivars	Fe^2+	Cu^2+	Mn^2+	Zn^2+	Na^+
July Flame	182.66 ± 3.05^a	11.16 ± 1.04^a	42.0 ± 0.02^a	24.50 ± 1.0^a	20.00 ± 0.04^a
Cary Mac	181.50 ± 1.32^a	11.56 ± 1.49^a	43.0 ± 0.02^a	27.00 ± 2.29^a	10.00 ± 0.01^b
Fair Time	182.16 ± 1.75^a	11.51 ± 1.50^a	36.0 ± 0.05^b	26.16 ± 2.08^a	10.00 ± 0.01^b
Crab apples
Manchurian	92.10 ± 2.65^a	14.50 ± 0.61^a	93.40 ± 1.85^a	45.40 ± 0.54^a	30.00 ± 0.01ª
John Downie	83.70 ± 2.33^b	11.80 ± 0.83^b	83.70 ± 2.33^b	43.00 ± 0.70^a	30.00 ± 0.01ª
Macronutrients (g/kg)	N-total	P	K^+	Ca^2+	Mg^2+
Species (S)	ns	ns	**	Ns	**
S (C ó C-A)	ns	ns	ns	Ns	ns
Micronutrients (mg/kg)	Fe^2+	Cu^2+	Mn^2+	Zn^2+	Na^+
Specie (S)	**	*	**	**	**
S (C ó C-A)	*	*	*	Ns	ns

Mean values ± standard deviation (n = 3 and 5, respectively); values with the same letter within each column for peach varieties and apple pollinators do not differ statistically (P ≤ .05; Tukey’s test and t-test, respectively). ns – not significant; *, ** significant at 5% and 1%, respectively. Data are expressed on a dry weight basis. C-A; Crab apples; C; cultivars

The AC values determined in the flowers are shown in Table 5. The AC shows only variation between species with ABTS (64.65 ± 1.8 and 75.03 ± 1.75 µmol TE (Trolox equivalents)/g) and FRAP (130.48 ± 0.96 and 153.21 ± 2.54 µmol Fe²⁺/g).

Table 5. Antioxidant capacity in edible flowers of some peach varieties and apple pollinators.

Peach-cultivars	ABTS	FRAP	DPPH
July Flame	70.66 ± 1.1^a	152.00 ± 1.41^a	75 ± 0.2^a
Cary Mac	64.65 ± 1.8^b	152.83 ± 1.79^a	70 ± 0.3^a
Fair Time	72.30 ± 1.9^a	153.21 ± 2.54^a	77 ± 0.3^a
Crab apples
Manchurian	72.47 ± 2.70^a	13.48 ± 0.96^a	72 ± 0.1^a
John Downie	75.03 ± 1.75^a	126.82 ± 1.72^b	77 ± 0.2^a
Species (S)	**	**	ns
S (C ó C-A)	ns	ns	ns

Mean values ± standard deviation (n = 3 and 5, respectively); values with the same letter within each column for peach varieties and apple pollinators do not differ statistically (P ≤ .05; Tukey’s test and t-test, respectively). ns – not significant; *, ** significant at 5% and 1%, respectively. Data are expressed on a dry weight basis; ABTS - 2,2′-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid (µmol TE (Trolox equivalents)/g); FRAP – ferric reducing/antioxidant power (µmol Fe²⁺/g); DPPH - 2,2-diphenyl-1-picrylhydrazyl (DPPH % inhibition). C-A; Crab apples; C; cultivars

Among the parameters evaluated for peach flowers (Table 6), Pearson’s correlation shows a negative correlation between Tan and Zn²⁺ (-0.770), TFl and P (-0.794). In apple flowers positive correlations were found between TA and Zn²⁺(0.681), TP and Fe²⁺(0.783), Mn²⁺(0.876), Cu²⁺(0. 876), Zn²⁺(0.768); TFl and Fe²⁺(0.875), Mn²⁺(0.946), Cu²⁺(0.842), Zn²⁺ (0.817), as well as TA and K⁺ (-0.817) which showed negative correlation.

Table 6. Pearson’s correlation coefficient for mineral composition, total soluble solids, titratable acidity, bioactive compounds and antioxidant capacity in flowers of some peach cultivars and crab apples.

Flower species		TSS	TA	TAn	TP	TFl
peach-cultivars	Nt	-0.233	0.510	0.255	0.239	-0.296
	P	-0.276	-0.441	-0.134	0.238	-0.794*
	K^+	-0.058	0.154	-0.125	0.379	-0.560
	Ca^2+	0.084	-0.603	-0.252	-0.357	-0.334
	Mg^2+	0.307	-0.542	-0.405	-0.170	-0.562
	Fe^2+	0.314	-0.065	0.065	-0.623	0.400
	Mn^2+	-0.322	0.133	0.045	0.001	0.097
	Cu^2+	0.274	0.134	-0.305	0.569	-0.392
	Zn^2+	0.406	-0.311	-0.770*	-0.121	-0.270
crab apples	Nt	0.402	-0.714	0.019	-0.468	-0.497
	P	0.112	0.170	-0.111	0.349	0.232
	K^+	0.140	-0.817**	-0.234	-0.277	-0.449
	Ca^2+	0.445	-0.356	0.208	-0.398	-0.286
	Mg^2+	0.051	-0.138	0.113	0.230	0.093
	Fe^2+	-0.090	0.323	0.655*	0.783**	0.875**
	Mn^2+	-0.195	0.453	0.619	0.876**	0.946**
	Cu^2+	-0.330	0.435	0.320	0.876**	0.842**
	Zn^2+	-0.110	0.681*	0.446	0.768**	0.817**

TSS: total solid soluble (°Brix); TA: titratable acidity (% malic acid); TAn: total anthocyanins (mg cyanidin-3-glucoside/100 g); TP: total phenols (mg GAE/g); TFl: total flavonoids (mg QE/100 g). *, ** significant at 1 and 5% respectively. ns: not significant

Discussion

Flowers generally have high moisture contents (≥88%), a condition favoring short shelf life. They also support an active microbial population of both fungi and bacteria.^[3] Moisture contents of petals of different colors of wild and cultivated dahlia species report values ranging from 88 to 92% [(wild: D. australis, D. appiculata, D. brevis, D. coccinea, D. campanulata and D. pinnata^[24] and cultivated: D. x hortorum].^[8] However, lower moisture contents are reported for rose (Rosa x grandiflora, 84.56 ± 0.122%) and sunflower (Helianthus annuus L., 86.45 ± 0.377%) by de Lima-Franzen et al.^[25] The range of results is likely associated with morphological variations in size and structure and the content of other components (fibers and minerals). There appear to be no clear standards for edible flower quality, with turgor, aroma and color being much affected by production system, management, harvest timing and postharvest handling.^[6,13]

These peach and apple flowers would seem to offer a healthy option as a fresh food as they are a source of carbohydrates and low calorific content. Flowers, including those of peach and apple, are considered a healthy food because of their minimal fat content ^[7] and high water content. In contrast, “Gala” apple flowers^[13] contain carbohydrates ranging from 20.63 ± 0.03 to 24.39 ± 0.01 g 100 g⁻¹. Similar values are reported for cactus flowers from Hidalgo in Mexico^[3] including from Cylindropuntia rosea (67.44 ± 0.45%, 1456.22 ± 1.45 kJ), Opuntia oligacantha, (57.31 ± 0.86%, 1338.97 ± 2.59 kJ), O. matudae (61.20 ± 0.63%, 1356.63 ± 1.54 kJ) and Echinocereus cinerascens (55.83 ± 0.11%, 1341.01 ± 9.06 kJ). Other flowers with similar carbohydrate contents are cultivated dahlia (D. x hortorum) (56.21 to 64.09%),^[4] colorin (Erythrina americana) (56.64 ± 1.23%), sabila (Aloe vera) (68.98 ± 1.11%) and garambullo (Myrtillocactus geometrizans) (68.13 ± 0.80%).^[7]

Consumption of flowers, including peach and apple, also provides some essential and non-essential amino acids, necessary for formation of proteins involved in cell structure and function.^[9,13] The protein percentages obtained in our study are similar to those reported in flowers of aloe vera (Aloe vera L.),^[7] cultivated dahlias (Dahlia x hortorum) (cherry, yellow, white, purple and red).^[6] However, in this same dahlia species, Martínez-Damián et al.^[8]report values of 18.54 and 19.25% for pink and purple petals, respectively. Such variation can be related to the degree of domestication, flowering stage, management, extraction method, conservation of samples etc.

Edible flowers can be a complementary source of mineral nutrients, often determined as ash content.^[3] The ash content we measure for “John Downie” flowers (6.25 ± 0.11 g 100 g⁻¹) is similar to that reported for flowers of “Gala” apple (6.47 ± 0.15 g 100 g⁻¹),^[13] everlasting flower (Helichrysum italicum) (6.31 ± 0.67 g 100 g⁻¹),^[26] but higher than that reported for yellow cosmos (Cosmos sulphureus cav.) (0.4 g 100 g⁻¹) and Rose “Purple Fragrance” (0.6 g 100 g⁻¹).^[27] However, none of the flowers so far analyzed exceed the values reported for Japanese pagoda tree (Sophora japonica L.) (10.38 ± 0.19 g 100 g-1) and black locust (Robinia pseudoacacia L.) (21.30 ± 0.93 g 100 g⁻¹),^[28] these differences relate mainly to the size of the flower or inflorescence, as well as to the drying process, where most reports consider drying with dry air and not by freeze-drying, which significantly reduces the mineral components, including ash.^[10]

There is increasing interest in flower consumption associated with improved eating habits and lifestyles. Globally, cookbooks, TV cooking programmes and culinary magazines all contribute to raising the standard of food presentation which includes use of the edible flowers of cultivated plants (ornamental, vegetable and medicinal) and wild plants. Flowers are presented fresh, dehydrated, and minimally or substantially processed (candied, preserved) as simple decorations or in dishes such as tamales and atoles.^[5,29,30] The colors of peach and apple flowers range from white, through pink, to purple and are a property of their absorption and reflectance of incident (sun)light. While their coloring has primarily to do with their attractiveness to pollinators their subtle shades also explain their aesthetic attraction to us.^[31] Interspecific variations in the degrees of flower pigmentation can be discrete or continuous, depending on the synthesis and accumulation in the petal’s epidermal cells of pigments that may include flavonoids, anthocyanins, carotenoids and betacyanins.^[9,16] In general, their bright colors have a positive visual impact, however, the consumer also associates different colors with different flavors, e.g., red (sweet cherry or strawberry flavors), yellow (citrus or acid flavors) and blue/purple with sugary foods.^[32] However, it is well known that flavor originates from specific concentrations of various compounds, including carbohydrates, organic acids, proteins, fatty acids and minerals, where the most abundant compounds are usually the sugars and organic acids.^[33] A study on “Idared” apple flowers^[34] reports the presence of organic acids (mg g⁻¹) including citric (4.0), malic (0.05), shikimic (0.0024) and fumaric (0.0008). Meanwhile, Pereira et al.^[35] indicate that the organoleptic properties in plant foods (including flowers) are associated with the balance between sugars and organic acids, where the latter contribute to the release of protons and while each of their different anions is responsible for a distinctive flavor.^[36] The metabolism and concentrations of these compounds can be affected by complex networks of environmental factors and agronomic managements,^[1] however, in the case of leaves and flowers, as they do not function as reserve structures, these contribute to their accelerated degradation, where organic acids are the main respiratory substrate for chemical energy generation.^[6]

One of the main factors that has stimulated interest in the consumption of flowers and inflorescences is their content of a range of secondary metabolites such as anthocyanins, phenols and flavonoids. These compounds are characterized by a high biological activity but they are also recognized their involvement in factors such as color, flavor, astringency and nutritional value.^[4,11] However, none of the flowers evaluated in this study are considered in the catalog of novel foods,^[37] which is why it is worthwhile generating baseline information on them to assess their nutritional potential as products for fresh consumption. Previous studies on flowers of some apricot cultivars (Prunus armeniaca L.) by Göttingerová et al.^[2] report a wide range of values for the content of total phenols (between 404.08 ± 0.28 and 768.45 ± 0.25 mg GAE 100/g) and for total flavonoids (between 198.76 ± 0.06 and 538.11 ± 0.04 mg EC/100 g), however, for total anthocyanins, the values obtained in our study exceeded those of most of the cultivars evaluated by these authors, with the exception of “Blenheim” (13.40 ± 0.1 mg/100 g) and “Vestar” (28.41 ± 0.07 mg/100 g), both with white petals. It has also been reported that the yield of secondary metabolites can be affected by extraction method – results varying with different solvents and drying methods (freeze-drying vs. air-drying at 25°C) – as observed for flowers of wood violet (Viola odorata L.)^[38] and Korean mint (Agastache rugosa).^[10] While it has been shown the purple hue is due to a mixture of phenolic compounds, anthocyanins, flavonoids and carotenoids, the results for total anthocyanins did not show much variation for either species with values ranging between 10.001 and 10.0002 mg/100 g.

The physiological functions of the human body require nutrition that includes large amounts of minerals (including P, K⁺, Ca²⁺, Mg²⁺, Mn²⁺, Na²⁺). Edible flowers offer a food source containing variable amounts of these but with low caloric value.^[12] Baseline information on the variation in mineral composition of flower petals of the familiar fruit species of the Rosaceae, including of apple and peach. However, levels of some mineral elements, such as K⁺, Ca²⁺ and Cu²⁺, in crab apples exceed those observed for these nutrients in flowers of “Gala” apple, K⁺ 4.931, Ca²⁺ 6.684 g kg⁻¹ and Cu²⁺ 2.16 mg kg^−1.[13] El-Jendoubi et al.^[14] reported values (g kg⁻¹) of N 26.8, P 4.5, K⁺ 20.5 and Ca²⁺ 7.0 in “Calanda” peach flowers. Reported variations in mineral composition can be attributed to genetic aspects of individual cultivars and extraction methods. In our study the flowers of both tree species (peach and apple) are an excellent source of minerals, especially of K⁺ (11.2 ± 0.01 and 22.0 ± 0.12 g kg⁻¹), Mg²⁺ (2.9 ± 0.05 and 6.6 ± 0.2 g kg⁻¹), Fe²⁺ (83. 70 ± 2.33 and 182.66 ± 3.05 mg kg⁻¹), Cu²⁺ (11.16 ± 1.04 and 14.50 ± 0.61 mg kg⁻¹), Mn²⁺ (36.00 ± 0.05 and 93.40 ± 1.85 mg kg⁻¹), Zn²⁺ (24.50 ± 1.0 and 45.40 ± .0.54 mg kg⁻¹) and Na⁺ (10.00 ± 0.01 and 30 ± 0.01 mg kg⁻¹), respectively. However, K⁺, Mg²⁺ and Zn²⁺ did not show much variation between cultivars. These results are comparable or higher to those in the edible flowers of some ornamental species (dry weights, mg kg⁻¹): Begonia cucullata var. cucullata (Fe²⁺ 67.4 ± 1.9, Cu²⁺ 7.40 ± 0.58), Dahlia pinnata Cav (Zn²⁺) (46.9 ± 5.3)^[39]; Paeonia lactiflora Pall. (Zn²⁺ 22.80 ± 16.68, Mn²⁺ 8.30 ± 6.55); Paeonia lactiflora “Yulou Hongxing” Na²⁺ (29.94 ± 4.03).^[40] For medicinal species (dry weights, mg kg⁻¹): flowers and fruits of Sambucus nigra L. contain (Cu²⁺) (9.2 and 5.4) and Zn²⁺ (36.1 and 10.3).^[41] For some types of fruits of Opuntia ficus-indica and Opuntia stricta (Zn²⁺) (36 ± 0.8 and 29 ± 0.4).^[42] Some of the most important minerals for the prevention of cardiovascular and oncogenic diseases are K⁺ and Na⁺ which, together, are involved in the regulation of osmotic pressure.^[43] We carried out an intensive literature search for the nutrients N-total, P, K⁺, Ca²⁺, Mg²⁺, Cu²⁺, Fe²⁺, Mn²⁺, Zn²⁺ and Na⁺ but many results were expressed relative to fresh weight, which prevents useful comparison.

Previous studies have demonstrated that edible flowers contain numerous chemicals with intense biological activities or antioxidant capacities, these include organic acids, ascorbic acid, flavonoids, polyphenols, anthocyanins and carotenoids.^[44,45] However, in most flowers, AC is defined by the presence of polyphenols, carotenoids and ascorbic acid,^[46] compounds that are widely recognized as important in human nutrition.^[37] The determination of antioxidant activity in extracts of flowers, fruits or leaves cannot be analyzed by a single, simple assay, due to the different properties of the compounds involved.^[47] In our study, ABTS (2,2-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid, ABTS^.+), FRAP (ferric 2,4,6-tripyridyl-s-triazine complex [Fe³⁺-(TPTZ)2]³⁺) and DPPH (2,2-diphenyl-1-picrylhydrazyl, DPPH.), where DPPH is a free radical, stable, commercially available and the ability to scavenge it constitutes one of the most widely used methods to evaluate the antioxidant properties of fruits and vegetables, because the samples do not require special treatment.^[48] Similar results have been reported (DPPH % inhibition) for edible flowers of fruit trees such as pomegranate (Punica granatum L.) (65.0 ± 0.7).^[47] However, our study results exceed those for papaya (Carica papaya L.) (50.5 ± 0.3), banana (Musa spp) (44.2 ± 4.6) and mahua (Madhuca longifolia) (81.9 ± 0.3).^[47] On the other hand, CA values determined with FRAP (between 64.65 ± 1.8 and 75.03 ± 1.75 µmol Fe²⁺ g⁻¹) and ABTS (between 126.82 ± 1.7 and 153.21 ± 2. 54 µmol TE (Trolox equivalents)/g) did not exceed those reported with these methods (µmol Fe²⁺ g⁻¹ and µmol TE (Trolox equivalents) g⁻¹, respectively) in edible flowers of fruit tree species such as almond (Amygdalus persica) (311 and 192), apricot (Armeniaca mume) (499 and 220), apple (Malus pumila var. domestica) (184 and 231), pomegranate (Punica granatum) (1275 and 460) and sour orange (Citrus x aurantium) (155 and 126).^[49] Oxidation of biological systems involves the transfer of electrons between molecules to a highly reactive oxidizing agent, hence the need to evaluate compounds (antioxidants) that eliminate or minimize this process. Edible flowers have different ways of preventing oxidation, including oxygen scavenging, binding pro-oxidants (primary antioxidants) and phenolic compounds (secondary antioxidants).^[2] In general, the presence of AC compounds in flowers helps minimize the processes of senescence and lipid peroxidation at the cell membrane level, which is linked to free radical activity with the consequent loss of ions and changes in osmotic pressure.^[10] Edible flowers, including those of peach and apple, are a potentially important source of a large group of non-essential nutrients which include: polyphenols, flavonoids, phenylpropanoids, stilbenoids, benzoic acid derivatives. All these offer benefits for human health due to their high biological and antioxidant activities.^[1]

Most of the compounds reported in edible flowers are considered secondary metabolites that allow the flower to interact with the environment for its fitness and survival. These serve as signaling agents for pollinating organisms, for seed dispersal and for defense against predators.^[37,50] Thus, secondary metabolites and micronutrients participate in redox reactions, electron transfer, structural components of enzymes and play important roles as precursors in the synthesis and accumulation of a great diversity of compounds, including polyphenolic compounds (phenylpropanoids and flavonoids), terpenes or isoprenoids, nitrogenous compounds (alkaloids, cyanogenic glycosides, glycosides and glucosinolates).^[51]

Conclusion

Our baseline analysis allows some understanding of the different nutritional values of peach and apple flowers. The crab apple “John Downie” showed the highest values of ash, protein and crude fat. Meanwhile, carbohydrate contents were higher in the peach cultivars “Fair Time” and “Cary Mac.” On the other hand, differences between species were found for total phenols and total flavonoids, however, only flavonoids were significant between cultivars and crab apples. Among the macronutrients, statistical variation between species was found for K⁺ and Mg²⁺ with “Fair Time,” “Manchurian” and “John Downie” standing out. The concentration of Fe²⁺, Cu²⁺, Mn²⁺, Zn²⁺ and Na⁺ was different between species, however, the values of Zn²⁺ and Na⁺ were similar between varieties. Likewise, with the exception of Fe²⁺, apple flowers were characterized by high concentrations of Cu²⁺, Mn²⁺, Zn²⁺ and Na⁺. Finally, the antioxidant capacity only showed inter-species variation with methods ABTS and FRAP. These findings allow us to elucidate peach and apple flowers as novel ingredients that can be considered as functional foods for fresh consumption. However, further research is needed for the flowers of these fruit trees, as none of them are considered in the catalog of novel foods.

Acknowledgments

The authors of this article thank Dr Jorge Jiménez Castro for his valuable assistance in the statistical analysis of the data.

Disclosure statement

No potential conflict of interest was reported by the author(s).