The Unexplored Potential of Edible Flowers Lipids

Edible flowers have been historically linked to traditional world cuisine and culture. They are often used as ingredients in food and beverages for medicinal or pharmaceutical purposes. However, little attention has been paid to the quality of their lipids, and therefore to their potential for oil extraction and use in the food and food supplements industries. This review summarizes the current knowledge on the lipid composition of several edible flowers, including fat content, fatty acids, vitamin E, and carotenoids profiles. Edible flower lipids were found to be rich in linoleic (C18:2) and α-linolenic (C18:3) acids, which are essential fatty acids. Furthermore, most flowers are a good source of α-tocopherol and xanthophylls, such as lutein and zeaxanthin. This review provides valuable information on the lipid profile of some edible flowers in order to better characterize them and to increase their popularization among the food industry and consumers, boosting agriculture demand for these products.


Introduction
Lipids are major and essential constituents of all plant cells, providing structural integrity and energy for various metabolic processes [1].In plants, the compartmentation of neutral lipids is mostly associated with seed tissues, where triacylglycerols are stored [2].As such, most of the research on the lipid composition of plants has mainly focused on the oil from their seeds [3][4][5][6].However, some non-seed tissues, such as leaves, flowers, and fruits, also synthesize and store lipids, although until now, their formation or function in these tissues is poorly understood [2].Indeed, lipids are among the least studied metabolites in flowers, but recently they began to be further explored.The lipid composition was reported to be significantly different among flowers' organs and tissues [7].Furthermore, the majority of studies on edible flowers lipids have focused on their essential oils including basil (Ocimum basilicum L.) [8], chrysanthemum (Chrysanthemum indicum L.) [9], marigold (Tagetes minuta L.) [10], yarrow (Achillea millefolium L.) [11], calendula (Calendula officinalis L.) [12], and rose (Rosa × damascena Herrm.)[13].However, the literature assigns more importance to pollen compared to other flowers' parts (petals, sepals, and buds), because of their distinctive fatty acid profiles, characteristically dominant in one or more fatty acids [14].However, pollen may detract flower's flavor and cause allergies in some people, and so it is usually removed when edible flowers are marketed.
In order to improve knowledge about the lipid composition of edible flowers, the purpose of this paper was to provide an overview of published data on the lipid content, fatty acids profile, tocols, and carotenoids in edible flowers, to increase their acceptability as potential food ingredients and therefore Viola × wittrockiana Sources: Flora-On: Flora de Portugal Interactiva.(2014).Sociedade Portuguesa de Botânica [19].

Lipid Content and Composition
Lipid contents reported in the literature for edible flowers are described in Table 1.Hibiscus flowers showed the highest fat content at 19 and 26 g/100 g dry weight (dw).In general, the fat content in other edible flowers ranges from 0.1 to 8.5 g/100 g dw for Centaurea cyanus and Antirrhinum majus L., respectively.However, since the main component is water, varying between 70% and 95%, the fat content in fresh edible flowers is low [20].Furthermore, the fat content in edible flowers is not very distinct from other aerial parts of the plant; on a 100 g dw basis, moringa flowers had 2.91 g of fat, leaves 4.96 g, and immature pods 1.28 g [21].Common mallow flowers had 2.84 g of fat, leaves 2.76 g, and leafy flowered stems 3.09 g [22].When comparing the fat contents of edible flowers with other vegetables, such as asparagus (3.99 g/100 g dw) [23], lettuce (0.25 g/100 g dw), cabbage (0.2 g/100 g dw), and spinach (0.38 g/100 g dw) [24], the values are similar.The major lipid classes-fatty acids and lipid-soluble components (vitamin E and carotenoids) are detailed in the next sections.
Palmitic acid is one of the most common SFA found in plants.Although associated with increased risk of developing cardiovascular diseases [35], oxidative DNA damage, DNA strand breakage, necrosis, and apoptosis in human cells in vitro [36,37], when consumed with other fatty acids, like PUFAs, which were also detected in edible flowers, SFA are unlikely to have any significant impact on human health [37,38].Furthermore, a recent review reported that more rigorous investigations are needed to understand the advantages and disadvantages induced by palmitic acid consumption, because there are some controversial results [39].Edible flowers also contain low amounts of other saturated fatty acids, such as stearic (C18:0) (0.01-16.8% for Hibiscus sabdariffa and Rosa canina, respectively), lauric (C12:0) (0.09-3.66% for Moringa oleifera and Calendula officinalis flowers, respectively), and myristic (C14:0) acids (0.1-24.9% for Chrysanthemum morifolium and Calendula officinalis flowers, respectively).
Among the PUFAs, two of the most important fatty acids, linoleic acid (omega (ω)-6 group) and α-linolenic acid (omega(ω)-3 group), are essential fatty acids.So, humans must obtain them through diet because the body lacks the desaturase enzymes required for their production.These PUFAs are present in high proportions in some flowers (>50%), such as Calendula officinalis (petals), Taraxacum sect.Ruderalia, Punica granatum, Rosa micrantha, and Trifolium angustifolium (Table 2).Both fatty acids have important roles in human growth and development, as well as in the prevention and treatment of coronary artery diseases, hypertension, diabetes, arthritis, other inflammatory and autoimmune disorders, and cancer [40][41][42][43][44]. So, the presence of ω-3 and ω-6 fatty acids in edible flowers could be a way to promote their consumption and inclusion in the human diet.Regarding MUFAs, they are mainly represented by oleic acid (C18:1), ranging from 0.01% (Hibiscus sabdariffa) to 28.5% (Gundelia tournefortii L.), followed by eicosenoic (C20:1) and erucic (C22:1) acids in low quantities.
In Table 3, PUFA and SFA predominate over MUFA due to the significant contribution of α-linolenic and linoleic, and palmitic acids, respectively.However, in all cases, unsaturated fatty acids predominate over saturated ones (generally higher than 53%), with one exception observed in calendula flowers (23.3%).Furthermore, high PUFA/SFA ratios reduce the risk of cardiovascular diseases [45].In general, all edible flowers studied until now showed high ratios of PUFA/SFA (higher than 0.45) [46] and low ω-6/ω-3 ratios (lower than 4.0) [33], which are recommended for the human diet, except calendula (PUFA/SFA ratio equal to 0.27) and dahlia (ω-6/ω-3 ratio equal to 4.25).Additionally, a ω-6/ω-3 ratio equal or lower than 4 is beneficial for reducing serum "bad cholesterol", and inhibiting a major receptor for oxidized low-density lipoprotein (ox-LDL) uptake [47], with potential to protect against obesity, insulin resistance, and inflammation [48].However, Tsoupras et al. [49] presented data that supports inflammation induced by several factors, with platelet-activating factor (PAF), as being strongly implicated in cardiovascular diseases, rather than serum cholesterol alone.Therefore, food antioxidants might be lipid counterparts on the onset of cardiovascular diseases.So, edible flowers are a healthy lipid source (rich in oleic, linoleic, and linolenic fatty acids), offering potential health benefits.

Tocopherols
Vitamin E is a class of lipid-soluble antioxidants synthesized by plants and photosynthetic organisms [59].There are four isoforms (α, β, γ, and δ) of tocopherols and tocotrienols, which differ in the number and positions of the methyl groups in the chromanol ring.In flowers, tocols are mostly located in petal leucoplasts [59].Tocopherols are also essential components of the human diet because they perform numerous critical functions, including quenching and scavenging of various reactive oxygen species (ROS) and free radicals, and protecting PUFA from lipid peroxidation [60].
Tocopherols identified and quantified in edible flowers are listed in Table 4.In the majority of the flowers analysed, only the four isoforms of tocopherols (α, β, γ, and δ) were detected (Figure 2), with α-tocopherol being the major compound.Calendula officinalis was the flower that had the highest content of α-tocopherol (56.78 mg/100 g dw), followed by Rosa micrantha (26.72 mg/100 g dw) and Taraxacum sect.Ruderalia (21.60 mg/100 g dw).These flowers presented higher contents of α-tocopherol when compared with some vegetables, such as wild asparagus (0.75-4.51 mg/100 g dw) or leafy vegetables (2.59-10.12mg/100 g dw) [61].The Academy of Sciences reports a Recommended Dietary Allowance (RDA) value for α-tocopherol of 15 mg/day [62], whereas the daily recommended dose for tocopherols consumption in adults is 300 mg/day [63].Despite the low amounts of tocopherols in edible flowers, their daily consumption may contribute to supplying this vitamin to the organism.In parallel, γ-tocopherol was also detected in almost all flowers studied, ranging from 0.16 to 7.68 mg/100 g dw in Gundelia tournefortii and Rosa micrantha, respectively.

Carotenoids
Carotenoids are lipophilic pigments widely distributed in nature, and they have different roles in the plant life cycle including photo-protective functions, and provision of substrates for plant growth, regulator of abscisic acid and other hormones [64][65][66][67], as well as, in human nutrition and health, providing provitamin A and having anti-cancer activities [68].Carotenoids can be classified into two classes: carotenes (α-carotene, β-carotene, and lycopene) and xanthophylls (β-cryptoxanthin, lutein, and zeaxanthin) [69].In flowers, carotenoids are found in all anatomical parts: sepals, pollen, anthers, stamens, and petals [70].Flowers offer distinct carotenoids profiles that depend on species and variety [71], as shown in Tables 5 and 6.The edible flowers studied have shown a very different range in values between species.
As expected, the carotenoid amounts were different according to the distinct parts of the plants.For example, leaves of caper (mean 5.02 and 8.09 mg/100 g fw, β-carotene and lutein respectively) had higher concentrations of β-carotene and lutein than flower buds (mean 1.17 and 2.24 mg/100 g fw, β-carotene and lutein respectively) [73]; petals of calendula (7.71 mg/g dw) had higher values of total carotenoids than pollen (1.61 mg/g dw), stems (0.18 mg/g dw), and leaves (0.85 mg/g dw) [74].
Furthermore, different carotenoids are also detected in different parts of the flower: the stems of calendula contained carotenoids typical of photosynthetic tissue (e.g., lutein and β-carotene), whereas petals and stems showed more furanoid-oxides (e.g., flavoxanthin, auroxanthin, luteoxanthin, and 9Z-antheraxanthin) [74].So, consumers of edible flowers can obtain different carotenoids according to the part of flower they eat.
Some studies found correlations between the color of the flowers and their carotenoids content [75,76], and that carotenoids in flowers are responsible for the yellow, orange, and red color classes of pigments [71].Pintea et al. [75] found that calendula flowers with distinct colors (different varieties) contain the same pigments but in different amounts.For example, the variety that is dark orange (Double Esterel Orange) presented the highest total content of carotenoids (276 mg/100 g fw).Similar results were detected by Park et al. [77], who reported that between different cultivars and colors of chrysanthemums, the yellow-orange flowers were those that showed the highest content of carotenoids, namely Il Weol (345.56 µg/g dw) and popcorn ball (189.57µg/g dw).So, carotenoids are important compounds in edible flowers, because the color of the flower is an essential attribute that influences the commercial acceptance of consumers [78].Some colors of edible flowers may induce a reluctant attitude by consumers during the purchase, whereas others are more appealing.Since color may influence taste, reddish flowers may suggest to the consumer that they have a "sweet cherry or strawberry flavor", whereas yellowish flowers may be associated with a sour or citrus flavour [79].Furthermore, at the time of purchase of edible flowers, color influences the consumers because they may like one color or combination of colors more than others.According to Kelley et al. [79], consumers prefer dark colors, such as orange (associated to carotenoids) and crimson, because they are more appealing.

Oil Extraction
Until now, the studies performed on oil extraction of edible flowers have been performed for identification and characterization purposes only.To the best of our knowledge, there is no information on oil extraction from edible flowers for commercial purposes, only for essential oils (topic not discussed in the present review).Concerning the completed experimental studies, only solvent-based extractions are reported, and most of the studies involved hot-Soxhlet extraction or cold maceration.Edible flowers used in extraction can be prepared either from fresh or dried flowers.In case of dried samples, flowers are initially subjected to drying (e.g., air and freeze-drying), followed by grinding, milling, or homogenization to reduce sample particle size and enhance the extraction efficiency.Various solvents are commonly used in the Soxhlet extraction, such as petroleum ether [22,30,52,57] and hexane [51], whereas in maceration, a mixture of solvents is mainly used, such as chloroform-methanol [21, 28,55].However, in the future, new extraction technologies may be tested in edible flowers to improve extraction time, oil yield, and reduce the amount of solvent or even use green solvents.Based on its compositional data, edible flowers can be a potential source of fat and oil that are currently unexploited that could to complement the existing sources.Furthermore, different edible flowers can offer a diversity of products that can be used for food flavoring and drink products.

Conclusions
In general, fresh edible flowers show low nutrient content, including fat, because water is their main component.Nevertheless, their oils have an interesting composition from a health point of view, supporting an increased use for food purposes or as food supplements.The fatty acid profile of most flowers is rich in essential fatty acids and their vitamin E is mainly represented by α-tocopherol-the vitamin E compound with the highest biological activity.Most carotenoids found in flowers are xanthophylls, such as lutein, although carotenes have also been reported (lycopene and β-carotene), all with interesting heath attributes.Regarding different species and varieties of edible flowers, some variability in their lipid profiles and compositions has been observed.
In summary, and based on the available literature, it is evident that a wide gap still persists in the scientific knowledge regarding many edible flowers used for culinary and therapeutic purposes.The lipid composition of edible flowers merits further investigation to search for prospective food industry applications.This increased demand for edible flowers, as is or for oil extraction, will require a strong response from agriculture to increase productivity and quality.

Figure 2 .
Figure 2. Chemical structures of the main lipophilic compounds detected in edible flowers.Figure 2. Chemical structures of the main lipophilic compounds detected in edible flowers.Source: Hastings, et al. [58].

Figure 2 .
Figure 2. Chemical structures of the main lipophilic compounds detected in edible flowers.Figure 2. Chemical structures of the main lipophilic compounds detected in edible flowers.Source: Hastings, et al. [58].

Table 1 .
Fat content (g/100 g dry weight) reported in the literature for some edible flowers.

Table 2 .
Fatty acids (%) profile of some edible flowers mentioned in the literature.

Table 4 .
Tocopherols determined in edible flowers mentioned in the literature.
nd: not detected.

Table 5 .
Total carotenoids contents in edible flowers reported in the literature.

Table 6 .
Individual carotenoids values in edible flowers.