BioMed Research International
Volume 2021 (2021), Article ID 6683877, 11 pages
https://doi.org/10.1155/2021/6683877

Review Article

Ugni molinae Fruit as a Source of Bioactive Compounds with Good Quality Traits

Ricardo I. Castro,¹ Patricio Ramos,2,3 Carolina Parra-Palma,2,4 and Luis Morales-Quintana⁵

¹Multidisciplinary Agroindustry Research Laboratory, Instituto Ciencias Químicas Aplicadas, Facultad de Ingeniería, Universidad Autónoma de Chile, Talca, Chile
²Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile
³Núcleo Científico Multidisciplinario-DI, Universidad de Talca, Talca, Chile
⁴Programa de Doctorado en Ciencias Mención Ingeniería Genética Vegetal, Universidad de Talca, Talca, Chile
⁵Multidisciplinary Agroindustry Research Laboratory, Instituto de Ciencias Biomédicas, Facultad de Ciencias de la Salud, Universidad Autónoma de Chile, Talca, Chile

Correspondence should be addressed to Luis Morales-Quintana; luis.morales@uautonoma.cl

Received 11 December 2020; Revised 3 April 2021; Accepted 15 April 2021; Published 24 April 2021

Academic Editor: Nahide Gulsah Deniz

Copyright © 2021 Ricardo I. Castro et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Since the intake of fruits and vegetables displays important effects on the incidence of several chronic diseases in humans, consumers’ attention worldwide is focused on the identification of functional foods. In this sense, Ugni molinae (murtilla or murta fruit) is an important source of molecules with a strong antioxidant capacity that is widely used as a medicinal plant in Southern Argentina-Chile. Research on murtilla berries showed that this fruit and its leaves can be an excellent source of polyphenols and bioactive compounds with antibacterial and antioxidant capacity. This review is aimed at providing valuable information and discussing the available literature focused on four principal points: (i) fruit quality and plant physiology, (ii) compound content with bioactive properties, (iii) health properties for consumers of the fruit and leaves, and (iv) challenges for future research. Based on these four points, we propose that murtilla fruit can be a potential ingredient for new functional food products.

1. Introduction

Murtilla, murta, or Chilean guava are the names given to the Ugni molinae Turcz plant. In the Mapuche language of Southern-Chile native inhabitants [1–3], it is called by the name of Uñi, which is a native Chilean and Argentinean species belonging to the Myrthaceae family. Murtilla is a new berry that has the potential not only to become a fruit that Chile and/or Argentina can export but also to become a functional food. Murta is a wild shrub growing in the central-southern region of Chile, especially in the Coast Mountain and the pre-Andean mountains between the Maule and Aysén regions, including the Archipelago of Juan Fernández. In Argentina, it grows in the Patagonian region [2, 4].

Murtilla is consumed as a fresh fruit because of its organoleptic characteristics, although it is also processed by the food industry for making juice, canned items, confections, jams, and liquor products [3]. This fruit has potential beneficial effects on human health and may be used as a preservative in food products [3, 4]. In this line, murtilla berries showed a higher content of the total beta-carotene, phenolic compounds, and flavonoids [5]. These compounds confer a high antioxidant capacity. For example, as evaluated by ORAC, the antioxidant capacity was observed in fresh fruit; however, when the fruits were treated with high temperatures (70–80°C), the antioxidant properties were maintained, indicating a high thermal stability [5]. Additionally, another example of a health benefit of murtilla fruits is its beneficial effects on the management of cardiovascular disease as described by Singleton et al. in 1999 [6]. With respect to the leaves, chemical components with antioxidant and anti-inflammatory capacity have been reported, indicating that the fruit can be used for health benefits [7–9]. For this reason, the present review is aimed at critically summarizing information of the past and recent years on the characteristics of the shrub, its fruit quality, physiology, and beneficial effects on health.

2. Plant and Fruit Morphology and Growth

The plant of murtilla is a polymorphic shrub of great foliage. The murtilla shrub can grow to approximately 2 meters. Its branches are compressed, covered by hairs, and have ascending stems and branching [10]. Its leaves are between 2 and 2.5 cm in length. The form of the leaf is petiolate, opposed, without stipules, ovate-oblong, with a sharp apex, green lamina, glaucous, and has marks on the underside [10]. Its pendulous flowers are hermaphroditic, axillary, solitary, and long pedunculated [10]. There are five sepals united at the base and bent outwards; five linear petals, sharp and rounded; numerous stamens; and a style longer than these. The flowering season is between November and December, while the fruit production is between February and April [10]. The murtilla plant is an evergreen plant that produces a small globoid berry fruit with an equatorial diameter of 7–13 mm. The unit weight reaches 0.45 g [10]. Its pulp is white, and depending on the different plant ecotypes, it develops a variety of fruit colors including soft green, yellow, fuchsia (purplish), and light and dark red [3, 10–12] (Figure 1).

(a)

(b)

Figure 1: Murtilla fruit. (a) Murtilla fruit in different developmental stages visible from the same plant. (b) Color and relative size of the murtilla fruit in ripe stage. Picture was taken in the mountains of Choshuenco (39°5011S–72°457W), Los Rios region, Chile.

3. Fruit Quality

The murtilla plant may grow in the wild or may be cultivated. Thus, murtilla fruits are consumed fresh due to its organoleptic characteristics, and they are also used for the preparation of jams, syrups, desserts, and liquors [10]. With respect to the quality of a fruit, it is defined as the set of internal and external features inherent to the fruit, thereby determining consumer acceptability. These characteristics, which are also known as “quality criteria” for the consumer, include appearance (size, color, and shape), texture, nutritional value, safety [14], flavor, and aroma [15, 16], and these characteristics of the murtilla fruits have been partially studied, defining some of those quality properties.

3.1. Aroma

The aroma is strongly related with the fruit flavor and is a critical component of the perceived fruit quality [16–18]. The aroma of fruits is determined by a large number of volatile compounds of different molecular types (alcohols, terpenes, esters, aldehydes, and others) that are part of the flavor; additionally, its biosynthesis involves different pathways, and depends on many factors, such as ripening stage, cultivar, agronomic management, and harvest and postharvest conditions [17, 19].

With respect to the aroma of murtilla fruits, the ripe murtilla fruit exhibits a special and surrounding aroma, although the volatile compounds have not yet been identified completely. However, the first description of the aroma compounds of murtilla fruits was provided by Scheuermann et al. in 2008. The authors showed that the volatile compounds identified in murtilla fruit aroma have been found in other aromatic fruits (tropical or traditional fruits) widely consumed around the world. To obtain the identification of the volatile compounds from murtilla fruit, the authors obtained fruit from 2.5-year-old murtilla plants from four ecotypes. These ecotypes were selected based on their agronomical and organoleptic characteristics. The major concentrations of volatile compounds in murtilla fruit aroma produced by the four ecotypes are as follows: methyl 2-methyl butanoate, ethyl butanoate, ethyl 2-methyl butanoate, methyl hexanoate, ethyl hexanoate, methyl benzoate, and ethyl benzoate characteristics (Table 1). Out of these compounds, the authors showed that the most important compounds are the ester types independent of the ecotype studied and similar to those of other berries described previously as strawberry or blueberry.

Table 1: Aroma volatile compound concentrations (μg kg⁻¹ fresh weight) from four ecotypes of the murtilla fruit at the initial storage temperature of 0°C. Table was adapted from Scheuermann et al. in 2008 [13], and the values represent deviation of the two replicates.

Volatile compound
Ecotype 14-4
Ecotype 17-2
Ecotype 19-1
Ecotype 33-5

Methyl 2-methyl butanoate

Ethyl butanoate

Methyl pentanoate

Ethyl 2-methyl butanoate

Methyl hexanoate

α-Pinene

Ethyl hexanoate

1,8-Cineole

D-Limonene

Methyl benzoate

3.2. Flavor, SSC, TA, Postharvest Life, and Nutritional Properties

For consumers, one of the most important determinants of the fruit quality is the fruit nutritional composition. In this sense, the sugar contents are determined from the fruit quality. During fruit development and ripening, the fruits can accumulate sucrose, fructose, and glucose compounds [20]. In 2009, González Enei [21] evaluated the soluble solid content (SSC) from murtillas fruit obtained from different growing areas of the Maule region in the center of Chile. The author observed considerable differences in the SSC values, with differences between 10 and 27 °Bx. Even when the differences were considerable, these are still very high SSC values, indicating the considerable sweetness of the fruit. Additionally, murtilla fruit contains a high amount of dietary fiber (near to 20.0%) [22] (Table 2). In several fleshy fruits, the SSC and titratable acidity (TA) are two important properties related with ripening, and they are the main determinants for fruit flavor [4, 16, 23]. Along this line, Table 2 shows SSC values of 6.5-28 °Bx and TA values of 3.5–5.2 pH.

Table 2: Proximal and chemical analyses of the Ugni molinae fruit.

Analysis type
Nutrient type
Per 100 g
References

Proximal
Water (%)
76.95–84.14
[48–50]

Calories (kcal)
75
[25]

Soluble solids (°Bx)
6.5–28
[13, 48, 49]

pH
3.5–5.2
[13, 48, 49]

Total protein (g)
1.15–17.98
[48–50]

Ash content (g)
0.60–0.89
[48]

Total lipid (g)
0.30–0.85
[48, 49]

Crude fiber (g)
2.50–3.24
[48]

Carbohydrate (g)
17.6–19.4
[48]

Dietary fiber (g)
21.6
[22]

Pectins (g)
0.32–1.14
[11]

Sugars
Total sugars (g)
58.2
[11]

Minerals
Calcium (mg)
90
[25, 26]

Phosphorum (mg)
20

Potassium (mg)
116

Vitamins
Vitamin C (mg)
4.53–2.55
[24]

Other important components in berries are the vitamin and mineral concentrations. Unfortunately, there are only a few reports that are related to the vitamin and mineral contents of murtilla fruit or leaves. Along this line, in 2008, Moraga [24] described that murtilla berries contain around 4.53 to 12.55 mg of vitamin C in 100 g of fresh berries. These values are low compared to other fruits such as blueberry. With respect to the mineral content, Merino in 2002 [25] and previously Schmidt-Hebbel et al. in 1990 [26] described that murtilla ripe fruit can accumulate 90 mg of calcium, 20 mg of phosphorus, and 116 mg of the potassium minerals (Table 2). A high water content of around 77 to 85% was documented in murtilla fruit, together with other nutritional components as shown in Table 2.

With respect to the postharvest life, a comparative study of the two most important commercial murtilla varieties (namely, South Pearl INIA and Red Pearl INIA) showed that South Pearl INIA has a short shelf life of 35 days of storage at 0°C [4]. In 2019, Fuentes et al. [4] reported that in a postharvest life assay for this two Murtilla varieties, Red Pearl INIA has a major potential for postharvesting after 20 days at 0°C when compared to the South Pearl INIA variety.

3.3. Principal Bioactive Compounds Described from Murtilla Fruit

Polyphenolic compounds (PCs) are important not only in terms of quality but also in terms of the PCs influence over visual fruit appearance related with fruit or vegetable color, and their influence over the taste [4, 16, 27, 28]. Additionally, from a biomedical point of view, the PCs have gained a great interest during the last decade because they appear to be associated with the prevention of different diseases [29].

The main PCs reported in murtilla fruits and leaves are shown in Table 3. Highlighting the most important PCs found in different plant parts, we have caffeic acid 3-glucoside, ferulic acid, kaempferol, kaempferol-3-glucoside, gallic acid, myricetin, and others, such as rutin, quercitrin, luteolin, luteolin-3-glucoside, and p-coumaric acid (Table 3). Different reports showed that the murtilla fruit has 32 μmol GAE g⁻¹ FW of total PCs, using the Folin-Ciocalteu method, while other reports showed that it has 34.9 mg GAE g⁻¹ DW of total PCs [30], these values being considered a high concentration compared to the commercial blueberry with 17 μmol GAE g⁻¹ FW [31]. However, in another study, the authors showed that the murtilla fruit has only 9.2 mg GAE g⁻¹ DW (Table 3). Along this line, in 2011, Arancibia-Avila et al. [32] showed that the levels of PCs of murtilla fruit are significantly higher than the most popular berries such as blueberries or raspberries. The antioxidant activities in murtilla were high in methanol extract when compared to the other berries, and the authors showed that the highest ability to scavenge free DPPH radical was found for murtilla nonripe methanolic extract, with values of for polyphenols and , , and for flavonoids, tannins, and flavanols, respectively [32].

Table 3: Principal phenolic compounds found in murtilla.

Plant source
Compound
Technique
References

Flavonoids

Fruit
Quercetin
HPLC/ESI-MS and LC-PDA–HR-ToF-ESI-MS
[46, 51]

Leaves
Quercetin (ethanol extract)
HPLC-UV-VIS/MS, HPLC-UV-VIS, and HPLC/ESI-MS/MS
[52–54]

Fruit
Kaempferol
HPLC/ESI-MS
[46]

Leaves
Kaempferol (ethanol extract)
HPLC-UV-VIS/MS and HPLC-UV-VIS
[52–54]

Fruit
Isoquercitrin
HPLC-PDA–HR-ToF-ESI-MS
[51]

Fruit
Rutin
HPLC/ESI-MS and LC-PDA–HR-ToF-ESI-MS
[46, 51–55]

Leaves
Rutin (ethanol extract)
HPLC-UV-VIS/MS
[53]

Leaves
Rutin (ethanol 50% and water extract)
HPLC-PDA-FL
[55]

Leaves
Rutin (methanol extract)
HPLC ESI-MS/MS
[52]

Fruit
Myricetin
HPLC/ESI-MS and LC-PDA–HR-ToF-ESI-MS
[46, 51]

Leaves
Myricetin (methanol extract)
HPLC-UV-VIS/MS and HPLC ESI-MS/MS
[53, 56]

Leaves
Myricetin (ethanol extract)
HPLC-UV-VIS/MS
[54]

Fruit
Luteolin
HPLC/ESI-MS
[46]

Leaves
Epicatechin (methanol and ethanol extract)
HPLC-UV-VIS/MS
[56]

Leaves
Catechin (ethanol 50% extract)
HPLC-PDA-FL
[55]

Leaves
Catechin (infusion)
HPLC-UV-VIS
[8]

Leaves
Amentoflavone (ethanol extract)
HPLC-UV-VIS/MS
[54]

Organic acids

Fruit
Gallic acid
HPLC/ESI-MS
[46]

Leaves
Gallic acid (infusion)
HPLC-UV-VIS
[8]

Leaves
Gallic acid (ethanol extract)
HPLC-UV-VIS/MS
[54]

Leaves
Ácido elágico (infusion)
HPLC-UV-VIS
[8]

Leaves
Ellagic acid pentoside (ethanol extract)
HPLC-UV-VIS/MS
[54]

Leaves
Chlorogenic acid (ethanol extract)
HPLC-UV-VIS/MS
[54]

Leaves
Digalloyl quinic acid (ethanol extract)
HPLC-UV-VIS/MS
[54]

Cinnamic acids and derivatives

Fruit
p-Coumaric acid
HPLC/ESI-MS
[46]

Fruit
Caffeic acid 3-glucoside
HPLC/ESI-MS
[46]

Fruit
Feruloyl-quinic acid
HPLC-PDA–HR-ToF-ESI-MS
[51]

Fruit
Chlorogenic acid
HPLC-PDA–HR-ToF-ESI-MS
[51]

Leaves
Sinapic acid hexoside (ethanol extract)
HPLC-UV-VIS/MS
[54]

Flavonoid glycosides

Fruit
Cyanidin-3-glucoside
HPLC/ESI-MS
[46]

Fruit
Pelargonidin-3-arabinose
HPLC/ESI-MS
[46]

Fruit
Delphinidin-3-glucoside
HPLC/ESI-MS
[46]

Fruit
Quercetin-3-glucoside
HPLC/ESI-MS
[46]

Leaves
Quercetin-3-glucoside (water, methanol, and ethanol extract)
HPLC-UV-VIS/MS
[56]

Fruit
Kaempferol-3-glucoside
HPLC/ESI-MS
[46]

Leaves
Kaempferol-3-glucoside (water, methanol, and ethanol extract)
HPLC-UV-VIS/MS
[56]

Fruit
Luteolin-3-glucoside
HPLC/ESI-MS
[46]

Leaves
Myricetin dirhamnoside (water, methanol, and ethanol extract)
HPLC-UV-VIS/MS
[56]

Leaves
Myricetin glucoside (water, methanol, and ethanol extract)
HPLC-UV-VIS/MS
[56]

Leaves
Quercetin dirhamnoside (methanol and ethanol extract)
HPLC-UV-VIS/MS
[56]

Leaves
Quercetin rhamnoside (methanol and ethanol extract)
HPLC-UV-VIS/MS
[56]

Leaves
Myricetin rhamnoside (water, methanol, and ethanol extract)
HPLC-UV-VIS/MS
[56]

Leaves
Myricetin rhamnoside (ethanol extract)
HPLC-UV-VIS/MS
[54]

Leaves
Myricetin xyloside (water extract)

Fruit
Neochlorogenic acid
LC-PDA–HR-ToF-ESI-MS
[53]

Fruit
Hyperoside
LC-PDA–HR-ToF-ESI-MS
[53]

Leaves
Galloyl myricetin hexoside (ethanol extract)
HPLC-UV-VIS/MS
[54]

Leaves
Quercitrin (ethanol 50% and water extract)
HPLC-PDA-FL
[55]

Isoflavones

Leaves
Daidzin (methanol extract)
HPLC/ESI-MS/MS
[52]

Leaves
Formononetin (methanol extract)
HPLC/ESI-MS/MS
[52]

Leaves
Biochanin A (methanol extract)
HPLC/ESI-MS/MS
[52]

Leaves
Genistein (methanol extract)
HPLC/ESI-MS/MS
[52]

HPLC: high-performance liquid chromatography; ESI-MS: electrospray ionization mass spectrometry; UV-VIS: ultraviolet-visible spectroscopy; PDA: photodiode detector; ToF/MS: time of flight mass spectrometry; HR-MS: high-resolution mass spectrometry.

3.3.1. Anthocyanins Found in Murtilla Fruit

Anthocyanins are naturally present in vegetables and fruits, and one of the most abundant types of these PCs are named flavonoids [29]. These compounds are vegetal pigments that promote health benefits to consumers due to their high antioxidant capacity [29, 33], and they are responsible for the blue, purple, and red colors in the flowers, vegetables, and fruits [27, 29]. To date, more than 600 anthocyanins have been identified in nature [29], including the anthocyanins described in murtilla fruit as shown in Table 4 along with their corresponding structures shown in Figure 2.

Table 4: Principal anthocyanin compound found in murtilla fruit.

No.
Plant source
Compound
Technique
References

1
Fruit
Petunidin 3-O-galactoside
LC/MS, LC-PDA–HR-ToF-ESI-MS, and HPLC-PDA
[34, 46, 51]

2
Fruit
Delphinidin 3-O-galactoside
LC/MS
[46]

3
Fruit
Delphinidin 3-O-arabinoside
LC/MS
[46]

4
Fruit
Cyanidin 3-O-glucoside
LC/MS and LC/MS ESI-IT
[46, 57]

5
Fruit
Cyanidin 3-O-arabinoside
LC/MS
[47]

6
Fruit
Malvidin 3-O-arabinoside
LC/MS
[47]

7
Fruit
Peonidin-malvidin 3-O-glucoside
LC/MS
[47]

8
Fruit
Peonidin 3-O-glucoside
LC/MS, LC-PDA–HR-ToF-ESI-MS, and HPLC-PDA
[34, 46, 51]

9
Fruit
Cyanidin 3-O-rutinose
LC-PDA–HR-ToF-ESI-MS and HPLC-PDA
[34, 51]

10
Fruit
Petunidin-3-O-rutinoside
LC-PDA–HR-ToF-ESI-MS and HPLC-PDA
[34, 51]

11
Fruit
Peonidin-3-O-arabinoside
LC-PDA–HR-ToF-ESI-MS and HPLC-PDA
[34, 51]

12
Fruit
Cyanidin-3-O-(6 succinoyl)-glucose
LC-PDA–HR-ToF-ESI-MS and HPLC-PDA
[34, 51]

13
Fruit
Peonidin-di-glucopyranoside
LC/MS ESI-IT
[57]

14
Fruit
Peonidin glucopyranoside
HPLC-PDA
[34]

HPLC: high-performance liquid chromatography; ESI-MS: electrospray ionization mass spectrometry; UV-VIS: ultraviolet-visible spectroscopy; PDA: photodiode detector; ToF/MS: time of flight mass spectrometry; HR-MS: high-resolution mass spectrometry; ESI-IT: electrospray ionization- (ESI-) ion trap (IT).

Figure 2: Structures of identified anthocyanins from murtilla fruit. The number of each structure is the same number given to the corresponding anthocyanin molecule described in Table 4.

Recently, in 2014, Brito et al. [34] evaluated the anthocyanin content in three different Chilean native berries (calafate, murtilla, and arrayán fruits). The authors reported that murtilla berries had a smaller anthocyanin content when compared to arrayán or calafate fruits with values of 6.9, 15.2, and 51.6 (mg cyanidin 3-O-glucoside g⁻¹ DW), respectively, even though a higher flavonoid content has been described in the Myrtaceae family [30, 31] (including murtilla fruits). Now, with respect to the principal anthocyanins found in murtilla ripe fruit, after an extraction in methanol-HCl and/or methanol, it was possible to identify malvidin-3-, delphinidin-3-, and peonidin-3-arabinoside; peonidin-3- and malvidin-3-glucoside (Table 4) [35].

4. Benefits to Consumer’s Health

The PCs, and in particular the anthocyanin compounds, are effective antioxidant compounds with different beneficial health effects, such as antiallergic, antimicrobial, anti-inflammatory, antiplatelet, anticarcinogenic, antimutagenic, and neuroprotective effects [4, 29, 36]. For this reason, multiple studies have been carried out searching for high levels of anthocyanins in different fruits. The berry fruits are interesting targets, because of their high concentrations of PCs and anthocyanins. Of course, this is the same for murtilla fruit due to its high concentrations of PCs. However, it is necessary to understand that the richness of any PCs found in each fruit or food is not necessarily related with the correct absorption in the human organism; for these reasons, the bioavailability of each PC should be studied to correlate the intake and the effects thereof [29]. In this sense, in 2018, Ah-Hen et al. [37] showed that at the end of the small intestine digestive step, the bioaccessibility index of PCs found in fresh murtilla berries and murtilla fresh juice achieved a relatively high value (around 70%). More specifically, the authors showed that the fresh murtilla fruit increased the release of bioactive compounds in the small intestine, while the murtilla fresh juice released the bioaccessible bioactive compounds in the gastric stage [37]. Between the different beneficial properties described, the murtilla fruits are considered useful for increasing visual acuity during the night and easing circulation disorders [38]. With respect to the skin, the fruit is useful for treating mouth conditions, such as thrush and stomatitis [38]. Other authors described that murtilla fruits might have beneficial effects in the protection against cardiovascular diseases [39]. The authors described murtilla fruit extract as rich in quercetin-3-β-D-glucoside, gallic acid, myricetin, catechin, kaempferol, and quercetin, and they also showed that these extracts contain significant antioxidant activity against ROS production and lipid peroxidation, with no toxic effects on human endothelial cells (Table 3).

4.1. Anti-Inflammatory Properties of the Murtilla

The inflammation process is a response to metabolic syndrome, autoimmune diseases, neurodegenerative diseases, and cardiovascular diseases [40]. Chronic inflammation produces higher reactive oxygen species (ROS) accumulation that affects various proteins triggering the release of inflammatory signals [4, 41–43]. Different authors showed that natural products, such as PCs [42] and/or terpenoids [44, 45], possess anti-inflammatory effects.

Firstly, with respect to the terpenoid compounds, Goity et al. in 2013 [44] identified 2 triterpenoids (molecules 2 and 4 in Table 5 and Figure 3) from murtilla leaf extracts in ethyl acetate and ethanol. The authors observed that these triterpenoids are responsible in part for the anti-inflammatory activity in an assay on mice ear edema induced by 12-O-tetradecanoylphorbol-13-acetate (TPA) [44].

Table 5: Principal triterpenoid compounds found in murtilla leaves.

No.
Plant source
Compound
References

1
Leaves
Betulinic acid
[45]

2
Leaves
Maslinic acid
[44, 45]

3
Leaves
Oleanolic acid
[45]

4
Leaves
Madecassic acid
[44, 45, 54]

5
Leaves
Ursolic acid
[45]

6
Leaves
Alphitolic acid
[7, 45]

7
Leaves
Corosolic acid
[7, 45]

8
Leaves
Asiatic acid
[44, 45, 54]

Figure 3: Structure of the principal triterpenes described from murtilla leaves: (1) betulinic acid, (2) maslinic acid, (3) oleanolic acid, (4) madecassic acid, (5) ursolic acid, (6) alphitolic acid, (7) corosolic acid, and (8) asiatic acid. The number of each structure is the same number given to the corresponding anthocyanin molecule described in Table 5.

Then, in 2016, Arancibia-Radich et al. [45] studied the activity of two extracts from murtilla leaves with ethyl acetate or ethanol, identifying eight triterpenoids from ten different Ugni molinae genotypes (molecules 1 to 8 in Table 5 and Figure 3). The results obtained showed that there is a quantitative difference between triterpenoid content and total phenolic compounds from two extracts, showing significant differences in anti-inflammatory activity, due to the high phenolic content present in the methanolic extract [45]. Previously, in 2006, Aguirre et al. [7] isolated and identified three triterpene acids (molecules 6 to 8 in Table 5 and Figure 3). The authors also reported the activity of 2α-hydroxy pentacyclic triterpene acids from murtilla leaves. Initially, only corosolic acid (molecule 7 in Table 5 and Figure 3) showed an activity in the anti-inflammatory assay when an edema was induced by TPA in mice ears, in which the activity showed a similar level that was described by an anti-inflammatory COX-2 selectively named nimesulide [7]. Additionally, molecules 6 and 8 (from Table 5 and Figure 3) showed an inhibition of the TPA-induced inflammation comparable to indomethacin (a methylated indole derivative nonsteroidal anti-inflammatory drug related to diclofenac, which inhibits prostaglandin production) [7].

With respect to the phenolic compounds, different authors showed a high content of quercetin (a flavonoid compound) suggesting its protective effect against inflammatory diseases (Table 3). Quercetin is mainly found as quercetin 3-rutinoside in fruits and vegetables, and this compound was described in fruits such as murtilla and in other berries such as calafate, commercial strawberry, Chilean strawberry, raspberry, and blueberry [4, 16, 33].

4.2. Antibacterial Properties of the Murtilla Extract

Today, one of the main problems in the pharmaceutical industry is the increasing resistance of microorganisms, leading to treatment failures [45]. Thus, the discovery of new and better antimicrobial compounds is crucial, and the South American natives’ berries, such as the murtilla fruits or leaves, are a good source of bioactive compounds. In this sense, extracts obtained from murtilla leaves and fruits have been used for different purposes. Junqueira-Gonçalves et al. in 2015 [46] determined the antimicrobial activity in extracts (obtained from ethanolic and methanolic extraction) from murtilla fruit over E. coli and S. typhi bacteria, showing that the extracts, obtained from methanol extraction, have an inhibitory activity against these bacteria very similar to that of standard antibiotics (Table 6) [46].

Table 6: Summary of antibiotics against S. typhi and E. coli. The activity was registered in inhibition halo diameter (mm) and Mueller-Hinton’s agar medium. (adapted from Junqueira-Gonçalves et al. in 2015 [46]).

Plant source
Type extract
Concentration
Antibiotics
E. coli
S. typhi

Commercial product
Not informed
Tetracycline

Not informed
Gentamicin

Not informed
Ampicillin

Fruit
Methanolic :water :HCl (75 : 24 : 1)
100 μL

No reported value
22.5

Additionally, extracts from murtilla leaves caused a decrease in the growth of Pseudomonas aeruginosa, Klebsiella pneumoniae, and Staphylococcus aureus (Table 7), and a significant correlation between PCs and antimicrobial activity over these bacteria was reported by Shene et al. in 2009 [47]. The authors showed a higher antimicrobial activity in leaf extracts than in fruit extracts. This could be attributed to the higher concentration of flavan-3-ols and other flavonol glycosides found in the leaves compared to that in the fruit [47].

Table 7: Summary of S. aureus ATCC 25923, K. pneumoniae ATCC 13883, and P. aeruginosa ATCC 27853. The activity was registered in inhibition halo diameter (mm) and Mueller-Hinton’s agar medium. (adapted from Shene et al. in 2009 [47]).

Plant source
Type extract
Concentration
Antibiotics
S. aureus ATCC 25923
K. pneumoniae ATCC 13883
P. aeruginosa ATCC 27853

Fruit
Ethanol
100 μL
—
a
—
—

b

c

Leave

100 μL
—
a
a
a

b
b
b

c
c
c

Letters indicate the location where the murtilla plants were obtained: (a) mountain, (b) coast, and (c) valley.

5. New Perspectives and Challenges

Berries in general are among the most popular fruits consumed worldwide since they are available throughout the year as fresh and/or frozen products. For this reason, the berry production is now in continuous growth and improvement due to the increasing demand by global consumers who require healthier and functional food. Thus, the promotion of scientific research to innovate and improve berry production is necessary, especially in topics that strengthen the quality of fruit. Thus, murtilla berries emerge as a rich source of phytochemicals and vitamins and has been highly ranked among the dietary sources of polyphenols with antioxidant and antibacterial capacity.

An important point is the lack of genetic information about genome information and also a lack of information at the transcriptional level of the key genes related to the polyphenols or any other bioactive compound biosynthesis in murtilla. Thus, the lack of genetic information regarding the molecular mechanism commanding the bioactive compound formation during the development of the murtilla fruit highlights the importance of developing investigative frameworks to better understand their regulation. Progress in this arena can be useful in breeding programs that are necessary to improve the fruit quality and beneficial properties present in the native murtilla plants. Finally, with the currently available information about the murtilla fruit, it is possible to suggest that this fruit meets the requirements to reach the category of a new functional food and a good source of bioactive compounds.

Data Availability

The requirement for data availability does not apply, because this is a review.

Disclosure

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflicts of Interest

The authors declare no competing financial interests.

Acknowledgments

C.P.-P. acknowledges CONICYT for a doctoral scholarship #21140812. The Agencia Nacional de Investigación y Desarrollo (ANID, Chile) (grant REDES #190093 to L.M.-Q. and R.I.C.; grant REDES #190078 to P.R. and L.M.-Q.) and the Universidad Autónoma de Chile (ENLACE-UA-2019-008 grant) supported the work.

References

F. Medel, “Prospección de arbustos frutales en el sur de Chile,” Agro Sur, vol. 7, pp. 94–97, 1979.

C. Fredes, “Antioxidants in Chilean native berries,” Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromática, vol. 8, pp. 469–478, 2009.

M. E. Schreckinger, J. Lotton, M. A. Lila, and E. G. de Mejia, “Berries from South America: a comprehensive review on chemistry, health potential, and commercialization,” Journal of Medicinal Food, vol. 13, no. 2, pp. 233–246, 2010.

L. Fuentes, C. R. Figueroa, M. Valdenegro, and R. Vinet, “Patagonian berries: healthy potential and the path to becoming functional foods,” Food, vol. 8, no. 8, p. 289, 2019.

K. Rodríguez, K. Ah-Hen, A. Vega-Gálvez et al., “Changes in bioactive compounds and antioxidant activity during convective drying of murta (Ugni molinaeT.) berries,” International Journal of Food Science & Technology, vol. 49, no. 4, pp. 990–1000, 2014.

V. L. Singleton, R. Orthofer, and R. M. Lamuela-Raventós, “Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent,” Methods in Enzymology, vol. 299, pp. 152–178, 1999.

M. C. Aguirre, C. Delporte, N. Backhouse et al., “Topical anti-inflammatory activity of 2α-hydroxy pentacyclic triterpene acids from the leaves of Ugni molinae,” Bioorganic & Medicinal Chemistry, vol. 14, no. 16, pp. 5673–5677, 2006.

M. Rubilar, M. Pinelo, M. Ihl, E. Scheuermann, J. Sineiro, and M. J. Nuñez, “Murta leaves (Ugni molinae Turcz) as a source of antioxidant polyphenols,” Journal of Agricultural and Food Chemistry, vol. 54, no. 1, pp. 59–64, 2006.

M. Suwalsky, P. Orellana, M. Avello, F. Villena, and C. P. Sotomayor, “Human erythrocytes are affected in vitro by extracts of Ugni molinae leaves,” Food and Chemical Toxicology, vol. 44, no. 8, pp. 1393–1398, 2006.

A. Hoffmann, Flora Silvestre de Chile, Zona Araucana, Ediciones Claudio Gay, Santiago, Chile, 2nd edition, 1991.

A. Torres, I. Seguel, G. Contreras, and M. Castro, “Caracterización físico-química de frutos de murta,” Agric Técnica, vol. 59, pp. 260–270, 1999.

A. A. Kader, Quality and Safety Factors: Definition and Evaluation for Fresh Horticultural Crops, University of California, 1992.

E. Scheuermann, I. Seguel, A. Montenegro, R. O. Bustos, E. Hormazábal, and A. Quiroz, “Evolution of aroma compounds of murtilla fruits (Ugni molinae Turcz) during storage,” Journal of the Science of Food and Agriculture, vol. 88, no. 3, pp. 485–492, 2008.

G. Paliyath, D. P. Murr, A. K. Handa, and S. Lurie, Postharvest biology and technology of fruits, vegetables, and flowers, Wiley-Blackwell Publishing, Ames, 2008.

M. A. Awad and A. de Jager, “Influences of air and controlled atmosphere storage on the concentration of potentially healthful phenolics in apples and other fruits,” Postharvest Biology and Technology, vol. 27, no. 1, pp. 53–58, 2003.

L. Morales-Quintana and P. Ramos, “Chilean strawberry (Fragaria chiloensis): an integrative and comprehensive review,” Food Research International, vol. 119, pp. 769–776, 2019.

C. Parra-Palma, C. Úbeda, M. Gil, P. Ramos, R. I. Castro, and L. Morales-Quintana, “Comparative study of the volatile organic compounds of four strawberry cultivars and it relation to alcohol acyltransferase enzymatic activity,” Scientia Horticulturae, vol. 251, pp. 65–72, 2019.

R. Azodanlou, C. Darbellay, J.-L. Luisier, J.-C. Villettaz, and R. Amadò, “Quality assessment of strawberries (Fragaria species),” Journal of Agricultural and Food Chemistry, vol. 51, no. 3, pp. 715–721, 2003.

J. F. Ayala-Zavala, S. Y. Wang, C. Y. Wang, and G. A. González-Aguilar, “Effect of storage temperatures on antioxidant capacity and aroma compounds in strawberry fruit,” LWT - Food Science and Technology, vol. 37, no. 7, pp. 687–695, 2004.

C. Conde, P. Silva, N. Fontes et al., “Biochemical changes throughout grape berry development and fruit and wine quality,” Food, vol. 1, no. 1, pp. 1–22, 2007.

G. González Enei, Libro de Valorización: Resultados y Lecciones en Productos Agroindustriales Ricos en Antioxidantes, a Base de Berries Nativos, Fundación para la Innovación Agraria (FIA), Santiago, Chile, 1st edition, 2009.

X. A. Durán, S. C. Saavedra, M. R. Bravo, and M. M. Gutiérrez, “Formulation and physicochemical evaluation of vinegars produced from murta (Ugni molinae turcz.) and maqui (Aristotelia chilensis (Molina) stunz) with bees’ honey (Apis mellifera L.) at laboratory scale,” Boletim do Centro de Pesquisa de Processamento de Alimentos, vol. 32, no. 2, pp. 167–176, 2014.

W. Batista-Silva, V. L. Nascimento, D. B. Medeiros et al., “Modifications in organic acid profiles during fruit development and ripening: correlation or causation?” Frontiers in Plant Science, vol. 9, p. 1689, 2018.

J. A. Moraga, Determinación del Calor Específico de Murta (Ugni molinae Turcz) y Arándano (Vaccinium corymbosum L.) en un Rango de Temperatura Entre 20°C y 80°C por el Método de la Calorimetría Diferencial de Barrido, [Ph.D. thesis], Universidad Austral de Chile, Valdivia, Chile, 2008.

F. S. Merino, Elaboración de Láminas de Fruta (“Fruit Leathers”) a Partir de Pulpa de Murta (Ugni molinae Turcz.) Congelada, [Ph.D. thesis], University Austral de Chile, Valdivia, Chile, 2002.

H. Schmidt-Hebbel, I. Pennachiotti, L. Masson et al., Tabla de composición química de los alimentos chilenos. Depto. de Química y Tecnología de los Alimentos, Universidad de Chile, Santiago, Chile, 1990.

C. Parra-Palma, L. Morales-Quintana, and P. Ramos, “Phenolic content, color development, and pigment-related gene expression: a comparative analysis in different cultivars of strawberry during the ripening process,” Agronomy, vol. 10, no. 4, p. 588, 2020.

P. Arancibia-Avila, J. Namiesnik, F. Toledo et al., “The influence of different time durations of thermal processing on berries quality,” Food Control, vol. 26, no. 2, pp. 587–593, 2012.

P. Ramos, R. Herrera, and M. A. Moya-León, “Anthocyanins: Food Sources and Benefits to Consumer’s Health,” in Handbook of Anthocyanins: Food Sources, Chemical Applications and Health Benefits, L. M. Warner, Ed., pp. 363–384, Nova Science Publishers Inc., 2014.

H. Speisky, C. López-Alarcón, M. Gómez, J. Fuentes, and C. Sandoval-Acuña, “First web-based database on total phenolics and oxygen radical absorbance capacity (ORAC) of fruits produced and consumed within the South Andes region of South America,” Journal of Agricultural and Food Chemistry, vol. 60, no. 36, pp. 8851–8859, 2012.

A. Ruiz, I. Hermosin-Gutierrez, C. Mardones et al., “Polyphenols and antioxidant activity of calafate (Berberis microphylla) fruits and other native berries from southern Chile,” Journal of Agricultural and Food Chemistry, vol. 58, no. 10, pp. 6081–6089, 2010.

P. Arancibia-Avila, F. Toledo, E. Werner et al., “Partial characterization of a new kind of Chilean murtilla-like berries,” Food Research International, vol. 44, no. 7, pp. 2054–2062, 2011.

C. Parra-Palma, E. Fuentes, I. Palomo, C. Torres, M. Moya, and P. Ramos, “Linking the platelet antiaggregation effect of different strawberries species with antioxidants: metabolomic and transcript profiling of polyphenols,” Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas, vol. 17, pp. 36–52, 2018.

A. Brito, C. Areche, B. Sepúlveda, E. Kennelly, and M. Simirgiotis, “Anthocyanin characterization, total phenolic quantification and antioxidant features of some Chilean edible berry extracts,” Molecules, vol. 19, no. 8, pp. 10936–10955, 2014.

M. C. Gómez-Guillén, M. Ihl, V. Bifani, A. Silva, and P. Montero, “Edible films made from tuna-fish gelatin with antioxidant extracts of two different murta ecotypes leaves (Ugni molinae Turcz),” Food Hydrocolloids, vol. 21, no. 7, pp. 1133–1143, 2007.

B. Russo, F. Picconi, I. Malandrucco, and S. Frontoni, “Flavonoids and insulin-resistance: from molecular evidences to clinical trials,” International Journal of Molecular Sciences, vol. 20, no. 9, p. 2061, 2019.

K. S. Ah-Hen, K. Mathias-Rettig, L. S. Gómez-Pérez, G. Riquelme-Asenjo, R. Lemus-Mondaca, and O. Muñoz-Fariña, “Bioaccessibility of bioactive compounds and antioxidant activity in murta (Ugni molinae T.) berries juices,” Journal of Food Measurement and Characterization, vol. 12, no. 1, pp. 602–615, 2018.

R. Rozzi and F. Massardo, “Las plantas medicinales chilenas II y III,” Informativos Nueva Medicina, vol. 1, pp. 16-17, 1994.

I. Jofré, C. Pezoa, M. Cuevas et al., “Antioxidant and vasodilator activity of Ugni molinae Turcz. (murtilla) and its modulatory mechanism in hypotensive response,” Oxidative Medicine and Cellular Longevity, vol. 2016, 11 pages, 2016.

M. Aswad, M. Rayan, S. Abu-Lafi et al., “Nature is the best source of anti-inflammatory drugs: indexing natural products for their anti-inflammatory bioactivity,” Inflammation Research, vol. 67, no. 1, pp. 67–75, 2018.

R. I. Castro, F. Valenzuela-Riffo, and L. Morales-Quintana, “In Silico and In Vitro Analysis of the 4,4,4-((1,3,5-Triazine-2,4,6-triyl)tris(azanediyl))triphenol), an Antioxidant Agent with a Possible Anti-Inflammatory Function,” BioMed Research International, vol. 2019, Article ID 9165648, 9 pages, 2019.

T. Hussain, B. Tan, Y. Yin, F. Blachier, M. C. B. Tossou, and N. Rahu, “Oxidative stress and inflammation: what polyphenols can do for us?” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 7432797, 9 pages, 2016.

S. Salzano, P. Checconi, E.-M. Hanschmann et al., “Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal,” Proceedings of the National Academy of Sciences, vol. 111, no. 33, pp. 12157–12162, 2014.

L. E. Goity, M.-J. Queupil, J. Daniela et al., “An HPLC-UV and HPLC-ESI-MS based method for identification of anti-inflammatory triterpenoids from the extracts of Ugni molinae,” Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas, vol. 12, pp. 108–116, 2013.

J. Arancibia-Radich, M. Peña-Cerda, D. Jara et al., “Comparative study of anti-inflammatory activity and qualitative-quantitative composition of triterpenoids from ten genotypes of Ugni molinae,” Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas, vol. 15, pp. 274–287, 2016.

M. Junqueira-Gonçalves, L. Yáñez, C. Morales, M. Navarro, R. A. Contreras, and G. Zúñiga, “Isolation and characterization of phenolic compounds and anthocyanins from murta (Ugni molinae Turcz.) fruits. Assessment of antioxidant and antibacterial activity,” Molecules, vol. 20, no. 4, pp. 5698–5713, 2015.

C. Shene, A. K. Reyes, M. Villarroel, J. Sineiro, M. Pinelo, and M. Rubilar, “Plant location and extraction procedure strongly alter the antimicrobial activity of murta extracts,” European Food Research and Technology, vol. 228, no. 3, pp. 467–475, 2009.

K. S. Ah-Hen, A. Vega-Gálvez, N. O. Moraga, and R. Lemus-Mondaca, “Modelling of rheological behaviour of pulps and purées from fresh and frozen-thawed murta (Ugni molinae Turcz) berries,” International Journal of Food Engineering, vol. 8, no. 3, 2012.

K. Ah-Hen, C. E. Zambra, J. E. Aguëro, A. Vega-Gálvez, and R. Lemus-Mondaca, “Moisture diffusivity coefficient and convective drying modelling of murta (Ugni molinae Turcz): influence of temperature and vacuum on drying kinetics,” Food and Bioprocess Technology, vol. 6, no. 4, pp. 919–930, 2013.

E. Taboada, P. Fisher, R. Jara et al., “Isolation and characterisation of pectic substances from murta (Ugni molinae Turcz) fruits,” Food Chemistry, vol. 123, no. 3, pp. 669–678, 2010.

J. E. Ramirez, R. Zambrano, B. Sepúlveda, E. J. Kennelly, and M. J. Simirgiotis, “Anthocyanins and antioxidant capacities of six Chilean berries by HPLC–HR-ESI-ToF-MS,” Food Chemistry, vol. 176, pp. 106–114, 2015.

M. Chacón-Fuentes, L. Parra, M. Lizama, I. Seguel, A. Urzúa, and A. Quiroz, “Plant flavonoid content modified by domestication,” Environmental Entomology, vol. 46, no. 5, pp. 1080–1089, 2017.

M. Chacón-Fuentes, L. Parra, C. Rodriguez-Saona, I. Seguel, R. Ceballos, and A. Quiroz, “Domestication in murtilla (Ugni molinae) reduced defensive flavonol levels but increased resistance against a native herbivorous insect,” Environmental Entomology, vol. 44, no. 3, pp. 627–637, 2015.

M. Peña-Cerda, J. Arancibia-Radich, P. Valenzuela-Bustamante et al., “Phenolic composition and antioxidant capacity of Ugni molinae Turcz. leaves of different genotypes,” Food Chemistry, vol. 215, pp. 219–227, 2017.

C. L. de Dicastillo, F. Bustos, X. Valenzuela, G. López-Carballo, J. M. Vilariño, and M. J. Galotto, “Chilean berry _Ugni molinae_ Turcz. fruit and leaves extracts with interesting antioxidant, antimicrobial and tyrosinase inhibitory properties,” Food Research International, vol. 102, pp. 119–128, 2017.

M. A. Avello, E. R. Pastene, E. D. Bustos, M. L. Bittner, and J. A. Becerra, “Variation in phenolic compounds of Ugni molinae populations and their potential use as antioxidant supplement,” Revista Brasileira de Farmacognosia, vol. 23, no. 1, pp. 44–50, 2013.

M. Suwalsky and M. Avello, “Antioxidant capacity of Ugni molinae fruit extract on human erythrocytes: an in vitro study,” The Journal of Membrane Biology, vol. 247, no. 8, pp. 703–712, 2014.