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Antioxidant activity and physico-chemical analysis of Campomanesia rufa (O.Berg) Nied. fruits

Atividade antioxidante e análise físico-química de frutos de Campomanesia rufa (O.Berg) Nied.

ABSTRACT

Campomanesia rufa (O. Berg) Nied. is a native Cerrado species that presents great edible potential. However, it is a species “in danger of extinction” as recommended by the International Union for the Conservation of Nature (IUCN). No technical and scientific information about the species exists, thus demonstrating the importance of its research. The present work aimed at the physical and chemical characterization of immature and mature C. rufa fruits. The fruits showed a change in coloration from green (b * = 25.11, h = 122.43) to yellowish-green (b * = 34.26 , h = 115.73), an increase in mass (6.54 g to 10.88 g), diameter (23.76 mm to 28.03 mm) and soluble solids (8.00 to 10.80%). The fruits presented high levels of total (1246.35 mg 100 g-1) and soluble pectin (195.93 mg 100 g-1), high water content (78.86 g 100 g-1), low pH value (3.40), and high citric acid content (1.2%). However, the fruits had low protein (0.81 g 100 g-1), lipid contents, and low caloric values (64.76 kcal 100 g-1). The fruits presented significant values of carotenoids, phenolic compounds (312.47 mg 100 g-1), vitamin C (263.60 mg 100 g-1) as well as good in vitro antioxidant activity (1862.81 µM g-1). The results obtained indicate that C. rufa fruits showed a similar composition to the fruits of other Campomanesia species, and their biological properties should be investigated additionally under in vivo conditions.

Index terms:
Cerrado; Myrtaceae; casaqueira; endangered species; vitamin C.

RESUMO

Campomanesia rufa (O. Berg) Nied. é uma espécie nativa do Cerrado que apresenta grande potencial comestível. No entanto, é uma espécie “em perigo de extinção”, segundo a União Internacional para a Conservação da Natureza (IUCN). Não existe informação técnica e científica sobre a espécie, demonstrando a importância das pesquisas. O presente trabalho teve como objetivo a caracterização físico-química de frutos imaturos e maduros de C. rufa. Os frutos apresentaram alteração na coloração de verde (b * = 25.11, h = 122.43) para verde amarelado (b * = 34.26, h = 115.73), aumento na massa (6.54 g para 10.88 g), diâmetro (23.76 mm a 28.03 mm) e sólidos solúveis (8.00 a 10.80%). Os frutos apresentaram altos teores de pectina total (1246.35 mg 100 g-1) e solúvel (195.93 mg 100 g-1), alto teor de água (78.86 g 100 g-1), baixo valor de pH (3.40) e alto ácido cítrico conteúdo (1.2%). No entanto, os frutos apresentaram baixo teor de proteína (0.81 g 100 g-1), teor de lipídios e baixo valor calórico (64.76 kcal 100 g-1). Os frutos apresentaram valores significativos de carotenóides, compostos fenólicos (312.47 mg 100 g-1), vitamina C (263.60 mg 100 g-1) e boa atividade antioxidante in vitro (1862.81 µM g-1). Os resultados obtidos indicam que os frutos de C. rufa apresentam composição semelhante aos frutos de outras espécies de Campomanesia, e suas propriedades biológicas devem ser investigadas adicionalmente em condições in vivo.

Termos para indexação:
Cerrado; Myrtaceae; casaqueira; espécie ameaçada de extinção; vitamina C.

INTRODUCTION

The Cerrado biome occupies 22% of the Brazilian territory and houses a vast and diverse genetic heritage that is unique in the world (Reis; Schmiele, 2019REIS, A. F.; SCHMIELE, M. Características e potencialidades dos frutos do Cerrado na indústria de alimentos. Brazilian Journal of Food Technology, 22:e2017150, 2019.). The Cerrado holds 40% of the endemic plant species and one-third of all Brazilian biodiversity (Luz et al., 2019LUZ, L. D. et al. Multiproxy analysis (Phytoliths, stable isotopes, and c/n) as indicators of paleoenvironmental changes in a Cerrado site, Southern Brazil. Revista Brasileira de Paleontologia, 22(1):15-29, 2019.). Many of the native Cerrado species produce fruits with commercial potential for natural consumption and the production of derivatives such as juices, jellies, and liquors (Neves et al., 2015NEVES, L. C. et al. Post-harvest nutraceutical behaviour during ripening and senescence of 8 highly perishable fruit species from the Northern Brazilian Amazon region. Food Chemistry , 174:188-196, 2015. ). In addition, they can also be employed to obtain secondary metabolites such as phenolic compounds, antioxidants, and antiproliferative agents of human carcinogenic cells (Araújo et al., 2018ARAÚJO, A. C. M. A. et al. Bioactive compounds and chemical composition of Brazilian Cerrado fruits’ wastes: pequi almonds, murici, and sweet passionfruit seeds. Food Science and Technology, 38:203-214, 2018. ).

However, there is a large deficit of scientific studies on the native Cerrado species (Arruda; Pastore, 2019ARRUDA, H. S.; PASTORE, G. M. Araticum (Annona crassiflora Mart.) as a source of nutrients and bioactive compounds for food and non-food purposes: A comprehensive review. Food Research International, 123:450-480, 2019. ). This reduces the possibilities of developing new products and expanding the use of species already consumed by the local populations (Carvalho et al., 2019CARVALHO, J. T. de G. de et al. Medicinal plants from Brazilian Cerrado: Antioxidant and anticancer potential and protection against chemotherapy toxicity. Oxidative Medicine and Cellular Longevity, 2019:1-16, 2019. ). For this reason, scientific studies were focused on properties and the uses of native plants (Arruda; Pastore, 2019ARRUDA, H. S.; PASTORE, G. M. Araticum (Annona crassiflora Mart.) as a source of nutrients and bioactive compounds for food and non-food purposes: A comprehensive review. Food Research International, 123:450-480, 2019. ).

The Myrtaceae family is second in terms of diversity in the phytogeographical domain of the Cerrado (Silvestre; Miranda; De-Carvalho, 2019SILVESTRE, G. J. S.; MIRANDA, S. C.; DE-CARVALHO, P. S. Levantamento das espécies de Myrtaceae Juss. na Serra do Abrante, Palmeiras de Goiás. In: MIRANDA, S. C. et al. (Ed.). Tópicos em conservação e manejo do cerrado: Biodiversidade, solos e uso sustentável. Goiâna: Kelps, p.31-64, 2019. ). The Campomanesiagenus belongs to the Myrtaceae family and possesses food, ornamental, and pharmaceutical potential (Zuninga et al., 2018ZUNINGA, A. et al. Capacidade antioxidantes de frutos nativos do Cerrado (Hancornia speciosa, Campomanesia xanthocarpa, Eugenia dysenterica): Uma breve revisão. Desafios, 5(1):128-134, 2018.; Carvalho et al., 2019CARVALHO, J. T. de G. de et al. Medicinal plants from Brazilian Cerrado: Antioxidant and anticancer potential and protection against chemotherapy toxicity. Oxidative Medicine and Cellular Longevity, 2019:1-16, 2019. ). It has a limited distribution in the phytogeographical domains of the Atlantic and Cerrado Forest in Minas Gerais state, Brazil (Reflora, 2020REFLORA. Campomanesia. In: Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. 2020. Available in: <Available in: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB10335 >. Access in: March, 09, 2020.
http://floradobrasil.jbrj.gov.br/reflora...
).

Chemical studies with Campomanesia genera such as Campomanesia adamantium, Campomanesia pubescens, Campomanesia cambessedeana, Campomanesia corimbosa, Campomanesia aurea, Campomanesia xanthocarpa, Campomanesia guazumifolia, Campomanesia reitziana, and Campomanesia lineatifolia showed high content of phenolic compounds, antioxidants, and vitamin C (Sá et al., 2018SÁ, S. et al. Phytochemistry and antimicrobial activity of Campomanesia adamantium. Revista Brasileira de Farmacognosia, 28(3):303-311, 2018.; Cardozo et al., 2018CARDOZO, C. M. L. et al. Therapeutic potential of Brazilian CerradoCampomanesiaspecies on metabolic dysfunctions. Molecules, 23(9):e2336, 2018. ; De Andrade Silva; Fonseca, 2016DE ANDRADE SILVA, C. A.; FONSECA, G. G. Brazilian savannah fruits: Characteristics, properties, and potential applications. Food Science and Biotechnology, 25(5):1225-1232, 2016. ; Da Silva et al., 2016DA SILVA, É. R. et al. Anti-inflammatory evaluation and toxicological analysis of Campomanesia xanthocarpa Berg. Inflammation, 39(4):1462-1468, 2016.; Emer et al., 2018EMER, A. et al. The physicochemical properties of fruits and seed germination of Campomanesia aurea O. Berg. Acta Scientiarum - Biological Sciences, 40:e35007, 2018.; Salmazzo et al., 2019SALMAZZO, G. R. et al. Chemical composition and antiproliferative antioxidant and trypanocidal activities of the fruits from Campomanesia xanthocarpa (Mart.) O. Berg (Myrtaceae). Natural Product Research, 1478-6427, 2019.; De Souza Duarte et al., 2020DE SOUZA DUARTE, L. et al. Campomanesia genus: A literature review of nonvolatile secondary metabolites, phytochemistry, popular use, biological activities, and toxicology. Eclética Química Journal, 45(2):12-22, 2020.).

Campomanesia rufa is used by the local population. However, studies on C. rufa are scarce (Sant’Ana et al., 2018SANT’ANA, C. R. O. et al. In vitro propagation of Campomanesia rufa: An endangered fruit species. Ciência e Agrotecnología, 42(4):372-380, 2018. ). It is classified as being ‘vulnerable’ by the Red List maintained by the International Union for Conservation of Nature - IUCN (1998INTERNATIONAL UNION FOR CONSERVATION OF NATURE - IUCN. The IUCN red list of threatened species. 1998. Version 2020-2. Available in: <Available in: https://www.iucnredlist.org/ >. Access in: March, 14, 2020.
https://www.iucnredlist.org/...
), thus demonstrating the importance of exploratory studies with the species. Such studies will enable us to understand how these fruits can be utilized commercially in a better manner (Araújo et al., 2018ARAÚJO, A. C. M. A. et al. Bioactive compounds and chemical composition of Brazilian Cerrado fruits’ wastes: pequi almonds, murici, and sweet passionfruit seeds. Food Science and Technology, 38:203-214, 2018. ).

Given the above arguments, this work aimed to characterize the physical and chemical properties of C. rufa during the immature and mature stages of development.

MATERIAL AND METHODS

Plant material

Immature and mature fruits of C. rufa (Figure 1) were collected from a natural population located at 21° 13’35.5” S latitude and 44° 59’00.7” W longitude in the region of Lavras, Minas Gerais state, Brazil. The climate in this region is characterized as a rainy season with dry winters and rainy summers with an average annual temperature of 19 ºC and an average annual rainfall of 1,530 mm.

Figure 1
Fruits of Campomanesia rufa.

The identification of the species was carried out by cross-checking with the plants maintaned in the ESAL Herbarium of the Federal University of Lavras with the collection number ESAL21198. Seeds with incomplete embryo development were considered immature fruits, and those with complete embryo development were considered mature fruits. For the analysis, both stages of fruits were used.

Diameter, mass, and pulp yield

The mean longitudinal and transverse diameters of the fruits were determined using a digital caliper. The average mass of the fruits was determined by the individual weighing of the fruits on a semianalytic scale.

To calculate the pulp yield, the initial weight of the ripe fruit, and the weight of the pulp was measured. The calculation was performed using the following equation: pulp weight/fruit weight * 100.

Color and firmness

The staining was determined using a Konica Minolta CR-400 colorimeter calibrated according to the CIE system with L*, a*, b*, h, and C* (Illuminant D65). The L* coordinate represented the brightness with values between 0 (totally black) and 100 (totally white). The coordinate a* assumed values between -80 to +100 in which the ends corresponded to green and red, respectively. The b* coordinate ranged from -50 to +70 with blue to yellow intensity. The hue angle (h) corresponded to the hue and identified the color between 0 ° and 360 ° and the Chroma (C*) was saturation or intensity of the color as outlined by McGuire (1992McGUIRE, R. G. Reporting of objective color mensurements. HortScience, 27(12):1254-1255, 1992. ).

The firmness was determined in a Stable Micro System model TATX2i texturometer using the P/6N probe (2 mm in diameter). The penetration force of the fruits was measured at a speed of 5 mm/s and with a penetration distance of 30 mm with values previously determined. An HDP/90 platform was used as the base. The firmness of the fruits was expressed in Newton (N).

Titratable Acidity (AT), pH, Soluble Solids (SS), and SS/AT ratio

The determination of titratable acidity (AT) was performed by titration with a 0.01 M sodium hydroxide solution (NaOH) using phenolphthalein as an indicator according to methods from the (Adolfo Lutz Institute - IAL, 2005INSTITUTO ADOLFO LUTZ - IAL. Métodos físico-químicos para análise de alimentos. 4. ed. Brasília: Ministério da Saúde. 2005. 1018p.). The results were expressed as percent citric acid. The pH of the pulp was determined using a TEC-3 MP Tecnal® pH meter according to the technique of the Adolfo Lutz Institute (IAL, 2005). The soluble solids content (SS) was determined using a digital refractometer, and the results were expressed in percentage. The soluble solids/titratable acidity ratio (SS/AT ratio) was determined by dividing the first variable by the second variable (IAL, 2005INSTITUTO ADOLFO LUTZ - IAL. Métodos físico-químicos para análise de alimentos. 4. ed. Brasília: Ministério da Saúde. 2005. 1018p.).

Proximate analysis

Proximate analysis (g 100 g-1) was performed according to the methods proposed by (Association of Official Analytical Chemistry - AOAC, 2012ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTRY - AOAC. Official methods of analysis. 19th ed. Gaithersburg, 2012. 3000p. ). The moisture content was determined by oven drying at 65 °C until a consistent weight was reached. The lipid content was determined in a Soxhlet apparatus. The protein content was determined by the Kjeldahl method considering a conversion factor of 6.25. The crude fiber was determined by the gravimetric method. Ash determination was performed by the gravimetric method of incineration in a muffle furnace at 550 ºC. Nitrogen-free extract (NFE) was determined from the formula: NFE = 100 - (moisture + lipids + proteins + fiber + ash). The results of the proximate analyses were expressed in g 100 g-1. The caloric value was estimated using Atwater’s conversion values: 9 kcal per g of lipids, 4 kcal per g of protein, and 4 kcal per g of carbohydrates (De Angelis, 1977DE ANGELIS, R. C. Fisiologia da nutrição: Fundamentos para nutrição e desnutrição. São Paulo: Edart, v. 1, p.43-53, 1977.).

Total and Soluble Pectin

The extraction of pectic substances was performed according to the technique described by McCready and McComb (1952)McCREADY, P. M.; McCOMB, E. A. Extraction and determination of total pectin material. Analytical Chemistry, 24(12):1586-1588, 1952.. Here, 5 g of fresh fruit was homogenized with 45 mL of 70% ethyl alcohol and the homogenate was left to stand for 18 h to remove the total sugars. Subsequently, the homogenate was filtered and washed thrice with 30 mL of 70% ethyl alcohol. The filtrate was used to determine the total sugars, and the alcohol-insoluble residue (AIR) was homogenized with 50 mL of distilled water for 1 h and again filtered to determine the soluble pectin.

For the determination of total pectin, 50 mL of versene solution (0.5% EDTA) was added to the homogenate (after the removal of sugars), and the pH was increased to 11.5 with NaOH solution. The mixture was allowed to stand for 30 min, and the pH was reduced to 5.5 using acetic acid. Further, 0.1 g of pectinase was added and stirred for 1 h. The mixture was filtered, and a total volume of 100 mL was obtained with versene solution.

For the determination of soluble pectin (after the extraction of sugars), the filtered residue (AIR) was placed in Erlenmeyer flasks, and 50 mL of distilled water was added. It was then homogenized on a shaker for 1 h and filtered with a quantitative filter paper.

The colorimetric quantification was performed by the technique of Bitter and Muir (1962BITTER, T.; MUIR, H. M. A modified uronic acid carbazole reaction. Analytical Biochemistry, 4(4):330-334, 1962. ). The results were expressed in mg of galacturonic acid 100 g-1 of pulp.

Total Sugars

The filtrate obtained from pectin extraction (AIR) was heated for evaporation of the alcohol until the volume was reduced to 10 mL. Distilled water was added to make a final volume of 50 mL. This solution was used for the quantification of sugars by the method of Somogyi adapted by Nelson (1944NELSON, N. A photometric adaptation of somogyi method for the determination of glucose. Journal of Biological Chemistry, 135:135-375, 1944.), and results were expressed in g of glucose 100 g-1 of pulp.

Vitamin C

For vitamin C determination, 2 g of the sample was homogenized in 20 mL of 0.5% oxalic acid using the Polytron crusher. Subsequently, the homogenate was transferred to the stirring table for 30 min and then filtered (qualitative filter paper, 15 cm in diameter, Unifil®). The extract obtained was used to determine vitamin C. The ascorbic acid content (after oxidation to dehydroascorbic acid) was determined by the colorimetric method using 2,4 dinitrophenylhydrazine according to the method of Strohecker and Henning (1967STROHECKER, R.; HNNEING, H. M. Análisis de vitaminas: Métodos comprobados. Madrid: Paz Montalvo, 1967, 428p. ). The results were expressed as mg of ascorbic acid 100 g-1 of pulp.

Carotenoids

A combination of solvents was used for the extraction of carotenoids: acetone/petroleum ether. The analysis consisted of sampling and sample preparation, extraction and partition with a solvent, saponification and washing, solvent concentration, chromatographic separation, and identification and quantification with a spectrophotometer. The extraction of carotenoids was performed according to Rodriguez-Amaya (2001RODRIGUEZ-AMAYA, D. B. A guide to carotenoid analysis in foods. Washington: Internacional Life Sciences Institute Press, 2001. 64p.). The sample (5 g) was kept in a flask in the dark, and 20 mL of cold acetone (P.A.) was added. The contents were stirred for 20 min and filtered in an Erlenmeyer Flask with the aid of a filter paper. The sample was then washed with acetone until the residue left on the filter paper turned transparent (washed thrice with 20 mL, 5 mL, and 15 mL of acetone (P.A.)). The filtrate was transferred to a separating funnel, and the funnel was covered with aluminum foil. Next, 30 mL of petroleum ether and 70 mL of distilled water were added to it. The denser liquid was discarded. This procedure was repeated thrice to remove acetone.

The extract was transferred to a 100 mL volumetric flask, and petroleum ether was added to make the final volume to 100 mL. The contents were filtered again and stored in a dark bottle until their absorbance was recorded. The “white” to reset the equipment was P.A.

Carotenoids were quantified using a spectrophotometric method (Rodriguez-Amaya, 2001RODRIGUEZ-AMAYA, D. B. A guide to carotenoid analysis in foods. Washington: Internacional Life Sciences Institute Press, 2001. 64p.). Carotenoids like α-carotene, β-carotene, δ-carotene, γ-carotene, and lycopene were measured at 444 nm, 450 nm, 456 nm, 462 nm, and 470 nm, respectively. The content of each carotenoid was calculated according to the formula: μg g1=A x V x 106/A1cm1% x M x 100. A was the absorbance of the solution at a specific wavelength, V was the final solution volume, A1 cm -1% was the coefficient of molar absorptivity of the pigment in a given specific solvent (petroleum ether), and M was the mass of the sample taken for analysis in g. Results were expressed in µg 100 g-1 fruit.

Total phenolic content and antioxidant activity

Extraction

The extraction was performed according to the methodology adopted by Rufino et al. (2010RUFINO, M. S. M. et al. Bioactive compounds and antioxidante capacities of 18 no-traditional tropical fruits from Brazil. Food Chemistry , 121(4):996-1002, 2010.). For this, 1 g of the sample was weighed in a 50 mL beaker, and 10 mL of 50% methanol was added to it; the solution was homogenized and left to stand for 20 min in the dark. Later, the solution was incubated in an ultrasound bath for 15 min and filtered (paper qualitative filter, 15 cm in diameter, Unifil®); the supernatant was transferred to a dark flask. To the residue of the first extraction, 10 mL of 70% acetone was added. The solution was homogenized and left to stand for 20 min in the dark. Subsequently, it was incubated in an ultrasound bath for 15 min and then filtered (qualitative filter paper, 15 cm of diameter, Unifil®). The supernatant was transferred to the dark flask containing the first supernatant, where they were homogenized again. The obtained extract was used to determine the total phenolic content and the antioxidant capacity by the ABTS and FRAP methods.

Total phenolic content

The total phenolic content was determined by the Folin-Ciocalteu method (Waterhouse, 2002WATERHOUSE, A. L. Determination of total phenolics. In: WROLSTAD, R. E. (Ed.). Current protocols in food analytical chemistry. United States of America: Wiley, p.1073-1080, 2002.). The blue color produced by the reduction of the Folin-Ciocalteu reagent by the phenols was measured spectrophotometrically at the absorption wavelength of 750 nm. The phenolic content was calculated by the equation of the straight line obtained from the standard curve of gallic acid. The results were expressed in milligrams of gallic acid equivalent (GAE) 100 g-1 pulp.

Antioxidant activity

For the determination of the antioxidant activity, the ABTS radical capture method and the iron reduction method (FRAP) were used.

The antioxidant activity by the ABTS °+ radical capture method was performed according to Rufino et al. (2007RUFINO, M. D. S. M. et al. Metodologia científica: Determinação da atividade antioxidante total em frutas pela captura do radical livre ABTSº+.Embrapa Agroindústria Tropical-Comunicado Técnico . 2007. 4p). The ABTS °+ radical capture solution was prepared by mixing a 5 mL stock solution of 7.0 mM ABTS with 88 mL of 140 mM potassium persulfate solution. The mixture was kept in the dark at room temperature for 16 h. Then, 1 mL of this mixture was diluted in ethyl alcohol until an absorbance of 0.70 nm ±0.05 nm was obtained at 734 nm.

The absorbance (734 nm) of the samples was determined at room temperature after 6 min of reaction time. Trolox (6-Hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid) was used as the reference antioxidant. The results were expressed in µM of Trolox g-1.

The total antioxidant activity by the FRAP method was performed according to Rufino et al. (2006RUFINO, M. D. S. M. et al. Metodologia científica: Determinação da atividade antioxidante total em frutas pelo método de redução do ferro (FRAP). Embrapa Agroindústria Tropical-Comunicado Técnico. 2006. 4p). The FRAP reagent was obtained from the combination of 25 mL of 0.3 M acetate buffer, 2.5 mL of a 10 mM TPTZ solution, and 2.5 mL of a 20 mM aqueous solution of ferric chloride.

The absorbance (595 nm) of the samples was determined after 30 min of reaction time in a water bath at 37 °C. Ferrous sulfate was used as a reference. The results were expressed as µM ferrous sulfate g-1.

Statistical analysis

For the analyses of longitudinal and transverse diameter, fresh mass, pulp yield, and staining and firmness, 30 replications per stage of maturation were used. For other analyses, ten replicates per stage of maturation were used. The design was completely randomized, the data were analyzed using the R software v. 3.5.2 (R Core Team, 2019R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2019. Available in: <Available in: https://www.R-project.org/ >. Access in: September, 29, 2020.
https://www.R-project.org/...
), and the means were compared by the Student’s t-test considering p <0.05 (Ferreira; Cavalcanti; Nogueira, 2014FERREIRA, E. B.; CAVALCANTI, P. P.; NOGUEIRA, D. A. ExpDes: An R Package for ANOVA and Experimental Designs. Applied Mathematics, 5(19): 2952-2958, 2014.) as significant.

RESULTS AND DISCUSSION

The fruits of C. rufa presented increased longitudinal and transverse diameters after ripening, and this was accompanied by an increase in their mass (Table 1). The pulp yield in the mature fruits was 51.35%.

Table 1:
Longitudinal and transverse diameters, fresh mass, L*, a*, b*, h, C*, firmness, total and soluble pectin in the immature and mature fresh C. rufa fruits.

It was possible to identify the color development associated with maturation (Table 1). In the mature fruits of Campomanesia cambesedeana, the coloration was darker (L* = 26.09) while Campomanesia pubescens changed from a darker (L* = 4.65) to a lighter color (L* = 36.80) during development (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ; Silva et al., 2009SILVA, E. P. D. et al. Caracterização física, química e fisiológica de gabiroba (Campomanesia pubescens) durante o desenvolvimento. Ciência e Tecnologia de Alimentos , 29(4):803-809, 2009. ). No representative changes were observed in the a* coordinate between the immature and mature fruits, and the fruits remained in the green region. However, the b* coordinate showed an increased intensity in the yellow region (Table 1, Figure 1).

The values of °h (hue angle) indicated that the coloration of the fruits was between pure yellow and pure green. The color changed from green to yellowish-green with maturation, thus demonstrating an increased chromaticity with maturation (Table 1).

C. pubescens fruits also showed increased yellowing during maturation that was different from the reddish color of mature C. cambessedeana fruits. For C. phaea fruits, the green color prevailed with decreased gloss and increased opacity with ripening (Silva et al., 2009SILVA, E. P. D. et al. Caracterização física, química e fisiológica de gabiroba (Campomanesia pubescens) durante o desenvolvimento. Ciência e Tecnologia de Alimentos , 29(4):803-809, 2009. ; Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ; Bianchini et al., 2016BIANCHINI, F. G. et al. Caracterização morfológica e química de frutos de cambucizeiro. Bragantia, 75(1):10-18, 2016. ).

The firmness values of the C. rufa fruits decreased during ripening; the values were 12.65 N and 1.27 N in the immature and mature fruits, respectively (Table 1, Figure 1). Firmness value is an important attribute of fruits for the industry chain because it directly affects the fruit quality, consumer preference, transportability, and shelf life. Moreover, it also affects the ability of the cultivars to be machine harvested and in reducing the financial and labor costs (Li et al., 2018LI, B. et al. Application of hyperspectral imaging for nondestructive measurement of plum quality attributes. Postharvest Biology and Technology , 141:8-15, 2018.; Cappai et al., 2018CAPPAI, F. et al. Molecular and genetic bases of fruit firmness variation in blueberry: A review. Agronomy, 8(9)1-20, 2018.).

Pectic substances are the main components responsible for the change in the texture of fruits and vegetables (Huang et al., 2019HUANG, W. et al. Morphology and cell wall composition changes in lignified cells from loquat fruit during postharvest storage. Postharvest Biology and Technology, 157:1-12, 2019.). The immature and mature fruits showed a high total pectin content (860.05 and 1246.35 mg 100 g-1, respectively) (Table 1) compared to the mature fruits of C. cambessedeana (258.54 mg 100 g-1) and Byrsonima crassifolia (746.81 mg 100 g-1) (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ). Similarly, the soluble pectin content in the mature fruits of C. rufa was 195.93 mg 100 g-1, whereas it was 131.15 mg 100 g-1 in C. cambessedeana and 72.18 mg 100 g-1 in B. crassifolia mature fruits (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ). Pectin gets solubilized with ripening and makes the fruit softer. This explains the increase in the soluble pectin concentration in the mature fruit of C. rufa compared to that in the immature fruits (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ) (Table 1).

The pH values decreased from 3.60 to 3.40 with the maturation of C. rufa fruits (Table 2). The mature fruits had higher levels of acidity than those of C. cambessedeana (4.25) and similar acidity values to that of the C. lineatifolia (3.47) fruits (Table 2) (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ; Lima et al., 2016LIMA, J. S. S. et al. Caracterização físico-química de gabiroba (Campomanesia lineatifolia) e murta (Blepharocalyx salicifolius) nativas da região serrana de Ibiapaba-CE. Revista Caatinga, 29(3):753-757, 2016. ). The C. phaea fruits displayed greater acidity (2.80) (Sanches et al., 2016SANCHES, A. M. C. et al. Physicochemical variability of cambuci fruit (Campomanesia phaea) from the same orchard, from different locations and at different ripening stages. Journal of the Science of Food and Agriculture, 97(2):526-535, 2016.). Thus, there existed a wide variation in the pH values of the Campomanesia species. It is influenced by environmental factors and maturation stages (Goldoni et al., 2019GOLDONI, J. et al. Physicochemical characterization of fruits of Campomanesia guazumifolia (Cambess.) O. Berg (Myrtaceae). Acta Scientiarum. Biological Sciences, 41(1):e45923, 2019. ).

Table 2:
Mean values of pH, titratable acidity (AT) expressed as citric acid, soluble solids (SS), SS/AT ratio, proximate composition, total sugars, and calorific value of fresh C. rufa fruits at two maturation stages.

In white-fleshed pitaya (Hylocereus undatus), a linear pH increase occurred that reached values between 3.06 and 4.5 (Magalhães et al., 2019MAGALHÃES, D. S. et al. Physical and physicochemical modifications of white-fleshed pitaya throughout its development. Scientia Horticulturae, 243:537-543, 2019. ) with maturation. According to Vallilo et al. (2005VALLILO, M. I. et al. Características físicas e químicas dos frutos do cambucizeiro (Campomanesia phaea). Revista Brasileira de Fruticultura , 27(2):241-244, 2005. ), fruits with high acidity are used in the industry to produce sweets. Fruit acidity is due to the presence of organic acids, such as malic and citric acids present in most mature fruits ( Batista-Silva et al., 2018BATISTA-SILVA, W. et al. Modifications in organic acid profiles during fruit development and ripening: Correlation or causation? Frontiers in Plant Science, 9:e1689, 2018. ).

Despite the variation in the pH between the two stages, no difference was observed in the titratable acidity (1.22 and 1.21% citric acid in immature and mature fruits, respectively) (Table 2). These values were lower compared to the 3.0% value of C. phaea but were close to that of C. pubescens (approximately 1.5%) and higher than that of C. cambessedeana (0.19%) (Valillo et al., 2005; Silva et al., 2009SILVA, E. P. D. et al. Caracterização física, química e fisiológica de gabiroba (Campomanesia pubescens) durante o desenvolvimento. Ciência e Tecnologia de Alimentos , 29(4):803-809, 2009. ; Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ).

The content of soluble solids increased as the green fruits ripened into the mature fruits (from 8.0 to 10.8%, respectively) (Table 2). These values were lower than those found in the accessions of C. phaea (12.50 to 13.30%) and C. lineatifolia (11.55%) (Bianchini et al., 2016BIANCHINI, F. G. et al. Caracterização morfológica e química de frutos de cambucizeiro. Bragantia, 75(1):10-18, 2016. ; Lima et al., 2016LIMA, J. S. S. et al. Caracterização físico-química de gabiroba (Campomanesia lineatifolia) e murta (Blepharocalyx salicifolius) nativas da região serrana de Ibiapaba-CE. Revista Caatinga, 29(3):753-757, 2016. ).

The SS/AT ratio is one of the best ways to evaluate sugar content (Teerachaichayut; Ho, 2017TEERACHAICHAYUT, S.; HO, H. T. Non-destructive prediction of total soluble solids, titratable acidity and maturity index of limes by near infrared hyperspectral imaging. Postharvest Biology and Technology , 133:20-25, 2017.). The SS/AT ratio increased in the mature fruits as compared with the green fruits (Table 2). SS increased gradually with the development of the fruit, whereas AT decreased (Sanches et al., 2016SANCHES, A. M. C. et al. Physicochemical variability of cambuci fruit (Campomanesia phaea) from the same orchard, from different locations and at different ripening stages. Journal of the Science of Food and Agriculture, 97(2):526-535, 2016.).

The high moisture value seen in C. rufa was closer to that observed in C. cambessedeana (77.02 g 100 g-1) and C. pubescens (81.4 g 100 g-1) and lower than that in C. phaea (88.80 g 100 g-1) (Sanches et al., 2016SANCHES, A. M. C. et al. Physicochemical variability of cambuci fruit (Campomanesia phaea) from the same orchard, from different locations and at different ripening stages. Journal of the Science of Food and Agriculture, 97(2):526-535, 2016.) (Table 2). The C. rufa stages did not show differences in their moisture content (Table 2). Thus, in general, the fruits of the Campomanesia genera displayed a high moisture value (De Paulo et al., 2020DE PAULO F. D. et al. A critical review of some fruit trees from the myrtaceae family as promising sources for food applications with functional claims. Food chemistry, 306:e125630, 2020. ). Factors such as plant age, water availability, fertilization, and climatic conditions may influence the moisture content (Sanches et al., 2016SANCHES, A. M. C. et al. Physicochemical variability of cambuci fruit (Campomanesia phaea) from the same orchard, from different locations and at different ripening stages. Journal of the Science of Food and Agriculture, 97(2):526-535, 2016.).

Considering the levels of ethereal extract and protein, the values obtained for C. rufa were lower than 1.0% and did not differ between the immature and mature fruits (Table 2). C. phaea presented low protein content (0.44%) and higher lipid content (1.53%). C. xanthocarpa presented higher levels of protein (1.1%) and lipids (1.9%) similar to the values of C. cambessedeana for proteins (1.43%) and lipids (1.32%) (Vallilo et al., 2005VALLILO, M. I. et al. Características físicas e químicas dos frutos do cambucizeiro (Campomanesia phaea). Revista Brasileira de Fruticultura , 27(2):241-244, 2005. ; Vallilo et al., 2008VALLILO, M. I. et al. Composição química dos frutos de Campomanesia xanthocarpa berg-myrtaceae. Ciência e Tecnologia de Alimentos , 28(1):231-237, 2008. ; Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ).

The crude fiber content in C. rufa did not differ between the immature and mature stages (Table 2). The values were close to those found in C. phaea (4.00 g 100 g-1) and lower than the C. xanthocarpa values (6.3 g 100 g-1) (Vallilo et al., 2005VALLILO, M. I. et al. Características físicas e químicas dos frutos do cambucizeiro (Campomanesia phaea). Revista Brasileira de Fruticultura , 27(2):241-244, 2005. ; Vallilo et al., 2008). According to the Collegiate Board Resolution (RDC) No. 54/12 of the National Health Surveillance Agency (ANVISA), a good source of crude fiber must contain at least 1.5 g 100 mL-1 of fiber (Brasil, 2012BRASIL. Resolução da Diretoria Colegiada - RDC Nº 54, de 12 de novembro de 2012. Ministério da Saúde - Agência Nacional de Vigilância Sanitária, 2012. Available at: <Available at: http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2012/rdc0054_12_11_2012.html >. Access in: March, 14, 2020.
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).

The mineral residue content did not differ between the immature and the mature fruit (Table 2) and presented similar values in C. cambessedeana (0.41 g 100 g-1) and C. pubescens (0.5 g 100 g-1) (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ; Silva et al., 2009SILVA, E. P. D. et al. Caracterização física, química e fisiológica de gabiroba (Campomanesia pubescens) durante o desenvolvimento. Ciência e Tecnologia de Alimentos , 29(4):803-809, 2009. ). Fruits are important sources of essential elements and minerals consumed in the human diet (Marles, 2017MARLES, R. J. Mineral nutrient composition of vegetables, fruits and grains: The context of reports of apparent historical declines. Journal of Food Composition and Analysis, 56:93-103, 2017.).

The nitrogen-free extract (NFE) differed approximately by 15 g 100 g-1 between the immature and mature fruits of C. rufa (Table 2). In C. cambessedeana, the carbohydrate value was 15.68 g 100 g-1 whereas it was 8.9 g 100 g-1 in C. xanthocarpa (Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ; Vallilo et al., 2008VALLILO, M. I. et al. Composição química dos frutos de Campomanesia xanthocarpa berg-myrtaceae. Ciência e Tecnologia de Alimentos , 28(1):231-237, 2008. ). The NFE, represented by glycols like sugars and starch, can include soluble fibers in the case of fruits. Since the sugar content in the C. rufa fruits ranged from 1.22 to 6.88, it was suggested that these fruits also contained soluble fiber that was not determined as crude fiber. Therefore, the presence of starch could not be ruled out.

The caloric value of C. rufa (Table 2) was higher than that of C. xanthocarpa (57.3 kcal 100 g-1) in the mature fruits (Vallilo et al., 2008VALLILO, M. I. et al. Composição química dos frutos de Campomanesia xanthocarpa berg-myrtaceae. Ciência e Tecnologia de Alimentos , 28(1):231-237, 2008. ). The low caloric value of C. xanthocarpa was due to the high moisture content and consequent decrease in the concentration of sugars, lipids, and proteins (Vallilo et al., 2008VALLILO, M. I. et al. Composição química dos frutos de Campomanesia xanthocarpa berg-myrtaceae. Ciência e Tecnologia de Alimentos , 28(1):231-237, 2008. ); this applies to the C. rufa fruits as well.

There was a decrease in the content of α and β-carotenes and an increase in γ-carotene content with the ripening of the housekeeper fruits. However, no difference was detected for δ-carotene and lycopene between the immature and mature fruits (Table 3). α-carotene was most abundant in the green fruits, and β-carotene was most abundant in the mature fruits (Table 3). β-carotene deserves attention because it has a higher pro-vitamin A activity (Reksamunandar et al., 2017REKSAMUNANDAR, R. P. et al. Encapsulation of β-carotene in polyvinylpyrrolidone) (PVP) by electrospinning technique. Procedia Engineering, 170:19-23, 2017.).

Table 3:
Mean values of carotenoids, total phenolics, vitamin C (ascorbic acid), and antioxidants, as determined by the method of ABTS ° + radical capture expressed in Trolox and by the iron reduction method (FRAP) expressed in ferrous sulfate of fresh weight in C. rufa fruits.

In Psidium guajava var. Paluma, the contents of β-carotene (366.3 µg 100 g-1), and lycopene (6999.3 µg 100 g-1) were higher than those in the C. rufa fruits (Table 3). Mangifera indica L. var. Tommy Atkins presented higher β-carotene content (1557.1 µg 100 g-1) and lower lycopene content (77.2 µg 100 g-1) (Oliveira et al., 2011OLIVEIRA, D. S. et al. Vitamina C, carotenoides, fenólicos totais e atividade antioxidante de goiaba, manga e mamão procedentes da Ceasa do Estado de Minas Gerais. Acta Scientiarum Health Sciences, 33(1):89-98, 2011. ) than that of the C. rufa fruits (Table 3). Carotenoids have antioxidant properties with functional potential for the prevention of non-transmissible chronic diseases such as cancer and cardiovascular diseases. Lycopene is one of the most studied carotenoids in this sense (Müller et al., 2016MÜLLER, L. et al. Lycopene and its antioxidant role in the prevention of cardiovascular diseases: A critical review. Critical Reviews in Food Science and Nutrition, 56(11):1868-1879, 2016.). However, the fruits of C. rufa generally do not stand out as sources of carotenoids compared to the fruits known to be rich in carotenoids.

The total phenolic value of C. rufa was higher than that of the C. lineatifolia fruits (229.37 mg 100 g-1) (Lima et al., 2016LIMA, J. S. S. et al. Caracterização físico-química de gabiroba (Campomanesia lineatifolia) e murta (Blepharocalyx salicifolius) nativas da região serrana de Ibiapaba-CE. Revista Caatinga, 29(3):753-757, 2016. ) (Table 3). The phenolic content was comparable to that of fruits traditionally considered rich in these compounds, such as strawberry and grape. Considering seven varieties of strawberry and grape, the phenolic content ranged from 205 to 318 mg 100 g -1 and 65 to 391 mg 100 g-1 (Pinto et al., 2008PINTO M. S. et al. Functionality of bioactive compounds in Brazilian strawberry (Fragaria x ananassa Duch.) cultivars: Evaluation of hyperglycemia and hypertension potential using in vitro models. Journal Agriculture and Food Chemistry , 56(12):4386-92, 2008. ) (Abe et al., 2007ABE, L. T. et al. Compostos fenólicos e capacidade antioxidante de cultivares de uvas Vitis labrusca L. e Vitis vinifera L. Ciência e Tecnologia de Alimentos, 27(2):394-400, 2007.), respectively. Phenolic compounds are mainly responsible for the color, smell, and protection of fruits and flowers (Martins; Barros; Ferreira, 2016MARTINS, N.; BARROS, L.; FERREIRA, I. C. In vivo antioxidant activity of phenolic compounds: Facts and gaps. Trends in Food Science & Technology, 48:1-12, 2016.). Moreover, the role of phenolic compounds lies in the stabilization and oxidation of lipids. Thus, they are directly related to antioxidant activity (Araújo; Souza, 2018ARAÚJO, E. F. L.; SOUZA, E. R. B. Phenology and reproduction of Campomanesia adamantium (Cambess.) O. Berg (Myrtaceae). Scientific Electronic Archives, 11(2):166-175, 2018. ). Despite each class of phenolic compounds being mainly responsible for specific bioactivity, they commonly evidence polyvalent reactions (Martins; Barros; Ferreira, 2016MARTINS, N.; BARROS, L.; FERREIRA, I. C. In vivo antioxidant activity of phenolic compounds: Facts and gaps. Trends in Food Science & Technology, 48:1-12, 2016.).

The ascorbic acid value of C. rufa exceeded that of C. phaea (33 mg 100 g-1) and C. lineatifolia (74.44 mg 100 g-1) but was lesser than that of C. cambessedeana (383.33 mg 100 g-1) (Vallilo et al., 2005VALLILO, M. I. et al. Características físicas e químicas dos frutos do cambucizeiro (Campomanesia phaea). Revista Brasileira de Fruticultura , 27(2):241-244, 2005. ; Lima et al., 2016LIMA, J. S. S. et al. Caracterização físico-química de gabiroba (Campomanesia lineatifolia) e murta (Blepharocalyx salicifolius) nativas da região serrana de Ibiapaba-CE. Revista Caatinga, 29(3):753-757, 2016. ; Morzelle et al., 2015MORZELLE, M. C. et al. Caracterização química e física de frutos de curriola, gabiroba e murici provenientes do cerrado brasileiro. Revista Brasileira de Fruticultura , 37(1):96-103, 2015. ). Ramful et al. (2011RAMFUL, D. et al. Polyphenol composition, vitamin C content and antioxidant capacity of Mauritian citrus fruit pulps. Food Research International , 44(7):2088-2099, 2011.) classified the fruits into three categories according to their ascorbic acid content: low (<30 mg 100 g-1), medium (30-50 mg 100 g-1), and high (>50 mg 100 g-1).

The vitamin C content of C. rufa was higher than that of several traditional fruits such as Citrus aurantium L. (125.76 mg 100 g-1) (Silva Júnior et al., 2010SILVA JÚNIOR, G. B. et al. Laranja-da-terra: Potential citric fruit for Piauí State. Semina: Ciências Agrárias, 31(3):557-562, 2010. ) and seven cultivars of strawberries that ranged from 65.0 to 112.0 mg 100 g-1 (Table 3) (Da Silva Pinto; Laojolo; Genovese, 2008DA SILVA PINTO, M.; LAJOLO, F. M.; GENOVESE, M. I. Bioactive compounds and quantification of total ellagic acid in strawberries (Fragaria x ananassa Duch.). Food Chemistry, 107(4):1629-1635, 2008. ). However, the vitamin C content was similar to that of the Hancornia speciose fruit (260 mg 100 g-1) (Silva et al., 2017SILVA, A. V. C. et al. Characterization of trees, fruits and genetic diversity in natural populations of mangaba. Ciência e Agrotecnologia, 41(3):255-262, 2017. ).

The values of the antioxidant activity detected by the ABTS radical capture method were higher than those found in the natural fruits of Malpighia emarginata (1336.42 µM g-1), Anacardium occidentale (254.34 µM g-1), and Psidium guajava (130.77 µM g-1) (Freire et al., 2013FREIRE, J. M. et al. Quantificação de compostos fenólicos e ácido ascórbico em frutos e polpas congeladas de acerola, caju, goiaba e morango. Ciência Rural, 43(12):2291-2295, 2013. ). These values also surpassed those found in the epicarp (543.18 µM g-1) and in the mesocarp (1,230.00 µM g-1) of Caryocar brasiliense (Morais et al., 2013MORAIS, M. L. et al. Determinação do potencial antioxidante in vitro de frutos do cerrado brasileiro. Revista Brasileira de Fruticultura, 35(2):355-360, 2013. ).

The antioxidant activity did not differ between the green and the mature fruits (Table 3) when detected by the iron reduction method (FRAP). The values found were lower than those found in the mesocarp (2085.70 µM g-1) of C. brasiliense and higher than those in the epicarp (14.99 µM g-1) of C. brasiliense and the pulp of Byrsonima verbascifolia (148.42 µM g-1) (Morais et al., 2013MORAIS, M. L. et al. Determinação do potencial antioxidante in vitro de frutos do cerrado brasileiro. Revista Brasileira de Fruticultura, 35(2):355-360, 2013. ).

The C. rufa fruit can be considered an important source of bioactive compounds since it presents high phenolic compounds, ascorbic acid levels, and antioxidant capacity (De Paulo et al., 2020). The consumption of high antioxidant foods is necessary to prevent damage caused by free radicals as these antioxidants help in neutralizing the free radicals (Alkadi, 2020ALKADI, H. A review on free radicals and antioxidants. Infectious Disorders-Drug Targets (Formerly Current Drug Targets-Infectious Disorders), 20(1):16-26, 2020.). However, the overload of free radicals over time may become irreversible and lead to certain diseases (Schiassi et al., 2018SCHIASSI, M. C. E. V. et al. Fruits from the Brazilian Cerrado region: Physico-chemical characterization, bioactive compounds, antioxidant activities, and sensory evaluation. Food Chemistry , 245:305-3110, 2018. ).

CONCLUSIONS

C. rufa fruits are succulent, and their maturation is marked by a color change from green to yellowish-green and an increase in pectin solubilization and soluble solids content. The fruits have a low caloric value, high levels of crude fiber, vitamin C, polyphenols, and high antioxidant activity under in vitro conditions. Moreover, the presence of high pectin levels and low pH indicates a potential for industrial use in the manufacturing of gels and jellies. These results suggest that C. rufa fruits with good nutritional value have the potential for additional studies on bioactive compounds such as polyphenols, and their biological properties need to be investigated under in vivo conditions.

ACKNOWLEDGMENTS

To CNPq (National Council for Scientific and Technological Development) and FAPEMIG (Research SupportbFoundation of the State Minas Gerais), which partially funded this research.

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Publication Dates

  • Publication in this collection
    16 Nov 2020
  • Date of issue
    2020

History

  • Received
    09 June 2020
  • Accepted
    21 Sept 2020
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