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DOI:
10.1016/j.lwt.2015.05.031
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YFSTL 4687
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13 May 2015
Please cite this article as: Pertuzatti, P.B., Sganzerla, M., Jacques, A.C., Barcia, M.T., Zambiazi,
R.C., Carotenoids, Tocopherols and Ascorbic Acid content in Yellow Passion Fruit (Passiflora Edulis)
Grown Under Different Cultivation Systems, LWT - Food Science and Technology (2015), doi: 10.1016/
j.lwt.2015.05.031.
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Carotenoids, Tocopherols and Ascorbic Acid content in Yellow Passion Fruit (Passiflora Edulis)
Grown Under Different Cultivation Systems
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Paula Becker Pertuzattia*, Marla Sganzerlab, Andressa Carolina Jacquesc, Milene Teixeira Barciab, Rui
Carlos Zambiazid
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Universidade Estadual de Campinas, Faculdade de Engenharia de Alimentos, Campinas 13083-862, So Paulo, Brazil
Universidade Federal do Pampa, Campus Bag, Bag 96413170, Rio Grande do Sul, Brazil
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Universidade Federal de Pelotas, Centro de Cincias Qumicas, Farmacuticas e de Alimentos, Pelotas 96010-900, Rio
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Universidade Federal de Mato Grosso, Campus Universitrio do Araguaia, Barra do Garas 78600-000, Mato Grosso,
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ABSTRACT
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The present study aimed to identify and compare the content of tocopherols, ascorbic acid and
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carotenoids in yellow passion fruit grown under different cultivation systems. The passion fruits were
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obtained from two systems: an organic pesticide-free system and a conventional system. Samples from
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both systems were obtained in 2008 from the same private property in Florianpolis, SC/Brazil. The
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tocopherols, carotenoids, and ascorbic acid analysis were carried out using high-performance liquid
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chromatography (HPLC). The results showed that the passion fruit grown under the organic cultivation
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approach contained a higher content of tocopherols than those cultivated using conventional methods
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(0.061 and 0.052 mg of tocopherols.100g-1 of fresh fruit, respectively). The major component in the
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samples produced by both systems was -tocopherols, which were found at a concentration of 0.045
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mg.100g-1 in the organic fruits and 0.042 mg.100g-1 in the conventional fruits. The amount of total
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ascorbic acid was 2.3x102 and 1.9x102 mg.100g-1 in the samples from the organic and conventional
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systems respectively. The quantification of individual carotenoids in both the organic and conventional
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passion fruit was 13.99 mg.100g-1and 25.10 mg.100g-1 respectively. The conventional passion fruit
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contained double the content of the carotenoids present in the organic fruits. -criptoxanthin was the
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1. Introduction
Fruits and vegetables containing vitamin C, vitamin E (tocopherols), and carotenoids (-
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carotene, -carotene, -cryptoxanthin, lutein, zeaxanthin, and lycopene) are believed to provide a
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natural source of antioxidants (Kchaou, Abbs, Attia & Besbes, 2014; Romojaro, Sanchez-Bel,
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Serrano & Pretel, 2013; Pertuzatti et al., 2014). Antioxidant activity is associated with decreases in
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DNA damage, a reduction in lipid peroxidation, maintenance of the immune function, and prevention
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of the development of some diseases (Gropper, Smith & Groff, 2005). Nowadays, it is commonly
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accepted that diets that are high in fruits and vegetables protect against several human diseases, some
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of which are especially serious such as cardiovascular diseases and cancer. Given the fact that many
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existing studies indicate that protective effects may result from intake of the antioxidants that are
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present in fruit and vegetables, an increasing amount of attention is being placed on identifying
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potentially antioxidant substances, such as carotenoids and vitamin C (Pertuzatti et al., 2014, Matheus-
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Roth, 1991; Rock, Fada, Jacob & Bowen, 1996; Halliwell, 1997; Fraser & Bramley, 2004; Melndez-
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Martnez, Vicrio & Heredia, 2004). The prevention of diseases that is provided by carotenoids is
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directly associated with the antioxidant activity offered by these substances due to singlet oxygen
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scavenging and the way in which they reaction with free radicals (Sentanin & Rodriguez-Amaya,
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Carotenoids are natural pigments that are found throughout the flowering plant kingdom as a
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pigment. They are mostly responsible for the yellow, orange and red color of fruits, and some of them
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are important vitamin A precursors (Silva et al. 2014). In one study, thirteen carotenoids were
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identified and separated in passion fruit using HPLC, with -carotene identified as the predominant
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compound. These compounds give visual appeal to juices and are important for their provitamin A and
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antioxidant activity (Mercadante, Britton & Rodriguez-Amaya, 1998; Talcott, Percival, Pittet-Moore &
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Celoria, 1998). The -carotene content in passion fruit pulp is 1362 g.100g-1and the total carotenoid
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content ranges between 27600 and 35400 g.100g-1 (Silva et al., 2014; Cavalcante, Dias, Nascimento
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& Freire, 2011). However, carotenoids and vitamin accumulation in passion fruit is variable and
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depends, among many factors, on the maturity stage of the fruit and the cultivation systems used to
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Vitamin C, or merely ascorbic acid (AA), is a hydrosoluble and thermolabil vitamin. AA is widely
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distributed in products of vegetable origin and is mainly found in citric fruits and green leaves (Zhang
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& Hamauzu, 2004). The Association of Official Analytical Chemists (AOAC) standard methodology
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for determination of Vitamin C employs a titration method; however, ascorbic acid can also be
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Cmara & Castilho, 2013). Liquid chromatographic methods have the potential for the simultaneous
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(dehydroascorbic acid) forms of AA are equally active; though the oxidized form is reduced in natural
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system, carrying hydrogen in the respiration process at the cellular level (Welch, 1995). Natural
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ascorbic acid levels have been reported at 40-65 mg/100 g for fresh passion fruit (Talcott, Percival,
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Pittet-Moore & Celoria, 1998; Spnola, Mendes, Cmara & Castilho, 2013).
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and , which contain unsaturated side chains. The -tocopherol is the most biologically active form.
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Most plant-derived foods, especially fruits and vegetables, contain low-to-moderate levels of vitamin E
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activity; however, due to the abundance of plant-derived foods in our diets, they provide a significant
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and consistent source of vitamin E (Eintemiller & Lee, 2004). Although some studies have reported
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the presence of tocopherol in oil extracted from the seeds of passion fruit (499.3 mg total
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tocopherol.kg-1)(Malacrida, 2012), no study has been carried out on the tocopherol content of passion
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fruit pulp.
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Around 120 species of Passiflora are native to Brazil, sixty of which produce fruits that could be
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direct or indirectly used as food sources. Yellow passion fruit (Passiflora edulis Flavicarpa) is the most
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cultivated fruit in Brazil, and it is predominantly utilized in juice processing (Meletti, 2011). In 2012,
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passion fruit production in Brazil was higher than guava and melon production, and production of this
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fruit is increasing due to the technological progress that is being witnessed in all regions of Brazil. This
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makes Brazil an important world exporter of passion fruit juice (Meletti et al., 2010; IBGE, 2012). A
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number of studies have attempted to characterize passion fruit composition; however, none of them
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have used HPLC analyses (carotenoids, tocopherols and vitamin C) to evaluate the quality traits of
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The present demand for health foods that are produced without environmental damage and with
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respect to biological diversity for not using chemical fertilizers and pesticides, is a tendency that favors
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the creation of new opportunities, especially those for small producers (Fischer et al., 2007).
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The present study aimed to compare the content of tocopherols (, and ), ascorbic acid (L-
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ascorbic and L-dehydroascorbic) and carotenoids (-carotene, -cryptoxanthin, lutein, lycopene and
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zeaxanthin) in yellow passion fruit grown under two different cultivation systems.
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2.1. Materials
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The passion fruits (Passiflora edulis Sims f. flavicarpa, Degener) of the organic and
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conventional system were obtained from the same private producer in the city of Florianpolis
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(SC/Brazil). The ripened fruits (surface totally yellow, pH 2.8 and 11-13Brix) were collected from a
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2008 harvest transported at 10oC in thermos boxes refrigerated with ice blocks, and stored in an ultra-
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freezer at -80C. The analyses were carried out after three days of storage in the chromatography
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laboratory/DCTA-UFPEL in Pelotas (RS/Brazil). Five batches of passion fruits from each cultivation
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system were evaluated. Each one was composed of 20 units. The samples were immediately evaluated
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in triplicate following preparation. The seeds were separated, and the pulp was homogenized in a
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mixer using approximately 200g of fruit. The standards of - and -tocopherols were obtained from
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Sigma Aldrich (Steinheim, Germany) with 96 and 90% of purity, respectively; - tocopherol was from
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Sigma Aldrich (Steinheim, Germany) with 99% of purity; the L-(+)-ascorbic acid was from Synth
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(Diadema, Brazil) (99% purity); and the L-(+)-dehydroascorbic acid from Fluka (Saint Louis, USA)
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with purity higher than 80%. The standards of the carotenoids -cryptoxanthin, lycopene, lutein, and
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zeaxanthin were obtained from Chromadex (Irvine, USA); and -carotene was from Fluka (Saint
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Louis, USA) at 97% of purity. All standards were dissolved in a mobile phase used in each method,
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The extraction of tocopherols was performed in accordance with the methodology described by
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Burns et al. (2003), with a number of minor modifications. The fruit extracts were obtained using cold
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acetone and mixed with petroleum ether. The ethereal phase was separated and centrifuged at 9000
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rpm for 10 minutes (microcentrifugue NT800 Nova Tcnica - So Paulo, Brazil) and then transferred
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liquid chromatography system (SHIMADZU - Kyoto, Japan), which consisted of a LC-10ATVP solvent
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delivery pump, FCV-10ALVPc degasser, DGU-14A reodyne pump, SCL-10AVP, CTO-10ASVP, column
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oven and an autosampler SIL-10AF. The chromatographic separation was performed in an analytical
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reversed-phase column Shim-Pak CLC-ODS (4.6 mm x 150 mm x 4 m) with octadecil groups as the
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stationary phase. A fluorescence detector RF 10AXL was used at an excitation wavelength of 290 nm
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and emission wavelength of 330 nm. 10 L of the sample was injected using an initial mobile phase
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acetonitrile/methanol/isopropanol (50:40:10, v/v/v) for 10 minutes. The mobile phase was linearly
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altered to acetonitrile/methanol/isopropanol (30:65:5, v/v/v) until 12 minutes passed; and then linearly
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returned to the initial mobile phase until 15 minutes of analyze. A constant flow of 1 mL.min-1 (Barcia,
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The peaks were identified by comparing the standards of tocopherols, and the quantification was
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performed according to the external standard calibration curve (- tocopherol, - tocopherol and -
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a 25 mL-aliquot of the extract was saponified with 25 mL of KOH 1.5 N solution in ethanol, following
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the procedure of Pertuzatti et al., 2012. The mixture was left for 18 h in the dark, after which it was
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transferred to a separatory funnel with 40 mL of water and 40 mL of petroleum ether. The lower phase
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was transferred to another separatory funnel (aqueous phase) and washed with 20 mL of petroleum
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ether. The upper phase was washed with 20 mL of water. The lower phase of both separatory funnels
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was discarded and the upper phases were put together, before being concentrated in a rotary evaporator
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at 35C and finally re-dissolved in 5 mL of methanol:acetonitrile, 30:70 v/v. The extract was
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centrifuged at 9000 rpm for 10 minutes (microcentrifugue NT800 Nova Tcnica - So Paulo, Brazil)
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and then transferred to a 1.5 mL vial for the analysis of carotenoids. A 25L aliquot of the resulting
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sample was injected into the system of high-performance liquid chromatography that consisted of the
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wavelength at 450nm. Where was used as initial mobile phase methanol/acetonitrile, 30/70 (v/v),
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which was altered to methanol/ acetonitrile/ ethyl acetate (10:80:10, v/v/v) for 10 minutes and then
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kept constant for a further 35 minutes. Following this, it was turned to methanol/acetonitrile/ethyl
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acetate (5:80:15, v/v/v) and maintained in this state for 40 minutes before it was finally returned to the
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initial mobile phase for 45 minutes so that it could be analyzed. A constant flow of 1mL.min-1 was
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used. The data was acquired and processed using the Class-VP software.
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The peaks were identified by comparing the retention times of the standards, and the
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quantification was evaluated according to the external standard calibration curve of -cryptoxanthin,
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lycopene, lutein, zeaxanthin and -carotene. The results were expressed in g.100g-1of fruit.
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The ascorbic acid was analyzed according to the methodology described by Vinci et al. (1995),
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with few modifications, as described by Jacques et al. (2010). Ten grams of ground sample was
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weighed, and 30 mL of metaphosphoric acid (4.5% in ultrapure water) solution was added, before the
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solution was left to rest for an hour in an amber flask. The solution was then transferred to a 50 mL
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volumetric flask, and the volume was completed with ultrapure water. The sample was filtered through
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filter paper, and the supernatant was centrifuged at 7000 rpm for 10 minutes (microcentrifugue NT800
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Nova Tcnica - So Paulo, Brazil). After that, the sample was transferred to 1.5 mL vial.
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10 L of the sample, which consisted of the modules described previously, was injected into the
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10AVVP with wavelength at 254 nm was employed. Ultrapure water with 0.1% of acetic acid as a
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mobile phase was employed with a flow of 0.8 mL/min. The data were acquired and processed using
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dehydroascorbic acid. The vitamin C quantification was evaluated according to the external standard
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calibration curve of L-(+)-ascorbic acid and the L-(+)-dehydroascorbic acid. The results were
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2.4. Moisture
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The moisture determination was performed in triplicate in accordance with the AOAC method
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(AOAC, 2006).
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The data were submitted to analyze the variance and compare means using the Tukey test at 5%
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level of significance. The statistical analysis was performed using Version 7.0 of the Statistica program.
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them with the information they need to develop a strategy that minimizes the development of poor-
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The initial moisture content of passion fruits cultivated in the conventional and organic system
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was 79.65 mg.100g-1 and 80.15 mg.100g-1 respectively. The fruit from the conventional system
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exhibited several chromatographic peaks under the HPLC analysis that had not previously been
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identified. Five carotenoids standards were used in this study. In a previous study by Mercadante,
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Britton & Rodriguez-Amaya (1998), thirteen carotenoids were conclusively identified in yellow
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passion fruit (Passiflora edulis) using electron impact mass spectrometry, complemented by UV-
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visible spectrophotometry and co-chromatography. Of these thirteen carotenoids, seven were identified
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for the first time. Also, the study did not report the variety and original location of where the fruits
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were cultivated.
According to the results presented in Table 1, both the cultivation systems used to grow passion
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fruits displayed significant difference for all carotenoids analyzed. The highest amount of carotenoid
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identified in both organic and conventional cultivation was -criptoxanthin; however, the content of -
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criptoxanthin in the fruit from the conventional crop was almost twice that of the organic crop. Lutein
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and zeaxanthin were present in the lowest concentrations in the analyzed fruits. The total concentration
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of carotenoids present in the conventional crop was twice that of the carotenoid content found in the
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fruits from the organic crop. Several existing studies indicate that organic cultivation results in higher
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phytochemical content (Cavalcante, Dias, Nascimento & Freire, 2011). However Borguini et al. (2013)
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analyzed the lycopene content of organic and conventional tomatoes and did not find any significant
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difference between the organic and conventional systems. The carotenoid content in fruits depends on
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many variables, including the process of cultivation; however, some authors have observed that
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additional factors, such as exposure to light, temperature and degree of fruit ripeness, also have an
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impact on the production of carotenoids (Abushita et al., 2000; Borguini et al., 2013). Therefore, the
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highest carotenoid content in conventional passion fruit could be due to different light incidences or
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The content of -carotene (0.582 mg.100g-1) found in sweet passion fruit by Souza et al.(2008)
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was much higher than the concentration found in this study (0.056 0.077 mg.100g-1). These authors
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attribute this variation not just to the geographic effect, but also to the maturation stage of the fruits at
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the point of harvest, crop year, variety and storage conditions. The content of carotenoids in vegetables
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cannot be considered to be an absolute value, and it may be affected by several factors. As a result of
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the many functions or properties attributed to the production of carotenoids, there is a worldwide effort
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to obtain reliable analytical data that provides deeper insights into the development of these
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compounds. Since there is high number of natural carotenoids, conclusive identification is difficult.
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The information about the carotenoid composition of fruits that is presented in existing literature is
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Three distinct peaks of the -, (+)- and -tocopherols, were identified by comparing the
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retention times between the sample and the corresponding standards. The second peak in the middle
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location corresponded to the sum of the - and -tocopherols, since these isomers were not resolved
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using RP-HPLC. The calibration curves exhibited excellent linearity (r2 > 0.997, n = 6 for all curves).
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Using -tocopherol as a reference, the response factors (relative fluorescence sensitivities) were 4.6
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Both systems used to cultivate passion fruit exhibited significant differences in terms of the
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contents of the tocopherols analyzed, as shown in Table 2. The contents of tocopherols in the fruits
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grown via organic cultivation were superior to those developed using conventional methods: 0.061
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mg of tocopherols per 100g-1 of fresh fruit and 0.052 mg of tocopherols per 100g-1 of fresh fruit,
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respectively. This could be due to the stressful conditions that are inherent in the organic cultivation
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system, which favor the synthesis of bioactive compounds from the secondary metabolism (Macoris
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et al., 2012). In both cultivation systems, the major component was - tocopherol, 0.045 mg of -
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system. The -tocopherol also was the main tocopherol found in passion fruit seed oil (Malacrida &
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Jorge, 2012). In terms of the content of - tocopherol, 0.016 mg -tocopherol.100 g-1 was present in
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the organic cultivar and 0.010 mg - tocopherol.100g-1 in the conventional cultivar. The presence of
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tocopherol was not confirmed in the passion fruits. Although the passion fruits only contained a
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small amount of tocopherols, the tocopherols present in the organic passion fruit were superior to
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those in the conventionally cultivated fruit. Data on the tocopherol content of fruits in existing
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literature is rare. In one research study that examined passion fruit pulp (Barcia, Jacques, Pertuzatti &
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Zambiazi, 2010) , a total of 0.043 mg.100g-1 tocopherol was identified and this content was lower
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than that present in the other fruits analyzed by the authors (blueberries, peaches, blackberries,
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pears).
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Figure 1 provides the typical chromatogram referent to the separation of ascorbic acid using
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HPLC. Peak 1 corresponds to L-dehydroascorbic acid with a retention time of 2.63 minutes, and Peak
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2 to L-ascorbic acid in 3.20 minutes. In terms of the total ascorbic acid content (Table 3), the fruit from
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the organic cultivation contained the highest concentration of ascorbic acid. Considering individually
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the two forms of ascorbic acid (L-ascorbic acid and L-dehydroascorbic acid) the fruit from the organic
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cultivation contained a higher concentration of L-ascorbic acid. As with the tocopherols, the total
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vitamin C content of the organic fruits was more expressive. It is widely accepted that vitamin C levels
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in fruits are subject to a wide variety of environmental factors (Genovese, Pinto, Gonalvez & Lajolo,
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2008). These variables include light, temperature, salts, and the presence of atmospheric pollutants,
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metals, and herbicides. This variable nature could explain the differences between the fruit produced
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via the two evaluated cultivation systems assessed in this work. Independently, the content of vitamin
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C found in this experiment was superior to the concentrations identified by Vinci et al.(1995) (64.00
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mg of ascorbic acid.100g-1). The present study evaluated two forms of ascorbic acid, L-ascorbic acid,
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and L-dehydroascorbic, and this could explain why the fruit contained higher levels of Vitamin C than
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that identified by Vinci et al. (1995). The content of L-ascorbic acid found in organic passion fruit was
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similar to the concentration found by Genovese et al. (2008) in commercial frozen passion fruit pulp
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4. Conclusion
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The tocopherols (vitamin E) and ascorbic acid (vitamin C) content was higher in the passion
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fruit that was organically cultivated. However, the carotenoids content was higher in the fruit that
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was conventionally cultivated. -criptoxanthin was the main carotenoid found in both fruits, of which
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+ tocopherols were in the highest volume. -tocopherol was not identified in the passion fruit
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analyzed.
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Acknowledgments
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The authors wish to thank the Coordenao de Aperfeioamento de Pessoal de Nvel Superior
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(CAPES), Fundao de Amparo a Pesquisa do Rio Grande do Sul (FAPERGS) and Conselho Nacional
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Table 1. Content of carotenoids in conventional and organic passion fruit (mg.100 g-1),
limit of detection (LOD) and limit of quantification (LOQ) to carotenoids analysis.
Lutein +
Zeaxanthin
- Criptoxantin
Licopene
- Carotene
Total
carotenoids
Organic crop
0.001 a
13.94 b
0.002 b
0.056 b
13.99 b
Conventional
crop
0.001 b
24.99 a
0.028 a
LOD
6.50x10-4
0.07
LOQ
2.17x10-3
0.24
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Passion fruit
25.10 a
9.89x10-3
8.62x10-3
30.00x10-3
2.87x10-2
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0.077 a
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Conventional crop
0.010 b
Tocopherol
Total
(+++)
0.045 a
nd
0.061 a
0.042 b
nd
0.052 b
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(+)-Tocopherol
Passion fruit
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Table 3. Content of ascorbic acid in conventional and organic passion fruit (mg.100 g-1).
Conventional
L- ascorbic acid
41.00 a
L- dehydroascorbic
acid
2.3x102 a
18.00 b
1.8x102 b
1.9x102 b
2.3x102 a
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Fig. 1. Vitamin C peaks of passion fruits from conventional (a) and organic (b) cultivation,
obtained by HPLC analysis using a reverse phase column (C18) and UV detector at 254nm. Peak
identification: (1) dehydro ascorbic acid; (2) L- ascorbic acid.
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Highlights
Organic cultivation displayed higher content of tocopherols than conventional cultivation.
The content of carotenoids in passion fruit from conventional cultivation doubled the
levels detected in fruits from organic cultivation.
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Ascorbic acid (vitamin C) content was higher in fruits from organic cultivation.
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