Assessment of a Maturity Index in Jabuticaba Fruit by the Evaluation of Phenolic Compounds, Essential Oil Components, Sugar Content and Total Acidity
Gilmara A.C. Fortes,
Sara S. Naves,
Fabiana F.F. Godoi,
Alessandra R. Duarte,
Pedro H. Ferri
Suzana C. Santos
Jabuticaba is a Brazilian tree with edible grape like fruits which are consumed fresh or used to prepare jams, liqueurs and wines. The aim of this study was to identify the optimal harvest period for winemaking by monitoring chemical parameters during jabuticabas development. Jabuticaba fruit was analysed at four developmental stages for total acidity, reducing sugars, anthocyanins, tannins, total phenols and essential oil composition. Total acidity significantly decreased (15.46-4.56 g citric acid 100 g-1), whereas reducing sugars increased about threefold in pulps up until the full ripe stage (32.52-88.92 g glucose equivalent 100 g-1). Anthocyanin levels underwent a sharp increase in the skins reaching 22.0 mg cyanidin 3-glucoside equivalent g-1 at complete maturation. Tannins and total phenols showed no significant differences in their levels between ripe and full ripe stages. The essential oil contains 88.1% of sesquiterpene compounds, being γ-eudesmol (33.9%) and α-eudesmol (15.5%) the major constituents. Some minor terpenoids changed significantly in their contents during jabuticabas maturation. The monoterpenes α-pinene, β-pinene, (E)-β-ocimene, linalool and α-terpineol increased while the sesquiterpenes amorpha-4,7(11)-diene, δ-amorphene, δ-cadinene and α-cadinene decreased from green to ripe stages. However the major terpenoids showed no significant changes. Results demonstrated that the use of sugar/acid ratio and anthocyanin concentration seemed to be the most effective parameters to reveal the optimal harvest period for winemaking.
to cite this article:
Gilmara A.C. Fortes, Sara S. Naves, Fabiana F.F. Godoi, Alessandra R. Duarte, Pedro H. Ferri and Suzana C. Santos, 2011. Assessment of a Maturity Index in Jabuticaba Fruit by the Evaluation of Phenolic Compounds, Essential Oil Components, Sugar Content and Total Acidity. American Journal of Food Technology, 6: 974-984.
Received: June 13, 2011;
Accepted: September 18, 2011;
Published: November 02, 2011
Jabuticaba (Myrciaria cauliflora Berg.) is a short multi-stemmed Brazilian
tree; its flowers and fruits grow directly on the main truck and stems (Reynertson
et al., 2006). Jabuticaba berries have a slightly acid to sweet taste
as well as thick and tough purple to blackish skin (Lima
et al., 2011). In the popular medicine, the decoction of the skins
is used as a treatment for hemoptysis, cough, bronchitis, asthma, diarrhea and
dysentery, as well as a rinse for chronic throat inflammation (Reynertson
et al., 2006; Stefanello et al., 2011).
Two depsides were isolated from deseeded fruits and exhibited antiradical activity
in DPPH assay, colon cancer cell cytotoxicity and inhibition of interleukin
IL-8 production, suggesting anti-inflammatory activity (Reynertson
et al., 2006). The fruit ethanol extract also showed inhibitory effect
against K. pneumoniae (Haminiuk et al., 2011),
while leaf extracts were effective against several oral bacteria and Candida
species (Macedo-Costa et al., 2009; Souza-Moreira
et al., 2010).
Several reports have described their antioxidant activity which is mainly attributed
to the high anthocyanin and flavonoid content in their skins (Einbond
et al., 2004; Reynertson et al., 2008;
De Assis et al., 2009; Romero
et al., 2010; Santos et al., 2010;
Rufino et al., 2010; Leite
et al., 2011; Haminiuk et al., 2011).
Recently, optimization of anthocyanin extraction from jabuticaba skins was performed
using high pressure CO2, ultrasound treatment and combination of
different solvents and pH (Santos and Meireles, 2011;
Santos et al., 2010; Montes
et al., 2005).
Besides its biological activities, jabuticaba berries have been used to produce
jams, liqueurs, distillates and wines, as an alternative to prevent post-harvesting
losses (Reynertson et al., 2006; Agostini
et al., 2009). In the last decade jabuticaba wine production has
grown and the success among consumers has increased. The target now is to improve
its quality (Da Silva et al., 2008; Duarte
et al., 2010b), through the optimization of fermentation conditions
(Duarte et al., 2011) or by managing the attributes
of jabuticaba berries (Danner et al., 2011).
The wine quality is affected directly by fruit composition which is influenced
by many extrinsic factors, such as climatic conditions, soil and harvesting
date (Gómez-Míguez, et al., 2007;
Perez-Magarino and Gonzalez-San Josw, 2006). It is well
known that phenolic and terpenoid compounds which are responsible for some of
wines organoleptic properties, such as colour, flavour, body and structure
of red wines (Gómez-Míguez et al.,
2007) alter during fruit development and ripening (Fadda
and Mulas, 2010; Coelho et al., 2006). However,
there is no information on the concentration of tannins, total phenols and terpenoid
compounds during jabuticaba growth and maturation. In addition, the composition
of jabuticabas essential oil has not been previously reported.
Therefore, the main objective of this paper was to assess the optimal harvest period for winemaking, through the analysis of the evolution of phenolic and essential oil compounds, reducing sugar and total acidity during jabuticabas development and ripening.
MATERIALS AND METHODS
Plants, materials and chemicals: Cultivated M. cauliflora fruits
var. Pingo de mel were collected in September and October 2008 at Jabuticabal
Winery (S 16° 55 25.9″, W 49° 21 41.0″), located
in the outskirts of Hidrolândia, Goiás State, Brazil. About 2 kg
of each fruit sample were obtained from 10 to 20 year-old trees. Fruit harvesting
was performed at four developmental stages: 16-, 23-, 30- and 37-days after
anthesis (DAA). After harvesting, part of the berries was washed with running
water and separated manually into its components (skin, pulp and seeds) and
100 g samples of berries and each separated part were blended with 50 mL distilled
water and freeze-dried. Dried samples were stored at -18°C until analysis.
Tannic acid and iron (III) chloride were purchased from Merck (Darmstadt, Germany).
Dinitrosalicylic acid, Folin-Ciocalteus phenol reagent and Bovine Serum
Albumin were purchased from Sigma-Aldrich (St. Louis, MO, USA). All other chemicals
used were of analytical grade. After each harvest, three groups of 50 fresh
berries were averaged for fresh weight measurement.
Extracts for reducing sugar and total acidity assay preparation: Freeze-dried berries or pulp (0.2 g) were extracted at 50°C with 10 mL of distilled water in an ultrasonic bath for 30 min. The extract was separated from the solid residue by centrifuging at 4,000 rpm for 15 min and transferred to a 25 mL volumetric flask. The same procedure was repeated twice with 10 and 5 mL of water for 15 min each. The extracts were combined in a final 25 mL volume and were prepared in triplicate.
Extracts for phenol assay preparation: One gram of freeze-dried berries or separated parts (skin, pulp and seeds) was homogenized with 10 mL of MeOH-formic acid (9:1) in a test tube and sonicated for 30 min. The extract was centrifuged, filtered and the marc extracted three more times for 15 min. Extracts were combined and concentrated under reduced pressure at 35°C and brought up to 25 mL in a volumetric flask. Extracts were prepared in triplicate.
Extraction of fruit essential oil: Frozen berries (ca. 500 g) were crushed in small pieces and submitted to hydrodistillation (2 h) by means of a modified Clevenger-type apparatus. At the end of each distillation essential oils were collected, dried with anhydrous Na2SO4, transferred to glass flasks and kept at a temperature of -18°C until analysis. Oil yields (%) were based on the fresh weight of fruit samples.
Determination of reducing sugar: Reducing sugar content was determined
by the 3,5-dinitrosalicylic acid (DNSA) method (Miller, 1959).
Results were expressed as glucose equivalent 100 g-1 dried fruit.
Measurements were performed in triplicate.
Determination of total acidity: Total acidity was measured by titrating an aliquot (5.0 mL) of the extract with 0.01 mol L-1 of NaOH to pH 8.2. The results were expressed as g citric acid 100 g-1 dried fruit. Measurements were performed in triplicate.
Determination of phenolic compounds: Total phenols were quantified by
the Folin-Ciocalteu method described by Escarpa and Gonzalez
(2001). Results were expressed as mg tannic acid equivalent g-1
dried fruit or its parts. Measurements were performed in triplicate.
Tannins were measured by protein precipitation assay with the use of Bovine
Serum Albumin (Hagerman-Butler method described by Waterman
and Mole (1994). Results were expressed as mg tannic acid equivalent g-1
dried fruit or its parts. Measurements were performed intriplicate.
Anthocyanin content was determined by the pH-differential method (Wrolstad
et al., 2005; Reynertson et al., 2008).
Pigment concentration is expressed as cyanidin 3-glucoside equivalents per g
of dry weight (DW). Measurements were performed in triplicate.
Fruit essential oil analyses: Oil sample analyses were performed on
a GC-MS Shimadzu QP5050A instrument under the following conditions: A CBP-5
(Shimadzu) fused silica capillary column (30 mx0.25 mm i.d., 0.25 μm film
thickness) connected to a quadrupole detector operating in the EI mode at 70
eV with a scan mass range of 40-400 m/z at a sampling rate of 1.0 scan/s; carrier
gas: He (1 mL min-1); injector and interface temperatures of 220
and 240°C, respectively, with a split ratio of 1:20. The injection volume
was 0.4 μL (ca. 20% in hexane) and the oven temperature was raised from
60 to 246°C with an increase of 3°C/min, then 10/min to 270°C and
the final temperature was held for 5 min. Individual components were identified
by comparing their linear retention indices, which were determined by a co-injection
with a C8-C32 n-alkanes series (Sigma, USA) and mass spectra
with those of the literature (Adams, 2007) and a computerized
MS-database using NIST libraries (NIST, 1998).
Statistical analysis: Experimental data were assessed by one-way ANOVA
using SAS GLM analyses (Statistical Analysis System, SAS Institute Inc., Cary,
NC, 1996). All data was checked for homoscedasticity with the use of Hartleys
test (Kanji, 2006). Whenever a difference was established,
a post-hoc Tukey test was performed. Results are shown as mean values and are
joined by the standard deviation of independent measurements in some cases.
The p-values below 0.05 were regarded as significant.
RESULTS AND DISCUSSION
The complete development of jabuticaba fruits usually takes 45-60 days after
anthesis (Magalhaes et al., 1996); however, fruits
may complete maturation in 35 days during a hot dry season with proper irrigation
and soil conditions (Andersen and Andersen, 1989). This
is the case at Jabuticabal Winerys orchard where berries grow rapidly,
therefore, four development stages were chosen: green (16 DAA), turning to purple
(23 DAA), ripe (30 DAA) and full ripe (37 DAA).
Fruit fresh weight, reducing sugars and titratable acidity: Results
for fruit weight, reducing sugars content and total acidity of jabuticaba fruits
are presented in Table 1. The fresh fruit weight increased
significantly until 30 DAA (2.51-7.67 g), from this date occurred a substantial
reduction to 5.02 g. The reduction in the fruits fresh weight could be
due to water loss. A similar growth pattern was observed in berries such as
myrtles, plums and grapes (Fadda and Mulas, 2010) and
this is the opposite for pomegranate fruit which has a continuous weight increase
during maturation (Shwartz et al., 2009).
Reducing sugars content in pulp had significant growth in all stages, while
for the whole fruit considerable differences were observed mainly from green
to full ripe stages (33.51-48.06 g 100 g-1). Non-structural jabuticaba
carbohydrates are composed mainly of reducing sugars, which make up about 90%
of total soluble sugars and accumulate mostly in the pulps, even though pulps
account to only 36 to 49% of the fruit (Barros et al.,
1996; Lima et al., 2011). Comparable to results
at full ripe stage (Table 1) when the reducing sugars content
in the pulps was 88.92 g 100 g-1, while the whole fruit contained
48.06 g 100 g-1 (ca. 50%). Maximum sugar content in the pulp at 37
DAA was very similar to 80 g 100 g-1 DW obtained for M. jaboticaba
at 60 days (Barros et al., 1996).
Throughout jabuticabas development, total acidity presented a constant
and significant decrease in all stages. The acidity values dropped from 15.46
to 4.56 g citric acid 100 g-1 which is a reduction of about 70% (Table
1). Similar results were observed in two jabuticaba varieties (Sabará
and Açú Paulista), in which succinic and citric acids reduced
71.3% on average in the pulp during maturation (Jham et
al., 2007); the same occurred with myrtle berries, which showed a 70%
decrease in titrable acidity (Fadda and Mulas, 2010).
The most abundant organic acids detected and quantified in jabuticaba fruits
were succinic and citric acids (Jham et al., 2007).
Malic, oxalic and acetic acids were also detected although in lower amounts
(Lima et al., 2011).
Changes in sugar and total acidity levels mean that sugar/acid ratio increased
during fruit development from 2.17 (16 DAA) to 10.5 (37 DAA). This ratio can
be used as a maturity index, which measures fruit quality for industrial purposes;
nevertheless, there are limitations as regards variability between fruits, cultivars
and year of observation (Kingston, 1992).
Total phenols, tannins and anthocyanins: Table 2 displays the results from anthocyanins, tannins and total phenols assays in parts and the whole jabuticaba fruit at four developmental stages.
A comparison of anthocyanin amounts during maturation (Table 2) showed a significant increase in the skins and also in the whole fruit levels, while seeds and pulps did not change.
||Average concentrationsa of fresh weight (g), reducing
sugars and total acidity (g 100 g-1, dry weight basis) in jabuticaba
fruit/parts during development
|aValues are Means±RSD (n = 3). bDays
after anthesis. Means followed by the same capital letter in the columns
and by the same small letter in the rows (for reducing sugars) did not share
significant differences at 5% probability by Tukeys test
||Average concentrationsa of anthocyanins, tannins
and total phenols (mg g-1, dry weight basis) in jabuticaba fruit/parts
|aValues are means (n = 3). Means followed by the
same capital letter in the columns and by the same small letter in the rows
did not share significant differences at 5% probability by Tukeys
Anthocyanins are phenolic compounds responsible for fruit colour (Abyari
et al., 2006). They accumulate in jabuticabas skin (22.0 mg
g-1), whereas the fruits pulp is whitish (0.63 mg g-1).
Their steep rise of about fiftyfold in the skins (0.43-22.0 mg g-1)
between 16 and 37 days is due to the production of cyanidin-3-glucose (Reynertson
et al., 2008) and petunidin-3-glucose (Montes
et al., 2005). A previous study on M. jaboticaba showed a
similar increase of about 48-fold in anthocyanidin contents from green to ripe
fruit (Magalhaes et al., 1996). Other fruits
also reveal the same drastic increase in pigment levels during ripening, such
as myrtle, American cramberry and pomegranate arils (Fadda
and Mulas, 2010; Vvedenskaya and Vorsa, 2004; Kulkarni
and Aradhya, 2005).
Total anthocyanin values for ripe jabuticabas (5.94 and 12.0 mg g-1)
were higher than those for M. cauliflora fruits grown in the USA (2.78
mg g-1) (Reynertson et al., 2008).
Climate parameters such as temperature could be responsible for this difference.
Anthocyanin accumulation is influenced by air temperature, particularly by temperature
variation between day and night (Treutter, 2010). As
has been reported for strawberries, hot days and cool nights increase the production
of pelargonidin and cyanidin glycosides (Wang and Zheng,
Anthocyanin levels in ripe jabuticabas are of crucial importance for wine production,
since higher quantities of anthocyanins extracted from fruits will enhance the
colour and antioxidant properties of the wine (Tuberoso
et al., 2007). Anthocyanin concentration may be yet another parameter
for maturity index, as its level grows until full ripeness.
Total tannin (condensed and hydrolysable) accumulated mainly in seeds and skins,
where they were about twofold higher than in pulps at all stages (Table
2). During ripening, tannin contents had a significant variation in all
parts and the whole fruit only from green to turning purple stages (seed 7.75-6.61,
pulp 4.02-3.90, skin 7.27-6.78 and fruit 8.16-7.20 mg g-1); in the
following stages its levels remain constant. This tendency is opposite from
skin and seed grape tannins that generally decline during all stages of maturation
(Kennedy et al., 2000; Obreque-Slier
et al., 2010). A continuous reduction in the tannin contents is also
usual for other fruits, such as myrtle and persimmon (Fadda
and Mulas, 2010; Del Bubba et al., 2009).
For the production of red wine, in which seeds and skins remain in contact
with must, it is necessary to become aware of the adequate amounts of tannins
in seeds and skins to avoid deficiency or excess of these compounds (Busse-Valverde
et al., 2010; Mercurio et al., 2010).
Total phenol (phenolic acids, depsides, flavonoids, anthocyanins and tannins)
levels of seeds, pulps and the whole fruit changed significantly from 16 to
23 DAA (seed 18.0-16.3, pulp 13.7-12.3 and fruit 24.2-18.5 mg g-1)
and from 23 to 30 DAA (seed 16.3-16.6, pulp 12.3-6.8 and fruit 18.5-14.9 mg
g-1). The phenols concentrations were significant different comparing
seed, pulp, skin and the whole jabuticaba fruit in all stages (see rows in Table
2); and they were about twofold and fivefold higher in the skins (32.9 mg
g-1) when compared to seeds (16.6 mg g-1) and pulp (6.8
mg g-1) in a full ripe fruit, respectively. The opposite trend was
observed for Carménère and Cabernet Sauvignon grapes which total
phenolics contents were about fifteenfold higher in seeds compared to skins
(Obreque-Slier et al., 2010).
During fruit maturation, total phenol amounts in skins did not alter significantly
(Table 2), whereas pulps reduced 7.4 mg g-1 from
green to ripe stages and the whole fruit had 11.5 mg g-1 less phenols
in the full ripe stage. This tendency to total phenol reduction during maturation
has also been observed in other fruits, such as myrtle, American cranberry and
apple (Fadda and Mulas, 2010; Vvedenskaya
and Vorsa, 2004; Renard et al., 2007).
Essential oils: Essential oils were analysed in three stages: green
(16 DAA), turning purple (23 DAA) and ripe (30 DAA). A total of 27 compounds
were identified, accounting for 96.0-97.3% of volatile constituents, with average
yields of 0.0009, 0.0020 and 0.0028 wt% (Table 3). Essential
oils from the three maturation stages were composed mainly of cyclic sesquiterpenes
(average of 88.1%); the same tendency was observed in the leaf oil from M.
cauliflora (Duarte et al., 2010a) and in
other species from Myrcia, Eugenia and Psidium genera of
the Myrtaceae family (Stefanello et al., 2011).
Major jabuticaba components were γ-eudesmol (33.9%) and α-eudesmol
(15.5%) which is an unusual essential oil composition for Myrtaceae, as (E)-caryophyllene
is generally the predominant sesquiterpene (Stefanello et
al., 2011). The leaf oil is also different from the fruit, as germacrene
D (24.1%) and β-eudesmol (16.5%) are the major compounds (Duarte
et al., 2010a). Among the monoterpenes, limonene, (Z)-, (E)-β-ocimene
and α-terpineol were the main compounds in all three stages; usually they
provide citric, green and flowery aromas (Bicas et al.,
During jabuticabas maturation stage, the monoterpene and sesquiterpene
groups (hydrocarbons and oxygenated) did not altered significantly. Only minor
compounds had a significant variation during fruit ripening, such as the most
odoriferous monoterpene alcohols α-terpineol and linalool that varied from
0.37 to 1.79% and from 0.01 to 1.01%, respectively (Table 3).
These monoterpenols are important aromatic components of muscat grape varieties
(Oliveira et al., 2004). The lack of variation
in terpenoids groups differs from results reported for mango var. Kensington
Pride and Vitis vinifera L. cv. Baga (Lalel
et al., 2003; Coelho et al., 2006),
in which sesquiterpenes increased sharply in ripe fruits. Sesquiterpenoids were
detected in several V. vinifera varieties; they are related to spicy
and wood aromas, which may contribute positively to the quality of wine aromas
(Coelho et al., 2006; Jiang
et al., 2007).
|| Average percentagesa of essential oil constituents
of jabuticaba fruits during development
|RI: Retention Index. aValues are means (n = 3).
Means followed by the same small letter in the rows did not share significant
differences at 5% probability by Tukeys test
Jabuticaba fruits showed some chemical changes during development and ripening. The use of sugar/acid ratio and anthocyanin concentration seemed to be the most effective parameters to reveal the optimal harvest period for winemaking. Tannins and total phenols were not useful as parameters for a maturity index, since their levels failed to show significant differences between ripe and full ripe stages. Anthocyanin levels and sugar/acid ratio reached their maximum in the full ripe stage which suggests that harvesting for wine production should occur after 35 DAA. In addition, jabuticaba volatile compounds, mainly sesquiterpene γ-, α- and β-eudesmols, may add an exotic feature to the wine aroma.
The authors are indebted to CNPq, PADCT III and FUNAPE/UFG for their financial support, as well as to CAPES for granting fellowships to G.A.C.F. and A.R.D. We also thank Dr. Paulo Antônio Silva from Jabuticabal Winery for providing valuable plant information and for helping with fruit collection.
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