Postharvest Biology and Technology 162 (2020) 111097

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Postharvest Biology and Technology

journal homepage: www.elsevier.com/locate/postharvbio

Ripening affects the physicochemical properties, phytochemicals and T

antioxidant capacities of two blueberry cultivars
Yang Lina,b, Guohui Huangc, Qi Zhanga, Yuehua Wanga, Vermont P. Diab,*, Xianjun Menga,*
a
College of Food Science, Shenyang Agricultural University, Shenyang, Liaoning, 110866, China
b
Department of Food Science, The University of Tennessee Institute of Agriculture, Knoxville, TN, 37996, United States
c
Department of Horticulture, Eastern Liaoning University, Dandong, Liaoning, 118003, China

A R T I C LE I N FO A B S T R A C T

Keywords: Ripening of fruit can lead to changes in quality parameters in blueberries. The objective was to determine the
Blueberry effect of ripening on taste and phytochemicals of two blueberry cultivars. Blueberry fruits of Bluecrop and
Ripening Northblue cultivars were divided into five ripening stages. Taste profiles, phytochemicals and antioxidant ac-
Phytochemical profiles tivities of blueberry fruit were evaluated. During ripening, sweetness, sourness and astringency showed a great
Antioxidant capabilities
response. Fruit color significantly changed from green to blue-purple, with anthocyanins, proanthocyanidins,
Taste characteristic
Anthocyanins
flavonoids and polyphenol compounds significantly altered. The contents of delphinidin-type and malvidin-type
anthocyanins, which are closely associated with blue-purple color, increased from first to fifth stage of maturity.
Changes on antioxidant activity during ripening were similar to total anthocyanins. Regardless of maturity stage,
Northblue cultivar displayed higher concentrations of phytochemicals and antioxidant activity. This study
showed how ripening can alter taste and phytochemicals in blueberry, which can help guide the industry for
optimum conditions during harvesting.

1. Introduction tongue has been successfully applied for food quality, including Chinese
bayberry (Yu et al., 2018), apple (Iglesias et al., 2012), roasted coffee
Blueberry (Vaccinium spp.) is an important economic crop and is beans (Dong et al., 2019), and pomegranate juice, in comparison with
widely cultivated and consumed in America and Asia. The United States sensory evaluation data (Benjamin and Gamrasni, 2015).
is the largest producer of blueberries throughout the world (Tan et al., Harvest stage is used to be judged through the color and firmness of
2018). Most of exported blueberry in Asia are from the northeast China. blueberry fruit. The color of blueberry peels is due to the diversity of
Blueberry has been regarded as the most representative berry which is the accumulation of pigments during fruit ripening. The pigments in the
rich in phenolic compounds in terms of displaying antioxidant prop- peels of blueberry fruit are mainly anthocyanins and proanthocyanidin,
erties (Qian et al., 2014). In vivo and in vitro experiments indicated that which exhibit pink, blue and purple colors (Michael et al., 2012). The
phytochemicals from blueberries can reduce the risk of obesity and physiological, biochemical and metabolic changes with fruit ripening
cancer (Baba et al., 2017), lower blood pressure (Elks et al., 2011), lead to variation of bioactive composition and antioxidant abilities
prevent aging (Zafra-Stone et al., 2010) and development of type 2 (Belwal et al., 2019). Although the changes of total anthocyanin and
diabetes (Vuong et al., 2009). There is a new trend in using dietary polyphenol during blueberry fruit maturation has been studied (Lin
compounds as potential chemopreventive agents. The quality, taste et al., 2018), specific anthocyanin compounds responsible for color and
characteristics and health benefits are critical, which can influence the antioxidant properties of blueberries remain unidentified. Hence, it is
commercial values and popularity of blueberry – one of the richest fruit necessary to consider the variation of individual anthocyanins during
sources of anthocyanins (ACN) and other polyphenols. ripening stages to better understand the difference on health benefits
Previous studies have shown that harvest stage affected flavor and and quality of blueberries. The aim of this study was to systematically
palatability of fruit (Xu et al., 2018). Liu et al. (2019) found that investigate the effects of ripening stage on the taste properties and
blueberries showed changes of total soluble solids and titratable acidity concentrations of four main blueberry fruit phytochemicals, in addition
(TA) during storage. However, little research has been done on the to the accumulation of individual anthocyanin compounds, related to
effect of early harvest on fruit taste, apart from sugars and acids. The E- the color of blueberry peels and antioxidant abilities. Moreover, the

⁎
Corresponding authors.
E-mail addresses: vdia@utk.edu (V.P. Dia), mengxjsy@126.com (X. Meng).

https://doi.org/10.1016/j.postharvbio.2019.111097
Received 13 June 2019; Received in revised form 4 December 2019; Accepted 16 December 2019
0925-5214/ Published by Elsevier B.V.
Y. Lin, et al. Postharvest Biology and Technology 162 (2020) 111097

changes in taste profiles of two blueberry cultivars as evaluated by E- 2.3. Physicochemical characteristics of blueberries
tongue and principal component analysis (PCA) is reported for the first
time in this study. Twenty blueberry fruit were randomly selected from each stage and
cultivar to measure the diameter, firmness, and color of the blueberry
2. Material and methods surface. The diameter was measured through digital vernier caliper
(Mitutoyo Corp., Japan). The weight was analyzed by an analytical
2.1. Plants and fruit sampling balance (DJ-150E, Mitutoyo Corp., Japan). Fruit firmness was de-
termined using a TA. XT Plus Texture analyzer (Stable Micro Systems
Blueberry fruit were harvested at an organic farm in Zhuanghe, Ltd., UK) with 8 mm diameter stainless steel probe and expressed as
China (122° 30ʹ E, 39° 75ʹ N) on July 18, 2017. Two cultivars, Vaccinium Newtons (N). Each fruit was crossed 5.0 mm and measurement was
corymbosum northern highbush cultivar designated here as Bluecrop performed at a speed of 1.0 mm s−1.
and the Vaccinium angustifolium × V. corymbosum half-highbush blue- For the assessment of moisture content, total soluble solids (TSS),
berry cultivar designated here as Northblue were evaluated in this titratable acidity (TA) and tannin content, three replicate samples (ten
study. These cultivars were chosen because they are known to have pieces per replicate) were wrapped in gauze and squeezed until no juice
significant difference of bioactive content and transcriptome (Lin et al., is released. Oven-drying method was used to measure the moisture
2018). Date of fruit setting of blueberry samples in this study was from content according to a previous report (Wolfe and Hai, 2003). TSS was
middle of May to July. Blueberry were manually picked (four plots × measured using a digital hand-held refractometer (PAL-1, Hangzhou
ten plants for each cultivar) and sorted into five different maturity Top Instrument co., Ltd., China). TA was determined by a titration
stages based on size and color according to a validated method for berry method, with 0.05 M NaOH to pH 8.2, and the result of TA was ex-
fruits harvesting (Herrera-Hernández et al., 2011; Lee et al., 2015; Ozga pressed as % citric acid (Chu et al., 2018). The tannin content was
and Saeed, 2006). The sorting was performed by the local cultivator determined by vanillin–HCl method as previously described by
who has experience with fruit harvesting. The fruits at each stage of Broadhurst and Jones (2010). Briefly, 1 mL sample solution was added
ripening are shown in Fig. 1. to 5 mL of 4 % vanillin reagent and mixed thoroughly. Then 3 mL of
concentrated HCl was added to the mixture and mixed. The mixture
2.2. E-tongue analysis was incubated in the dark for 900 s at room temperature and the ab-
sorbance was read at 500 nm using a UV–vis spectrophotometer (TU-
Taste attributes of fruit from different stages of ripening were ana- 1810, PuXi, China). Catechin was used as a standard to calculate the
lyzed using an electronic tongue system (TS-SA402B, Intelligent Sensor tannin content of sample and was expressed as mg of catechin
Technology, Inc., Japan) consisting of an auto-sampler, reference equivalent as kg on fresh weight basis (mg kg−1 CE).
electrodes, multichannel lipid/polymer membrane electrodes and a The color of blueberry surface was determined using a chroma
chemometric software package (Zhao et al., 2016). Blueberry sample meter CR 400 (Konica Minolta Sensing Inc., Japan), based on the
(0.1 kg) was chopped and homogenized with 0.1 L distilled water for 60 Commission International de l’Eclairage (CIE) and expressed as the
s and centrifuged for 600 s at 3500 g before analysis. The supernatant lightness (L*), a* and b* values. From these values, hue angle (h°) and
juices were collected for nine taste indices analysis (sourness, saltiness, chroma (C*), representing color saturation or intensity, were calculated
bitterness, sweetness, umami, aftertaste astringency, aftertaste bitter- according to the following formulas: ℎ°= tan−1 (b*/a*) and C* =
ness, richness, and astringency), and all measurements were done as (a*2+b*2)1/2.
previously reported (Kobayashi et al., 2010).
2.4. Determination of total anthocyanin, total polyphenol, total
proanthocyanidin and total flavonoid

Ten g blueberry samples, in triplicate, were extracted with 100 mL

of acidified methanol (0.1 % HCl) for 60 min in an ultrasonic bath at 40
°C. After filtration, the extracts were concentrated by rotary evapora-
tion and dissolved in 10 mL of acidified water (pH 3.0). The determi-
nation of total anthocyanin content (TAC) and total polyphenols con-
tent (TPC) was performed according to our previous study (Lin et al.,
2018). Total proanthocyanidin content (TPAC) was measured by va-
nillin assay and quantified using a catechin standard curve (Sun et al.,
1998). Briefly, 20 μL blueberry extracts was combined with 50 μL of 1
% vanillin in methanol and 50 μL of 25 % sulphuric acid in methanol,
incubated for 600 s at room temperature and the absorbance was
measured at 500 nm. Results of TPAC were expressed as g of catechin
equivalent as kg of fresh weight basis (g kg−1 CE). The total flavonoid
content (TFC) was determined using a modified colorimetric method
(Jianming, 1999). Briefly, 20 μL each sample was mixed with 80 μL 30
% ethanol solution (in distilled water) and 10 μL NaNO2 (0.5 M) in 96-
well plate. After 300 s, 10 μL AlCl3 (0.3 M) was added, followed by 40
μL NaOH (0.1 M) 360 s afterwards. The absorbance was measured at
510 nm using a microplate reader (ELx800; Biotek, Winooski, VT, USA).
TFC was calculated from a calibration curve, using rutin as the standard
to express as g of rutin equivalent as kg on fresh weight basis (g kg−1
RE).

2.5. Characterization and quantification of anthocyanins

Fig. 1. Photographs and code of the blueberry fruit during different ripening
stage. Characterization of anthocyanin compounds was carried out by

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Y. Lin, et al. Postharvest Biology and Technology 162 (2020) 111097

comparing their elution order, UV/Vis spectra and MS data with MS

information described in previous reports. The HPLC-ESI-MS system
and conditions used to identify anthocyanins were described in Lin
et al. (2019), with slight modifications in gradient program. Blueberry
extracts were detected by mobile phase consisted of 0.5 % formic in
water (A) and 0.5 % formic in acetonitrile (B). The quantification of
anthocyanins was performed through calculating the corresponding
peak area percentage.

2.6. Quantification of in vitro antioxidant activity

The antioxidant capacity of blueberry fruit in this study was mea-

sured by oxygen radical absorbance capacity (ORAC) and the peroxyl
radical scavenging capacity (PSC). The ORAC assay was performed as
described by Huang et al. (2002), by measuring the compounds ability
to scavenge a free radical from 2,2′-azobis(2-amidinopropane) dihy-
drochloride (ABAP) compared to that Trolox. ORAC value was ex-
pressed as millimoles of Trolox equivalent as kg of fresh weight (mmol
kg−1 TE).
A method developed by Adom and Liu (2005) with slight mod-
ifications was used for PSC assay. Briefly, the blueberry extracts were
diluted by 75 mM phosphate buffer (pH 7.4) and 100 μL diluted sample
or standard were mixed with equivalent volume of 13.26 μM DCFH-DA,
and then the ABAP was added. The fluorescence intensity was read
every 120 s for twenty cycles at excitation of 485 nm and emission of
535 nm at 37 °C by the multi-functional fluorescence detector (ZDY-07,
Shanghai Zhicheng Instrument co., Ltd., China). Vitamin C was used as
standard and the results of PSC assay were expressed as mmol vitamin C
as kg on fresh weight basis (mmol kg−1 vitamin C).

2.7. Statistical analysis

The experiments were performed using a completely randomized

design. For each cultivar and stage, all experiments were performed in
at least three independent replicates and results were presented as the
mean ± standard deviation values. To compare the taste characteristics
of blueberry fruits at different ripening stage, PCA was performed with
the statistical software JMP (version 11 SAS Institute Inc., NC, USA). E-
tongue data were derived to two principal components which presented
in 2D plot (Fig. 2). Analysis of variance (ANOVA) and Duncan’s mul-
tiple test was applied to verify significant differences among phyto-
chemicals and antioxidant activities of five ripening stages of blueberry
at a level of p < 0.05, using SPSS 23.0 software (SPSS Inc., Chicago, IL).
Pearson’s correlation matrix was performed with SPSS 23.0 software
(SPSS Inc., Chicago, IL).

3. Results and discussion

3.1. Taste characteristics Fig. 2. The E-tongue response for the blueberry fruit at different ripening
stages. Radar charts of E-tongue response of Bluecrop (A) and Northblue (B)
cultivar blueberry fruit during ripening. PCA results of different ripening stage
The taste of blueberry samples from different developmental stages
of blueberry fruit from two cultivars (C: Score plot, D: Loading plot).
of both cultivars is shown in Fig. 2A–B. It was found that the taste
corresponding signals of blueberry juice are abundant, and four kinds of
taste indices namely sweetness, sourness, astringency and bitterness mainly responsible for the sample discrimination in the direction of
showed a great response to every sample by the electronic tongue. The PC1, whereas saltiness, richness and aftertaste-B contributed more to
two blueberry cultivars showed obvious increase of sweetness and de- the separation along with the direction of PC2. There was a separation
crease of sourness as the blueberry fruit matures. The responses for of the samples in relation to the different maturity stages of the Blue-
signal of bitterness and astringency slightly changed with the ripening crop blueberries, so that the B1, B2, B3 and B4 were positioned in the
of blueberry fruit. PCA was used on the dataset of the taste corre- positive quadrants and the B5 was located in the negative quadrants.
sponding signals to evaluate the influence of developmental stage and The B1, B2 and B3 samples were differentiated by saltiness and richness
cultivar on taste characteristics of blueberries (Fig. 2C–D). PC1 (main with positive score values at PC1 and PC2, and the aftertaste-B with
axis 1) and PC2 (main axis 2) account for 66.28 % and 17.21 % of the positive score values at first principal component. The B4 samples was
total variance, respectively; with the total cumulative variance con- differentiated by astringency, sourness and aftertaste-A with positive
tribution for 83.39 %, which indicates they are sufficient to explain the score values at PC 1 and negative score values at PC 2. The N1, N2 and
total variance in the dataset (Wold et al., 1987). As shown in Fig. 2D, N3, N4 were located in opposite quadrants because they have high
the sweetness, bitterness, astringency, sourness and umami were concentrations of distinct chemical composition and N5 is far from

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Y. Lin, et al. Postharvest Biology and Technology 162 (2020) 111097

Table 1
Fruit maturity and quality assessments of ‘Bluecrop’ and ‘Northblue’ blueberries picked at five different development stages. Data are presented as mean ± SD (n =
3).
Cultivar Fruit Fruit weight Moisture Volume Firmness TSS TA Tannins
diameter (g) content (ml) (N) (%) (% citric ac.) (mg kg−1 CE)
(cm) (%)

Bluecrop B1 2.23 ± 0.16 0.73 ± 0.02 93.19 ± 0.47 0.77 ± 0.06 5.19 ± 1.44 9.80 ± 0.10 1.29 ± 0.03 123.21 ± 1.72
B2 2.75 ± 0.12 1.11 ± 0.11 89.27 ± 0.51 1.20 ± 0.10 2.26 ± 0.48 10.08 ± 0.18 1.22 ± 0.06 119.19 ± 1.41
B3 2.80 ± 0.02 1.35 ± 0.14 86.89 ± 0.74 1.37 ± 0.21 1.29 ± 0.14 10.92 ± 0.08 1.04 ± 0.01 115.64 ± 1.28
B4 2.93 ± 0.07 1.61 ± 0.22 84.55 ± 0.39 1.53 ± 0.25 1.09 ± 0.10 12.65 ± 0.13 0.85 ± 0.05 114.26 ± 1.73
B5 3.14 ± 0.05 1.79 ± 0.14 75.23 ± 0.67 1.73 ± 0.15 0.87 ± 0.24 14.18 ± 0.08 0.66 ± 0.01 111.27 ± 1.80
Northblue N1 2.29 ± 0.03 0.65 ± 0.05 91.74 ± 0.85 0.67 ± 0.06 4.48 ± 1.13 11.52 ± 0.13 1.29 ± 0.05 111.62 ± 1.93
N2 2.54 ± 0.10 0.86 ± 0.01 89.27 ± 0.52 0.90 ± 0.10 3.10 ± 0.43 12.12 ± 0.13 1.23 ± 0.02 109.19 ± 1.22
N3 2.64 ± 0.05 0.92 ± 0.09 88.36 ± 0.54 1.03 ± 0.06 2.00 ± 0.18 12.82 ± 0.10 1.08 ± 0.06 99.85 ± 1.81
N4 2.65 ± 0.04 1.09 ± 0.02 87.19 ± 0.35 1.13 ± 0.06 1.79 ± 0.24 14.00 ± 0.15 0.83 ± 0.04 85.33 ± 1.01
N5 2.84 ± 0.08 1.35 ± 0.02 81.94 ± 0.61 1.33 ± 0.15 1.24 ± 0.20 17.62 ± 0.13 0.70 ± 0.04 58.70 ± 3.89

Cultivar Code Chromatic coordinates H C*

L* a* b*

Bluecrop B1 53.84 ± 2.97 −3.26 ± 2.79 15.80 ± 3.39 −0.98 ± 1.02 16.34 ± 3.41
B2 46.15 ± 3.78 6.13 ± 2.89 10.02 ± 4.99 0.96 ± 0.38 12.55 ± 3.27
B3 37.35 ± 2.31 5.86 ± 2.28 −4.12 ± 1.64 −0.39 ± 0.30 8.93 ± 1.38
B4 32.12 ± 1.70 3.34 ± 1.06 −3.36 ± 0.71 −0.86 ± 0.18 6.24 ± 0.68
B5 35.27 ± 2.85 2.59 ± 1.17 −4.40 ± 1.24 −1.05 ± 0.29 5.36 ± 0.79
Northblue N1 60.18 ± 2.84 −5.20 ± 2.52 27.29 ± 2.30 −1.00 ± 1.03 27.86 ± 2.58
N2 40.18 ± 2.78 11.68 ± 2.35 6.60 ± 3.98 0.51 ± 0.29 13.95 ± 2.15
N3 31.75 ± 2.32 7.60 ± 5.15 −1.06 ± 3.50 −0.31 ± 0.40 8.33 ± 5.17
N4 29.26 ± 2.14 6.62 ± 2.22 0.65 ± 2.72 0.00 ± 0.36 7.03 ± 2.52
N5 28.24 ± 1.92 4.36 ± 1.49 −0.83 ± 1.30 −0.25 ± 0.32 4.65 ± 1.31

Northblue blueberry at different maturity stages. The results of E- For many berries, such as sweet cherry, raspberry, blueberry, the
tongue indicate that taste characteristics are different between the two fruit color is one of the most important criteria of fruit maturity (Krüger
cultivars. et al., 2011; Lobos et al., 2018; Stavang et al., 2015; Usenik et al.,
2015). As shown in Table 1, during fruit maturation, L* showed an
initial decrease and a subsequent increase in the Bluecrop cultivar. For
3.2. Fruit quality and fruit color
fruit from the Northblue cultivar, a sharp decrease of L* can be ob-
served from the early stage (N1, 60.18) to commercial harvest (N5,
The five developmental stages showed a wide variability of the
28.24). The decrease of L* value indicate that the surface of fruit in
observed quality characteristics regardless of cultivars (Table 1). Both
commercial harvest stage became much darker than fruit in early stage.
of fruit diameters and weight showed an upward trend during blueberry
At the early stage of both cultivar blueberry fruit, a* had negative va-
fruit ripening. The rate of increase in diameter and weight for samples
lues, corresponding to green color; this then transitioned to positive a*
from Bluecrop was faster than samples from Northblue. During ri-
values or red color with fruit ripening. The b* parameter decreased
pening, the moisture content of samples from Bluecrop cultivar de-
during berry development in Bluecrop and Northblue cultivar, in-
creased from 93.19 % (B1) to 75.23 % (B5), and the moisture content of
dicating that the color of fruit changes from yellow and green to blue
samples from Northblue cultivar decreased from 91.74 % (N1) to 81.94
and red. There was a decrease of C* and h° which reflect the changes in
% (N5). Firmness is an important sensory quality attributes for blue-
fruit color, from green to dark-blue/purple. The variation of L*, a*, b*
berries influencing their marketability, commercialization and shelf-
values along with h° showed similar trends in Bluecrop and Northblue
life. The firmness remarkably decreased with coloration and maturation
cultivars, which was also consistent with the surface color of fruit
stage, from 5.19 N (B1) to 0.87 N (B5) and from 4.48 N (N1) to 1.24 N
shown in Fig. 1.
(N5).
The flavor of blueberry can be greatly influenced by many chemical
constituents, including TSS, TA and tannin content. An increase in TSS
3.3. Correlation between E-tongue analysis and chemical properties
of both cultivar blueberry was noted continuously during fruit ma-
turation, even at early stages, also after commercial harvest. Increase of
In order to determine the relationship between the taste char-
TSS during maturation was common, it is also observed in other fruit
acteristics measured by E-tongue analysis and different phytochemical
such as guabiju, sapota-do-Solimões (Monteiro et al., 2018). The TA
concentrations at different stages of maturity, a correlation matrix was
decreased during ripening for both cultivars from 1.29 % to 0.66 % in
performed between taste characteristics, TA, TSS, TPC and Tannins
Bluecrop and 0.70 % in Northblue. This is in agreement with research
(Table 2). Good correlations were found between the TA and sourness
on other berries, where the TSS increase and TA decrease with fruit
(p < 0.05), TSS and sweetness (p < 0.01), Tannins and astringency
maturation (Fawole and Opara, 2013; Krüger et al., 2011). The con-
(p < 0.01). Benjamin and Gamrasni (2015) showed the sensor for as-
sumption of organic acids as a substrate for respiration during fruit
tringency were significantly (p < 0.05) correlated with the tannin
maturation leads to the increase of TSS and pH, and the decrease of TA
content in juice. The correlations of TA and sourness, TSS and sweet-
(Usenik et al., 2013). The changes in tannins for two cultivars showed
ness, and Tannins and astringency provide evidence that the E-tongue
the same trend during fruit maturation. Tannin content in samples of
can possibly detect the compounds responsible for sourness, sweetness
Bluecrop cultivar was slightly reduced from the early stage B1, 123.21
and astringency in blueberry. This indicates that E-tongue could be a
mg kg−1 CE to commercial harvest stage B5, 111.27 mg kg−1 CE.
promising technique for discrimination of blueberry at different stages
However, tannin content in Northblue cultivar significantly dropped
of maturity.
from 111.62 mg kg-1 CE (N1) to 58.70 mg kg-1 catechin (N5).

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Table 2
Correlation matrix (Pearson test) for E-tongue sensor signals and TSS, TA, TPC and Tannins in blueberries of different developmental stage. *, ** Significant at
p < 0.05 and 0.01, respectively.
Variables Sourness Aftertaste-A Sweetness Bitterness TPC Richness Astringency Saltiness Aftertaste-B Umami TSS TA Tannins

Sourness 1 0.679* −0.979** −0.941** −0.128 0.545 0.986** 0.500 0.032 −0.914** −0.934** 0.701* 0.969**
Aftertaste-A 1 −0.758* −0.755* 0.413 0.558 0.653* 0.261 −0.028 −0.709* −0.775** 0.877** 0.665*
Sweetness 1 0.980** 0.117 −0.582 −0.981** −0.471 0.051 0.907** 0.970** −0.732* −0.975**
Bitterness 1 0.120 −0.660* −0.961** −0.504 0.197 0.839** 0.956** −0.721* −0.961**
TPC 1 0.294 −0.159 0.199 0.327 0.150 0.068 0.436 −0.183
Richness 1 0.627 0.847** 0.005 −0.225 −0.627 0.594 0.559
Astringency 1 0.567 −0.002 −0.856** −0.942** 0.665* 0.982**
Saltiness 1 0.324 −0.133 −0.554 0.509 0.433
Aftertaste-B 1 0.036 −0.050 0.197 −0.133
Umami 1 0.839** −0.650* −0.887**
TSS 1 −0.816** −0.904**
TA 1 0.612
Tannins 1

Fig. 3. TAC (g kg−1 cyanidin-3-glucoside equivalent, C3GE) A, TPC (g kg−1 gallic acid equivalent, GAE) B, TPAC (g kg−1 catechin equivalent, CE) C, and TFC (g
kg−1 rutin equivalent, RE) D, in the Bluecrop and Northblue cultivar during fruit maturation. Values are presented as mean ± SD (n=3). Vertical bars represent the
SD of the means. The different superscripts show significant differences at p < 0.05 for different ripening stage from same cultivar blueberry through using Tukey’s
test.

3.4. Total contents of anthocyanins, polyphenols, proanthocyanidins and of cultivars. TPC significantly (P < 0.05) decreased toward fruit ma-
flavonoids turation and with the maximum in the green blueberry fruit (Bluecrop
2.48 g kg−1 gallic acid, Northblue 3.24 g kg−1 gallic acid). Consistent
Blueberry fruit contain large amounts of anthocyanins, polyphenols, results from other studies showed that TPC decreased and TAC in-
proanthocyanidins and flavonoids, which are important in antioxidant creased when fruit changed from white/green/pink (unripe) to dark
defense and human health (Wang et al., 2017). Anthocyanins are the blue/purple (ripe) (Belwal et al., 2019; Elmastaş et al., 2017;
major pigment compounds responsible for red and purple color Siriwoharn et al., 2004). The rise of TAC and drop of TPC were influ-
(Serrano et al., 2005). Total anthocyanin content (TAC) (Fig. 3A) ac- enced by each other as the fruit proceed towards maturation; phenolics
cumulated in substantial quantities in ripening fruit in both cultivars. were being oxidized and used to biosynthesis of the flavylium ring,
Compared with the first stage, TAC of blueberry in Bluecrop cultivar leading to the accumulation of anthocyanins during ripening (Shwartz
and Northblue cultivar significantly (P < 0.05) increased by 2.77-fold et al., 2009). TPAC in Bluecrop cultivar and Northblue cultivar de-
and 23.27-fold, respectively, during maturation. Higher TPC (Fig. 3B) creased during ripening from 0.47 and 0.94 to 0.12 and 0.21 g kg-1 CE
was found in the early stage than commercial harvest stage regardless (Fig. 3C). Decreases of TPC and tannin content have been reported

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Table 3
The identification of anthocyanin and the corresponding peak area percentage in ‘Bluecrop’ (A) and ‘Northblue’ (B) blueberries picked at five different development
stages. Data are presented as mean ± SD (n = 3). The different superscripts show significant differences within a row at p < 0.05 through using Turkey’s test.
A.

Peak RT (min) Molecular (m/z) Fragment (m/z) Tentative identification B1 B2 B3 B4 B5

1 17.25 611 449/287 Cyanidin-3,5-dihexoside 0.14 ± 0.03a trA ndB nd nd

2 18.66 465 303 Delphinidin 3-galactoside 8.87 ± 0.36e 20.87 ± 0.24d 25.56 ± 0.26c 26.46 ± 0.11b 30.66 ± 0.22a
3 19.29 435 303 Delphinidin 3-arabinoside 25.95 ± 0.05c 27.48 ± 0.18b 28.32 ± 0.25a 24.60 ± 0.28d 13.44 ± 0.08e
4 20.24 449 287 Cyanidin 3-galactoside 31.99 ± 0.12a 18.59 ± 0.19b 13.53 ± 0.14c 10.95 ± 0.26d 9.16 ± 0.09e
5 21.06 479 317 Petunidin 3-glucoside 23.10 ± 0.11a 15.35 ± 0.26b 14.07 ± 0.10c 9.88 ± 0.08d 6.15 ± 0.12e
21.3 419 287 Cyanidin 3- arabinoside tr tr tr tr tr
21.59 449 317 Petunidin 3-arabinoside nd tr tr tr tr
6 21.77C 463 301 Peonidin 3-glucoside nd 5.89 ± 0.16c 5.90 ± 0.14c 11.29 ± 0.12b 16.92 ± 0.14a
493 331 Malvidin 3-galactoside 2.59 ± 0.20d
7 22.70D 493 331 Malvidin 3-glucoside 5.44 ± 0.16d 7.30 ± 0.16c 8.27 ± 0.13b 8.50 ± 0.07b 9.35 ± 0.09a
433 301 Peonidin 3-arabinoside nd nd nd nd
8 23.02 463 331 Malvidin 3-arabinoside 0.29 ± 0.02d 3.67 ± 0.28c 3.97 ± 0.16c 7.71 ± 0.16b 9.59 ± 0.09a
9 25.27 491 287 Cyanidin-3-acetylhexoside 1.62 ± 0.09a 0.84 ± 0.03b 0.38 ± 0.02c 0.43 ± 0.02c nd
10 25.64 521 317 Petunidin-3-acetylhexoside nd nd nd tr 1.11 ± 0.07a
11 26.26 465 303 Delphinidin 3-glucoside tr tr tr tr 1.12 ± 0.08a
12 27.23 535 331 Malvidin 3-acetylhexoside nd nd nd nd 2.50 ± 0.11a
28.90 611 465/303 Delphinidin 3-rutinoside nd nd nd nd tr
13 30.01 449 287 Cyanidin-3-glucoside tr tr tr tr nd

B.

Peak RT (min) Molecular (m/z) Fragment (m/z) Tentative identification N1 N2 N3 N4 N5

e d c b
1 18.66 465.00 303.00 Delphinidin 3-galactoside 10.52 ± 0.14 19.78 ± 0.16 24.39 ± 0.31 27.04 ± 0.40 27.61 ± 0.29a
2 19.29 435.00 303.00 Delphinidin 3-arabinoside 34.03 ± 0.15a 31.24 ± 0.29b 27.31 ± 0.19c 25.64 ± 0.25d 16.86 ± 0.19e
3 20.24 449.00 287.00 Cyanidin 3-galactoside 24.20 ± 0.27a 22.09 ± 0.11b 15.09 ± 0.25c 14.63 ± 0.09d 12.89 ± 0.22e
4 21.06 479.00 317.00 Petunidin 3-glucoside 17.50 ± 0.12a 16.38 ± 0.16b 14.09 ± 0.15c 11.96 ± 0.17d 1.88 ± 0.09e
21.30 419.00 287.00 Cyanidin 3- arabinoside trA tr tr tr tr
21.59 449.00 317.00 Petunidin 3-arabinoside ndB nd tr tr tr
5 21.77 463.00 301.00 Peonidin 3-glucoside nd nd
493.00 331.00 Malvidin 3-galactoside 4.54 ± 0.14d 4.18 ± 0.43d 5.90 ± 0.11c 8.70 ± 0.13b 20.36 ± 0.15a
6C 22.70 493.00 331.00 Malvidin 3-glucoside 5.99 ± 0.15c 2.86 ± 0.14e 6.44 ± 0.13b 5.23 ± 0.09d 10.65 ± 0.14a
433.00 301.00 Peonidin 3-arabinoside nd nd
7D 23.02 463.00 331.00 Malvidin 3-arabinoside 3.21 ± 0.13de 3.47 ± 0.12d 5.90 ± 0.16bc 6.18 ± 0.14b 9.74 ± 0.14a
8 25.27 491.00 287.00 Cyanidin-3-acetylhexoside nd nd 0.42 ± 0.03a 0.32 ± 0.03b nd
9 25.64 521.00 317.00 Petunidin-3-acetylhexoside nd nd 0.16 ± 0.02a tr nd
10 26.26 465.00 303.00 Delphinidin 3-glucoside nd tr nd tr tr
11 27.23 535.00 331.00 Malvidin 3-acetylhexoside nd nd nd tr tr
12 30.40 449.00 287.00 Cyanidin 3-glucoside nd nd nd tr tr
A
‘tr’ means detected traceable amount by MS.
B
‘nd’ means not detected.
C
Peonidin 3-glucoside coeluted with malvidin 3-galactoside.
D
Peonidin 3-arabinoside coeluted with malvidin 3-glucoside.

leading to improve sensory attribute in fruit by reducing the as- (2017) found that anthocyanin fraction of the berries are the major
tringency and bitterness of fruit (Kulkarni and Aradhya, 2005). Many antioxidant compounds, which showed around 2-fold higher of anti-
studies suggested that astringency is a tactile sensation induced by the oxidant capability than phenolic fraction. Consequently, we assumed
precipitation of a complex composed of proline-rich proteins present in that the accumulation of anthocyanins can then lead to increased an-
the human saliva with tannins or phenolic compounds present in bev- tioxidant activity of blueberry during ripening.
erages such as tea or red wines (Cala et al., 2012; Ferrer-Gallego et al.,
2014; Freitas and Mateus, 2012). The blueberry fruit at stage one used 3.5. Identification of anthocyanin
in this study can be greatly used to produce fruit wines and tea due to
high TPC, TFC, TPAC and flavor of astringency because of high tannin The anthocyanin composition in ripened blueberry fruit has been
level. In the present study, a decrease in tannin content, TA and TPC studied extensively. Approximately 22 species of anthocyanin have
and an increase in TSS toward fruit maturation also marked the shift in been reported in the blueberry extracts (Wang et al., 2017). In the
the taste characteristic of blueberry fruit, which means the ripened present study, 18 individual anthocyanins from five groups of antho-
blueberry fruit are more popular and directly edible. While anthocya- cyanidins (delphinidin, cyanidin, petunidin, peonidin, malvidin), were
nins and proanthocyanidins share a common biosynthetic pathway, identified from two blueberry cultivars extracts using HPLC-ESI-MS2
their accumulation showed a typically opposite trend. The proantho- (Table 3). Only 13 and 12 peaks of Bluecrop and Northblue cultivar
cyanidins levels were greater in the early stage of fruit, anthocyanins blueberry extracts, respectively, were found in the chromatograms due
accumulated in substantial quantities toward fruit ripening. The switch to the two coelutions and several anthocyanins which were traceable by
from proanthocyanins to anthocyanins is related to the shift in strategy MS (Figs. S1 and S2). The coelutions of peonidin 3-glucoside with
from protecting fruit against herbivory to promoting seed dispersal by malvidin 3-galactoside and malvidin 3-glucoside with peonidin 3-ara-
larger herbivores (Michael et al., 2012). Fruit exhibited a decrease of binoside were commonly found in berries (Lohachoompol et al., 2008).
TFC (Fig. 3D) during maturation, being lowest in the ripe fruit of two As the fruit ripened and the skin color changed from green to blue-
cultivars (B5: 4.95 g kg−1 RE; N5: 4.18 g kg−1 RE). Coklar and Akbulut purple, the prominent anthocyanin were delphinidin-type and

6
Y. Lin, et al. Postharvest Biology and Technology 162 (2020) 111097

3.6. Total antioxidant activities of blueberry extracts

The total antioxidant activities of blueberry extracts were evaluated

by ORAC and PSC assays, and the result are shown in Fig. 4. At the same
development stage, Northblue showed higher values of ORAC and PSC
than Bluecrop, which indicates a higher antioxidant capacity of
Northblue cultivar. The highest PSC and ORAC values were found at
ripened stage in both cultivars. The values of ORAC and PSC were
higher at the first stage compared with the second stages, and gradually
increased as the fruit ripens reaching a peak at the fully ripened stage
(B5, N5). This is consistent with total antioxidant activities in other
berries during ripening (Giné-Bordonaba et al., 2017). The antioxidant
showed a decreased tendency in the beginning of fruit development,
because the contents of TPAC, TPC and TFC were highest at the first
stage of blueberry fruit. Proanthocyanidins, polyphenols and flavonoids
are known antioxidants. In contrast, the antioxidant activity obviously
increased at stage three, because the TAC was significantly higher than
the first stage and reached the peak at fifth stage. In most berry fruit,
the high antioxidant capability is mostly attributed to the polyphenols,
especially anthocyanins (Coklar and Akbulut, 2017).
The ORAC values (Fig. 4A) of Bluecrop significantly increased from
B1 to B5, ranged from 21.77 to 74.54 mmol kg−1 TE. The highest ORAC
value was observed in N5 (101.07 mmol kg-1 TE), which have the
highest anthocyanin content. Compared with other fruits, ripe blue-
berry samples reported in this study have higher ORAC values than
those of apple (45.92 mmol kg−1 TE), pomegranate (44.79 mmol kg−1
TE) and red grape (26.05 mmol kg-1 TE) (Liu, 2013). PSC capacity
(Fig. 4B) in both cultivars increased during ripening and highest ac-
tivity was observed at B5 and N5, as 36.42 and 42.45 mmol kg−1 vi-
tamin C, respectively. Researchers also have reported that fruits had
strong antioxidant activities, and the blueberry’s PSC value was sig-
nificantly higher than other fruits, including apple (30.92 mmol kg−1
vitamin C), cranberry (10.20 mmol kg−1 vitamin C), and grape (20.19
Fig. 4. Total antioxidant activities detected by ORAC (mmol kg−1 Trolox mmol kg−1 vitamin C) (Adom and Liu, 2005). Anthocyanin accumu-
equivalent, TE) A, and PSC assay (mmol kg−1 Vitamin C equivalent, VitCE) B, lation, deepening of color and ripening are associated with strong an-
in different ripening stage of blueberry fruit from the Bluecrop and Northblue tioxidant ability in blueberry which may guide commercial producers
cultivar (mean ± SD, n=3). Vertical bars represent the SD of the means. The in harvesting blueberry with good antioxidant properties.
different superscripts show significant differences at p < 0.05 for different ri-
pening stage from same cultivar blueberry through using Tukey’s test.
4. Conclusions

malvidin-type anthocyanins instead of cyanidin-type anthocyanins, In this study, impact of cultivars and ripening stages on the taste
which is consistent with previous results (Michael et al., 2012). characteristic, phytochemical profile and antioxidant activity of blue-
In comparison with different stages of blueberry fruit, individual berry was assessed. In both cultivars, sweetness, sourness and as-
anthocyanins decreased with fruit development in Bluecrop cultivar, tringency showed a great taste response concomitant with increased
including, cyanidin 3-galactoside (4), petunidin 3-glucoside (5), cya- TSS and decreased TA and tannins during ripening. The unripened
nidin-3-acetylhexoside (9). From B1 to B5, the peak area percentage of blueberry fruit were better harvested for polyphenols, tannins and as
cyanidin 3-galactoside (4), petunidin 3-glucoside (5) and cyanidin-3- raw material to produce wine or tea. Maturation of blueberry was ac-
acetylhexoside (9) decreased by 41.41 %. Delphinidin 3-arabinoside companied by increase in anthocyanin content and decrease in proan-
increased slightly from B1 to B3, but dropped at B4. The cyanidin-3,5- thocyanidin, polyphenol, and flavonoid concentration. The changes in
dihexoside (1) was detected (0.14 %) in unripened fruit and dis- physical and sensory characteristics were in accordance with the
appeared in ripened fruit (Table 3). Individual anthocyanins from changes in individual compounds and antioxidant properties of blue-
groups of delphinidin, malvidin and peonidin increased during Blue- berries during ripening. This study can help the blueberry industry in
crop blueberry fruit maturation. In accordance with their deep colora- determining when to harvest for optimum quality and health promoting
tion, blue-purple delphinidin-type anthocyanins accumulated dramati- properties.
cally.
For Northblue cultivar, 8 anthocyanins were detected in N1 stage
while 14 were detected in N5 stage (Table 3). A significant level of Author statement
delphinidin 3-arabinoside was quantified in the N1 stage of Northblue
blueberry at 34.03 %, followed by the cyanidin 3-galactoside and pet- YL performed the experiments. YL and XM designed the experi-
unidin 3-glucoside at 24.20 % and 17.50 %, respectively. These then ments. YL, GH, QZ, YW, VPD and XM analyzed and interpreted the data.
decreased to 16.86 %, 12.89 % and 1.88 % at N5 stage. Four individual YL, VPD and XM wrote the manuscript. YL and VPD edited the final
anthocyanins, delphinidin 3-galactoside, malvidin 3-galactoside, mal- version of the manuscript.
vidin 3-glucoside and malvidin 3-arabinoside remarkably accumulated
in Northblue blueberry during ripening with concentrations of 17.09 %, Declaration of Competing Interest
15.82 %, 4.66 % and 6.53 %, respectively.
The authors declare no conflict of interest.

7
Y. Lin, et al. Postharvest Biology and Technology 162 (2020) 111097

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