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Journal of Food Composition and Analysis
Journal of Food Composition and Analysis
Journal of Food Composition and Analysis
A R T I C L E I N F O A B S T R A C T
Keywords: The spatial distribution and time-course evolution of polyphenol compounds in response to exogenous light and
Kyoho temperature in grape berry (Vitis labruscana cv. ‘Kyoho’) were examined. Results demonstrated that the poly
Flavanols phenol biosynthesis was induced via the up-regulated gene transcription levels during berry ripening. The
Anthocyanins
polyphenol biosynthesis was differentially observed in skins, stems, leaves and seeds, and the more polyphenols
Maturity stage
Spatial distribution
were accumulated in seeds; and the polyphenols were significantly distributed in bottom berries of grape clus
Polyphenol ters. Additionally, the lower temperature (4 ℃) accelerated the polyphenol biosynthesis by 1.3 times after
storage of 28 days, whereas the light exposure slightly inhibited the polyphenol biosynthesis of berry during
storage at 25 ℃. In conclusion, the data presented in this study shed more light on deeper understanding of the
spatial accumulation and time-course evolution of polyphenols in grape berry.
1. Introduction characteristic red, blue and purple colors, widely exist in grape tissues,
especially in berry skins (Askari-Khorasgani and Pessarakli, 2019a;
Grape vine is a highly profitable product rich in natural bioactive Zhang et al., 2015). The pathway of polyphenol biosynthesis has been
compounds (Wang et al., 2020). Up to now, there are thousands of grape well studied, which has been proved through the phenylpropanoid and
varieties cultivated throughout the world, while numerous cultivars are flavonoid pathway. Firstly, the phenylalanine as the initial substrate of
bred by crossing of different Vitis species (Guo et al., 2016). Vitis lab phenylpropanoid pathway, and 4-coumaroyl-coA is formed by catalysis
ruscana cv. ‘Kyoho’, firstly developed by Japanese scientists, is one of of phenylalanine ammonia lyase (PAL), cinnamate-4-hydroxylase (C4H)
the economically grape varieties due to its large berries (12− 14 g), rich and 4-coumaroyl-coA synthase (4CL) in sequence. Phenolic acids and
juice and pleasing taste (Xu et al., 2018; Deng et al., 2006). Its physio precursors of stilbenes are mainly produced during phenylpropanoid
logical characters including strong adaptability, cold tolerance, and pathway. Subsequently, the flavanones, flavanols and flavonols are
disease resistance are also extremely attractive (Xu et al., 2018). produced in the beginning, which are further reduced and modified to
Polyphenols are the important bioactive secondary metabolites and generate anthocyanidins in the flavonoid pathway. In the end, the an
natural antioxidants in berry, which are outstandingly beneficial to thocyanins are synthesized by glycosylation and methylation of antho
human health. As a class of phytochemicals, polyphenols mainly include cyanidins. In recent years, grape polyphenols have been studied by a
phenolic acids, stilbenes, and flavonoids. Flavonoids can be divided into significant number of works due to an array of beneficial biological
flavonols, flavanols, flavanones and anthocyanins (Askari-Khorasgani properties such as antioxidant, anti-inflammatory, and anti-diabetes as
and Pessarakli, 2019a). Anthocyanins, which generally exhibit well as prevention of cancer, osteoporosis, and cardiovascular diseases
* Corresponding author at: Key Laboratory for Agro-Products Postharvest Handling of Ministry of Agriculture and Rural Affairs, College of Biosystems Engineering
and Food Science, Zhejiang University, Hangzhou, 310058, China.
E-mail addresses: qiming123@zju.edu.cn (M. Qi), luozisheng@zju.edu.cn (Z. Luo), xjuwubin0320@sina.com (B. Wu), wangley@zju.edu.cn (L. Wang), ymy008@
zju.edu.cn (M. Yang), xiaochen_zhang@zju.edu.cn (X. Zhang), xingyu@zju.edu.cn (X. Lin), xuyanqun@zju.edu.cn (Y. Xu), lixihong606@163.com (X. Li), lili1984@
zju.edu.cn (L. Li).
https://doi.org/10.1016/j.jfca.2021.104353
Received 22 June 2021; Received in revised form 22 November 2021; Accepted 11 December 2021
Available online 13 December 2021
0889-1575/© 2021 Elsevier Inc. All rights reserved.
M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
Fig. 2. Quality traits in ‘Kyoho’ berries at different maturity stages (A-F) and in berries differentially located in grape cluster (G-L). Error bars represent standard
deviations of three replicates. Different letters represent significant differences between groups (p < 0.05).
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M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
Table 1
Polyphenolic compounds identified in ‘Kyoho’ grape.
Peak No. Compound Wavelength (nm) Ion mode RT (min) m/z ration Product ions
Phenolic acids
1 Gallic acid 280 – 7.35 169.0160 169.02
2 Caftaric acid 280 – 13.91 311.0948 179.04; 135.04
3 Coutaric acid 280 – 19.70 295.0460 163.04
Flavonols
4 Myricetin-3-glucoside 280 – 37.89 479.0827 316.02
5 Quercetin-3-rhamnose-glucuronide 280 – 46.76 477.1400 301.04
6 Quercetin-3-rhamnoside 280 – 56.86 447.1699 301.03
Flavanols
7 (+)-Gallocatechin 280 – 11.13 305.0673 125.02
8 Proanthocyanidin dimer B3 280 – 15.11 577.1351 425.10; 407.08; 289.07
9 (-)-Epigallocatechin 280 – 15.41 305.0677 125.02
10 Proanthocyanidin tetramer-1 280 – 15.55 1153.2665 575.13; 287.06
11 Proanthocyanidin dimer B1 280 – 15.82 577.1872 425.09; 407.08; 289.07
12 (+)-Catechin 280 – 17.83 289.1073 245.08
13 Proanthocyanidin trimer-1 280 – 18.96 865.2004 577.14; 287.06
14 Proanthocyanidin tetramer-2 280 – 20.46 1153.2674 575.12; 287.06
15 Proanthocyanidin dimer B4 280 – 23.34 577.1860 425.09; 407.08; 289.07
16 (-)-Epicatechin 280 – 24.89 289.0721 245.08
17 Proanthocyanidin trimer-2 280 – 32.54 865.1995 577.14; 287.07
18 Proanthocyanidin trimer-3 280 – 33.77 865.2007 577.14; 287.06
19 Proanthocyanidin dimer B2 280 – 35.10 577.1356 425.09; 407.08; 289.07
20 Proanthocyanidin tetramer-3 280 – 35.96 1153.2655 575.12; 287.06
21 (-)-Epicatechin gallate 280 – 42.56 441.0830 289.07; 169.01
Anthocyanins
22 Malvidin-3,5-diglucoside 520 + 18.42 655.1864 331.08
23 Peonidin-3-glucoside 520 + 28.52 463.1235 301.07
24 Malvidin-3-glucoside 520 + 31.06 493.0982 331.08
25 Peonidin-3− 6′ ′ -p-coumaroyl-glucoside-5-glucoside 520 + 55.16 771.2134 301.07
26 Malvidin-3− 6′ ′ -p-coumaroyl-glucoside-5-glucoside 520 + 57.23 801.2247 331.08
27 Cyanidin-3-glucoside 520 + 61.27 449.1092 287.06
28 Petunidin-3-glucoside 520 + 62.10 479.1182 317.07
29 Cyanidin-3− 6′ ′ -p-coumaroyl-glucoside 520 + 62.49 595.1440 287.05
30 Petunidin-3− 6′ ′ -p-coumaroyl-glucoside 520 + 62.69 625.1557 317.07
31 Peonidin-3− 6′ ′ -p-coumaroyl-glucoside 520 + 63.21 609.1594 301.08
32 Malvidin-3− 6′ ′ -p-coumaroyl-glucoside 520 + 63.31 639.1706 331.08
(Ferreyra et al., 2012; Silva et al., 2020). Furthermore, effects of biotic et al., 2016). Li et al. (2019a) reported that ‘Kyoho’ grape contained
and abiotic factors such as pathogens, temperature, light and drought higher concentration of polyphenols than other red grape varieties (Gold
(Askari-Khorasgani and Pessarakli, 2019a; Li et al., 2016; Romero et al., Finger, Hakuho, White Olympia, Shine Muscat, Beni Fuji and Moldova).
2020), on the polyphenol profile and synthesis of grapevine are getting In the vineyard, the weight, total soluble solids (TSS), titratable acidity
more and more attention. (TA), alcoholic degree, aromatic composition as well as polyphenolic
Recent studies indicated that the accumulation and biosynthesis of composition variations within grape cluster have been studied to
grape polyphenols are very complex in dependence of berry variety, improve the cultivating quality and to provide useful information for
maturity stage, genetic diversity, soil, environmental stress, and agro wine quality prediction (Rutan et al., 2018; Figueiredo-Gonzalez et al.,
nomic management practices (Askari-Khorasgani and Pessarakli, 2019a; 2013; Noguerol-Pato et al., 2012). Furthermore, the altered microcli
Li et al., 2019a). A series of physicochemical and biochemical processes matic sunlight conditions were evident to influence the development
take place as evolution of berry development and ripening, which and composition of berries (Gao et al., 2021). Noguerol-Pato et al.
contributed to the presence of variation in polyphenol composition and (2012) reported that there was presence of variability in the aromatic
antioxidant capacities (Nedomova et al., 2017; Fuentes et al., 2016). composition between the shoulder and tip berries in grape clusters. As
Previous studies showed that anthocyanins and flavonols increased as for polyphenols, exposure to sunlight could promote the accumulation
berry ripening, while flavanols content remained constant or declined of flavonols and modulate the concentration and composition of the
from post-veraison to harvest time in ‘Nebbiolo’ and ‘BRS Vitoria’ grape anthocyanins in berry skins (Downey et al., 2006).
berry (Locatelli et al., 2016; Colombo et al., 2021). Additionally, the It is worthwhile to mention the polyphenolic profiles in grapevine
spatial distribution of grapes directly or indirectly affects the poly were considerably affected by exogenous abiotic stress, such as tem
phenolic accumulation in berry. The quality of the grape juice and wine perature and light. According to previous studies, there is no common
produced has partly been dependent on the polyphenolic profiles trend in the change of grape total polyphenol content in response to
(Biniari et al., 2020). Grape skins, stems, leaves and seeds are rich in postharvest preservation treatment (Azuma et al., 2012; Romero et al.,
polyphenols, which provide valuable information for their antioxidant 2020; Šamec and Piljac-Žegarac, 2011). Šamec and Piljac-Žegarac
potential and great commercial value as agricultural by-products (2011) found that the contents of total phenols, total flavonoids and
(Biniari et al., 2020; Perez-Navarro et al., 2019; Pastrana-Bonilla total anthocyanins in red grapes increased at the end of storage at 4 ℃
et al., 2003). It is demonstrated that the flavan-3-ols and proanthocya and 25 ℃, and the increase might be due to a release of phenolic com
nidins are predominant polyphenols in the grape seeds, while flavonols pounds from their complexes with other components like proteins and
and anthocyanins are abundant in the skins of 13 grapevine varieties carbohydrates. In ‘Pione’ grape, the flavonoid biosynthesis was appar
such as ‘Cabernet Sauvignon’, ‘Merlot’ and ‘Prokupac’ grapes (Pantelic ently enhanced when grape clusters were exposed to light or low
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M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
Fig. 3. Identification of polyphenols in ‘Kyoho’ grape. HPLC chromatograms of the grape extract (skin, stem, leaf and seed) recorded at 280 nm, 320 nm and 520 nm.
The numbered identified peaks are listed in Table 1.
temperature, whereas the flavonoid biosynthesis was inhibited in the and the effect of exogenous light and temperature on endogenous
dark (Azuma et al., 2012). Under specific environmental conditions, polyphenol biosynthesis was investigated. Additionally, the gene tran
grapevine receives information to activate or inhibit related gene scriptions involved in berry polyphenol biosynthesis were determined.
expression and metabolic pathways, such as producing more bioactive Results from the present study shed new light on the comprehensive
compounds like flavonoids to activate defense mechanisms against UV understanding and efficient utilization of bioactive substance in berries.
light and biotic stress stimuli (Azuma et al., 2012; Askari-Khorasgani
and Pessarakli, 2019b). It was indicated that the accumulation of fla 2. Materials and methods
vonoids hindered protein aggregation and relieved the stress injury
resulted from the electrolyte leakage, oxidative damage, and inactiva 2.1. Chemicals
tion of photosynthesis to improve the plant survivability in cold stress
(Askari-Khorasgani and Pessarakli, 2019b). Catechin and quercetin standards were purchased from Aladdin
Based on above, it is essential to investigate the polyphenols distri Reagent Co., Ltd. (Shanghai, China); cyanidin-3-glucoside standard was
bution and evolution as berry development and ripening, in order to not obtained from Macklin Biochemical Co., Ltd., (Shanghai, China). Stan
only perceive the repertoire of polyphenol compounds, but also provide dards were used for high performance liquid chromatography with
evidence for value-added utilization. Up to now, there has been very diode array detector (HPLC-DAD) analysis to quantify the polyphenolic
limited information available about the polyphenol profiles in ‘Kyoho’ compounds. Methanol and acetonitrile of HPLC grade were purchased
grape (Li et al., 2013; Yang et al., 2020). In the present study, both the from Macklin Biochemical Co., Ltd., (Shanghai, China), while phos
bio-distribution (in skins, stems, leaves, seeds and berries located on top, phoric acid, hydrochloric acid and ethanol of analytical-reagent grade
middle and bottom of grape cluster) and spatial accumulation of poly were purchased from Sinopharm Chemical Reagent Co. Ltd. (Shanghai,
phenol compounds in berry (Vitis labruscana cv. ‘Kyoho’) were studied; China). Deionized water was prepared by water purification system
4
M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
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M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
Fig. 4. Heatmap of relative expression profiles of 14 genes involved in polyphenolic biosynthesis. The log2 of relative expression levels are shown, measured by RT-
qPCR. Relative expression level in grape skin was set as control.
26–50 % area browning, 3 = 51–70 % area browning and 4 = 76–100 % DAD was set between 190 and 600 nm at steps of 2 nm. The polyphenols
area browning. were quantified at 280 nm (flavanols), 320 nm (phenolic acids and
flavonols) and 520 nm (anthocyanins). Quantitative determinations of
2.4. Extraction of polyphenolic compounds flavanols, phenolic acids and flavonols, and anthocyanins were carried
out with the calibration curves obtained for catechin (6.25− 400 mg
Frozen samples of each group were ground to powder in liquid ni L− 1), quercetin (6.25− 400 mg L− 1) and cyanidin-3-glucoside (6.25− 400
trogen using porcelain mortars and pestles. Polyphenols were extracted mg L− 1) external standards, respectively. Results were expressed as mg
by adding 1.0 g of sample powder to 10 mL of 1% HCl-methanol. The kg− 1 fresh weight of tissues. All values were obtained from three
homogenates were vortexed for 10 min and stored in dark at 4 ◦ C for 12 samples.
h. The mixtures were then centrifuged (4 ◦ C, 10,000×g) for 15 min and
the residues were re-extracted twice. The supernatants were subse 2.6. Real-time quantitative PCR (RT-qPCR) and gene expression analysis
quently filtered by 0.22 μm microporous membrane for following high
performance liquid chromatography quadrupole time of flight mass Genes involved in polyphenolic biosynthesis pathway were selected
spectrometry (HPLC-Q-TOF-MS) and HPLC-DAD analysis. based on the website of Kyoto Encyclopedia of Genes and Genomes
(KEGG) pathway. The details of primers are given in Table S1. RT-qPCR
experiment was carried out in three steps. Firstly, the total RNA was
2.5. HPLC-Q-TOF-MS and HPLC-DAD analysis
extracted using the rapid cetyl trimethyl ammonium aromide (CTAB)
method. CTAB method can remove impurities such as proteins, poly
The identification of polyphenolic compounds was performed using
saccharides and phenolic compounds from plant tissues, and precipitate
HPLC system (LC-20AD, Shimadzu, Japan) coupled to Q-TOF-MS (Triple
RNA with ethanol. The RNA concentrations were measured using a
TOF™ 5600+, 130 SCIEX incorporation, United States) with an elec
microplate reader (TECAN, Spark®, Switzerland). Then, mRNA was
trospray ionization source (ESI) system. An AQ-C18 column (water-
reversely transcribed into cDNAs using a PrimeScript™ RT reagent kit
based, 5 μm, 4.6 × 250 mm, Welch Materials incorporation, Shanghai,
(Code DRR047A, TaKaRa, Japan). Finally, RT-qPCR reaction was done
China) was used to separate individual polyphenolic compounds with a
in ABI Step One RT-PCR system, the reaction mixture was comprised of
flow rate of 1 mL min− 1. Polyphenols were eluted with the following
10.0 μl of SYBR Premix Ex Taq™ (RR820A, TaKaRa, Japan) in a total
gradient of solvent B (acetonitrile) in solvent A (1 % phosphoric acid in
volume of 20 μl. The genes transcript levels were calculated by the
water): 0− 10 min, 2 % B; 10− 55 min, 10 % B; 55− 65 min, 18 % B;
house-keeping gene glyceraldehyde-3-phosphate dehydrogenase
65− 68 min, 50 % B; 68− 69 min, 80 % B; 69− 79 min, 2 % B. Mass
(GAPDH) according to the 2− ΔΔCT method. Three biological replicates
spectra were performed in the ESI both negative ion and positive ion
were used.
modes in the 100− 1500 m z− 1 scan range under the following condi
tions: source voltage, -4.5 kV and 5.5 kV; source temperature, 550 ◦ C;
2.7. Statistical analyses
Gas 1 (Air) and Gas 2 (Air), 50 psi; and curtain gas (N2), 35 psi. The
polyphenols were detected at 280 nm and 520 nm depending on their
Data were presented as mean ± standard deviation (SD) values. The
types and identified according to their retention time, rate of mass to
statistical significance analysis of measurement data was analyzed using
charge, and the fragment ion compared to references (Lambert et al.,
one-way analysis of variance (ANOVA), the mean comparisons were
2015; Colombo et al., 2021). Chromatographic system and mass spectra
performed by Duncan’s multiple rage test at the significance level of p <
data were managed and processed using the Peak View software version
0.05 with SPSS software 25.0.
1.2, and a maximum error of 5 ppm was accepted.
For quantifying polyphenols, HPLC equipped with a DAD (SPD-M
20A, Shimadzu, Japan) were used, and the HPLC conditions were the
same as those for HPLC-Q-TOF-MS analysis. The scanning range of the
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M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
Table 3 Data are shown in mean ± standard deviation (n = 3). Different letters of the
The polyphenol concentrations in berries at different maturity stages (mg kg− 1 same component represent statistically significant difference, respectively (p <
skin FW). 0.05). ND: not detected.
Compound Berry in Berry in Berry in
green veraison purple
Phenolic acids
Gallic acid ND ND ND
Caftaric acid 5.41 ± 0.54b 7.75 ± 0.76a 7.99 ± 0.59a
Coutaric acid 32.54 ± 50.15 ± 50.38 ±
0.62b 0.55a 0.40a
Flavanols
(+)-Gallocatechin 3.76 ± 0.25c 13.90 ± 17.37 ±
0.65b 0.56a
Proanthocyanidin dimer B3 76.00 ± 121.79 ± 99.25 ±
1.70c 0.56a 1.73b
(-)-Epigallocatechin 1.80 ± 0.79b 1.38 ± 0.29b 3.67 ± 0.20a
Proanthocyanidin tetramer-1 0.98 ± 0.03c 3.27 ± 0.13b 5.59 ± 0.37a
Proanthocyanidin dimer B1 954.71 ± 1124.59 ± 958.58 ±
39.46b 2.31a 16.17b
(+)-Catechin 41.95 ± 106.90 ± 121.26 ±
1.91c 1.05b 2.62a
Proanthocyanidin trimer-1 48.65 ± 98.74 ± 114.84 ±
2.01c 1.98b 1.23a Fig. 5. Correlation matrix analysis of polyphenols and quality indexes in
Proanthocyanidin tetramer-2 172.19 ± 335.99 ± 416.09 ± ‘Kyoho’ berries at different maturity stages. * values are significant at p < 0.05.
7.90c 1.41b 4.80a
Proanthocyanidin dimer B4 6.80 ± 0.18c 17.82 ± 20.22 ±
0.13b 0.36a 3. Results and discussion
(-)-Epicatechin 28.23 ± 48.73 ± 48.84 ±
1.85b 0.97a 0.23a 3.1. Berry color index, firmness, TSS, TA and morphology
Proanthocyanidin trimer-2 12.57 ± 32.22 ± 39.55 ±
0.98c 0.50b 0.70a
Proanthocyanidin trimer-3 7.03 ± 0.41c 20.28 ± 24.37 ±
The color index L* value was continuously decreased, the value of a*
0.12b 0.55a increased while the value of b* decreased, which indicated the berry
Proanthocyanidin dimer B2 3.40 ± 0.29c 6.12 ± 0.06b 7.28 ± 0.61a surface became darker as grape ripening (Fig. 2A-C). Similarly, previous
Proanthocyanidin tetramer-3 3.37 ± 0.41c 7.25 ± 0.15b 13.33 ± study reported that the color tonality, indicating the proportion between
0.18a
yellow and red colors increased during berry development (Locatelli
(-)-Epicatechin gallate 1.14 ± 0.99c 5.07 ± 1.28b 7.27 ± 0.15a
Total flavanol content 1362.59 ± 1944.07 ± 1897.52 ± et al., 2016). Firmness and TA of the berries gradually decreased, while
56.77b 7.04a 19.07a TSS rapidly increased during grapes ripening (Fig. 2D-F). The noticeable
changes were in agreement with the previous studies (Fuentes et al.,
Anthocyanins 2016; Walker et al., 2001). Based on the above results, the ripening
Malvidin-3,5-diglucoside ND 3.31 ± 0.16b 10.45 ±
process of ‘Kyoho’ grape was accompanied by the color purpling, berry
4.21a
Peonidin-3-glucoside ND 4.77 ± 0.21b 11.35 ± softening, and sugar accumulation, and ‘Kyoho’ grape reached the
0.21a maturity stage approximately 15 days after veraison, which is faster
Malvidin-3-glucoside ND 2.34 ± 0.08b 5.37 ± 0.30a than other grape varieties (Colombo et al., 2021). Furthermore, artificial
Peonidin-3− 6′ ′ -p-coumaroyl- ND 0.50 ± 0.02b 1.14 ± 0.02a sensing systems such as electronic noses (EN), electronic tongues (ET)
glucoside-5-glucoside
Malvidin-3− 6′ ′ -p-coumaroyl- ND 9.85 ± 0.43b 22.26 ±
and electronic eyes (EE) were recently developed to monitor grape
glucoside-5-glucoside 0.35a ripening based on the analysis of physico-chemical traits (Orlandi et al.,
Cyanidin-3-glucoside ND 1.35 ± 0.09b 2.93 ± 0.08a 2019; Gliszczynska-Swiglo and Chmielewski, 2017).
Petunidin-3-glucoside ND 1.12 ± 0.04b 2.62 ± 0.01a There were obvious difference in firmness, TA and TSS values of
Cyanidin-3− 6′ ′ -p-coumaroyl- ND 0.29 ± 0.03b 0.95 ± 0.02a
grape berry according to different parts of the grape clusters. It was
glucoside
Petunidin-3− 6′ ′ -p-coumaroyl- ND 0.47 ± 0.04b 1.48 ± 0.03a interesting that bottom berries exhibited the lowest firmness and the
glucoside highest TA values, while top berries had the lowest TSS value (Fig. 2J-L).
Peonidin-3− 6′ ′ -p-coumaroyl- ND 4.00 ± 0.33b 9.37 ± 0.19a In addition, the berries located in middle of cluster had the highest L*
glucoside and b* values and the lowest a* value. Results demonstrated that the
Malvidin-3− 6′ ′ -p-coumaroyl- ND 5.59 ± 0.23b 15.21 ±
bottom berries had the lowest firmness and the highest TSS/TA ratio as
glucoside 0.29a
Total anthocyanin content 33.59 ± 83.14 ± well as the closest color to purple, which provided evidence that bottom
0.76b 3.98a berries are the ripest berries in grape clusters.
Total polyphenol content 1420.99 ± 2079.04 ± 2125.87 ± The morphology of grape clusters was influenced by exogenous light
57.48b 9.73a 15.46a
and temperature (Fig. 1). During storage at 25 ◦ C, the abscission rate,
the rotten index of berries and the browning rate of the grape stems
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M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
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M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
Table 5
1
The time-course accumulation of polyphenol concentrations in ‘Kyoho’ berries (mg kg− skin FW).
Total phenolic acid content Total flavonol content Total flavanol content Total anthocyanin content Total polyphenol content
c c a e
0 day 56.92 ± 1.16 80.83 ± 10.29 1908.76 ± 43.26 111.86 ± 4.68 2158.37 ± 49.37bc
3 days 62.03 ± 0.62b 89.32 ± 8.44bc 1787.42 ± 38.62b 137.21 ± 3.28d 2075.99 ± 41.10b
Light
25 ℃ 6 days 45.41 ± 0.98d 118.31 ± 4.21a 1417.66 ± 5.82c 208.74 ± 8.05a 1790.12 ± 4.63c
3 days 64.40 ± 2.19a 98.45 ± 4.12b 1847.38 ± 114.45ab 151.38 ± 3.62c 2161.61 ± 108.71bc
Dark
6 days 64.86 ± 0.94a 88.42 ± 1.31bc 1913.04 ± 24.96a 171.17 ± 4.24b 2237.49 ± 21.82a
0 day 46.60 ± 0.64b 72.99 ± 1.37a 2089.69 ± 26.79e 121.75 ± 2.68h 2331.02 ± 27.98d
7 days 37.96 ± 1.99c 42.38 ± 0.34e 1854.78 ± 65.08f 134.74 ± 0.66g 2069.86 ± 65.26e
14 days 33.70 ± 1.16d 42.42 ± 0.63e 1829.29 ± 73.22f 173.22 ± 1.06f 2078.63 ± 72.86e
Light
21 days 43.86 ± 2.92b 59.29 ± 0.78c 2351.60 ± 74.32d 244.91 ± 2.48c 2699.66 ± 69.30c
4℃ 28 days 46.60 ± 0.64b 72.99 ± 1.37a 2606.15 ± 61.70bc 278.66 ± 6.88b 3004.39 ± 63.85b
7 days 40.72 ± 0.91c 35.88 ± 1.67f 2327.64 ± 23.97d 194.99 ± 5.21e 2599.24 ± 27.90c
14 days 51.59 ± 3.11a 53.40 ± 0.39d 3236.36 ± 117.01a 206.08 ± 4.82d 3547.43 ± 111.25a
Dark
21 days 45.03 ± 0.40b 61.70 ± 1.26b 2529.72 ± 70.60c 290.70 ± 3.61a 2927.15 ± 73.67b
28 days 50.90 ± 1.29a 53.80 ± 1.79d 2673.32 ± 63.34b 251.82 ± 7.30c 3029.83 ± 59.10b
Data are shown in mean ± standard deviation (n = 3). Different letters of the same component represent statistically significant difference (p < 0.05). The data of 25 ℃
and 4 ℃ are compared separately.
phenolic composition profiles become an available tool for grape variety mechanism of polyphenol metabolism. Phenylpropanoids are a diverse
differentiation, principally anthocyanins, flavonols and flavan-3-ols group of plant secondary metabolites, and the flavonoid pathway is the
located in grape skins and seeds. Highest levels of total polyphenols last step of flavonoid synthesis, which is directly linked to the qualitative
were found in seeds, followed by stems, leaves and finally skins, and the and quantitative characteristics of the flavonoids (Li et al., 2019b). The
total polyphenol content of seeds were approximately 6.3 times rela transcriptional profiles of polyphenol biosynthesis genes using RT-qPCR
tively to the total polyphenol content of skins, even though only flava are shown in Fig. 4. The transcript levels of chalcone isomerase (VvCHI),
nols were most abundant in seeds (Table 2). Among flavanols group, dihydroflavonol 4-reductase (VvDFR), leucoanthocyanidin reductase
(+)-catechin showed the highest concentration in the seeds (4868 ± 27 (VvLAR), anthocyanidin reductase (VvANR) and flavonol synthase
mg kg− 1 seed FW), while skins, leaves and stems were rich in proan (VvFLS) in stems and leaves, as well as VvANR and VvFLS in seeds were
thocyanidin dimer B1 (1041 ± 49 mg kg− 1 skin FW, 3417 ± 83 mg kg− 1 higher than those of skins, which was consistent with our results that
leaf FW and 3055 ± 26 mg kg− 1 stem FW). Previous studies also showed there were more flavanols in stems, leaves, and seeds than in skins. ANR
that the maximum concentration of total polyphenols was found in seeds and LAR are both specific enzymes for the generation of flavan-3-ols.
among different grape tissues (Pastrana-Bonilla et al., 2003; Souquet ANR is a key enzyme in the biosynthesis of proanthocyanidin, and
et al., 2000). Besides, the proanthocyanidins and flavan-3-ols were the plays a key role in the downstream of this biosynthetic pathway (Liang
most abundant in the grape seeds, while the skins of red grapes were rich et al., 2021).
with anthocyanins (Pantelic et al., 2016). Notably, few flavanol mono
mers were detected in leaves (Table 2). The results suggested the low 3.3.2. Polyphenols and gene expression analysis in different maturity stages
and high condensation degree of flavan-3-ols in seeds and leaves, Several studies demonstrated that the berry ripeness and the accu
respectively. Gallic acid was only identified in seeds, which was in mulation of polyphenols have a significant correlation. Generally, the
contrast to a previous report that gallic acid was one of the major phe content of polyphenols in grape skins shows a rising trend during
nols in seeds and leaves of ‘Muscadine’ grape (Pastrana-Bonilla et al., ripening (Zhou et al., 2019). Table 3 shows that two phenolic acids,
2003). Flavonols in grapes were mainly myricetin-3-glucoside, querce three flavonols, and fifteen flavanols were found in grapes at different
tin-3-rhamnose-glucuronide and quercetin-3-rhamnoside, while maturity stages, while eleven anthocyanins only exist in the veraison
myricetin-3-glucoside was not presented in seeds. and purple berries. Additionally, the results indicated that almost all
Quercetin-3-rhamnose-glucuronide showed the highest concentration. identified polyphenol compounds increased during ripening, the total
The leaves were rich with quercetin-3-rhamnose-glucuronide content, polyphenol contents of green, veraison and purple berries were 1420 ±
11.1 times more than skins (Table 2). Nevertheless, several studies 57, 2079 ± 9 and 2125 ± 15 mg kg− 1 skin FW, respectively. Moreover,
showed that quercetin-3-glucoside and quercetin-3-glucuronide were the total contents of polyphenols, phenolic acids, flavonols, flavanols
the major flavonols in other grape cultivars (Blancquaert et al., 2019; and anthocyanins were positively correlated with each other (r =
Colombo et al., 2021). The difference indicated that the flavonol profiles 0.72− 0.99), and they were positively correlated with a* value and TSS,
could be potential approach to distinguish ‘Kyoho’ grape, which is while negatively correlated with L* value, b* value, firmness and TA
especially abundant in quercetin-3-rhamnose-glucuronide. In addition, (Fig. 5). The correlation matrix analysis reflects positive correlation
there were eleven anthocyanin compounds identified and quantified in between berry ripeness and polyphenol accumulation. On the other
the skins and six in stems, whereas none of them was determined in the hand, the total contents of flavonols and anthocyanins displayed sig
leaves and seeds. The skins exhibited the highest concentrations in the nificant negative correlations with b* value, respectively (p < 0.05),
total anthocyanins content (111 ± 4 mg kg− 1 skin FW) and each indi which indicated a strong relationship between color and total flavonol
vidual anthocyanin with a significant difference in comparison to other content and total anthocyanin content (Fig. 5). However, proantho
tissues. The most abundant anthocyanins in skins were malvidin de cyanidin B3 and proanthocyanidin B1 showed a trend from rising to
rivatives, most of which was malvidin-3− 6′′ -p-coumar decline, and displayed the highest value at the veraison stage (Table 3).
oyl-glucoside-5-glucoside, accounted for more than 34.9 % of total The results were consistent with the previous study, where the content of
anthocyanins in skins followed by malvidin-3− 6′′ -p-coumaroyl-gluco proanthocyanidin dimers in the skins decreased in the course of matu
side. Similarly, Li et al. (2013) reported that malvidin-3-( ration (Colombo et al., 2021). Furthermore, there were no significant
trans)-coumaroyl-5-diglucoside and malvidin-3-glucoside were the most changes in phenolic acid content after veraison stage. It suggested
abundant anthocyanins in fresh skins of ‘Kyoho’ and ‘Cabernet Sau polyphenol content could remain constant or declined when grapes
vignon’ grapes, respectively. reached a certain level of ripeness. Locatelli et al. (2016) reported that
Moreover, the genes expression involved in phenylpropanoid and during ripening, the caftaric acid content drastically decreased and the
flavonoid pathways were investigated to elucidate the molecular highest value of coutaric acid was exhibited at veraison completion.The
9
M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
synthesis of hydroxycinnamates occurred mainly before veraison and eliminating the free radicals, as the phenol hydroxyl is easily oxidized.
their concentration decreased while fruit size increased and the solutes The environmental stress can lead to lots of reactive oxygen and free
diluted due to their accumulation occurred prevalently in the pulp radicals of fruit, and polyphenols are consumed when they are involved
(Locatelli et al., 2016). Previous study demonstrated that there were in scavenging of these free radicals (Xia et al., 2015; Radovanovic et al.,
strong correlations between total polyphenol content and antioxidant 2009). Additionally, Table 5 reflects that total flavanols were nearly
capacity (Fuentes et al., 2016; Ban et al., 2020). The present work also 25.7 % lost after storage at 25 ℃/light, while it was essentially main
provided the evidence that ‘Kyoho’ grapes could be potentially used as a tained after storage at 25 ℃/dark. On the contrary, increasing trends of
promising functional source due to the high content of polyphenols. the total flavanol content were exhibited in grapes stored at 4 ℃ light
In the present study, RT-qPCR result shows almost all genes were up- and dark, from 2089 ± 26 mg kg− 1 skin FW to 2606 ± 61 and 2673 ± 63
regulated during ripening, except VvANR and VvFLS, as they exhibited mg kg− 1 skin FW, respectively. The considerably higher levels of fla
higher transcript levels in green berries (Fig. 4). In flavonoid biosyn vanols in grapes stored at 4 ℃ indicated that flavan-3-ols underwent
thesis, the flavonols produced by FLS, and anthocyanidin serves as the more marked polymerization and condensation reactions. The higher
substrate for the synthesis of epicatechin by ANR (Liu et al., 2013), thus accumulation of flavan-3-ols derivatives in the grapes grown under a
the decrease of VvFLS and VvANR gene transcription levels may cold climate were also observed by Serratosa et al. (2014). In present
contribute to the accumulation of anthocyanins. These results indicated study, the concentrations of total anthocyanins were increased in four
the notably up-regulated gene transcription of polyphenol metabolism storage groups, whereas anthocyanins rose more sharply under light
which contributed to the rapid accumulation of polyphenols. than that in dark. Correspondingly, Romero et al. (2020) reported that
low temperature postharvest storage and application of light irradiation
3.3.3. Polyphenols and gene expression analysis in different cluster parts could increase anthocyanin levels. Moreover, total polyphenol contents
Most of polyphenolic components in bottom berries had a higher varied similar to total flavanol contents in four storage groups, respec
concentration than top and middle berries except caftaric acid, (-)-epi tively, since the flavanol accounted for a large proportion in polyphenol
gallocatechin, (-)-epicatechin gallate, proanthocyanidin tetramer-1, content.
proanthocyanidin dimer B2, malvidin-3,5-diglucoside, and cyanidin- The metabolic regulation of polyphenol biosynthesis pathway is
3− 6′′ -p-coumaroyl-glucoside (Table 4). The total polyphenol content in partially dependent on the transcriptional level, including transcrip
bottom berries was 12.4 % higher than that in top berries and 12.2 % tional regulation in response to various abiotic stresses, such as the light
higher than that in middle berries, while there was no significant dif and temperature. Polyphenols, especially flavonoids, are closely related
ference between total polyphenol contents in middle and top berries. to plant resistance (Ferreyra et al., 2012). The expression level of most of
Correspondingly, almost all genes in bottom berries had higher genes increased during the storage at 25 ℃, while chalcone synthase
expression levels than that in top and middle berries while the expres (VvCHS), anthocyanidin-3-glucosyltransferase (Vv3GT) and VvLAR were
sion levels of these genes in top and middle berries were approximately down-regulated. Furthermore, most of the genes were inhibited during
equal. These results were in agreement with the study by Figueir the storage at 4 ℃, whereas the expression of VvCHS, VvCHI, flavanone
edo-Gonzalez et al. (2013), which found that total anthocyanins and 3β-hydroxylase (VvF3H) and VvDFR increased. Nevertheless, it is
total flavonols exhibited higher upward trends in tops than that in notable that CHS, which is the first enzyme in the flavonoid pathway and
shoulders within the ‘Mouratón’ grape clusters during ripeness. How provides the precursors for various flavonoids (Ghasemzadeh et al.,
ever, Figueiredo-Gonzalez et al. (2012) reported that no significant 2014), was down-regulated at 25 ℃ but up-regulated at 4 ℃, which was
difference in anthocyanin and flavonol contents collected from both in good agreement with changing trend of polyphenol concentrations.
positions of ‘Gran Negro’ grape. Grapes located inside the top and Previous studies showed that low temperature promoted the accumu
middle positions receive less sunlight radiation than bottom berries, lation of polyphenols by up-regulating the gene expression in the poly
which could explain the different accumulations of polyphenols phenol biosynthesis pathway, while the effect of high temperature on
observed for different grape cluster parts. In ‘Pinot noir’ grape, the polyphenol metabolism was controversial (Azuma et al., 2012; Zhang
significant changes in flavonols and anthocyanins were found between et al., 2015). High temperature may reduce the polyphenol content via
shaded and light-exposed berries (Cortell and Kennedy, 2006). Never suppressing the gene expression or accelerated degradation of poly
theless, in ‘Cabernet franc’ and ‘Chardonnay’ grapes, the interior clus phenols (Azuma et al., 2012; Zhang et al., 2015; Mori et al., 2007).
ters had lower total flavonol concentrations than the exterior clusters, Moreover, RT-qPCR result shows that VvCHI, VvF3H, flavonoid 3′ -hy
while the position of clusters in the canopy had no major impacts on the droxylase (VvF3′ H), flavonoid 3′ 5′ -hydroxylase (VvF3′ 5′ H), VvDFR,
composition of anthocyanins and flavan-3-ols (Gao et al., 2021). The leucoanthocyanidin dioxygenase (VvLDOX), anthocyanin 3′ -methyl
results indicated that the distribution of polyphenolic compounds was transferase (VvOMT), VvFLS and flavonoid 3′ ,5′ -methyltransferase
affected by sunlight conditions around grape clusters. It was previously (VvAOMT) in grapes stored at 25 ℃/dark were more expressed than 25
studied that the different distribution of polyphenols in grape cluster ℃/light, while the difference of gene expression had no obvious regu
could be attributed to the blockage of phloem elements into the berry larity between grapes stored at 4 ℃/dark or light. Previous studies
and as a consequence, different influx of solutes (sugars, e.g.) among showed that light had a dual effect on polyphenol metabolism. The
top, middle and bottom berries (Figueiredo-Gonzalez et al., 2013). It prolonged and high intensity light can cause different degrees of adverse
was also demonstrated that the chemical compounds in berries are not effects on plants (Wei et al., 2013; Interdonato et al., 2011; Savitch et al.,
only sensitive to microclimate (especially sunlight radiation), but also 2001). Azuma et al. (2012) studied the interrelationships between light
influenced by intrinsic factors. and temperature effects on flavonoid biosynthesis of grape berries in
early stages of veraison, they found that the accumulation of anthocy
3.3.4. Polyphenols and gene expression analysis in response to light and anins was dependent on both light and low temperature. Our result
temperature indicated that light had a negative effect on total polyphenols at 25 ℃,
During storage period, the phenolic acid content in grapes declined and gene expression results supported this hypothesis.
stored at 25 ℃/light, while it increased stored at 25 ℃/dark (Table 5).
The variations of phenolic acid content during the first 14 days of grapes 4. Conclusions
stored at 4 ℃/light and 4 ℃/dark were similar to those in grapes stored
at 25 ℃/light and 25 ℃/dark, respectively. However, the contents of In the present study, it was demonstrated that the higher polyphenol
phenolic acids were recovered later (Table 5). Besides, the total flavonol concentration was accumulated in seeds than that in stems, leaves and
content in grapes stored at 25 ℃ were found to be increased, whereas it skins, whereas phenolic acids, flavonols, and anthocyanins were rare or
decreased in grapes stored at 4 ℃. Polyphenols have a strong ability for absent. Polyphenol biosynthesis was significantly enhanced as berry
10
M. Qi et al. Journal of Food Composition and Analysis 106 (2022) 104353
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Writing – review & editing, Supervision, Project administration, Fund Gao, X.T., Sun, D., Wu, M.H., Li, H.Q., Liu, F.Q., He, F., Pan, Q.H., Wang, J., 2021.
ing acquisition. Influence of cluster positions in the canopy and row orientation on the flavonoid and
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Declaration of Competing Interest Ghasemzadeh, A., Nasiri, A., Jaafar, H.Z.E., Baghdadi, A., Ahmad, I., 2014. Changes in
phytochemical synthesis, chalcone synthase activity and pharmaceutical qualities of
The authors report no declarations of interest. sabah snake grass (Clinacanthus nutans L.) in Relation to Plant Age. Molecules 19
(11), 17632–17648. https://doi.org/10.3390/molecules191117632.
Gliszczynska-Swiglo, A., Chmielewski, J., 2017. Electronic nose as a tool for monitoring
Acknowledgments the authenticity of food. A review. Food Anal. Methods 10 (6), 1800–1816. https://
doi.org/10.1007/s12161-016-0739-4.
Guo, D.L., Yu, Y.H., Xi, F.F., Shi, Y.Y., Zhang, G.H., 2016. Histological and molecular
The research was funded by the National Natural Science Foundation characterization of grape early ripening bud mutant. Int. J. Genomics 2016,
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