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Received: 17 April 2022    Revised: 14 June 2022    Accepted: 18 June 2022

DOI: 10.1002/fsn3.2957

ORIGINAL RESEARCH

Effects of different iron treatments on wine grape berry quality

and peel flavonoid contents

Shu Zhang1  | Heting Chen1 | Ming Gao1 | Chaofeng Gu1 | Rui Wang1,2,3

1
College of Agronomy, Ningxia University,
Yinchuan, P.R. China Abstract
2
Ningxia Grape and Wine Research In this study, eight-­year-­old wine grape plants (Cabernet Sauvignon) were subjected to
Institute, Yinchuan, P.R. China
3
five different iron treatments: ferrous sulfate, ferric ethylenediaminetetraacetic acid
China Wine Industry Technology
Institute, Yinchuan, P.R. China (EDTA-­Fe), ferric citrate, ferric gluconate, and ferric sugar alcohol, and conventional
fertilization. Foliar spraying with clear water was used as the control treatment. The
Correspondence
Rui Wang, College of Agronomy, Ningxia effects of different iron treatments on berry quality and flavonoid accumulation in
University, Yinchuan 750021, P.R. China. grape peels were explored. All five iron treatments affected the sugar, acid, and peel
Email: [email protected]
flavonoid contents of grape berries, but the contents varied greatly among the dif-
Funding information ferent iron treatments. Foliar spraying with iron increased berry sugar content and
Ningxia Natural Science Foundation,
Grant/Award Number: 2020AAC03281; reduced acid content. In addition, foliar spraying with ferrous sulfate, EDTA-­Fe, fer-
National Key Research and Development ric gluconate, and ferric sugar alcohol reduced the total anthocyanin, flavanol, and
Project, Grant/Award Number:
2019YFD1002500 flavonol contents in the peel. The unique flavonoid monomer content of the peel was
significantly higher under ferric citrate treatment than under the control and other
iron treatments. Moreover, the results showed that foliar spraying with ferric citrate
balanced the berry sugar–­acid ratio and also increased the anthocyanin, flavanol, and
flavonol contents of the grape peel, thereby improving the overall nutritional status of
the berries and the final wine quality. The results obtained in this study demonstrate
that different iron treatments could improve grape berry quality and clarify the ef-
fects of different exogenous iron treatments.

KEYWORDS
anthocyanin, flavonoid, iron, wine grape quality

1  |  I NTRO D U C TI O N it difficult for various elements that were originally insufficient to

meet the nutritional requirements for the normal growth of grapes.
The eastern foothills of Helan Mountain in Ningxia are among the Foliar fertilization is one of the main methods used to improve
best ecological regions for wine grapes in China. However, the fertil- the berry yield and quality during grape cultivation. Foliar applica-
ization method used for wine grape cultivation is inclined to supple- tion is the most rapid and effective method for satisfying the spe-
ment traditional macronutrient fertilizers, ignoring the importance cific nutritional needs of plants (Fernandez et al., 2009). The effect
of trace elements. The mineral nutrient availability in the alkaline soil of foliar iron application on the composition of grapes is highly
in this area is low, the effective iron content is far lower than the na- dependent on the grape variety and the duration and form of iron
tional average, and the mobility of iron in plants is not strong, making used (Abadia et al., 2002; Alvarez-­Fernàndez et al., 2006; Yunta

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2022 The Authors. Food Science & Nutrition published by Wiley Periodicals LLC.

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3598    
wileyonlinelibrary.com/journal/fsn3 Food Sci Nutr. 2022;10:3598–3607.
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ZHANG et al.       3599

TA B L E 1  Chemical characteristics of the soil before the trial

et al., 2013). Iron fertilizers can be divided into three categories: in-
commenced (g kg−1)
organic, organic compound, and chelated iron fertilizers. Inorganic
iron fertilizer is inexpensive and has a fast fertilizer effect, but it is Soil depth (m) pH N P K Fe

easily oxidized, resulting in an unsustainable fertilizer effect. Ferrous 0–­0.2 8.45 5.17 2.54 7.22 16.32
sulfate is the most common fertilizer. Organic compound iron fertil- 0.2–­0.4 8.55 3.25 2.12 6.90 15.41
izers are relatively stable and easily degradable, and the most com- 0.4–­0.6 8.61 3.15 2.07 6.82 14.65
mon ones are ferric gluconate and ferric sugar alcohol. The chelated
iron fertilizers are mainly ferric ethylenediaminetetraacetic acid
(EDTA-­Fe), ethylenediamine-­N,N′-­bis(2-­hydroxyphenylacetic acid) In this study, we investigated the effects of foliar treatment with
(EDDHA-­Fe), and ferric citrate. Furthermore, studies have shown different forms of iron on berry quality and flavonoid accumulation
that the application of chelated iron can significantly increase the in the peel of Cabernet Sauvignon grapes, thereby providing a the-
soluble sugar and phenolic acid contents of grapes under alkaline oretical basis for improving wine grape cultivation in alkaline soil at
soil conditions (Karimi et al., 2019). the eastern foothills of the Helan Mountain in China.
The quality of grapes is related to the balance between primary
and secondary metabolites. Glucose and fructose are the main
sugars in berries, and the contents of these primary metabolites 2  |  M ATE R I A L S A N D M E TH O DS
are affected by variety, climate, and nutritional status, while the
accumulation of sugar in berries can improve the volatile aromatic 2.1  |  Test materials and experimental design
compound content (Ali et al., 2010; Zheng et al., 2009). Phenols are
important components that determine the quality of grape ber- The experiment was conducted from April to October, 2021 at
ries and have various functions in plants, including as antioxidants, Lilan Winery (105°58′20′′E, 38°16′38′′N), which is in a wine grape-­
protecting against ultraviolet (UV) radiation, and combating patho- producing area at the eastern foothills of the Helan Mountain in
genic infections (Tian et al., 2019). Studies have shown that iron is China. The study site was located at an altitude of 1129 m, with
related to the function of phenolic synthase; thus, iron deficiency an annual average precipitation of 190 mm and a frost-­free period
affects the synthesis of phenolic compounds via the shikimate of 180 days. Eight-­year-­old Cabernet Sauvignon grape vines were
pathway (Bavaresco et al., 2005). In addition, iron concentration used in this study. The vine shape was “厂” and the row spacing was
can affect pectin degradation and antioxidant capacity of pheno- 0.6 × 3.5  m. The basal fertilizer, comprising organic sheep manure
lic compounds (Vidot et al., 2020). Many phenolic compounds are fertilizer, was ditched in early May and applied once at 10,500 kg
found in grapes at high concentrations. These phenolic compounds hm−2 by drip irrigation. The soil type was calcareous gravel. Table 1
can be divided into flavonoids and nonflavonoids, where flavo- lists the chemical characteristics of the soil before the start of the
noids comprise flavanols, flavonols, and anthocyanins, and nonfla- experiment.
vonoids include resveratrol, benzoic acid, and cinnamic acid (Liang The experiment had a randomized block design with six treat-
et al., 2013). The expression levels of genes related to anthocyanin ments and three replicates for each treatment, with a total of 18
biosynthesis are affected by developmental and environmental cells, and each cell area was 10.5 m2. Each iron fertilizer treatment
factors, including temperature, light, sugar content, and mineral was sprayed three times (on July 12, July 27, and August 11) with an
content. Karimi et al. (2019) found that exogenous iron could electric sprayer at the grape expansion and color-­changing stages,
regulate the anthocyanin content of berries. Zheng et al. (2009) where a 5 L solution of each treatment was applied. Table 2 shows
showed that carbohydrates can promote the expression of flava- the total amounts of iron received for each treatment after the three
none 3-­hydroxylase (EC 1.14.11.9), which is a key enzyme in antho- applications. Excluding the different forms of iron fertilizer, all other
cyanin synthesis, thereby increasing berry anthocyanin content. treatments and management measures were consistent with those
Flavonols are produced by the flavonoid biosynthesis pathway and used in the vineyard. During the optimal grape harvest period, 15
mainly comprise quercetin, myricetin, kaempferol, and isorhamne- representative grapes were randomly selected from each treatment
tin (Mattivi et al., 2006). Flavan-­3-­alcohol is a basic component and transported rapidly to the laboratory. One hundred grapes were
of proanthocyanidins and condensed tannins, including catechin, immediately frozen in liquid nitrogen and ground to determine berry
epicatechin, gallocatechin, epigallocatechin, and epigallocatechin quality. For each treatment, 30 grapes were randomly selected,
gallate. Flavonoids and flavanols are mainly distributed in the washed with distilled water, peeled, frozen in liquid nitrogen, and
grape seeds, peel, and berry stems. Flavanols have important ef- stored at −80°C to determine the peel metabolites.
fects on astringency, bitterness, and structure of wine (Zimman
et al., 2002). Foliar spraying with iron can increase the anthocyanin
(Shi et al., 2017), flavonol, and flavanol (Shi et al., 2018) contents 2.2  |  Determination of grape berry quality
of grape berries. However, previous studies have not comprehen-
sively investigated the effects of different forms of iron on the Frozen grape berries were ground to determine the total soluble sol-
flavonoid content of grapes. ids (TSS), reducing sugar, and titratable acid contents (TAC). The TSS
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3600      ZHANG et al.

TA B L E 2  Iron treatments applied to grapevines

Indexes Form of iron fertilizer Solution concentration (%) Iron fertilizer application rate (kg hm−2) Iron dosage (kg hm−2)

Control –­ –­ –­
FB1 Ferrous sulfate 0.09 4.44 0.89
FB2 EDTA-­Fe 0.15 7.14 0.89
FB3 Ferric citrate 0.08 3.99 0.89
FB4 Ferric gluconate 0.16 7.76 0.89
FB5 Ferric sugar alcohol 0.19 8.93 0.89

Note: Ferrous sulfate (Fe 20.10%), EDTA-­Fe (Fe 12.50%), ferric citrate (Fe 22.40%), ferric gluconate (Fe 11.50%), and ferric sugar alcohol (Fe 100 g L−1).

content was determined using a handheld glucose meter. The reduc- alternatively connected to an ESI–­triple quadrupole linear ion trap
ing sugar content was determined using the 3,5-­dinitrosalicylic acid (QTRAP)–­MS.
method. TAC was determined by titration using standard 0.1 mol L−1 Linear ion trap (LIT) and triple quadrupole (QQQ) scans were ac-
NaOH (endpoint pH  8.2) (Jin et al.,  2016; Ma et al., 2019; Wang quired using a triple quadrupole–­linear ion trap mass spectrometer
et al., 2019). (QTRAP; AB4500 Q TRAP UPLC/MS/MS System) equipped with
an electrospray ionization (ESI) turbo ion-­
spray interface, which
was operated in positive and negative ion modes and controlled by
2.3  |  Extraction of anthocyanin and flavonoid Analyst 1.6.3 software (AB Sciex). The ESI source operation param-
compounds from peel eters were as follows: ion source, turbo spray; source temperature,
550°C; ion-­spray voltage (IS), 5500 V (positive ion mode)/−4500 V
Grape peel samples were vacuum dried and frozen for 24 h in a lyo- (negative ion mode); ion source gas I (GSI), gas II (GSII), and curtain
philizer (Scientz-­100F) and then ground (30 Hz, 1.5  min) into pow- gas (CUR) were set to 50, 60, and 25.0 psi, respectively; collision-­
der using a grinder (MM 400, Retsch). The powdered peel (100 mg) activated dissociation (CAD) was high. Instrument tuning and mass
was extracted with 70% methanol solution (1.2 ml) before mixing calibration were performed using 10 and 100 μmol L−1 polypropylene
six times in a vortex shaker for 30 s each at 30 min intervals and glycol solutions in the QQQ and LIT modes, respectively. QQQ scans
standing overnight at 4°C. The homogenate was centrifuged at were acquired as multiple reaction monitoring (MRM) experiments
12,000 rpm (revolutions per minute) for 10 min and the supernatant with collision gas (nitrogen) set in the medium. Declustering poten-
was aspirated and filtered through a microporous membrane (pore tial and collision energy (DP and CE) for individual MRM transitions
size  =  0.22 μm) for UPLC–­
MS/MS (ultrahigh performance liquid were calculated with further DP and CE optimization. A specific set
chromatography tandem spectrometry) analysis. Three independent of MRM transitions was monitored for each period according to the
extractions were performed for each treatment group. metabolites eluted within this period.

2.3.1  |  UPLC–­MS/MS conditions 2.4  |  Qualitative and quantitative analyses of

anthocyanin and flavonoid compounds
The sample extracts were analyzed using an UPLC–­
ESI–­
MS/MS
system (ultrahigh performance liquid chromatography–­electrospray The ion current intensities and retention times were compared with
ionization tandem mass spectrometry) (UPLC, SHIMADZU Nexera those of our self-­
developed “metware” database (MWDB data-
X2, www.shima​dzu.com.cn/; MS, Applied Biosystems 4500 Q TRAP, base). Qualitative and quantitative analyses of the compounds were
www.appli​edbio​syste​ms.com.cn/). The analytical conditions were as conducted according to the secondary spectrum information. The
follows: UPLC column, Agilent SB-­C18 (1.8 μm, 2.1 × 100 mm); mo- contents of different metabolites were analyzed according to the
bile phase solvent A comprising pure water with 0.1% formic acid metabolite detection multimodal diagram.
and solvent B comprising acetonitrile with 0.1% formic acid. Sample
measurements were performed with a gradient program using start-
ing conditions of 95% A/5% B. After 9 min, a linear gradient of 5% 2.5  |  Statistical analysis
A/95% B was programmed, and a composition of 5% A/95% B was
maintained for 1 min. Subsequently, the composition was adjusted Microsoft Excel 2010 and SPSS 21.0 software were used to pro-
to 95% A/5.0% B within 1.1 min and maintained for 2.9 min. The cess and analyze the data. Origin2018 was used to plot the data.
flow velocity was 0.35 ml per minute. The column oven temperature Significant differences were accepted at p < .05 (n = 5). All data are
was set to 40°C. The injection volume was 4  μl. The effluent was expressed as the mean ± standard error.
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ZHANG et al.       3601

3  |  R E S U LT S A N D D I S CU S S I O N Dp. The contents of Cy, Pt, Dp, and their derivatives in grape peel
were significantly lower under the different iron treatments than in
3.1  |  Effects of different iron treatments on the the control, except for FB3 and FB4. The contents of most antho-
physicochemical properties of grape berries cyanins were significantly higher under FB3 than under the other
treatments, except for Decoum. The different iron treatments had
Table 3 shows that the TSS and reducing sugar (RS) contents of grape significant effects on the total anthocyanin content of berry peel,
berries increased under all of the iron treatments, where the high- where the anthocyanin content was the highest under FB3, which
est TSS and RS contents were observed under FB3 (ferric citrate), was 14.20%, 32.37%, 29.06%, 16.20%, and 35.16% higher than that
which were 4.70% and 12.40% higher than those in the control, re- in the control, FB1, FB2, FB4, and FB5, respectively.
spectively. The TSS contents of grape berries did not differ signifi-
cantly among the treatments, whereas the RS contents did. The RS
contents were significantly higher under FB3 and FB5 (ferric sugar 3.3  |  Effects of different iron treatments on
alcohol) than under the control and the other iron treatments, where flavanols and flavonols in grape peel
the contents followed the order of: FB3 > FB5 > FB4 > FB2 > FB1.
Except under FB3, the TAC values were lower under the iron treat- The flavonoids detected in grape berry skin are shown in Table 5,
ments than under the control. The TAC value was the lowest under where 19 flavanols and 42 flavonols were detected. The abbrevia-
FB4 (ferric gluconate) (16.67% lower than that in the control). The tions for these compounds are listed in Table  5 (only some rep-
iron treatments had significant effects on the sugar–­acid ratio in resentative data are presented in the table). Flavanols included
grape berries. Compared with the control, the sugar–­acid ratios were catechins, epicatechins, and gallocatechins, while flavanones in-
14.63%, 8.12%, 4.47%, 20.28%, and 16.04% higher under FB1 (fer- cluded quercetin, myricetin, kaempferol, and 6-­hydroxy kaemp-
rous sulfate), FB2 (EDTA-­Fe), FB3, FB4, and FB5, respectively. The ferol derivatives. In particular, Ca, Hydro, Ga, Cid, and αCadih
iron treatments also significantly increased the 100-­berry weight were the main flavanols detected. The content of most individual
compared with the control, but the differences in the weights were flavanols was higher in grape skin under FB3 than in the control,
not significant between the different iron treatments. except for Hydro and Ga. However, the contents of Hydro and
Ga were significantly higher under FB1, FB4, and FB5 compared
with the control, where the Hydro content was the highest under
3.2  |  Effects of different iron treatments on FB1, i.e., 4.08% and 15.91% higher than those under the control
anthocyanin contents of grape peel and FB3, respectively. The Ga content was the highest under FB5,
as it was 28.39% and 42.82% higher than those under the control
The UPLC–­MS (ultrahigh performance–­mass spectromtery) analysis and FB3, respectively. The total individual flavanol contents of the
detected 22 compounds (Table  4) in the grape peel, which mainly grape peel were lower under the iron treatments than under the
comprised cyanidins (five), paeoniflorins (four), petunidins (four), control, except for FB3. The total individual flavanol content was
malvidins (five), delphinidins (three), and pelargonidin (one). The the lowest under FB2, where it was 23.12% lower than that under
abbreviations used for these compounds are presented in Table 4. the control. However, the total individual flavanol contents did
The contents of the anthocyanin monomers such as Cyacte, Dpacet, not differ significantly under FB1, FB4, and FB5, where they were
Cycoum, Mv, and Decoum were the highest in the peel. The iron 9.31%, 4.80%, and 9.31% lower, respectively, than that under the
treatments significantly increased the content of Mv and its vari- control.
ous morphological derivatives, but did not have significant ef- Different iron treatments affected flavonol content. The con-
fects on the contents of the anthocyanins such as Pn, Pndigl, and tents of 12 monomer flavonols, including Ka, Qugluco, sQuglu, My,

TA B L E 3  Effects of different iron treatments on the physicochemical properties of grape berries

Index Control FB1 FB2 FB3 FB4 FB5

TSS 26.87 ± 0.05e 27.87 ± 0.06ab 27.67 ± 0.05bc 28.07 ± 0.10a 26.93 ± 0.09d 27.47 ± 0.02c

RS 17.84 ± 0.08c 17.86 ± 0.06c 18.70 ± 0.07b 20.06 ± 0.08a 18.91 ± 0.14b 19.82 ± 0.05a
TAC 0.84 ± 0.01a 0.76 ± 0.01bc 0.80 ± 0.01ab 0.84 ± 0.01a 0.70 ± 0.02d 0.74 ± 0.01cd
TSS/TAC 31.97 ± 0.21d 36.64 ± 0.12b 34.56 ± 0.14c 33.39 ± 0.11cd 38.45 ± 0.09a 37.09 ± 0.13ab
WB 94.78 ± 0.36c 115.42 ± 1.04a 110.66 ± 0.92b 117.05 ± 1.16a 113.63 ± 1.88ab 111.48 ± 0.98b

Note: Different lowercase letters indicate significant differences between treatments, according to Tukey's HSD (honest significant difference) test
(p < .05).
Abbreviations: RS, reducing sugar (expressed as gram equivalent glucose L−1); TAC, titratable acid content (expressed as gram equivalent tartaric acid
L−1); TSS, total soluble solids content (%); WB, weight of 100 berries (g).
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3602      ZHANG et al.

rKaglu, Kaneo, * rQuglu, Qu, Quneo, rQuglu, Se, and Me, were the in grape berries under the iron treatments indicates that iron can
highest in grape peel. The contents of the two monomeric flavonol promote berry ripening, as also observed in pears (“Deveci” and
compounds, rKaglu and Kaneo, were the highest, and their levels “Santa Maria”) (Ozturk et al., 2019), table grapes (cv. “Thompson
also differed significantly among the iron treatments. The rKaglu Seedless”) (Taghavi et al., 2020), and wine grapes (Vitis vinifera cv.)
and Kaneo contents were the highest under FB3, where they were (Shi et al., 2017). Reductions in RuBisCO (ribulose-­1,5-­bisphosphate
72.41% and 70.67% higher than those of the control, respectively. carboxylase-­oxygenase) activity levels and lower chlorophyll and
The rKaglu and Kaneo contents were the lowest under FB5 (43.33% carotenoid contents in iron-­deficient plants lead to a lower leaf CO2
and 38.32% lower, respectively), compared with the control. The exchange rate and photosynthetic efficiency, which may explain
contents of other flavonol monomers also varied greatly among dif- the higher sugar content under iron treatment in the present study
ferent treatments, where the levels of zero, 10, 14, two, zero, and 16 (Chen et al., 2004). We found that the glycolic acid contents of grape
individual flavonols were the highest in FB1, FB2, FB3, FB4, FB5, and berries differed significantly among the iron treatments, while the
the control, respectively. TSS contents were also higher and the sugar contents were lower
under FB2, FB3, FB4, and FB5 than under FB1. Organic chelated iron
is a small molecule that is absorbed by the leaves when chelated by
3.4  |  Principal component analysis of grape sugar alcohols and amino acids, thereby avoiding the oxidation and
berry flavonoids precipitation of ferrous sulfate when sprayed alone (FB1), facilitating
the absorption of nutrient iron (Fernández & Ebert, 2005). In addi-
The different iron treatments had significant effects on the con- tion, sugar alcohols and amino acids are small organic molecules with
tent and proportion of sugar acids and flavonoids in grape berries. good moisture retention, permeability, and ductility characteristics;
Principal component analysis (PCA) was conducted to determine the thus, they can reduce the surface tension and improve the capac-
overall differences in flavonoids under different iron treatments. ity of leaf surfaces to absorb iron (Singh et al., 2013). Tartaric acid
Figure  1 shows that the first two PCs accounted for 42.20% and and malic acid are the main organic acids present in grape berries.
32.30% of the variance, respectively, and thus, 74.50% of the total We found that iron treatment decreased TAC, except for FB3 (fer-
variance. PC1 was mainly explained by flavanones such as Qu, Se, ric citrate), possibly because external application of iron promoted
and Pt, and PC2 was mainly explained by anthocyanins and flavanols the accumulation of sugars and accelerated berry ripening, whereas
such as My and Qu. The scoring plot in Figure  1a shows that the the malic acid content of berries gradually decreased as the berry
results obtained under the different iron treatments and the control matured (Karimi et al., 2019). Malic and citric acids are the main sub-
were clearly separated, with FB1, FB2, and FB5 in a single cluster, strates for plant respiration. The TSS and reducing sugar contents
and the control, FB3, and FB4 in three separate clusters. The loading of berries increased under FB3 (ferric citrate), whereas TAC did not
plot in Figure 1b shows that the sugar content and the contents of change compared with the control, probably because the externally
Mv, Pt, Ca, Ep, Qu, and their derivatives were well separated in the applied ferric citrate was consumed by respiration to decrease the
control and iron treatment groups, thereby indicating that the iron decomposition of malic acid; thus, TAC was higher under FB3 (fer-
treatments affected the sugar, acid, and flavonoid contents of grape ric citrate) compared with other iron treatments (Chen et al., 2004;
berries. However, FB1, FB2, and FB5 were grouped in the same clus- Schlegel et al., 2006). The weight of berries is determined by their
ter (A1), thereby indicating that the effects of these three iron treat- size and density, which are important factors that affect the quality
ments on the quality indices for grape berries and flavonoid contents of grapes. The weights of the grape berries were significantly higher
were not significantly different, and that these treatments increased under the iron treatments than under the control, possibly because
the contents of Qugal, Ga, Mymal, Mv, and their derivatives. FB4 iron increased the metabolic activity of the plants. Iron deficiency
clustered separately (A2) and TSS/TAC, WB, and the content of fla- during grape growth is known to reduce membrane integrity, leaf
vanols, such as gGoglu, increased under ferric gluconate (FB4) treat- CO2 content, exchange rate, and chlorophyll photosynthetic effi-
ment. FB3 was within the confidence interval (A3), showing that RS ciency to inhibit the accumulation of dry matter, which may explain
and almost all flavonoids in grape berries were increased under ferric why iron treatment significantly increased the weight of the berries
citrate treatment. in the present study (Bertamini & Nedunchezhian, 2005).
The types and quantities of anthocyanins detected in grape peel
in the present study were generally consistent with those previously
4  |   D I S C U S S I O N reported (Arozarena et al., 2002; Mattivi et al., 2006; Shi et al., 2017).
Anthocyanins are important pigments in red grape. The proportions
Alvarez-­Fernàndez et al., (2006) showed that iron deficiency de- and quantities of anthocyanins were determined based on the spe-
creases berry sugar content. The sugar–­
acid ratio is generally a cific variety and cultivation conditions. Studies have shown that
measure of berry ripeness. In the present study, spraying with dif- iron is an important factor affecting anthocyanin synthesis (Ahmed
ferent forms of iron improved the quality of wine grapes, where et al., 1997). In the present study, we found that spraying different
TSS increased, and sugar content and TAC decreased, thereby in- forms of iron increased the content of specific anthocyanins. In par-
creasing the sugar–­acid ratio. The increase in the sugar–­acid ratio ticular, foliar application of ferric citrate (FB3) and ferric gluconate
 ZHANG et al.

TA B L E 4  Effects of different iron treatments on contents of anthocyanins in grape peel

Flavonoids Control FB1 FB2 FB3 FB4 FB5

Cy 0.18 ± 0.02ab 0.08 ± 0.02c 0.12 ± 0.01bc 0.22 ± 0.02a 0.13 ± 0.02bc 0.09 ± 0.02c

Pl 4.15 ± 0.21b 2.93 ± 0.23c 3.19 ± 0.21bc 5.29 ± 0.48a 3.81 ± 0.61bc 2.80 ± 0.15c
Pn 3.28 ± 0.21b 3.02 ± 0.18b 3.35 ± 0.20b 4.80 ± 0.14a 3.67 ± 0.43b 3.03 ± 0.15b
Cygala 2.01 ± 0.06b 1.15 ± 0.06c 1.15 ± 0.08c 3.03 ± 0.20a 1.76 ± 0.33b 1.10 ± 0.05c
Cygluc 1.66 ± 0.03b 0.99 ± 0.06cd 0.89 ± 0.05d 2.65 ± 0.22a 1.41 ± 0.24bc 0.85 ± 0.08d
Pngluc 5.18 ± 0.12b 3.91 ± 0.22c 4.17 ± 0.33bc 6.74 ± 0.29a 4.49 ± 0.67bc 3.80 ± 0.21c
Mv 25.33 ± 0.47d 34.13 ± 0.55ab 36.50 ± 1.48a 32.00 ± 1.06bc 30.07 ± 0.66c 31.57 ± 1.30bc
Pt 8.37 ± 0.10ab 7.51 ± 0.27bc 7.16 ± 0.12c 8.66 ± 0.38a 7.58 ± 0.26bc 6.15 ± 0.40d
Cyacet 93.13 ± 3.37a 53.77 ± 2.49b 59.60 ± 5.37b 103.7 ± 4.23a 87.20 ± 13.06a 53.20 ± 4.33b
Pncaff 7.93 ± 0.50a 6.07 ± 0.10c 6.78 ± 0.49abc 8.11 ± 0.42a 7.69 ± 0.26ab 6.29 ± 0.81bc
Dpacet 47.70 ± 1.87a 37.63 ± 3.21b 35.07 ± 1.43b 51.10 ± 2.21a 48.20 ± 1.71a 37.27 ± 1.79b
Ptacet 12.93 ± 0.27a 10.83 ± 0.24bc 11.10 ± 0.47abc 12.77 ± 0.66ab 12.33 ± 0.83ab 9.27 ± 0.77c
Mvacet 11.77 ± 0.74b 13.6 ± 0.38a 13.80 ± 0.42a 12.40 ± 0.35ab 13.03 ± 0.15ab 13.43 ± 0.72ab
Mvmalo 1.80 ± 0.13c 2.42 ± 0.06ab 2.76 ± 0.15a 1.96 ± 0.16bc 2.38 ± 0.14ab 2.04 ± 0.17bc
Cycoum 30.83 ± 1.45b 20.3 ± 1.37c 20.37 ± 1.13c 56.83 ± 2.89a 27.03 ± 3.09b 19.10 ± 1.31c
Decoum 23.5 ± 1.29a 15.40 ± 1.06b 14.4 ± 0.15b 21.27 ± 1.57a 15.83 ± 0.47b 16.37 ± 0.23b
Ptarab 0.15 ± 0.02c 0.18 ± 0.01bc 0.19 ± 0.01abc 0.19 ± 0.01abc 0.24 ± 0.03a 0.22 ± 0.01ab
Ptcoum 20.70 ± 0.75b 17.23 ± 0.43c 17.60 ± 0.20c 25.07 ± 1.12a 21.50 ± 1.51b 16.90 ± 0.25c
Pndigl 2.87 ± 0.11a 2.05 ± 0.03a 2.18 ± 0.23a 2.71 ± 0.20a 2.82 ± 0.61a 2.26 ± 0.21a
Dp 18.03 ± 0.29ab 17.77 ± 0.54ab 22.10 ± 2.52a 16.07 ± 0.17b 20.8 ± 0.93a 15.00 ± 1.80b
cMvcoum 3.35 ± 0.09b 3.35 ± 0.03b 3.14 ± 0.11b 3.16 ± 0.14b 4.05 ± 0.25a 3.33 ± 0.10b
Mvdi 1.77 ± 0.18c 2.97 ± 0.23b 4.2 ± 0.17a 1.88 ± 0.27c 2.99 ± 0.18b 2.61 ± 0.28b
Total anthocyanins 326.45 ± 4.13b 257.33 ± 5.92c 269.92 ± 7.25c 380.50 ± 10.69a 318.87 ± 19.88b 246.71 ± 11.65c

Note: Different lowercase letters indicate significant differences between treatments, according to Tukey's HSD (honest significant difference) test (p < .05).
Abbreviations: Cy, cyanidin; Pl, pelargonidin-­3-­O-­glucoside; Pn, peonidin-­3-­O-­arabinoside; Cygala, cyanidin-­3-­O-­galactoside*; Cygluc, cyanidin-­3-­O-­glucoside (kuromanin)*; Pngluc, peonidin-­3-­O-­glucoside;
Mv, malvidin-­3-­O-­arabinoside; Pt, petunidin-­3-­O-­glucoside; Cyacet, cyanidin-­3-­O-­(6′′-­O-­acetyl)glucoside; Pncaff, peonidin-­3-­O-­(6′′-­O-­acetyl)glucoside; Dpacet, delphinidin-­3-­O-­(6′′-­O-­acetyl)glucoside;
Ptacet, petunidin-­3-­O-­(6′′-­O-­acetyl)glucoside; Mvacet, malvidin-­3-­O-­(6′′-­O-­acetyl)glucoside; Mvmalo, malvidin-­3-­O-­(6′′-­O-­malonyl)glucoside; Cycoum, cyanidin-­3-­O-­(6′′-­O-­p-­coumaroyl)glucoside;
Decoum, delphinidin-­3-­O-­(6′′-­O-­p-­coumaroyl)glucoside; Ptarab, petunidin-­3-­O-­glucoside-­5-­O-­arabinoside; Ptcoum, petunidin-­3-­O-­(6′′-­O-­p-­Coumaroyl)glucoside; Pndigl, peonidin-­3,5-­O-­diglucoside; Dp,
delphinidin-­3,5-­di-­O-­glucoside; cMvcoum, malvidin-­3-­O-­(6′′-­O-­p-­coumaroyl)glucoside; Mvdi, malvidin-­3,5-­di-­O-­glucoside (malvin).
|       3603

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 | 3604     

TA B L E 5  Effects of different iron treatments on the flavanol and flavonol contents of grape peel

Flavonoid Control FB1 FB2 FB3 FB4 FB5

Ca 3.73 ± 0.11b 3.11 ± 0.16c 2.58 ± 0.13d 4.84 ± 0.10a 2.98 ± 0.07cd 3.36 ± 0.19bc

Hydro 2.45 ± 0.08ab 2.55 ± 0.21a 2.53 ± 0.06a 2.20 ± 0.03c 2.36 ± 0.08b 2.33 ± 0.10b
Ga 4.65 ± 0.15cd 5.42 ± 0.10b 4.73 ± 0.13c 4.18 ± 0.02d 5.09 ± 0.32bc 5.97 ± 0.07a
Cid 7.31 ± 0.62b 5.87 ± 0.50bc 4.30 ± 0.20d 9.46 ± 0.47a 7.00 ± 0.69b 5.14 ± 0.23cd
αCadih 5.87 ± 0.21b 4.28 ± 0.03c 3.24 ± 0.06d 7.16 ± 0.41a 5.05 ± 0.49bc 4.20 ± 0.13c
Total Flavan-­3-­ols 33.30 ± 1.04b 30.20 ± 0.68b 25.60 ± 0.42c 38.76 ± 1.04a 31.70 ± 1.65b 30.20 ± 0.82b
Ka 18.77 ± 0.87a 17.5 ± 1.56a 17.23 ± 0.74a 16.43 ± 1.69ab 12.05 ± 2.53b 17.13 ± 0.03a
Qugluco 16.3 ± 0.00ab 16.53 ± 1.21a 17.23 ± 0.67a 17.13 ± 0.87a 13.60 ± 1.11b 15.57 ± 0.56ab
sQuglu 20.63 ± 0.45a 19.33 ± 0.58ab 20.97 ± 1.14a 20.00 ± 0.90ab 16.43 ± 2.02b 18.40 ± 1.31ab
My 17.5 ± 0.53b 19.77 ± 0.79ab 21.97 ± 1.42a 19.73 ± 1.52ab 17.73 ± 0.65b 17.30 ± 0.66b
rKaglu 42.3 ± 0.60b 25.63 ± 0.72d 26.10 ± 1.72d 72.93 ± 3.29a 32.30 ± 2.86c 23.97 ± 1.09d
Kaneo 40.37 ± 2.08b 25.27 ± 1.17c 25.27 ± 2.29c 68.9 ± 6.29a 34.53 ± 4.63bc 24.9 ± 0.70c
*rQuglu 25.57 ± 1.25a 16.53 ± 1.05c 16.20 ± 0.55c 22.43 ± 0.98b 16.47 ± 0.24c 18.60 ± 0.55c
Qu 24.57 ± 1.33a 16.00 ± 0.79c 16.33 ± 0.37c 21.43 ± 0.98b 16.50 ± 0.38c 17.57 ± 0.24c
Quneo 21.90 ± 0.83a 14.70 ± 1.10b 15.53 ± 0.22b 21.37 ± 0.59a 15.33 ± 0.50b 16.63 ± 0.77b
rQuglu 25.57 ± 0.76a 16.67 ± 1.09c 16.67 ± 0.79c 21.67 ± 1.22b 16.50 ± 0.56c 17.80 ± 0.55c
Se 19.53 ± 0.83b 16.3 ± 0.67c 15.30 ± 0.93c 24.50 ± 1.18a 21.83 ± 1.12ab 16.30 ± 0.79c
Me 15.40 ± 1.21bc 13.37 ± 0.52c 13.43 ± 0.12c 23.57 ± 1.04a 18.03 ± 1.26b 13.17 ± 0.71c
Total flavonoids 439.41 ± 8.19b 349.16 ± 13.68c 370.82 ± 8.02c 491.88 ± 18.92a 345.96 ± 17.98c 351.03 ± 5.32c

Note: Different lowercase letters indicate significant differences between treatments, according to Tukey's HSD (honest significant difference) test (p < .05).
Ca, catechin*; Hydro, 4′-­hydroxy-­5,7-­dimethoxyflavanone; Ga, gallocatechin*; Cid, cinchonain Id; αCadih, catechin-­(7,8-­bc)-­4 α-­(3,4-­dihydroxyphenyl)-­dihydro-­2-­(3H)-­one. Ka, kaempferol-­7-­O-­glucoside*;
Qugluco, quercetin-­7-­O-­glucoside*; sQuglu, quercetin-­4′-­O-­glucoside (Spiraeoside)*; My, myricetin-­3-­O-­glucuronide; rKaglu, kaempferol-­3-­O-­glucoside-­7-­O-­rhamnoside; Kaneo, kaempferol-­3-­O-­
neohesperidoside; *rQuglu, quercetin-­3-­O-­glucoside-­7-­O-­rhamnoside; Qu, quercetin-­7-­O-­rutinoside; Quneo, quercetin-­3-­O-­neohesperidoside; rQuglu, quercetin-­3-­O-­(4′′-­O-­glucosyl)rhamnoside; Se,
sexangularetin-­3-­O-­glucoside-­7-­O-­rhamnoside; Me, 6-­C-­methylquercetin-­3-­O-­rutinoside.
ZHANG et al.

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ZHANG et al.       3605

F I G U R E 1  Principal component analysis (PCA) results obtained based on the correlation matrix for the physical and For Review Only
chemical indexes and flavonoid components of grapes: (a) scoring plot and (b) loading plot. The abbreviations used in (b) are defined in
Tables 3, 4, and 5

(FB4) significantly increased the contents of some individual antho- EDTA-­Fe (FB2), ferric gluconate (FB4), and ferric glycol (FB5) compared
cyanins and the total anthocyanins in the grape peel, probably be- with the control, and the total flavanol content was higher when treated
cause glucose, fructose, and sucrose can induce the accumulation of with ferric citrate (FB3). Thus, the foliar application of iron affected the
anthocyanin in grape berries (Zheng et al., 2009). Indeed, the sugar flavanol content of grape skins. However, there were differences in the
content of grape berries increased significantly under these two results of the different treatments, which may be due to two reasons.
treatments, thereby promoting anthocyanin synthesis in grape peel. First, Fe2+ is the most important factor affecting flavanol synthesis
However, we also found that under treatment with ferrous sulfate (Perron & Brumaghim, 2009; Zeng et al., 2019). Ferrous sulfate is easily
(FB1), EDTA-­Fe (FB2), and ferric sugar alcohol (FB5), the levels of oxidized to ineffective iron in the air, and the organic compound iron
some individual anthocyanins (Cyacet, Dpacet, and Cycoum) were is not as stable as the chelated iron. In the process of iron ions being
lower than those in the control, resulting in the total anthocyanin absorbed by plants through osmosis, chelated iron will not dissolve on
content being lower than that in the control as well. In contrast, pre- the surface of the cuticle, and the chelate will reduce the permeability
vious studies found that anthocyanin content increased under iron of calcium ions in the cuticle by a factor of 7; thus, iron is more easily
treatment (Ahmed et al., 1997; Singh et al., 2013), where different absorbed by plants. Second, the absorption and utilization of iron by
iron treatments significantly increased the content of Mv and its plants depend on substances such as siderophores and alkyl gluco-
morphological derivatives. Cy and Dp are considered the precursors sides in surfactants. Ferric citrate surfactants and other compounds
of Pn, Mv, and Pt (He et al., 2010), respectively. Iron treatment led can significantly improve the efficiency of foliar fertilizers. Flavonoids
to an increase in the contents of Mv and its morphological deriva- are present in most higher plants and are products of flavonoid biosyn-
tives, which may explain the decrease in the contents of Cy and Dp. thesis, while flavonols are closely related to anthocyanin biosynthesis
Anthocyanins that contain more methoxy groups in the B ring may (Gonzalez-­Manzano et al., 2009; Jaakola, 2013; Mattivi et al., 2006).
contribute to the redness of grapes. Methylated anthocyanins, in- We found that the different iron treatments had significantly differ-
cluding Pn, Mv, and their derivatives, are relatively stable and are the ent effects on the contents of specific flavonols in a manner similar
main anthocyanins in mature grape berries (He et al., 2012). Thus, to the changes in the anthocyanin content, possibly because the en-
anthocyanins, such as Pn and Mv, have very important effects on zymes involved in the production of flavonols overlap greatly with
wine grapes (De Gaulejac et al., 2001). Therefore, iron is important those involved in the production of anthocyanins (Gonzalez-­Manzano
for improving grape berry quality. et al., 2009). In addition, these classes of compounds share the same
Flavanols and flavonols are subclasses of flavonoids. The types and skeleton and differ only in the oxidation state of the central pyran
quantities of flavanols and flavonols detected in grape peel in the pres- ring (Jaakola,  2013). Alvarez-­Fernandez et al. (2011) found that iron
ent study were generally consistent with those reported by Mattivi treatment can improve the photosynthetic efficiency of grape vines
et al. (2006). Grape peel is the main site of flavonoid synthesis and the and affect the synthesis of phenolic compounds or other secondary
main source of flavonoids in wine (Gonzalez-­Manzano et al., 2009). In metabolites using precursors. However, further research is required to
this study, we found that the Hydro and Ga contents of grape skins understand why different forms of iron can have different effects on
were higher when the leaves were sprayed with ferrous sulfate (FB1), the phenolic compound content in grape peel.
 |

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3606      ZHANG et al.

Bavaresco, L., Civardi, S., Pezzutto, S., Vezzulli, S., & Ferrari, F. (2005).
5 | CONCLUSION Grape production, technological parameters, and stilbenic com-
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iological responses to iron deficiency. Journal of Plant Nutrition, 28,
affected the fructose, acid, and flavonoid contents of Cabernet
737–­749.
Sauvignon grapes, and that the various iron treatments also had dif-
Chen, L. S., Smith, B. R., & Cheng, L. L. (2004). CO2 assimilation, photo-
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ferrous sulfate, EDTA-­Fe, ferric gluconate, and ferric sugar alcohol Horticultural Science, 129, 738–­744.
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Anthocyanin in grape skins during maturation of Vitis vinifera L.
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This study was supported by the National Key Research and
He, F., Liang, N. N., Mu, L., Pan, Q. H., Wang, J., Reeves, M. J., & Duan,
Development Project (2019YFD1002500) and Ningxia Natural C. Q. (2012). Anthocyanins and their variation in red wines I.
Science Foundation (2020AAC03281). We thank our colleagues for Monomeric anthocyanins and their color expression. Molecules, 17,
their comments on this paper, and the journal's editors and anony- 1571–­1601.
He, F., Mu, L., Yan, G. L., Liang, N. N., Pan, Q. H., Wang, J., Reeves, M. J.,
mous reviewers for their critical reviews and comments regarding
& Duan, C. Q. (2010). Biosynthesis of anthocyanins and their regu-
this manuscript.
lation in colored grapes. Molecules, 15, 9057–­9091.
Jaakola, L. (2013). New insights into the regulation of anthocyanin bio-
DATA AVA I L A B I L I T Y S TAT E M E N T synthesis in fruits. Trends in Plant Science, 18, 477–­483.
The data that support the findings of this study are available from Jin, Z., Sun, H., Sun, T., Wang, Q., & Yao, Y. (2016). Modifications of ‘gold
finger’ grape berry quality as affected by the different rootstocks.
the corresponding author upon reasonable request.
Journal of Agricultural and Food Chemistry, 64, 4189–­4197.
Karimi, R., Koulivand, M., & Ollat, N. (2019). Soluble sugars, phenolic
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Shu Zhang  https://orcid.org/0000-0003-3267-5881 and nitrogen. Acta Physiologiae Plantarum, 41, 117.
Liang, N.-­N., Pan, Q.-­H., He, F., Wang, J., Reeves, M. J., & Duan, C.-­Q.
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