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Journal of Taibah University for Science
ISSN: 1658-3655 (Online) Journal homepage: www.tandfonline.com/journals/tusc20
Effects of plasma-activated water treatment on
seed germination and growth of mung bean
sprouts
Liumin Fan, Xiufang Liu, Yunfang Ma & Qisen Xiang
To cite this article: Liumin Fan, Xiufang Liu, Yunfang Ma & Qisen Xiang (2020) Effects of
plasma-activated water treatment on seed germination and growth of mung bean sprouts,
Journal of Taibah University for Science, 14:1, 823-830, DOI: 10.1080/16583655.2020.1778326
To link to this article: https://doi.org/10.1080/16583655.2020.1778326
© 2020 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 12 Jun 2020.
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JOURNAL OF TAIBAH UNIVERSITY FOR SCIENCE
2020, VOL. 14, NO. 1, 823–830
https://doi.org/10.1080/16583655.2020.1778326
Effects of plasma-activated water treatment on seed germination and growth
of mung bean sprouts
Liumin Fan , Xiufang Liu , Yunfang Ma and Qisen Xiang
College of Food and Biological Engineering, Zhengzhou University of Light Industry, Zhengzhou, PR People’s Republic of China
ABSTRACT ARTICLE HISTORY
The present work aimed to investigate the effect of plasma-activated water (PAW) on seed germi- Received 19 March 2020
nation and seedling growth of mung bean sprouts. Distilled water was exposed to non-thermal Revised 11 May 2020
plasma for 15, 30, 60, and 90 s to prepare PAW, which was defined as PAW15, PAW30, PAW60, and Accepted 21 May 2020
PAW90, respectively. The germination rate, growth characteristics, total phenolic and flavonoid KEYWORDS
contents were all maximized when mung bean seeds were treated by PAW15, then followed Plasma-activated water;
by a decline over the prolonged plasma activation time (30–90 s). PAW15 caused no remark- mung bean; germination;
ably changes in the antioxidant capacity of sprouts as compared to DW (p > 0.05). However, the phytochemical; antioxidant
antioxidant activity of sprouts prepared with PAW30, PAW60, and PAW90 were decreased signif-
icantly (p < 0.05) compared with that of sprouts soaked in distilled water. In summary, PAW may
be used to improve the production of sprouts, but the process parameters should be optimized
for each application.
1. Introduction
Over the past decade, plasma-activated water (PAW)
Mung bean sprouts are widely consumed as one of has shown promising applications at various stages of
the most popular vegetables for their greater health the food supply chain, such as inactivation of microor-
benefits and fewer calories. In decade years, numbers ganisms [5,6], preservation of fruits [7], vegetables [8],
of physical, chemical, and combination intervention and seafood products [9] with less adverse effects on
strategies have been implemented to stimulate seeds the quality characteristics of food products. Recently,
germination and production of bean sprouts [1,2], such the application of PAW has been extended to agricul-
as gamma irradiation, ultrasound, X-irradiation, elec- ture, especially for regulating seeds germination and
tromagnetic field, cold plasma, electrolyzed oxidizing plant growth. It has been reported that the germina-
water, and pesticides [3,4]. However, these technologies tion rate of PAW-treated rye seeds was increased when
are associated with multiple serious adverse effects, compared to the untreated samples [10]. Similar find-
such as high cost, time consuming, leaving chemical ings were also observed in PAW treated-soybean seeds
residues to environment, and raising ecological issues. [1]. However, a decrease in germination rate of PAW-
Therefore, it is still necessary to develop cost-efficient watered lentil seeds was observed by Zhang et al. [5].
and environment-friendly technologies to improve the Nowadays, limited research has been conducted
production of sprouts. on the effects of PAW on germination and growth
CONTACT Qisen Xiang xiangqisen2006@163.com College of Food and Biological Engineering, Zhengzhou University of Light Industry, NO.136,
Kexue Road, Zhengzhou 450001, People’s Republic of China
© 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original work is properly cited.Page 3
824 L. FAN ET AL.
characteristics of mung bean seeds, especially the phy- incubated for 5 days, keeping away from illumina-
tochemicals and bioactivities of sprouts. Therefore, the tion at 25 °C and 85% relative humidity. The seeds
purpose of this study was to examine the effects of PAW were watered daily with distilled water, PAW15, PAW30,
on seed germination, seedling growth, phytochemical PAW60, and PAW90 (100 mL × 3 times) until the har-
components, and antioxidant capacity of mung beans vesting [14].
sprouts. In addition, the main physical and chemical
properties of PAW were also evaluated to explain the 2.5. Determination of water uptake and
underlying mechanisms of PAW. germinability of mung bean seeds
Water uptake of seeds was determined by measuring
2. Materials and methods
the weight of mung bean seeds (approximately 20 g)
2.1. Materials and chemicals before and after the soaking in distilled water or PAW.
At fixed intervals of 0, 2, 4, 6, 8, and 10 h, the seeds were
Mung bean seeds (Zhonglv 5) were provided by the
taken out, dried with absorbent paper, and weighted.
Institute of Crop Sciences, Chinese Academy of Agricul-
The water absorption rate (Wa ) of mung bean seeds in
tural Sciences (Beijing, China). Folin-Ciocalteu’s phenol
each group was calculated according to the following
reagent, ferrous ammonium sulfate, xylenol orange, 2,2-
formula:
dipheny l-1-picrylhydrazyl (DPPH•), potassium sulphate,
W1 − W0
2,4,6-tris(2-pyridyl)-1,3,5-triazine (TPTZ), Trolox, gallic Wa (%) = × 100% (1)
W0
acid, 2,2? -azinobis (3-ethylbenzothiazoline-6-sulfonic
Where W0 is the initial weight of seeds; W1 is the final
acid) diammonium salt (ABTS), and rutin were pur-
weight of seeds after absorbing water at fixed intervals
chased from Aladdin Industrial Co. (Shanghai, China).
of time [1].
Germination percentage of mung bean seeds were
2.2. Preparetion of PAW measured after being placed in seedling trays with
The atmospheric pressure plasma jet (APPJ) device distilled water or PAW for 12, 15, 18, 21, and 24 h, respec-
was used to prepare PAW [11]. The plasma genera- tively. The emergence of radicle elongated to 2 mm
tor was energized by a high-frequency high-voltage from the seed coat was taken as the criteria for germi-
power supply (5 kV, 40 kHz). The distance between the nation [15]. Germination rates of mung bean seeds were
atmospheric-pressure plasma jet nozzle and the water calculated as following:
surface was 5 mm and the plasma discharge power was N1
Germination rate(%) = × 100% (2)
set at 750 W. Approximately 200 mL of distilled water N0
was exposed to plasma for 15, 30, 60, and 90 s to prepare Where N0 is the total number of seeds in each group and
PAW, which was referred to as PAW15, PAW30, PAW60, N1 is the number of germinated seeds.
and PAW90, respectively.
2.6. Growth characteristics of mung bean seeds
2.3. Measurements of properties of PAW
The stem and root length of mung bean sprouts were
The pH and electric conductivity of PAW were measured measured with a graded ruler after sowing for 5 days
with a pHS-3C digital pH metre and a DDS-307A elec- [16]. The final results were expressed as the average
trical conductivity metre (INESA Scientific Instrument length and weight of mung bean sprouts in each group.
Co., Ltd., Shanghai, China), respectively. ORP was deter- Meanwhile, the weight of sprouts was also determined.
mined by using a 501 rechargeable ORP composite elec-
trode (INESA Scientific Instrument Co., Ltd, Shanghai, 2.7. Preparation of extract
China) connected to a dual channel pH metre. The lev-
els of H2 O2 and NO2 − in PAW were measured according The extract of mung bean sprouts were prepared by the
to the method described in the previous study [6]. The reported method [17]. In brief, freeze-dried mung bean
contents of NO3 − in PAW were measured according to sprouts were prepared and grinded into powder. The
the method reported by Shen et al. [12]. acetone/water/acetic acid mixture (70: 29.5: 0.5, v/v/v)
was selected as the extraction solvent. The ground
sprouts samples (1.0 g) were extracted with 10.0 mL of
2.4. Production of mung bean sprouts
extraction solvent at room temperature for 3 h with con-
Mung bean seeds (approximately 20 g) of similar size tinuous shaking at 150 rpm. After centrifugation at 6800
and shape were soaked in 100 mL of distilled water, × g for 15 min at 25 °C, the supernatant was stored
PAW15, PAW30, PAW60, and PAW90 for 6 h at ambi- and the residues were re-extracted. The obtained super-
ent temperature, respectively [13]. Then, the hydrated natants were combined and made up to 9.0 mL with
seeds were placed in seedling trays filled with wet fil- the fresh extracting solvent. All extracts were stored in
ter paper (20.5 cm × 13.5 cm) and all seedlings were a refrigerator at 4 °C until analysis.Page 4
JOURNAL OF TAIBAH UNIVERSITY FOR SCIENCE 825
2.8. Measurement of total phenolic and flavonoid studies [23], which may be related to the formation of
contents nitrous acid, nitric acid, and peroxynitrous acid inside
liquid water during plasma activation. ORP refers to
Total phenolic contents in extracts of mung bean
the ability of solution to gain or lose electrons. Accord-
sprouts were measured using the Folin–Ciocalteu assay
ing to Figure 1E, the ORP of PAW samples remarkably
[11] and the results were expressed as gallic acid equiv-
increased over plasma discharge time from 15 s to 90 s.
alent (GAE) in milligrams per gram of dry weight (DW) of
A similar increase in ORP of PAW was also reported by
mung bean sprouts (mg GAE/g DW). The total flavonoid
Ma et al. [24]. Additionally, as a measure of the ability
content was estimated by aluminium chloride (AlCl3 )
of water to pass an electrical current, electric conductiv-
colorimetric method and the results were shown as mg
ity has been widely used to estimate the level of active
rutin equivalent (RE) per gram dry weight (mg RE/g
ions in PAW [20]. From Figure 1F, the electric conduc-
DW) [18].
tivity of PAW samples significantly increased as a func-
tion of plasma activation time (p < 0.05) and soared to
2.9. Analysis of antioxidant properties of mung 677.67 µS/cm at 90 s, indicating the formation of active
bean sprouts extracts ions in PAW.
The antioxidant capacity of mung bean sprouts extracts
was measured by ABTS•+ and DPPH• assays [11]. The 3.2. Influences of PAW on water uptake of mung
results were expressed as milligrams trolox equiva- bean seeds
lent per gram dry weight (mg Trolox/g DW). The
Water uptake is an essential step for the initiation of
ferric reducing antioxidant power (FRAP) of mung
seed germination, leading to swelling and softening
bean sprouts extracts was estimated according to the
seed coat or testa [25]. As displayed in Figure 2, PAW sig-
method previously reported by Benzie and Strain [19]
nificantly increased the water absorption rate of mung
and the results were expressed as mg FeSO4 /g DW.
bean seeds with the prolonged discharge time. After
being soaked for 10 h, the water absorption rate of
2.10. Statistical analysis PAW90-soaked seeds reached to 74.26 ± 5.94%, which
was significantly (p < 0.05) higher than that of dis-
The data were expressed as mean ± standard deviation
tilled water-treated seeds (65.70 ± 5.79%). In another
(SD). All statistical analyses were performed with SPSS
study, a sharply changed structure was observed on
for Windows (version 21.0, IBM, Chicago, IL, USA). Sta-
the surface of PAW-treated seeds by scanning elec-
tistical significance between multiple groups was eval-
tron micrograph [26]. The author speculated that the
uated by one-way analysis of variance (ANOVA) with
high concentration of RONS produced in PAW might
the least significant difference (LSD) test at p < 0.05.
be responsible for the chapping of seed coat, and fur-
Correlations among the total phenolic content, total
ther could facilitate seed to absorb more water and
flavonoid content, and antioxidant activity were evalu-
nutrients.
ated by Pearson’s correlation analysis.
3.3. Influences of PAW on germination rate of
3. Results and discussion
mung bean seeds
3.1. Physicochemical characteristics of PAW
The effects of PAW treatment on seed germination are
During plasma treatment, reactive oxygen and nitrogen presented in Figure 3. When the seeds were treated
species (RONS) are generated in PAW, such as •OH, O2 •− , by PAW15 for 30 h, the germination rate increased to
1 O , O , H O , NO − , and NO − [20]. In agreement with 93.01 ± 2.59%, which was higher than 84.41 ± 8.62% of
2 3 2 2 2 3
previous studies, a clear formation of NO2 − , NO3 − , and distilled water-treated seeds (p < 0.05). However, PAW
H2 O2 was observed in PAW (Figure 1A, 1B, and 1C). After prepared with longer discharge time (30–90 s) signifi-
being activated by plasma for 90 s, the concentration of cantly inhibited germination of mung bean seeds. At
NO2 − , NO3 − , and H2 O2 in PAW increased almost linearly the same incubation time of 30 h, the germination rate
to 62.05, 118.39, and 0.90 mg/L (p < 0.05), respectively. of mung bean seeds watered by PAW30, PAW60, and
These long-lived reactive species are supposed to play PAW90 decreased by 0.29%, 3.47%, and 6.07%, respec-
significant roles in the regulation of seed dormancy and tively, when compared with that of PAW15-treated sam-
germination [21,22]. ples. In other studies, inconsistent results were found
Moreover, as noticed in Figure 1D, the pH value of for the effects of PAW treatment on germination rates
PAW significantly decreased with the increasing dis- of agricultural seeds, such as the increased effect [10],
charge time. After being activated by plasma for 15 s, the inhibition [5], and also no significant change [1].
the pH value drastically reduced to 3.38 compared As shown in Figure 1, the reactive species in PAW,
with 6.30 of distilled water. Water acidification dur- such as H2 O2 , NO2 − , and NO3 − was clearly observed
ing plasma discharge have been reported in previous and lasting increased over the plasma discharge time.Page 5
826 L. FAN ET AL.
Figure 1. Physicochemical characteristics of PAW. The values of (A) NO2 − , (B) NO3 − , (C) H2 O2 , (D) pH, (E) ORP, and (F) electric con-
ductivity of PAW were measured as described in the Materials and methods section. Different letters indicate significant differences
between groups (p < 0.05).
Generally, reactive species are recognized as playing
crucial roles in seed physiology, depending on the
dynamic equilibrium between their generation and
metabolism [21, 22]. At low concentration, reactive
species may act as positive signal molecules to alle-
viate seed dormancy and stimulate seed germination
by involving in abscisic acid/gibberellic acid signalling
pathways and so on [27]. However, the excessive accu-
mulation of reactive species can lead to toxic effects to
Figure 2. Water absorption rate of mung bean seeds watered seeds [27]. Nowadays, due to the different conditions
by distilled water or PAW for the indicated soaking time. of each experiment such as discharge mode, feed gas,Page 6
JOURNAL OF TAIBAH UNIVERSITY FOR SCIENCE 827
with longer discharge time ( > 15 s) had significant neg-
ative effect on seedling growth. The stem length, root
length and average weight of PAW90-watered sprouts
were significantly decreased by 14.73%, 32.83%, and
10.46% (p < 0.05), respectively, as compared with
those of distilled water-treated sprouts. Similar results
have been reported by Porto et al. [1]. In this study,
PAW prepared with plasma for 1 min achieved more
efficient in average stem length than that of 5 min.
Figure 3. Average germination rate of mung bean seeds The authors revealed that the negative effect might
watered by distilled water or PAW during the indicated incuba- be attributed to the more acidity of the latter than
tion time. former, affecting the beneficial microorganism, which
could degrade organic matter and transfer nutrients for
and solution types, the chemical compositions of PAW plant [1]. In another research, Sivachandiran & Khacef
are quite different [28]. So, the various types and con- explored the influences of cold plasma and PAW on ger-
centration of reactive species are possibly the main rea- mination and growth of three types of seeds: tomato,
sons for the inconsistent results in seeds responding to radish, and sweet pepper [23]. They observed that
PAW treatment, while the exact mechanisms are not the average stem length of tomato seeds treated by
completely understood. Further work is still needed to PAW was shorter than that of control group, while
clearly illuminate the role of each reactive species in contrary to the results in radish. In summary, there
PAW on the germination of seeds and the underlying was great difference in the effects of PAW on vari-
molecular mechanisms. ous seeds. Hence, the plasma discharge time and PAW
treatment time should be optimized for each type
of seeds.
3.4. Effect of PAW treatment on seedling growth
The growth characteristics of mung bean sprouts grown
3.5. Changes in total phenolic and flavonoid
after 5 days, such as stem length, root length, and
contents
weight, are recorded in Figure 4. It was observed that
the sprouts prepared with PAW15 showed significantly Phenolic and flavonoid compounds are the major
increase in stem length and average weight by 8.09% bioactive compounds in mung bean sprouts, which
and 12.75%, respectively, compared to distilled water- offer many promising health benefits [29]. As shown
treated samples (p < 0.05). However, PAW prepared in Figure 5, the changes in the total phenolic and
Figure 4. Effects of PAW treatment on the growth characteristics of mung bean sprouts. (A) Schematic diagram of mung bean sprout,
(B) stem length, (C) root length, (D) weight of mung bean sprouts after sowing for 5 days. Different letters indicate statistically
significant differences between groups (p < 0.05).Page 7
828 L. FAN ET AL.
Figure 5. The content of total phenolic (A) and total flavonoid (B) over the plasma discharge time. Different letters indicate significant
differences between groups (p < 0.05).
flavonoid contents were very similar with the ten- 3.6. Changes in antioxidant activity of mung bean
dency in seed germination and growth. After sow- sprouts
ing for 5 days, the total phenolic and flavonoid con-
The influences of PAW on the antioxidant capacity of
tents of PAW15-watered samples remarkably increased
mung bean sprouts extract was also investigated in
by 3.53% and 2.22% (p < 0.05), respectively, com-
the present work. According to Table 1, the PAW15
pared with that of control group. However, when the
treatment didn’t lead to remarkably changes in the
plasma exposure time prolonged to 90 s (PAW90), the
in vitro antioxidant potential of mung bean sprouts
contents of total phenolic and flavonoid were signif-
as compared to distilled water (p > 0.05). In addi-
icantly reduced to 3.68 mg GAE/g DW and 1.72 mg
tion, the three different analysis methods resulted in
RE/g DW, respectively, which were lower than that of
a consistent foundation that the antioxidant capacity
the sprouts produced with distilled water (p < 0.05).
of mung bean sprouts extract decreased with plasma
Mildaziene et al. found a substantial increase in phe-
exposure durations range of 15–90 s (p > 0.05). For
nolic acids (cichoric acid, caftaric acids, and chloro-
instance, as measured by ABTS assay, the antioxidant
genic acid), vitamin C, and radical scavenging activity
activity reduced by 16.44% in PAW90-watered sprouts
of purple coneflower seeds after a short-time treat-
in contrast with the control group of 8.69 mg Trolox/g
ment of cold plasma, which might be beneficial to
DW. Beside known phenolic and flavonoid compounds,
improve the defensive response against unfavourable
other components in sprouts, such as polypeptides and
conditions [30]. Besides, Michalak also pointed out
polysaccharides, also show potential antioxidant activ-
that the regulation of phenolic metabolism serves as a
ity [32], which may produce the inconsistent trends
response for oxidative damage induced by heavy metal
between the changes in the antioxidant activity and
stress [31]. Therefore, summarizing these findings, plant
total phenolic and flavonoid contents of mung bean
tissue might accumulate phenolic compounds as a
sprouts.
defensive response against oxidative stress induced
As shown in Table 2, there was a strong correlation
by PAW.
between the antioxidant activity of mung bean sprouts
Table 1. Effect of PAW treatment at different exposure durations on the antioxidant activity of mung bean sprouts.
DPPH• scavenging activity ABTS•+ scavenging activity
Group (mg Trolox/g DW) (mg Trolox/g DW) FRAP (mg FeSO4 /g DW)
Distilled water-treated sprouts 1.69 ± 0.11a 8.69 ± 0.25a 20.29 ± 0.61ab
PAW15-watered sprouts 1.64 ± 0.03a 8.91 ± 0.29a 21.38 ± 0.71a
PAW30-watered sprouts 1.50 ± 0.03b 8.11 ± 0.32b 19.41 ± 1.48bc
PAW60-watered sprouts 1.40 ± 0.04c 7.37 ± 0.13c 18.05 ± 1.41d
PAW90-watered sprouts 1.36 ± 0.06c 7.26 ± 0.18c 18.52 ± 0.27cd
Note: The results are expressed as the mean ± standard deviation. Different letters in the same column indicate significant differences between groups
(p < 0.05) as determined by the LSD test.
Table 2. Pearson’s correlation analysis between total phenolic and flavonoid content & antioxidant activity.
DPPH• scavenging ABTS•+ scavenging
TPC TFC activity activity FRAP
TPC 1.000
TFC 0.812** 1.000
DPPH• scavenging activity 0.716** 0.834** 1.000
ABTS•+ scavenging activity 0.873** 0.848** 0.834** 1.000
FRAP 0.759** 0.746** 0.606** 0.809** 1.000
Note: TPC, total phenolic content; TFC, total flavonoid content. **p < 0.01.Page 8
JOURNAL OF TAIBAH UNIVERSITY FOR SCIENCE 829
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