Lilium brownii is a perennial herbaceous bulbous plant. Its
underground bulbs aggregate into rosettes with multiple fleshy and spoon-shaped
white scales. It tastes slightly sweet and has medicinal properties (Wang et al. 2018). L. brownii is used as medicine and food (Luo et al. 2017). It is believed that it has
healing effects for heart, lung, cures cough, and has soothing effect on
nerves. Studies have shown that L.
brownii contains antioxidant, has anti-tumor and anti-inflammatory effects,
and it is involved in immune regulation, it has hypoglycemic and antidepressant
properties (Luo et al. 2017; Hu et al. 2018; Wang et al. 2019). L. brownii
contains nutrients such as sugar, protein, fat and vitamins, and a variety of
physiologically active substances beneficial for health, such as steroidal
saponins, flavonoids polyphenols and polysaccharides. There is variety in L. brownii products, such as beverages,
powder, and health products. The fresh L.
brownii scales are crispy and sweet and have all nutrients and active
substances. However, the L. brownii
loses a lot of nutrients during processing and dried product tastes bad.
Therefore, the fresh L. brownii is preferred by the
public. L. brownii is one of the fine varieties of lily, distributed
in Hunan, Hubei, Jiangxi and some other provinces of China. However, fresh L. brownii bulbs are prone to
rot, oxidative discoloration, and loss of physiologically active substances
during storage.
Traditional preservation
methods include sand storage, soil storage, cold storage, and use of
preservatives (Luan 2016). Studies have shown
that bulbs coated with natamycin chitosan can significantly reduce the decay
index and weight loss rate, inhibit the accumulation of malondialdehyde content
and degree of browning, slowing down the reduction of vitamin C and reducing
sugar and soluble protein content during storage (Gong et al. 2016).
However, during storage problems such as weight loss, rot, and oxidative
discoloration occur (Wei et al. 2017).
Some
researchers studied the changes
of carbohydrate content and amylase activity of Lanzhou lily bulbs during cold
storage. The results showed that with the extension of refrigeration
time, the starch content
decreased significantly (Ma et al. 2018).
The current researches
mainly focus on starch processing of lily, preservation of fleshy flowers and
extraction of medicinal ingredients. There
were few reports on the changes of pharmacological active substances
during the fresh-keeping period.
Compared with other methods used for lily
preservation, controlled atmosphere storage (CAS) has the characteristics of
large storage capacity, long storage period, multiple types of storage, good
quality and high safety, and is suitable for the seasonal harvest of lilies. CAS refers to a technology that achieves the
preservation of fruits and vegetables by artificially changing the composition
of ambient gases on the basis of low-temperature storage. Specifically, the air
conditioner changes the composition ratio of oxygen, carbon dioxide and
nitrogen while refrigerating and keeping the product fresh by maintaining an
appropriate low temperature and suppressing the respiration rate, environmental
microorganisms and regulating the production of hormones involved in ripening
and senescence (Zhang 2015). The controlled
atmosphere can slow down the degradation of fruits and vegetables by regulating
the temperature, humidity and gaseous composition of the storage system,
regulating the synthesis and activity of enzyme and inhibiting microorganisms
in the environment (Xu et al. 2016).
Recently, modified atmosphere preservation has
been widely used to protect fresh fruits and vegetables. However, there are a
few studies on CAS in kiwi, cherry and pear. Study should be done on the most
suitable box-type spontaneous atmosphere of refrigerated Kiwi (Actinidia
arguta) to improve the storage and transportation effect of Kiwi. CAS can
delay the decline of the titratable acidity and vitamin C, delay the ripening
of the fruit to ensure the content of soluble solids, and inhibit the
development of respiratory peak and ethylene production rate (Zhang et al. 2017).
CAS also inhibits the respiration rate and reduces polyphenol oxidase activity
thereby effectively reducing the enzymatic browning during storage, and
maintains a high soluble protein content, and improves the storage stability of
Agaricus bisporus (Sun et al. 2016). Li and
Zhang (2019) explored the entire process of sulfur-free color protection and
ultrasonic technology to keep fresh Lanzhou lilies in modified atmosphere
packaging. Zhang explored the changes in lily enzyme activity in the modified
atmosphere experiment and concluded that after treatment with ozone
cleaning-ultraviolet irradiation-atmosphere, packaging-low temperature storage
integrated fresh-keeping technology effectively inhibit the activity of
browning-related enzymes, reduce cell membranes damage and extends shelf life
(Zhang 2018). However, there are few reports on the changes in physiologically
active components during CAS.
Cleaning can remove soil and reduce
microorganisms but it may also make the product more susceptible to infection
by new
microorganisms. Ozone is often used as a disinfectant in the industry because
of its oxidizing properties. In this paper, the fresh L. brownii bulbs were used to explore the
effects of cleaning and ozone treatments on the
active constituents of L.
brownii. The weight
loss rate, saponins, flavonoids and polyphenols were measured and the changes
of active substances in the process of CAS were studied during the atmosphere
storage, and the causes of the changes were analysed that provides a
theoretical basis for the preservation and storage of L. brownii.
The experiment was carried out with L. brownii
which were bought from Baoqing
Agricultural Products Import & Export Co., Ltd., Hunan Province, China. L. brownii bulbs were spherical,
about 3.5 cm in radius,
scales were
lanceolate, knotless, white, stem height 40~70 cm. The
experimental L. brownii bulbs were collected in Oct 2018 in L.
brownii base of Baoqing Agricultural Products Import & Export
Co., Ltd. The planting area was about 21 km2. The base was located in the subtropical humid monsoon climate
where the climate was mild, the details are shown in Table 1.
Dioscin was purchased from Chengdu
Mansite Biotechnology Co., Ltd. Anhydrous rutin was purchased from China Food
and Drug Control Institute and all other reagents used were of analytical grade.
Controlled atmosphere storage
The bulbs of mature L. brownii with or without mold and pests were
selected; their radius was ~3.8 cm and weight was about 350 g. The storage
conditions were set as 2.0~4.0°C, oxygen content 3.0~5.0%, CO2
content 0~5.0%, and the humidity was maintained about 80~90%. L. brownii were divided into four
groups, DN: with mud and no-ozone group; DC: with mud and ozone group; XN:
clean and no-ozone group; XC: clean and ozone group. The ozone content was 200
mg h-1; the sterilized water was used to clean L. brownii. The L. brownii
was stored in a
L. brownii
bulbs were weighed every
week.
The weight loss rate of bulbs during the CAS process was determined:
Where w
is
the weight loss (%) of L. brownii
during CAS,
m1 was the storage quantity (g) of and m2 represents the mass of the
bulbs (g) L. brownii
after specific storage time.
Extraction of saponins, flavonoids and
polyphenols: L. brownii bulbs were taken and
homogenized. Saponin, flavonoids, and polyphenols were dissolved by extracting
in a water bath at 80°C for 30 min, centrifuged (VELOCITY 14R centrifuge,
Dynamica Scientific Ltd.) at 8571×g
for 30 min and the supernatant was taken as sample.
Determination of total
saponin content: Determination
of saponin content by the perchloric acid method (Chen et al. 2018) with appropriate modifications.
The standard curve for saponin is shown in Table 2. When measuring the lily
saponin content, 0.3 mL of the extract was taken,
evaporated to dryness, and reacted with 4.0 mL of perchloric acid in a 70°C
water bath for 30 min. After completion of the water bath, sample was shifted
to an ice water bath for 10 min and then absorbance was measured at 408 nm.
Determination of flavonoid content: The total flavonoid
content of L.
brownii was determined by the method of (Dong et al. 2013).
The standard curve for flavonoid is shown in Table 2. We determined the concentration of
flavonoids in the extract according to the standard curve. 2 mL of lily extract
was taken and added de-ionized water to 10 mL and added 1 mL 50 g/L
nitrite solution, 1 mL 100 g/L
aluminum nitrate solution, and 4 mL 200 g/L sodium hydroxide. The solution was
allowed to settle to 25 mL for 15 min and the absorbance was measured by
UV-1780 ultraviolet spectrophotometer (Shimadzu Instruments Co., Ltd.,
Japan) at a wavelength of 510 nm.
Table 1: The growth information of L. brownii used in this study
Category |
Information |
Stem height (cm) |
40~70 |
Bulbs radius (cm) |
about 2~4.5 |
Bulbs form |
spherical, scales are lanceolate, knotless,
white |
Collection location |
L. brownii base |
Planting area (km2) |
21 |
Average temperature (°C) |
11~17 |
Sunshine time (h) |
>7 |
Table 2: The standard curve of saponins, flavonoids
and polyphenols
Standard curve name |
Regression equation |
Correlation coefficient |
Linear range |
Saponin standard curve |
Y=0.0449x-0.0346 |
0.9993(n=6) |
20~80 μg L-1 |
Flavonoid standard curve |
Y=0.5297x - 0.0012 |
0.9997(n=6) |
0~1.0 mg L-1 |
Polyphenol standard curve |
Y=0.0155x+ 0.0006 |
0.9998(n=6) |
0~50 mg L-1 |
Fig. 1: The weight-loss ratio variation of L. brownii during CAS. Differences among four different treatments were compared using Duncan's multiple range test at P
≤ 0.05. DN: group of with mud and
no-ozone; DC: group of with mud and ozone; XN: group of clean and no-ozone; XC:
group of clean and ozone
Determination of
polyphenol content: The
content of polyphenols in Lilium was determined by the method of Mei et al. (2016) with modifications. The
standard polyphenol curve
is
shown in Table
2. 1
mL of lily extract was taken, added 1.0 mL of folin phenol as chromogenic agent,
3 mL 8% sodium carbonate solution, and
diluted to 10 mL.
After 60 min reaction at 25°C,
the absorbance was
measured at 765 nm wavelength to obtain the concentration of the assay
solution.
The presented values were the means ± standard
errors (S.E.) of three replicates for every six L. brownii bulbs.
The test results were plotted with Excel 2007 and the statistical analysis was
conducted using SPSS. Differences among the four different treatments and
different periods were compared using Duncan's multiple range tests at P ≤ 0.05.
The weight loss rate of different groups of L. brownii during CAS was between 0.81 and 3.59% (Fig. 1). There was no
significant difference between the two groups within 0–6 weeks, which was a
similar subset. In the seventh and eighth weeks, DC and XC were a similar
subset, and the remaining two groups were similar subsets.
As storage time increased, the weight continued to lose. Before the 7th weeks,
the weight loss under
different conditions was similar, and multiple comparative analysis showed that
there was no significant difference in the weight loss rate among the groups at
the same time (P > 0.05). There
were fluctuations in the third and fifth weeks and it could be indirectly
speculated that the L. brownii was a climacteric type of plant. After the 6th week, the
weight loss rate increased and the changes in different conditions were
different. The weight loss rate of each group without ozone increased
significantly, and weight loss rate of each group was statistically significant
in ozone treated groups (P < 0.05).
Under the condition of no ozone, the weight loss rate was large and consistent.
In case of ozone, the weight loss rate in the 8th week of storage
was lower than that of the two groups without ozone.
The low temperature, high humidity and modification of gaseous
composition can reduce the loss of water to some extent and effectively inhibit
the growth of microorganisms. It remains relatively fluctuating in 0~6 weeks.
It could be observed that the ozone reduces the weight loss of bulbs to some
extent which indicated that the ozone had a positive effect on the weight of
the L. brownii bulb. Under the condition of no ozone, the difference between the
weight loss rate of the bulbs washed and the L. brownii bulbs was smaller (P > 0.05)
indicating that cleaning or non-cleaning has no relationship with the weight
loss of the L. brownii.
The content of L. brownii saponins before storage
was about 0.33 μg/g (Fig. 2). The content of L. brownii saponin in each group was between 0.27 and 0.61 μg/g during storage. The higher content of saponin at the end of the fresh-keeping period was observed
for the L. brownii stored in CAS. After
the third week, the DN group was significantly different from the other three groups in different
periods during the CAS and the saponin
content was 0.20 μg/g higher than the original. The other three
groups of L. brownii were gently undulated based on the initial saponin content, and the
final saponin content was not significantly different from the initial saponin content.
The changes of flavonoids
content in L. brownii bulbs under different
conditions are shown in Fig. 3. The initial value of L. brownii flavonoids
was about 12 mg·g-1, and the content of flavonoids in L. brownii bulbs was 11.24 ~ 18.94
mg·g-1. In the multiple comparison analysis, there was no
significant difference in the flavonoid content of the different treatments in
the first 5 weeks, but after 5 weeks, the flavonoid content of the DC group
showed a difference with other three groups (P < 0.05). However, under ozone treatment groups, the flavonoid
content of the DC group decreased after 5 weeks, and the flavonoid content was
significantly lower than that of other three groups (P < 0.05). In analysis within
the group, the flavonoid content of the DN group and the XN group without ozone
treatment increased during storage (P < 0.05), and the flavonoid content of the XN group at the 8th week of storage was 6.19 mg g-1 higher than that of the original.
Fig. 2: The saponin content variation of L.
brownii during CAS. The homogeneity test of variance was performed at P
≤ 0.05 using SPSS. The
analysis of variance between groups was performed. DN:
group of with mud and no-ozone; DC: group of with mud and ozone; XN: group of
clean and no-ozone; XC: group of clean and ozone.
Fig. 3: The total flavonoid content variation of L.
brownii during CAS. Differences among the four different treatments were compared using Duncan's multiple range test at P
≤ 0.05. DN: group of with mud and no-ozone; DC: group of with mud and ozone; XN: group of
clean and no-ozone; XC: group of clean and ozone.
Fig. 4: The total polyphenol
content variation of L. browni
during
CAS. The homogeneity test
of variance was performed at P ≤ 0.05. DN: group of with mud and no-ozone; DC: group of with mud and
ozone; XN: group of clean and no-ozone; XC: group of clean and ozone.
The polyphenol content of L. brownii varied between 6.21
mg·g-1 and 8.21 mg·g-1 during storage
(Fig. 4). During the storage period,
the content of polyphenols in four different treatments had differences. The
content of polyphenols in DN group increased during the storage period and the
content of polyphenols in the 0, 1, and 2nd week were similar, and
the polyphenols content were similar during 3rd, 4th and
5th week. Similarly, polyphenols content was same during 5, 6 and 7th
week. Polyphenol content in XN group increased significantly after the fourth
week; the polyphenol content in the clean and ozone group increased
significantly after the sixth week. Polyphenol content increased
during the storage period in DN group, however the polyphenol content in the
second and fifth weeks were reduced; the clean and no ozone group
showed significantly increase of polyphenol content after the fourth week.
In the correlation
analysis, the weight loss rate of L. brownii bulbs of different
conditions had no correlation with physiologically active substances, and the
measured indicators showed an extremely significant or moderately significant
(0.5 ≤ | r | < 0.8) positive correlation (Table 3). Correlation analysis showed that the weight loss rate of L. brownii bulbs in CAS was less correlated with polyphenols, flavonoids and
saponins. There
were significant correlations
between polyphenols and flavonoids of L. brownii with no ozone and ozone-free conditions. There were significant
correlations between the three groups of saponins and flavonoids with mud-free
ozone, and the polyphenols and saponins with mud ozone and ozone-free
conditions. The correlation of active substances between different conditions
needs further studies.
In this study, the saponin of L. brownii with mud had a steady upward trend under the condition of ozone-free
and the condition of cleaned and ozone-free was conducive to maintain
polyphenols and flavonoids in L. brownii. The physiologically active substances measured during the modified
atmosphere storage of lily did not decrease, and the group without ozone
exposure had better performance. During the storage, L. brownii bulbs
undergo a series of reactions, which were affected by gas regulation,
respiration, enzyme catalysis and microbes. The weight loss rate of this study
was significantly lower than that of Gong et al.
(2016), about 2.23~18.71%. The
reason for the difference in weight loss rate was possibly because of different
storage temperatures. The low storage temperature promotes chilling damage,
while the high temperature increases respiration rate thus reduces storage
life.
As the moisture content
decreased, there was no upward trend in the saponin content of the three
conditions which indicated that the saponin in storage had been lost under the
corresponding conditions. Saponins in plants are generally combined with sugar.
Major ginsenosides such as Rb1, Rb2, Rc, Rd, Rg1 and Re-formed by transforming
different glycos groups (such as glucosyl, arabinosyl, xylosyl, rhamnosyl) into
the aglycone protopanaxadiol or aglycone protopanaxatriol, and the sugar chain
on ginsenoside is closely related with the function of ginsenoside (Liu et
al. 2019). Since the saponin in L. brownii are mainly composed of steroidal sapogenin and carbohydrate, and the saccharide as a
substrate for L. brownii respiration, it affects the metabolism of saponin in plant cells. The saponin content was lower
than that of domestic saponin extraction (Gao et al. 2012; He et al. 2014),
because of the
variety, origin and different extraction method used. The
relative content of active ingredients had a certain relationship with the water
content of lily bulbs, and the saponin concentration may
change with moisture percentage. The investigation of weight loss
rate during the modified atmosphere storage revealed that the moisture contents are decreased during the storage. Flavonoids show free radical scavenging effects by self-reducing
phenolic oxidation, which had a significant effect on scavenging OH- free
radicals (Sun and Tang 2001). Conditions such low temperature can reduce the
respiration rate and of loss of water, related enzyme activities and
physiological and biochemical reactions at the cellular level. However, due to
environmental disadvantages or aging of fruit and vegetable cells, the rate of
free radical production was accelerated. Ozone as an oxidant accelerates the
production of free radicals, so the content of flavonoid in the ozone
conditions was reduced. L. brownii that were not exposed to ozone had less loss of flavonoids due to the
absence of oxidative ozone.
A wide variety of phenolic substances such as
flavonoids, tannins, phenolic acids are secondary metabolites produced by the
metabolic pathways of phenylpropanoids and are the main substances causing
enzymatic browning. Total phenols were associated with scavenging free radicals
and in most of fruits and vegetables these are converted to non-oxidative
scavenging free radicals by phenolic groups (Topalović et al. 2013). The stability of
polyphenols is affected by light, temperature, time and biochemical reactions.
According to a report, total phenols generally remain stable during frozen
storage (Zhan et al. 2018). In this
study, the L. brownii was stored at low temperature and protected from light, thus polyphenol
content changed slowly. Schotsmans et al.
(2007) believe that polyphenolic compounds are oxidized with air and the
oxidized polyphenols are no longer detected in the assay reaction that may be
reason for lower polyphenol content compared with flavonoid content. Light
exposed bulbs show changes of total polyphenols in L. brownii during low temperature storage
from the perspective of dormancy at low-temperature, and the polyphenols
increased significantly in the early stages (Sun et al. 2004). Besides this, some reports indicated the change of
polyphenol content and benzene. There was a significant positive correlation
between alanine ammonia-lyase activity and free phenylalanine content.
Washing mud and ozone do not have a positive
effect on the quality of L. brownii bulbs and the maintenance of physiologically active substances, which
was contrary to expectations. The reason was that the soil attached to the
roots and vegetables could protect the fruits and prevent the exposure to air. In addition, the introduction of
ozone in the atmosphere storage environment reduced the relative humidity to a
certain extent, increased the proportion of the oxidant and easily accelerates
the water loss of the L. brownii bulb. When the soil as a
protective film was removed, the bulb weight and physiological activity changes
due to direct exposure to air. The physical and chemical
indicators of fresh fruits and vegetables and the content of each component
were affected by various factors during storage. A series of physical and
chemical reactions and biological metabolic reactions occurred. Metabolic process
with in in plants regulates the synthesis and degradation of their substances
to maintain an equilibrium. Kan
et al. (2019) used Yixing lily as experimental material to study the
relationship between membrane lipid peroxidation and browning of lily scales
during low-temperature storage after harvest. The results showed that during
low-temperature storage, the browning degree, cell membrane permeability,
superoxide anion radical (O2-·) production rate, H2O2, and
propyl of different parts of lily scales increased. The dialdehyde content
increased with storage time (Kan et al. 2019). In this study, the ozone had strong oxidizing properties. In the later period of
storage, the lipids in membrane of L. brownii cells were more susceptible to oxidation reaction with ozone, which
destroyed the lipid film to form peroxide. Oxides could continue to react with
proteins and active carbonyl compounds, eventually leading to deterioration of L. brownii bulb
texture (Zhao et al. 2017). The enzymatic browning free radical damage
hypothesis (Gong and Wang 2012) believed that when fresh fruits
and vegetables were in an adverse environment or self-aging produces more free
radicals, the generation of free radicals and the removal of free radicals are
no longer balanced, causing the lipid membrane to be destroyed and causing
enzymatic browning. The dynamic synthesis of phenolic compounds in the
metabolic pathways during the fresh-keeping process might be an important
reason for the saponin, flavonoids and polyphenols to have no downward trend
and the changes did not had obvious rules. The
synthesis of phenolic substances in plants was a dynamic process. The phenolic substances in
different kinds of plants and different plant organs were different, and the
content in plants also changes with time and growth stages. The environment
also caused differences in phenolic content (Jing
2012; Baxter and Stewart 2013). On the other hand,
saponins, flavonoids, and polyphenols were oxidized as active substances to
scavenge free radicals produced by plants and their content was reduced.
The weight loss and active ingredients of bulbs
were affected by various factors. Both polyphenols and flavones belonged to the
secondary metabolites of plants, which had a high degree of correlation. This
situation was similar to the changes in polyphenols and flavones during the
freshness preservation of the roots of Echinochloa
japonica (Li 2009). The correlation of flavonoids, polyphenols and saponins of L. brownii in modified atmosphere storage might be related to the fact that
several active substances belongs to benzene ring-derived compounds, and their
properties and metabolism are similar.
There were
also some shortcomings in this study, such as insufficient quality indicators
measured during the preservation process, which made it difficult to carry out
accurate quality assessment. In the next experiment, we will increase the
determination of bad fruit rate, respiration rate, color difference, related
enzyme activity and free radical content. The quality change mechanism can be
further studied through these indicators. With
the expansion of the lily market, the application of modified atmosphere
preservation technology in lily storage had broad development prospects and a
huge potential. The research on the mechanism of product quality change after
CAS for a certain period of time and the establishment of a fresh-keeping
kinetic model could be the next research direction. In addition, the
fresh-keeping lily through dynamic modified atmosphere storage and CAS will
become the trend in the future. The control
index of storage conditions was
based on adapting to the physiological characteristics of the bulbs. According
to the requirements of the gaseous components of the fruit during the storage
phase, the modification of gaseous component can improve the storage period. A fine modified atmosphere technology could effectively delay the metabolic processes and maintain a
good edible quality and flavour. The modification of respiration rate can help
improve the storage of fruits and vegetables of the genus Lilium such as L. brownii var. viridulum Baker
and L. lancifolium.
In this study, the bulbs of L. brownii were air-conditioned for 8 weeks. The results showed that the
physiologically active substances in L. brownii bulbs could be maintained to a certain extent during storage. The
weight loss rate of L. brownii showed a sudden increase after the sixth week of the preservation
process, the saponin content had a steady upward trend
under the condition of ozone-free, and the condition of cleaned and ozone-free
was conducive to maintain polyphenols and flavonoids in L. brownii. There was a certain correlation
between the changes of lily materials in modified atmosphere preservation, and
various indicators of fresh plants are affected during storage that requires
further investigations.
We acknowledge the scientific research projects
of Hunan Provincial Department of Education Excellent
Youth Project (18B427),
the Key Laboratory of Soybean Product Processing and
Safety Control of Huan (2019NK4229) and Hunan
Province Graduate Innovation Project (CX20190971).
LY and DL conceived
and designed the experiments, CL, AY and YL performed the experiments, and PH and LL analysed the data.
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