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Citation: Zhao, Q.; Zhong, X.-L.; Zhu,
S.-H.; Wang, K.; Tan, G.-F.; Meng,
P.-H.; Zhang, J. Research Advances in
Toona sinensis, a Traditional Chinese
Medicinal Plant and Popular
Vegetable in China. Diversity 2022,14,
572. https://doi.org/10.3390/
d14070572
Academic Editor: Jesús
Fernando Ayala-Zavala
Received: 26 June 2022
Accepted: 16 July 2022
Published: 17 July 2022
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diversity
Review
Research Advances in Toona sinensis, a Traditional Chinese
Medicinal Plant and Popular Vegetable in China
Qian Zhao 1,2, Xiu-Lai Zhong 1, Shun-Hua Zhu 1, Kun Wang 1, Guo-Fei Tan 1,3,* , Ping-Hong Meng 1, *
and Jian Zhang 3, *
1Institute of Horticulture, Guizhou Academy of Agricultural Sciences, Guiyang 550006, China;
zhaoq217@163.com (Q.Z.); gzzyzxl@foxmail.com (X.-L.Z.); zsh2801@163.com (S.-H.Z.);
wangkunfun@hotmail.com (K.W.)
2
Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry
of Education), Collaborative Innovation Center for Mountain Ecology & Agro-Bioengineering (CICMEAB),
College of Life Sciences/Institute of Agro-Bioengineering, Guizhou University, Guiyang 550025, China
3Faculty of Agronomy, Jilin Agricultural University, Changchun 131018, China
*Correspondence: tagfei@foxmail.com (G.-F.T.); mengph322@163.com (P.-H.M.); jian.zhang@ubc.ca (J.Z.)
Abstract: Toona sinensis, a perennial and deciduous tree belonging to the Meliaceae family, has been
cultivated for more than 2000 years in China. Storing the buds of T. sinensis is difficult, as it is easy for
them to rot during storage, which seriously affects their edible and commodity value. Young leaves
and buds of T. sinensis plants are excellent source of flavonoids, terpenoids, phenylpropanoids, and
more. In addition, the bioactive components of T. sinensis possess numerous health benefits, such
as antiviral, antioxidant, anti-cancer, anti-inflammatory, and hypoglycemic effects. In this review,
we summarize the storage and preservation, nutritional components, specific chemical compounds,
pharmacological value, function genes, and omics of T. sinensis. This review aims to provide basic
knowledge for subsequent future research seeking to understand the comprehensive biology and use
of T. sinensis as a favored Chinese food and pharmacological resource.
Keywords: T. sinensis; preservation; nutritional components; pharmacology; functional gene; omics
1. Introduction
Toona sinensis (A. Juss.) Roem (Figure 1) belongs to the Meliaceae family and is
commonly called Chinese toon or Chinese mahogany. It is a woody perennial deciduous
tree [
1
]. T. sinensis has a cultivation history stretching back more than 2000 years in China [
2
];
it is widely distributed throughout China, ranging from Liaoning in the east to Gansu in the
west, Guangdong, Guangxi, and Yunnan in the south, and southern Inner Mongolia in the
north. Of all the provinces, Anhui, Shandong, Henan, and Hebei have the most areas under
T. sinensis cultivation [
3
,
4
]. T. sinensis is a medicinal and edible vegetable, and different
tissues of this plant have been used to treat a wide variety of diseases [
5
,
6
]. Phytochemical
investigations of T. sinensis have showed that its main constituents include terpenoids,
phenylpropanoids, and flavonoids [
7
–
9
], and that the plant has many pharmacological
activities, including anti-tumor, anti-oxidant, anti-diabetic, anti-inflammatory, antibacterial,
and anti-virus action [10–12].
T. sinensis is divided into two types based on the color of tender leaves and petioles:
red T. sinensis and green T. sinensis [13,14]. Red T. sinensis is rich in anthocyanins, thus the
leaves and petioles are purple [
15
]. Red T. sinensis is more popular with consumers. This
plant has a short harvest period, and storage is difficult; the edibility and commodity value
is lost after 2–3 days at normal temperature [16].
Diversity 2022,14, 572. https://doi.org/10.3390/d14070572 https://www.mdpi.com/journal/diversity
Diversity 2022,14, 572 2 of 14
Diversity 2022, 14, x FOR PEER REVIEW 2 of 14
Currently, T. sinensis has aroused considerable public interest in terms of storage and
preservation, nutritional components, medicinal use, and gene and omics research. How-
ever, there has been no systemic review of these aspects. Consequently, this paper aims
to summarize the current advances in storage and preservation, nutritional components,
medicinal use, and gene and omics studies of T. sinensis. Furthermore, this paper discusses
potential future development perspectives on T. sinensis.
Figure 1. Seeds (A), seedlings (B), plant and buds (C–E) of T. sinensis, and cooked with eggs (F).
2. Storage and Preservation of T. Sinensis Buds
Storage environmental conditions, including temperature [17], humidity [18], gas
composition [19], etc., have been shown to affect the quality of the T. sinensis buds. Cur-
rently, researchers often use physical, chemical, and biological means to store and pre-
serve T. sinensis buds. Although the principles of the three means are different, they all
delay the duration and rot process of T. sinensis by controlling the water evaporation, res-
piration, and relative humidity of the environment of this plant and improve preservation
time and quality of T. sinensis buds.
2.1. Physical Preservation Method
2.1.1. Temperature Control Preservation Technology
Temperature control preservation technology mainly includes low temperature
preservation, low temperature and high humidity preservation, and quick-frozen preser-
vation. Low temperature preservation can delay the metabolic process of T. sinensis after
harvest; the buds of T. sinensis are packed into a plastic bag and stored at 0 °C, and can be
stored for up to two months [20]. The low temperature and high humidity preservation
method can slow down the loss of nutrients in the vegetables; this method can effectively
inhibit the activity of polyphenol oxidase and maintain the quality of the plant [21,22].
Quick-frozen preservation can maximally maintain the natural quality of T. sinensis buds,
which could be stored for about a year using this method [23].
2.1.2. Dehydration Preservation Technology
Fresh buds of T. sinensis contain up to 90% water, and the leaves are prone to wilting
after picking. Dehydration preservation technology reduces the water content of vegeta-
bles to keep the color and nutrient content of vegetables unchanged [24]. Zhao et al. (2014)
Figure 1. Seeds (A), seedlings (B), plant and buds (C–E) of T. sinensis, and cooked with eggs (F).
Currently, T. sinensis has aroused considerable public interest in terms of storage
and preservation, nutritional components, medicinal use, and gene and omics research.
However, there has been no systemic review of these aspects. Consequently, this paper aims
to summarize the current advances in storage and preservation, nutritional components,
medicinal use, and gene and omics studies of T. sinensis. Furthermore, this paper discusses
potential future development perspectives on T. sinensis.
2. Storage and Preservation of T. sinensis Buds
Storage environmental conditions, including temperature [
17
], humidity [
18
], gas
composition [
19
], etc., have been shown to affect the quality of the T. sinensis buds. Cur-
rently, researchers often use physical, chemical, and biological means to store and preserve
T. sinensis
buds. Although the principles of the three means are different, they all delay the
duration and rot process of T. sinensis by controlling the water evaporation, respiration,
and relative humidity of the environment of this plant and improve preservation time and
quality of T. sinensis buds.
2.1. Physical Preservation Method
2.1.1. Temperature Control Preservation Technology
Temperature control preservation technology mainly includes low temperature preser-
vation, low temperature and high humidity preservation, and quick-frozen preservation.
Low temperature preservation can delay the metabolic process of T. sinensis after harvest;
the buds of T. sinensis are packed into a plastic bag and stored at 0
◦
C, and can be stored for
up to two months [
20
]. The low temperature and high humidity preservation method can
slow down the loss of nutrients in the vegetables; this method can effectively inhibit the
activity of polyphenol oxidase and maintain the quality of the plant [
21
,
22
]. Quick-frozen
preservation can maximally maintain the natural quality of T. sinensis buds, which could be
stored for about a year using this method [23].
2.1.2. Dehydration Preservation Technology
Fresh buds of T. sinensis contain up to 90% water, and the leaves are prone to wilting
after picking. Dehydration preservation technology reduces the water content of vegetables
to keep the color and nutrient content of vegetables unchanged [
24
]. Zhao et al. (2014) used
Diversity 2022,14, 572 3 of 14
the methods of hot drying, microwave drying, vacuum drying, and vacuum freeze drying
to treat T. sinensis, among which vacuum freeze drying best maintained the nutritional
composition of the plant [
25
]; the sensory quality was better and the rehydration rate
reached 51.05%. Lv (2010) conducted research about vacuum freeze-drying of T. sinensis
buds. The products were obviously better than those obtained by pickled storage and
ordinary refrigeration; the buds of T. sinensis had a shelf life of up to two years and were
essentially the same in terms of nutrient content [26].
2.1.3. Modified Atmosphere Preservation Technology
Modified atmosphere preservation is used to adjust the proportion of gases in the
storage environment, in order to inhibit the respiration and evaporation of fruits and
vegetables [
27
,
28
]. Zhu et al. (2014) used two types of modified atmosphere packaging
materials with difference thickness (0.01 and 0.03 mm), namely, low density polyethylene
(LDPE) and high density polyethylene (HDPE), on T. sinensis storage, and the experimental
results showed that the packaging material of low-density polyethylene (thickness
0.03 mm
)
effectively inhibited the defoliation phenomenon of T. sinensis buds and delayed the aging
of T. sinensis [29].
2.2. Chemical Preservation Method
Chemical preservation means are mainly used to extend the preservation time of
buds of T. sinensis by adding chemical preservatives. Although the preservation effect is
good, it may be harmful to the human body and the environment. There are three main
types of preservatives: adsorption, anti-corrosion, and inhibition. Ethylene adsorbent
is often used in the storage and preservation of T. sinensis. It can delay post-ripening
and achieve the preservation effect of buds of T. sinensis [
30
]. Preservatives mainly use
carbendazim to kill pathogenic microorganisms on the surface of T. sinensis buds to attain
the effect of preventing T. sinensis bud rot [
31
]. 6-Benzylaminopurine is a common inhibitory
preservative in T. sinensis preservation which can prevent the aging of T. sinensis. Results
show that after 45 days of storage, the color and fragrance of T. sinensis are basically
unchanged [32].
2.3. Biological Preservation Method
Bio-preservatives are natural substances extracted from plants or animals. With the
advantages of low pollution and low cost, bio-preservation technology is widely used in
the market [
33
]. Chen et al. (2015) treated T. sinensis with 8 mmol
·
L
−1
exogenous betaine;
the resulting rotting of T. sinensis buds after sixteen days of storage was not serious, the loss
of chlorophyll, Vc, and total flavonoid content was alleviated, and the plant retained its
commercial value [
34
]. Zhang et al. (2009) treated T. sinensis buds with Allium macrostemon
Bunge extracts; the results showed that A. macrostemon Bunge extracts could significantly
reduce the decay rate of T. sinensis and inhibit the decline of Vc content while extending
the shelf life of T. sinensis buds by more than seven days [35].
3. Eating and Processing of T. sinensis
3.1. Cooking Methods
There are three traditional ways to eat T. sinensis buds: (1) fresh T. sinensis buds; (2) old
dish T. sinensis buds; and (3) fried T. sinensis buds. Fried T. sinensis buds are mainly eaten
with flour or lotus root. T. sinensis buds can be wrapped directly with flour paste, or the
T. sinensis
buds can be chopped and used to fill the holes of lotus root, then wrapped with
flour paste and fried with oil before sprinkling them with spices. These edible methods are
very popular and taste very delicious.
3.2. Processing of T. sinensis Buds
In recent years, with people obtaining a deeper understanding of the health value
of T. sinensis, more and more ways to eat T. sinensis have been developed. In addition to
Diversity 2022,14, 572 4 of 14
traditional eating methods, this plant is often processed into various products (Table 1).
There are no studies reporting on T. sinensis bud preservation using radiation exposure,
which could be a safe and low-cost procedure.
Table 1. Processed products using T. sinensis.
Products Reference
Natural T. sinensis powder [36]
Red T. sinensis lactone tofu [37]
Liquid flavoring agent [38]
Canned T. sinensis [39]
T. sinensis bread [40]
T. sinensis noodles [41]
T. sinensis biscuit [42]
T. sinensis Hotpot condiment [43]
T. sinensis seasoning oil [44]
T. sinensis juice [45]
T. sinensis coffee ice-cream [46]
T. sinensis yogurt [47,48]
4. Nutrient Composition of T. sinensis
T. sinensis is an excellent source of minerals, proteins, carbohydrates, fatty acids, amino
acids, carotene, vitamins, dietary fiber and other compounds [
49
,
50
]. The nutritional
components of different tissues and varieties of the plant are different.
Jin and Dong (1994) analyzed the content of amino acids, soluble sugars, and fatty
acids in T. sinensis tender buds (Table 2); the results showed that the essential amino acid and
total amino acid content accounted for 8.51% and 27.43% of dry weight (DW), respectively.
Gas chromatography (GC) detected 22.05% palmitic acid, 1.88% stearic acid, 3.44% oleic
acid, 30.16% linoleic acid, and 42.47% linolenic acid. The older leaves of
T. sinensis
are
rich in nutrient composition as well, and yield more than the young buds [
51
]. However,
the old leaves are often discarded. Hou et al. (1997) analyzed the protein, amino acid
(Table 3), fat, crude fiber, and mineral content (Table 4) of old leaves, and found that their
crude protein, amino acid, and fat contents were richer than those of corn, showing the
old leaves of T. sinensis to be a better animal feed [
52
]. Xu et al. adopted the full-distance
equal division method to rank different varieties based on their content of nutritional
compositions, resulting in the following ranking: Red Chinese toon > Red-leaved Chinese
toon > Sprout Chinese toon > Black-oil Chinese toon > Red-oil Chinese toon > Brown
Chinese toon > Green-oil Chinese toon > Green Chinese toon > Peach Chinese toon [3].
Table 2. Amino acids found in T. sinensis buds.
Amino Acid Content (%) Amino Acid Content (%)
Threonine * 1.04 Aspartate 2.29
Valine * 1.39 Serine 1.28
Methionine * 0.58 Glutamic acid 7.24
Leucine * 1.13 Proline 2.75
Isoleucine * 1.97 Glycine 1.44
Phenylalanine * 1.19 Alanine 1.49 *
Lysine * 1.21 Cystine —
Tryptophan *
Arginine
—
1.15
Tyrosine
Histidine
0.89
0.39
Note: * Represents essential amino acids.
Diversity 2022,14, 572 5 of 14
Table 3. Amino acids found in old leaves of T. sinensis.
Amino Acid Content (%) Amino Acid Content (%)
Threonine * 0.74 Aspartate 1.11
Valine * 0.83 Serine 0.80
Methionine * 0.30 Glutamic acid 2.60
Leucine * 1.36 Proline 0.73
Isoleucine * 0.72 Glycine 0.80
Phenylalanine * 0.86 Alanine 0.94
Lysine * 0.66 Cystine 0.04
Tryptophan * — Tyrosine 0.68
Arginine 0.89 Histidine 0.16
Note: * Represents essential amino acids.
Table 4. The content of main mineral elements in old leaves of T. sinensis (content per gram).
Zn (mg) Cu (mg) Mn (mg) Na (mg) Fe (mg) Mg (mg) K (mg) Ca (mg)
0.059 0.022 0.047 0.807 0.187 3.504 20.300 5.931
Many researchers have reported that the content of nutritional composition in different
provenances and harvest periods is different. For instance, Yang et al. investigated the
changes of nutritional composition at four different harvest periods from six different
provenances [
53
], and Wang et al. analyzed the nutritional composition at five different
harvest periods from five different provenances [
54
]. Both studies found significant dif-
ferences in content of amino acids, proteins, soluble sugars, and vitamin C in T. sinensis
at the same period from different provenances or at different harvest periods from the
same provenance.
5. Characteristic Chemical Compounds of T. sinensis
5.1. Volatile Compounds
The headspace solid phase microextraction (HS-SPME) and gas chromatography-
mass spectrometry (GC-MS) technologies can be used to extract and analyze the volatile
components of plants. Yang et al. (2016) used an ultrasonic-assisted method to extract
volatile components from T. sinensis leaves and identified 73 volatile compounds using
GC-MS. The main volatile compounds included arachidonic acid ethyl ester, benzothiazole,
pentadecanoic acid methyl ester, n-heneicosane, β-caryophyllene, benzoic acid hexylester,
1, 2-benzenedicarboxylic acid butyl octyl ester, limonene, heptacosane, n-hexadecanoic
acid, and others [
55
]. Ji et al. (2018) used HS-SPME and GC-MS techniques to identify
32 volatile compounds from T. sinensis leaves, and found that (3E)-3-Hexenyl acetate,
(Z)-Hex-3-en-1-ol, caryophyllene, and (Z)-Butanoic acid-3-hexenyl ester were the major
constituents [
56
]. Gao et al. (2016) used the same methods to identify volatile components
in T. sinensis leaves, flowers, and seeds, and further analysis showed 36 volatile compounds
in leaves, 37 volatile compounds in flowers, and 26 volatile compounds in seeds. Among
them, beta-Elemene, germacrene B, L-calamenene, and alpha-Cubebene were the most
common [
57
]. Comparing the volatile components of three T. sinensis varieties (Ximu red
from Yantai city in Shandong province, Jiaozuo red from Jiaozuo city in Henan province,
and Heiyou purple from Taihe county in Anhui province), Liu et al. (2013) discovered that
the Ximu and Jiaozuo red cultivars contain thiophenes and terpenes, although their exact
contents differ, and the Heiyou purple cultivar contains terpenes and esters [58].
5.2. Terpenoid Compounds
After the first terpenoid compound, toosendanin, was extracted in 1972, ongoing
research has identified various terpenoids in T. sinensis leaves; triterpenoids are main
type of terpenoid. Hu et al. (2020) used various chromatographic techniques (e.g., sil-
ica gel, Sephadex LH-20, MCI gel, and ODS gel) to isolate and characterize terpenoids
Diversity 2022,14, 572 6 of 14
from 80% ethanol extract of T. sinensis leaves; the results showed that eight terpenoids
could be extracted and identified from the leaf extract of T. sinensis: cedrelone, cedrodorol
B, toonayunnanin D, toonaciliatone D, toonaciliatone A, 8
β
-hydroxypimar-15-en-19-oic
acid methyl ester, 11
β
-acetoxyobacunol, and 11
β
-hydroxygedunin [
59
]. Yang et al. (2013)
extracted the triterpenoids betulinic acid and ursolic acid for the first time [
60
]. Two triter-
penoids, 6-acetoxyobaconicate and 7
α
-actoxydihydron, were first isolated and identified
from the leaves of T. sinensis [
61
]. Moreover, another study first extracted and identified
the terpenoids 11
β
-hydroxy-7
α
-oba-conylacetate and 11
β
-oxocneorin G from T. sinensis
leaves [62].
5.3. Flavonoid Compounds
Flavonoids are widely distributed in plants, and the flavonoid content in T. sinensis
leaves is 2~3 times than that of Ginkgo biloba L.. Zhao et al. (2016) used high-performance
liquid chromatography (HPLC) to extract four flavonoids (rutin, quercetin, kaempferol,
and gallic acid) from old leaves of T. sinensis [
63
]. Chen et al. (2019) separated and purified
extracts from old leaves using column chromatography and HPLC, then used nuclear
magnetic resonance (NMR) and infrared spectroscopy (IR) to identify substances such as
rutin, epicatechin, quercetin, isoquercetin, and guava glucoside [
64
]. Ge et al. (2017) used
ultra-high performance liquid chromatography to determine the flavonoid compounds
in T. sinensis shoots, ultimately detecting glycosides, rutinoside, myricitrin, hyperoside,
isoquercitrin, guaijaverin, astragalin, quercitrin, and afzelin [
65
]. Moreover, Miao et al.
(2016) found five flavonoids identified from the T. sinensis leaf extract using the NKA9
macroporous adsorption resin method [
66
]. The total flavonoid content in stems, leaves,
and flowers of T. sinensis plants were comparatively analyzed, and the results showed
that the total flavonoid content in the leaves was highest, followed by the flowers and
stems [67].
5.4. Phenylpropanoid Compounds
Phenylpropanoids commonly exist in natural plants, and mainly include lignins
and coumarins. Nine phenylpropanoid compounds have been isolated and identified
from different tissues of T. sinensis, namely, cedralins A and B [
68
], lyoniresinol, toonin
C (Figure 2), matairesinol [
6
], 7-dimethoxy-5-methylcoumarin [
69
], scopoletin [
70
], and
ficusesquilignans A and B [
71
]. Phenylpropanoid compounds often have pharmacological
activities, such as antiviral, anti-inflammatory, antitumor, and antibacterial activity.
Diversity 2022, 14, x FOR PEER REVIEW 6 of 14
After the first terpenoid compound, toosendanin, was extracted in 1972, ongoing re-
search has identified various terpenoids in T. sinensis leaves; triterpenoids are main type
of terpenoid. Hu et al. (2020) used various chromatographic techniques (e.g., silica gel,
Sephadex LH-20, MCI gel, and ODS gel) to isolate and characterize terpenoids from 80%
ethanol extract of T. sinensis leaves; the results showed that eight terpenoids could be ex-
tracted and identified from the leaf extract of T. sinensis: cedrelone, cedrodorol B,
toonayunnanin D, toonaciliatone D, toonaciliatone A, 8β-hydroxypimar-15-en-19-oic acid
methyl ester, 11β-acetoxyobacunol, and 11β-hydroxygedunin [59]. Yang et al. (2013) ex-
tracted the triterpenoids betulinic acid and ursolic acid for the first time [60]. Two triterpe-
noids, 6-acetoxyobaconicate and 7α-actoxydihydron, were first isolated and identified
from the leaves of T. sinensis [61]. Moreover, another study first extracted and identified
the terpenoids 11β-hydroxy-7α-oba-conylacetate and 11β-oxocneorin G from T. sinensis
leaves [62].
5.3. Flavonoid Compounds
Flavonoids are widely distributed in plants, and the flavonoid content in T. sinensis
leaves is 2~3 times than that of Ginkgo biloba L.. Zhao et al. (2016) used high-performance
liquid chromatography (HPLC) to extract four flavonoids (rutin, quercetin, kaempferol,
and gallic acid) from old leaves of T. sinensis [63]. Chen et al. (2019) separated and purified
extracts from old leaves using column chromatography and HPLC, then used nuclear
magnetic resonance (NMR) and infrared spectroscopy (IR) to identify substances such as
rutin, epicatechin, quercetin, isoquercetin, and guava glucoside [64]. Ge et al. (2017) used
ultra-high performance liquid chromatography to determine the flavonoid compounds in
T. sinensis shoots, ultimately detecting glycosides, rutinoside, myricitrin, hyperoside,
isoquercitrin, guaijaverin, astragalin, quercitrin, and afzelin [65]. Moreover, Miao et al.
(2016) found five flavonoids identified from the T. sinensis leaf extract using the NKA9
macroporous adsorption resin method [66]. The total flavonoid content in stems, leaves,
and flowers of T. sinensis plants were comparatively analyzed, and the results showed
that the total flavonoid content in the leaves was highest, followed by the flowers and
stems [67].
5.4. Phenylpropanoid Compounds
Phenylpropanoids commonly exist in natural plants, and mainly include lignins and
coumarins. Nine phenylpropanoid compounds have been isolated and identified from
different tissues of T. sinensis, namely, cedralins A and B [68], lyoniresinol, toonin C (Fig-
ure 2), matairesinol [6], 7-dimethoxy-5-methylcoumarin [69], scopoletin [70], and fi-
cusesquilignans A and B [71]. Phenylpropanoid compounds often have pharmacological
activities, such as antiviral, anti-inflammatory, antitumor, and antibacterial activity.
HO
O
O
O
O
O
OH
Figure 2. Structure of toonin C.
Diversity 2022,14, 572 7 of 14
6. Pharmacological Characteristics of T. sinensis
The medicinal use of T. sinensis was first recorded in the Tang Materia Medica, which
is a famous Traditional Chinese Medicine (TCM) monograph written in Tang dynasty
China; this plant has thus been used as an herbal medicine for thousands of years [
72
,
73
].
The “Compendium of Materia Medica” and “Dictionary of Traditional Chinese Medicine”
introduced the medicinal uses of the roots, bark, petioles, leaves, fruits, and seeds of
T. sinensis
[
74
,
75
]. In Chinese folk medicine, T. sinensis is described as an herbal medicine
with good anti-inflammatory, detoxifying, and hemostatic effects, and it was commonly
used to treat enteritis, dysentery, urinary tract infections, leukorrheal diseases, and skin
itch [
76
]. Modern studies of T. sinensis have mainly focused on the extraction and identi-
fication of bioactive components from the leaves of T. sinensis [
77
,
78
], while few studies
have reported the bioactive ingredients in the bark and seeds [
79
]. Extensive studies have
shown that bioactive components from T. sinensis possess numerous health benefits, such
as antiviral, antibacterial, antioxidant, anti-cancer, anti-inflammatory, and hypoglycemic
effects [80–84].
6.1. Antioxidant Effect
Previous research reports have indicated that the extracts of T. sinensis are natural
antioxidant agents [
85
,
86
]. Several reports have shown that phenolic compounds in the
extract of T. sinensis have the ability to scavenge free radicals [
87
–
89
]. In addition, Hsieh
et al. (2004) reported that extract of T. sinensis has antioxidant effects on hydrogen peroxide-
induced oxidative stress [90].
6.2. Antiviral and Antibacterial Effect
T. sinensis possess notable antiviral and antibacterial effects. Chen et al. found that
extract of T. sinensis leaves had antiviral activity against SARS-CoV
in vitro
, with an IC50
value of 30
µ
g
·
mL
−1
[
91
]. You et al. (2013) reported that extract of T. sinensis leaves
could be used an alternative treatment and prophylaxis against the H1N1 virus [
92
]. In
addition, the extract of T. sinensis leaves has been found to possess promising antibacterial
potential against E. coli,Salmonella, and Staphylococcus [
93
,
94
]. At present, the antiviral and
antibacterial effects of T. sinensis are an increasing concerned of the pharmaceutical industry.
6.3. Anti-Inflammatory Effect
Many natural anti-inflammatory products isolated form the extracts of T. sinensis
have been reported, and play important roles in preventing and treating inflammatory
disease [
95
]. In 2012, Yang and Chen (2012) published a research report showing that total
polyphenols extracted from the seeds of T. sinensis had a significant effect on the treatment
of rat arthritis [
96
]. Chen et al. (2017) reported 7-deacetylgedunin (7-DGD) extracted from
the fruit of T. sinensis, conducted
in vivo
and
in vitro
tests on mice, and the results showed
that 7-DGD alleviated mice mortality induced by LPS [
97
]. This substance improves
inflammation by activating the Keap1/Nrf2/HO-1 signaling pathway. In addition, many
natural substances isolated from T. sinensis have been reported to possess notable anti-
inflammatory effects [98,99].
6.4. Anti-Cancer Effect
As a natural anti-cancer drug, extract of T. sinensis is attracting increasing atten-
tion. Zhang et al. (2014) extracted four compounds from T. sinensis leaves (quercetin-
3-O-
α
-L-rhamnopyranoside, kaempferol-3-O-
α
-L-rhamnopyranoside, 1,2,3,4,6-penta-O-
galloyl-
β
-D-glucopyranose and ethyl gallate), and reported that Kaempferol-3-O-
α
-L-
rhamnopyranoside can inhibit the proliferation of HepG
2
human liver cancer cells and
MCF-2 human breast cancer cells as well as induce apoptosis [
100
]. The leaves of T. sinensis
are rich in gallic acid, an important anti-cancer substance that can promote DU145 prostate
cell apoptosis through the production of reactive oxygen species and mitochondrial path-
ways [
101
] as well as induce the apoptosis of oral squamous cancer cells by up-regulating
Diversity 2022,14, 572 8 of 14
the pro-apoptotic genes (TNF-
α
,TP53BP2 and GADD45A) and down-regulating the anti-
apoptotic genes (Survivin and cIAP1) [
102
]. In addition, betulonic acid and 3-oxours-12-en-
28-oic acid are both found in T. sinensis, which block the proliferation of MGC-803 and PC3
cancer cells and induce their apoptosis through the mitochondrial p53, bax, caspase 9, and
caspase 3 pathways [103].
6.5. Hypoglycemic Effect
For nearly twenty years studies on the hypoglycemic effects of T. sinensis extracts have
been reported, which could be beneficial for diabetes patients. In 2003, Yang et al. (2013) re-
ported that ethanol extracts of T. sinensis leaf could enhance cellular glucose uptake in basal
and insulin-stimulated 3T3-L1 adipocytes [
104
]. Hsieh et al. (2005) reported the inhibitory
effect of T. sinensis extracts on LDL glycation induced by glucose and glyoxal [
105
]. Two
studies have indicated that flavonoids of T. sinensis might be the active constituents corre-
sponding to the hypoglycemic effects of this plant [
106
,
107
]. Furthermore, studies on the
extract of T. sinensis have revealed that the mechanisms of TSL stimulating glucose uptake
and ameliorating insulin resistance might be related to AMPK activation in skeletal muscles
and to up-regulation of PPARγand normalized adiponectin in adipose tissues [108].
7. Research on Genes and Omics
7.1. Function Genes
T. sinensis is rich in lignin and anthocyanin, two substances that are important in-
dicators of bud quality. Cinnamic alcohol-CoA reductase (CCR) and cinnamyl alcohol
dehydrogenase (CAD) are the key enzymes in lignin biosynthesis, and chalcone isomerase
(CHI) and anthocyanidin reductase (ANR) are required for plant anthocyanins biosynthe-
sis. Based on the RNA-seq data of T. sinensis,TsCCR [
109
], TsCCR1 [
110
], TsCAD1 [
111
],
TsCHI [
112
], TsANR [
113
] were identified and cloned. The TsCCR gene contained an open
reading frame of 975 bp and encoded putative polypeptides of 324 amino acid residues [
109
],
and the TsCCR1 gene contained an open reading frame of 924 bp and encoded putative
polypeptides of 307 amino acid residues [
110
]. The TsCAD1 gene contained an open reading
frame of 1,068 bp and encoded putative polypeptides of 355 amino acid residues [
111
]. The
TsCHI gene contained an open reading frame of 717 bp and encoded putative polypeptides
of 238 amino acids [
112
]. The TsANR gene contained an open reading frame of 1011 bp and
encoded putative polypeptides of 336 amino acids [113].
Few studies have reported the expression patterns of the four genes (TsCCR,TsCAD1,
TsCHI, and TsANR) in different tissues of the T. sinensis plant; the results showed that the
expression level of TsCCR and TsCHI genes in stems were significantly higher than those in
roots and leaves, and the transcript level of TsCAD1 gene in roots was significantly higher
than in the stems and leaves. The results of real-time PCR showed the highest relative
expression of TsANR gene in the leaves of T. sinensis seedlings.
Moreover, the expression pattern of these four genes under different stress treatments
were investigated, and the results showed that the expression pattern of the TsCCR gene
was first temporarily up-regulated and then down-regulated after cold treatment, which
is the opposite of the expression pattern of this gene during heat treatment. During a salt
stress treatment (200 mmol
·
L
−1
NaCl), TsCCR expression decreased significantly in the
first 4 h, then increased rapidly, decreased, increased, and then decreased again during
200 g
·
L
−1
PEG6000 drought stress treatment [
109
]. During 24 h 38
◦
C heat treatment,
TsCAD1 expression first decreased and then increased significantly, while it first increased
and then decreased during 24 h 4
◦
C cold treatment. TsCAD1 expression first decreased,
then increased, and then decreased again during 24 h drought stress treatment (200 g·L−1
PEG 6000), although the relative expression level was lower than control. The expression
trend during a 200 mmol
·
L
−1
NaCl salt stress treatment for 24 h first decreased and then
increased, although the relative expression level was lower than the control [
111
]. Under
high temperature (38
◦
C), drought stress (200 g
·
L
−1
PEG 6000 solution) and salt stress
(200 mmol
·
L
−1
NaCl solution), TsCHI expression was higher than that of the control, and
Diversity 2022,14, 572 9 of 14
showed an upward trend as the processing time was extended [
112
]. These results provide
a theoretical basis for genetically engineering T. sinensis to cultivate resistances against
extreme environmental conditions. With 24 h of high temperature treatment (38
◦
C), TsANR
gene expression increased significantly at 1 h, then returned to the level of control [113].
7.2. Omics
T. sinensis omics research has mainly focused on genomic and transcriptomic studies.
Ran et al. (2020) sequenced the transcriptomes of the buds of the T. sinensis varieties
‘Heiyouchun’ and ‘Qingyouchun’ during four developmental periods, then analyzed the
expression pattern of anthocyanin biosynthesis genes. Among the key genes expressed in
anthocyanin synthesis by KEGG analysis, five genes, namely, phenylalanine ammonia lyase
(PAL), coumarin-Coa ligase (4CL), Chalketone synthase (CHS), flavonoid 3-hydroxylase
(F3
0
H), and anthocyanin synthase (ANS), were up-regulated in ‘Heiyouchun’, while C3’H
and flavonol synthase (FLS) were down-regulated in ‘Heiyouchun’ [
114
]. Zhao et al. (2017)
analyzed the RNA-seq data of ‘Heiyouchun’ sprouts and found 467 unigenes involved in
terpenoid biosynthesis related to flavor formation, including 226, 71, 86, and 84 unigenes
for terpenoid backbone, monoterpenoid, sesquiterpenoid (triterpenoid), and diterpenoid
biosynthesis, respectively [
115
]. Sui et al. (2019) analyzed the RNA-seq data of young leaves
and mature leaves of T. sinensis, and found that the KEGG pathways for phenylpropanoid,
naringenin, lignin, cutin, suberin, and wax biosynthesis were significantly enriched in
mature leaves [116].
Xiang et al. (2021) assembled the complete T. sinensis chloroplast genome using second-
generation high-throughput sequencing technology. The chloroplast genome contained
138 genes in total, including 89 protein-coding genes, seven rRNA genes, forty tRNA
genes, and two pseudogenes [
117
]. Liu et al. (2019) sequenced the chloroplast genome of
T. sinensis
using an Ilumina sequencing platform, and found that the chloroplast genome
is a characteristic four-party structure with a length of 157,228 bp which contains two
26,994 bp
inverted repeats (IRs), an 85,971 bp large single-copy, and a 17,269 bp small
single-copy. A total of 126 genes, including 82 protein-coding genes, 36 tRNA genes, and
eight rRNA genes, were identified [
118
]. Ji et al. (2021) reported a high-quality T. sinensis
genome assembly with scaffolds anchored to 28 chromosomes, an assembled length of 596
Mb, and a total of 34,345 genes predicted in the genome after homology-based and de novo
annotation analyses [119].
8. Conclusions
This paper comprehensively presents the storage, preservation, processing, nutrient
compounds, chemical compounds, phytochemistry, function genes, and omics of T. sinensis.
There are three kinds of storage and preservation methods of T. sinensis buds; although
they can extend the shelf life of T. sinensis, the nutrients in this vegetable plant experience
different degrees of loss. Because bio-preservation methods have the advantages of being
natural, safe, and simple, it has become one of the research hotspots of food preservation
technology. However, there has been less research on bio-preservation methods for T. sinen-
sis. Furthermore, in order to extend the consumption period of T. sinensis, it is processed
into a wide variety of foods.
Additionally, in the present review, volatile, terpenoids, phenylpropanoids, and
flavonoids from different parts of this plant were summarized; the existing pharmacologi-
cal investigations have revealed that this plant have a wide spectrum of pharmacological
effects, in particular for its anti-cancer and anti-inflammatory activities. However, a large
amount of pharmacological activity is associated with gallic acid, and the pharmacological
activity of other bioactive substances has been less studied. Therefore, the pharmacological
effects of other chemical components and the drug development of T. sinensis extracts need
a great deal of additional detailed research.
At present, research on genes of T. sinensis mainly focuses on two aspects, namely,
anthocyanin-related genes and lignin-related genes. In the storage process, T. sinensis is
Diversity 2022,14, 572 10 of 14
prone to anthocyanin degradation and lignin accumulation, which affects the edible taste
of T. sinensis buds. By studying anthocyanin-related genes and lignin-related genes, the
problems of anthocyanin degradation and lignin accumulation during the shelf life of
T. sinensis
buds can be further solved by genetic means. This basic research can provide a
certain theoretical basis for germplasm innovation with T. sinensis.
In conclusion, this paper highlights the importance of this plant and provides direction
for future food and drug development and germplasm innovation with T. sinensis by
providing detailed information T. sinensis as a plant diversity resource.
Author Contributions:
Conceptualization, Q.Z., P.-H.M. and G.-F.T., J.Z.; methodology, Q.Z., G.-F.T.,
X.-L.Z. and S.-H.Z.; data curation, Q.Z., S.-H.Z., K.W.; writing—original draft preparation, Q.Z. and
G.-F.T.; writing—review and editing, Q.Z., G.-F.T., X.-L.Z., S.-H.Z., K.W., visualization, Q.Z.; funding
acquisition, P.-H.M., G.-F.T. and J.Z. All authors have read and agreed to the published version of
the manuscript.
Funding:
This research was funded by the Project of Guizhou Academy of Agricultural Sciences
(Support of Guizhou Academy of Agricultural Sciences No. [2021] 05, Germplasm Resources of
Guizhou Academy of Agricultural Sciences No. [2020] 10); Jilin Agricultural University High Level
Research Grant (JAUHLRG20102006); High Level Innovative Talents Training, Hundred Level Talents
Project (Qiankehe talent [2015] 4024).
Institutional Review Board Statement: Not applicable.
Data Availability Statement: Not applicable.
Acknowledgments: Data can be found within the manuscript.
Conflicts of Interest: There is no conflict of interest.
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