Theoretical phytoextraction rates evaluating the application potential of two Cd accumulators from Crassulaceae for cleaning Cd-contaminated farmland

Xumei Huang; Yanshuang Li; Ngueuyim Nono Josy Karel; Haisheng Tang; Na Hu; Xiong Li; Xumei Huang; Yanshuang Li; Ngueuyim Nono Josy Karel; Haisheng Tang; Na Hu; Xiong Li

doi:10.48130/cas-0024-0018

2024 Volume 4

Article Contents

Abstract

References

Next Previous

ARTICLE Open Access

Theoretical phytoextraction rates evaluating the application potential of two Cd accumulators from Crassulaceae for cleaning Cd-contaminated farmland

1.
School of Forestry, Southwest Forestry University, Kunming 650224, China
2.
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China
3.
Honghe Center for Mountain Futures, Kunming Institute of Botany, Chinese Academy of Sciences, Honghe 654400, China
4.
School of Ecology and Environment, Yunnan University, Kunming 650500, China
5.
University of Chinese Academy of Sciences, Beijing 100049, China
^# Authors contributed equally: Xumei Huang, Yanshuang Li

More Information

Corresponding author: lixiong@mail.kib.ac.cn

Received: 01 August 2024
Revised: 09 December 2024
Accepted: 16 December 2024
Published online: 30 December 2024
Circular Agricultural Systems 4, Article number: e018 (2024) | Cite this article

Abstract

Phytoextraction based on heavy metal accumulators is a promising strategy for cleaning heavy metal-contaminated arable soils for food safety. In this study, the cadmium (Cd) tolerance and accumulation capacities of two Crassulaceae species were explored via pot experiments. The morphological and physiological results revealed that both Phedimus aizoon and Kalanchoe blossfeldiana could cope with heavy soil Cd contamination (50 mg·kg⁻¹) at least by triggering an antioxidant system for Cd detoxification. After 3 months of growth, the Cd concentrations in the dry leaves, stems, and roots of P. aizoon were 212.0, 104.0, and 83.5 mg·kg⁻¹_, and of K. blossfeldiana were 101.5, 53.7, and 125.0 mg·kg⁻¹, respectively. The bioconcentration factor (BCF) and translocation factor (TF) in P. aizoon leaves and stems were greater than the threshold of Cd hyperaccumulators, whereas the TFs in K. blossfeldiana leaves and stems was lower than this threshold. These results revealed that P. aizoon is a potential Cd hyperaccumulator and K. blossfeldiana is a high-Cd-accumulating species. To evaluate the Cd phytoextraction potentials of P. aizoon and K. blossfeldiana in the field, a new index, the theoretical phytoextraction rate (TPR), was introduced through the integration of the Cd accumulation level, plant biomass, and plant shape and size. Interestingly, it was found that K. blossfeldiana rather than P. aizoon had a higher TPR value. These findings demonstrate the decisive effect of plant shape on planting density is of importance for screening ideal phytoextraction resources in addition to plant biomass and heavy metal accumulation levels. This study offers new resources for phytoextraction of Cd-contaminated soils and a novel theoretical method to evaluate phytoextraction efficiency.
- Cadmium,
- Phytoremediation,
- Hyperaccumulator,
- Crassulaceae,
- Theoretical phytoextraction rate

Introduction

Huangqin tea (HQT, Fig. 1), also called Huangjin tea in Chinese, has a long history of consumption in China^[1]. It is a healthy herbal tea crafted from the aerial parts of Scutellaria baicalensis Georgi, S. scordifolia Fisch, S. amoena C. H. Wrigh, and S. viscidula Bung^[2−4]. Unlike traditional tea made from Camellia sinensis (L.) O. Kuntze, HQT lacks stimulating components and is renowned for clearing heat and dry dampness, eliminating toxins, promoting digestion, and soothing fire^[1,5]. It can be enjoyed both as a hot beverage and as a cold drink, and modern research suggests that HQT exhibits several pharmacological properties, such as anti-inflammatory, chemopreventive effects of colorectal cancer^[6], anti-aging^[7], cardiovascular protection, hypoglycemic effect, hypolipidemic effect, anti-tumor, anti-bacterial, anti-influenza virus, and enhance human resistance^[8−12]. The predominant compounds found in HQT are flavonoids and essential oils and its potential health benefits are likely attributed to the presence of distinctive flavonoids, including isocarthamidin-7-O-β-D-glucuronide, carthamidin-7-O-β-D-glucuronide, apigenin-7-O-β-D-glucopyranside, chrysin-7-O-β-D-glucuronide, scutellarin, baicalin, wogonoside, and chrysin^[13−18].

Figure 1. The aerial parts of S. baicalensis Georgi, dried and brewed Huangqin tea.

DownLoad: Full-Size Img PowerPoint

HQT is made using simple ingredients and has a straightforward preparation method. Traditionally, the above-ground portions of Scutellaria species have been utilized for crafting HQT, with the differentiation between stems and leaves remaining unessential. During the hot summer season (July to August), the aerial parts (stem, leaves, flowers) of these species of Scutellaria from a single source are collected and cut into small sections, which are then directly dried for later use. Alternatively, freshly harvested branch and leaf sections may undergo a transformative process through multiple rounds of steaming and subsequent drying within a steamer. Once suitably conditioned, they find their place within sealed containers, poised for extended storage periods. The brewing ritual commences by incorporating 7−8 g of this tea into 2 L of water, with subsequent replenishments of water at intervals 2−3 times. As the brewing ritual concludes, HQT graces the senses with a resplendent golden infusion—earning it another name, 'Huangjin tea'.

HQT boasts a range of health advantages and is frequently gathered from the upper sections of Scutellaria species plants cultivated in the vicinity, intended for tea consumption. In recent years, large planting bases have been established in several regions, such as Beijing, Inner Mongolia Wuchuan, Yakeshi, Hebei Chengde, Shanxi Province, and Shandong Province, to comprehensively develop S. baicalensis resources. HQT has gained more attention and is now produced by specialized operating companies in various grades, such as bulk tea, bagged tea, and unique tea culture^[12].

To provide up-to-date information on the chemical composition, bioactivity, and safety aspects of the Scutellaria genus from HQT, this review paper has collected related literature from various databases, such as PubMed, Web of Science, Sci Finder, Scopus, Baidu Scholar, China National Knowledge Internet (CNKI), Wanfang and Weipu Data. This paper aims to draw attention to the need for further research and application of HQT in preventing and managing certain chronic diseases.

Chemical components of Huangqin Tea

HQT can be derived from several Scutellaria species. S. baicalensis is the most extensively cultivated, with a significant biomass in its aerial parts. Consequently, the primary source of HQT is the aerial part of S. baicalensis, and research focused on these aerial parts is also the most extensive.

The aerial part and the root of S. baicalensis share similarities in their primary constituents, notably the significant presence of flavonoids, which are regarded as the main active components. However, there are specific chemical differences between the above-ground and underground parts of S. baicalensis. Our preliminary experiments have revealed the disparities in chemical composition between these two parts^[18]. Notably, the root of S. baicalensis finds its primary use in medicinal applications, characterized by notably higher expression levels of specific 4′-deoxyflavones compared to the aerial organs. In contrast, the above-ground parts of the plant are employed to prepare tea. This differentiation in utilizing these plant components reflects the accumulated wisdom of generations cultivated through extensive periods of tasting and experience.

This section provided an in-depth review of the chemical composition of the plant from which HQT is derived. Additionally, a specific emphasis on reviewing the aerial parts of S. baicalensis, which serve as the primary source of HQT has been placed.

Flavonoids

In the 1970s, researchers began to study the chemical composition of the aerial parts of S. baicalensis. The flavonoids are the most abundant chemical components in the aerial parts (flowers, stems, and leaves), and about 54 flavonoid compounds were identified (Table 1, Fig. 2). Most of them are flavonoids, dihydro flavonoids, and glycosides. The main glycoside-forming sugars are arabinose, glucose, and glucuronide, with the most abundant glucuronide glycosides. The optimization of extraction processes can yield a remarkable total flavonoid content of up to 5% in the stems and leaves of S. baicalensis^[19].

Table 1. Flavonoids of HQT.

Number	Name	Formula	Species	Ref.
1	2',5-Dihydroxy-3',6,7,8-tetramethoxyflavone	C₁₉H₁₈O₈	S. baicalensis	[17]
2	2',6-Dihydroxyflavone	C₁₅H₁₀O₄	S. baicalensis	[16]
3	3',4',5,5',7-Pentamethoxyflavone	C₂₀H₂₀O₇	S. baicalensis	[16]
4	4',5-Dihydroxy-3',5',6,7-tetramethoxyflavone	C₁₉H₁₈O₈	S. baicalensis	[22,27]
5	4',5-Dihydroxy-7-methoxyflavanone	C₁₆H₁₄O₅	S. baicalensis	[16]
6	5,4′-Dihydroxy-6,7,8,3′-tetramethoxyflavone	C₁₉H₁₈O₈	S. baicalensis	[17]
7	5,2′-Dihydroxy-6,7,8-trimethoxyflavone	C₁₈H₁₆O₇	S. baicalensis	[17]
8	5,2′-Dihydroxy-6,7,8,3′-tetramethoxyflavone	C₁₉H₁₈O₈	S. baicalensis	[17]
9	5,2′-Dihydroxy-7,8-dimethoxyflavone	C₁₇H₁₄O₆	S. baicalensis	[17]
10	5,2′-Dihydroxy-7,8,6′-trimethoxyflavone	C₁₈H₁₆O₇	S. baicalensis	[17]
11	5,6,7,3',4'-Pentahydroxyflavone-7-O-glucuronide	C₂₁H₂₀O₁₃	S. baicalensis	[13]
12	5,6,7,4'-Tetrahydroxydihydroflavone	C₁₅H₁₂O₆	S. baicalensis	[17]
13	5,6,7-Trihydroxy-4'-methoxyflavone	C₁₆H₁₂O₆	S. baicalensis	[15]
14	5,7-Dihydroxy-6-methoxyflavanon	C₁₆H₁₄O₅	S. baicalensis	[17]
15	5,7,4′-Trihydroxy-6-methoxyflavanone	C₁₆H₁₄O₆	S. baicalensis	[22]
16	5,7,4'-Trihydroxyflavanone	C₁₅H₁₂O₆	S. baicalensis	[13]
17	(2S)-5,7,8,4'-Tetrahydroxyflavanone 7-O-β-D-glucuronopyranoside	C₂₁H₂₀O₁₂	S. baicalensis	[21]
18	(2S)-5,6,7,4'-Tetrahydroxyflavanone 7-O-β-D-glucuronopyranoside	C₂₁H₂₀O₁₂	S. baicalensis	[21]
19	6-Hydroxyluteolin-7-O-glucuronide	C₂₁H₁₈O₁₃	S. baicalensis	[13]
20	7-Methoxychrysin	C₁₆H₁₄O₄	S. baicalensis	[16]
21	Apigenin	C₁₅H₁₀O₅	S. baicalensis, S. amoena, S. scordifolia, S. viscidula	[17,21−25]
22	Apigenin-4'-glucopyranside	C₂₁H₂₀O₁₀	S. baicalensis	[17]
23	Apigenin-6-C-glucoside-8-C-arabinoside	C₂₆H₂₈O₁₄	S. baicalensis	[13]
24	Apigenin-7-O-β-D-glucopyranside	C₂₁H₂₀O₁₀	S. baicalensis	[17]
25	Apigenin-7-O-β-D-glucuronide	C₂₁H₁₈O₁₁	S. baicalensis, S. amoena, S. scordifolia	[13,23,24]
26	Apigenin-7-O-methylglucuronide	C₂₂H₂₀O₁₁	S. baicalensis	[28]
27	Baicalein	C₁₅H₁₀O₅	S. baicalensis, S. amoena, S. scordifolia, S. viscidula	[22−25]
28	Baicalein-7-O-D-glucopyranside	C₂₁H₂₀O₁₀	S. baicalensis	[22]
29	Baicalin	C₂₁H₁₈O₁₁	S. baicalensis, S. amoena, S. scordifolia, S. viscidula	[16,23−25]
30	Carthamidin	C₁₅H₁₂O₆	S. baicalensis	[13,20]
31	Carthamidin-7-O-β-D-glucuronide	C₂₁H₂₀O₁₂	S. baicalensis	[22]
32	Chrysin	C₁₅H₁₀O₄	S. baicalensis, S. amoena, S. scordifolia	[13,21−24]
33	Chrysin-7-O-β-D-glucuronide	C₂₁H₂₀O₉	S. baicalensis, S. amoena	[23,29]
34	Dihydrobaicalin	C₂₁H₂₀O₁₁	S. baicalensis	[22,28]
35	Dihydrooroxylin A	C₂₁H₂₀O₁₁	S. baicalensis	[13]
36	Genkwanin	C₁₆H₁₂O₅	S. baicalensis	[16]
37	Isocarthamidin	C₁₅H₁₀O₆	S. baicalensis	[20,28]
38	Isocarthamidin-7-O-β-D-glucuronide	C₂₁H₂₀O₁₂	S. baicalensis	[28]
39	Isoschaftside	C₂₆H₂₈O₁₄	S. baicalensis	[13,16]
40	Isoscutellarein	C₁₅H₁₀O₆	S. baicalensis	[21,30]
41	Isoscutellarein 8-O-β-D-glucuronide	C₂₁H₁₈O₁₂	S. baicalensis	[21]
42	Kaempferol 3-O-β-D-glucopyranoside	C₂₁H₂₀O₁₁	S. baicalensis	[13,28]
43	Luteolin	C₁₅H₁₀O₆	S. baicalensis	[22,30]
44	Norwogonin-7-O-glucuronide	C₂₁H₁₈O₁₂	S. baicalensis, S. amoena	[13,17,23]
45	Oroxylin A	C₁₆H₁₂O₅	S. baicalensis, S. amoena	[17,23]
46	Oroxylin A-7-O-D-glucopyranside	C₂₂H₂₂O₁₀	S. baicalensis	[22,28]
47	Oroxylin A-7-O-β-D-glucuronide	C₂₂H₂₀O₁₁	S. baicalensis, S. amoena	[13,23]
48	Pinocembrin	C₁₆H₁₂O₅	S. baicalensis	[13]
49	Pinocembrin-7-O-glucuronide	C₂₁H₂₀O₁₁	S. baicalensis	[13,16,22]
50	Salvigenin	C₁₈H₁₆O₆	S. baicalensis	[21]
51	Scutellarein	C₁₅H₁₀O₆	S. baicalensis	[28]
52	Scutellarin	C₂₁H₁₈O₁₂	S. baicalensis, S. amoena, S. scordifolia, S. viscidula	[23−25,29]
53	Wogonin	C₁₆H₁₂O₅	S. baicalensis, S. amoena, S. scordifolia, S. viscidula	[21−25]
54	Wogonoside	C₂₂H₂₀O₁₁	S. baicalensis, S. viscidula	[13,25]

| Show Table

DownLoad: CSV

Figure 2. Chemical structure of flavonoids in HQT.

DownLoad: Full-Size Img PowerPoint

In 1976, Takido et al.^[20] isolated two flavanone derivatives, carthamidin and isocarthamidin, for the first time as natural products from the leaves of S. baicalensis. Later, Yukinori et al.^[21] identified two new flavanones, (2S)-5,7,8,4'-tetrahydroxyflavanone 7-O-β-D-glucuronopyranoside and (2S)-5,6,7,4'-tetrahydroxyflavanone 7-O-β-D-glucuronopyranoside), in the leaves of S. baicalensis. Eight compounds of chrysin, wogonin, apigenin, salvigenin, scutellarein, isoscutellarein, apigenin 7-O-glucuronide, and isoscutellarein 8-O-glucuronide were also isolated. Wang et al.^[15] used column chromatography to isolate seven flavonoids (wogonin, chrysin, 5,6,7-trihydroxy-4'-methoxyflavone, carthamindin, isocarthamidin, scutellarein, and chrysin 7-O-β-D-glucuronide) from a water extract of the leaves of S. baicalensis. Liu et al.^[13] identified 21 flavonoids in the stems and leaves of S. baicalensis by HPLC-UV/MS and NMR, and found one flavonone (5,6,7,3',4'-Pentahydroxyflavone-7-O-glucuronide) was a new compound. Zhao^[17] firstly isolated 5,6,7,4′-tetrahydroxyflavanone 7,5,7-dihydroxy-6-methoxyflavanone, oroxylin A, 5,4′-dihydroxy-6,7,8,3′-tetramethoxyflavone, 5,2′-dihydroxy-6,7,8,3′-tetramethoxyflavone, 5,2′-dihydroxy-7,8,6′-trimethoxyflavone, 5,2′-dihydroxy-7,8-dimethoxyflavone, 5,2′-dihydroxy-6,7,8-trimethoxyflavone, apigenin 4'-β-D-glucopyranoside, and apigenin-7-β-D-glucopyranoside from the aerial parts of S. baicalensis. Ma^[22] firstly isolated 5,7,4'-trihydroxy-6-methoxyflavone, 5,4'-dihydroxy-6,7,3',5'-tetramethoxyflavone, from stems and leaves of S. baicalensis. Wang et al.^[16] isolated 5,4'-dihydroxy-7-methoxyflavanone, genkwanin, 7-methoxychrysin, 3',4',5,5',7-pentamethoxyflavone from 60% ethanol extracts for stems and leaves of S. baicalensis for the first time. Also, the compounds of carthamidin-7-O-β-D-glucuronide, oroxylin A-7-O-β-D--glucuronide, and chrysin were isolated from this plant for the first time．

The concentration of these chemical components in HQT varies depending on the plant part utilized. Employing the HPLC-DAD method, Shen et al.^[18] established that the aerial parts (stems, leaves, and flowers) of S. baicalensis are rich in flavonoids, resembling the roots in composition but exhibiting significant disparities in content. The contents of isocarthamidin-7-O-β-D-glucuronide (106.66 ± 22.68 mg/g), carthamidin-7-O-β-D-glucuronide (19.82 ± 11.17 mg/g), and isoscutellarein-8-O-β-D-glucuronide (3.10 ±1.73 mg/g) were the highest in leaves. The content of apigenin-7-O-β-D-glucopyranoside (18.1 ± 4.85 mg/g) and chrysin-7-O-β-D-glucuronide (9.82 ± 5.51 mg/g) were the highest in flowers. HQT has a high content proportion of flavone glycosides, which is closely related to the activity of HQT. The concentrations of the nine main flavonoids in HQT infusions were measured using HPLC. The content of isocarthamidin-7-O-β-D-glucuronide (52.19 ± 29.81 mg/g) was the highest; carthamidin-7-O-β-D-glucuronide (31.48 ± 6.82 mg/g), chrysin-7-O-β-D-glucuronide (10.65 ± 0.40 mg/g) and apigenin-7-O-β-D-glucopyranside (5.39 ± 0.92 mg/g) were found at moderate levels in HQT samples. As for flavone aglycones, scutellarin (12.77 ± 1.14 mg/g), baicalin (1.88 ± 0.48 mg/g), isoscutellarein-8-O-β-D-glucuronide (2.84 ± 0.60 mg/g), wogonoside (0.23 ± 0.02 mg/g) and chrysin (0.03 ± 0.01 mg/g) has lower content in HQT^[6].

Although there are few studies on the chemical constituents of the aerial parts of S. amoena, S. scordifolia, and S. viscidula it has been shown that the compounds of the aerial parts are similar to S. baicalensis. The aerial parts of S. amoena contain the compounds of baicalein, baicalin, oroxylin A, oroxylin A-7-O-β-D-glucuronide, wogonin, chrysin, chrysin-7-O-β-D-glucuronide, norwogonin, 5,7-dihydroxy-6,8-dimethoxyflavone, scutellarin^[23]. Zhang et al.^[24] identified compounds of chrysin, wogonin, baicalein, apigenin, apigenin-7-O-β-D-glucoside, baicalin, and scutellarin in whole plants of S. scordifolia. The stems and leaves of S. viscidula all contain compounds of wogonoside, apigenin, baicalein, wogonin, baicalin, and scutellarin. The contents of baicalein, wogonoside, wogonin, and apigenin in the stem of S. viscidula were higher than those in the stem of S. baicalensis. In the leaves of the two species, the content of scutellarin was higher, while the content of other compounds was lower^[25]. The content of scutellarin in S. viscidula was stem (2.30%) > leaf (1.78%) > flowers (0.38%)^[26].

Essential oils

The aerial parts of S. baicalensis are rich in essential oils, and the taste of HQT is closely related to this. The flowers of S. baicalensis are thought to have a Concord grape aroma, while HQT has a bitter flavor with distinctive herbal notes. Extensive analysis has identified 145 components in the essential oil obtained from the aerial parts of S. baicalensis. These components span various chemical classes, such as alkanes, carboxylic acids, fatty acids, monoterpenes/oxygenated monoterpenes, sesquiterpenes triterpenoids and Vitamins (Supplemental Table S1), which have demonstrated their efficacy in combatting bacteria, reducing inflammation and inhibiting tumor growth^[27−31]. Among these, major constituents include germacrene D (5.4%−39.3%), β-caryophyllene (29.0%), caryophyllene (18.9%), eugenol (18.4%), caryophyllene (15.2%), caryophyllene oxide (13.9%), (E)-β-caryophyllene (11.6%), 5-en-3-stigmasterol (11.3%), carvacrol (9.3%), thymol (7.5%), vitamin E (7.4%), neophytadiene (7.3%), γ-elemene (6.2%), 1-octen-3-ol (6.1%), allyl alcohol (5.5%), bicyclogermacrene (4.8%), myristicin (4.7%), acetophenone (4.6%), α-amyrin (4.6%), β-amyrin (4.4%), germacrene d-4-ol (4.3%), spathulenol (4.2%), β-pinene (4.1%), α-humulen (4.0%), 1-vinyl-1-methyl-2-(1-methylvinyl)-4-(1-methylethylidene)-cyclohexane (4.0%) are found in the aerial parts of S. baicalensis from different places^[27−31].

Takeoka et al.^[27] identified 64 components in volatile components of S. baicalensis flowers by solid-phase microextraction and analyzed them by GC and GC-MS. These flowers were collected at San Francisco State University (USA). Among the flower volatiles, the content of β-caryophyllene, germacrene D, δ-cadinene, γ-muurolene, and γ-cadinene were more than 3%. The essential oil obtained from the stem of S. baicalensis is mainly composed of diphenylamine, 2,2-methylenebis (6-tert-butyl-4-methylphenol), bornyl acetate, β-caryophyllene, germacrene D and 1-octen-3-ol.^[32]. Gong et al.^[28] analyzed and identified the specific chemical constituents of the aerial parts of S. baicalensis by using GC-MS technology and identified 37 compounds in total, such as allyl alcohol, acetophenone, caryophyllene, α-humulene, germacrene D, and γ-elemene. The plant material was collected in the Qinling Mountains in China. Lu et al.^[29] found a big difference in essential oil components between the aerial and root of S. baicalensis from Kunming Botanical Garden, Yunnan Province (China). The aerial part of S. baicalensis mainly contained enols and sterols such as neophytadiene and vitamin E. However, it has the same compounds as the roots, such as nerolidol, hexadecanoic acid, 1,2-benzenedicarboxylic acid, squalene, stigmast-4-en-3-one, and partial alkanes. Recently, Wang et al.^[31] found the essential oil level of the aerial parts of S. baicalensis was 0.09% (v/w, based on fresh weight) while its density was 0.93 g/mL, and obtained 31 components accounting for 97.64% of the crude essential oil, including sesquiterpenoid, monoterpenoids, phenylpropanoids, and others. It is also reported that the major components of the essential oil from the aerial parts of S. baicalensis were myristicin, eugenol, caryophyllene, caryophyllene oxide, germacrene D, spathulenol, and β-pinene, with eugenol as the most abundant. The sample of the aerial parts were harvested from Tangshan City (China). The composition of S. baicalensis essential oils varies according to the plant part used, geographical location, and growing conditions.

Others

Zgórka & Hajnos^[33] identified the phenolic acid compounds of aerial parts of S. baicalensis by solid-phase extraction and high-speed countercurrent chromatography: p-coumaric acid, ferulic acid, p-hydroxybenzoic acid, and caffeic acid. Chirikova & Olennikov^[34] found that the aerial part of S. baicalensis contains 11 kinds of saturated fatty acids and nine kinds of unsaturated fatty acids, among which the palmitic acid content is the highest. Chlorogenic acid, fernlic acid, protocatechuic acid, vanillic acid, rosmarinic acid, caffeic acid, p-hydroxybenzoic acid, and p-coumaric acid were also detected.

Zhao ^[17] isolated four sterol compounds: β-sitosterol-3-O-β-D-glucoside, α-apinasterol, β-sitosterol, and four ester compounds: methoxyphaeophorbide, p-hydroxybenethyl ethanol hexadecanoic methyl ester, ethoxyphaeophorbide, and n-octadecanol, lutein from the aerial parts of S. baicalensis.

It is reported that flavonoids and diterpenes are the two main groups of active constituents in the genus Scutellaria. However, only one diterpene (scutebaicalin) was identified in the stems and leaves of S. baicalensis^[35].

By atomic absorption spectrophotometry, Yuan et al.^[36] determined the contents of 11 metal elements in different parts of S. baicalensis. It was found that the leaves and stems of S. baicalensis were rich in Mg, K, Cr, Ni, Co, Fe, Mn, and Pb. Meanwhile, Yan et al.^[37] developed an inductively coupled plasma mass spectrometry method and determined 23 kinds of inorganic elements in the stems and leaves of S. baicalensis from eight regions. Although there were no differences in the types of inorganic elements in the stems and leaves of S. baicalensis from the different areas, the content of these elements varied significantly. Among these elements, Fe, Zn, Cu, Mn, Cr, Co, Ni, Sr, B, and Ni were essential human body elements. The content of Al (516.83 μg/g) and Fe (700.62 μg/g) was the highest, while the content of B (31.54 μg/g), Ti (23.10 μg/g), Mn (65.64 μg/g), Sr (62.27 μg/g), and Ba (89.68 μg/g) was relatively high.

Olennikov et al.^[38] studied the water-soluble polysaccharides from the aerial parts of S. baicalensis from Russia and found that the polysaccharides from S. baicalensis gradually accumulated before flowering and progressively decreased after flowering.

Yan et al.^[39] found that the stems and leaves of S. baicalensis were rich in amino acids, and there was no difference in the kinds of amino acids among different producing areas, but there was a significant difference in the contents of amino acids. The content of proline, threonine, glutamic acid, lysine, glutamine, and arginine was higher, and the content of methionine, hydroxyproline, and citrulline was low．

Functional properties

Several studies have focused on the functional properties of HQT, with increasing attention given to the aerial parts of S. baicalensis as the main raw material for HQT production. S. baicalensis stems and leaves flavonoids (SSF) are considered the functional components of HQT. Modern pharmacology has shown that the flavonoids extracted from the stem and leaf of S. baicalensis have been found to possess anti-inflammatory, anti-bacterial, antiviral, antipyretic and analgesic, anti-tumor, hepatoprotective, antioxidant, hypoglycemic, hypolipidemic, detoxification, myocardial ischemia protection, brain injury protection, and immunomodulatory effects. However, few studies have been conducted on the individual flavonoid compounds in the total flavonoid extract from S. baicalensis. Therefore, this paper aims to summarize and supplement the current research on the functional properties of HQT and its primary raw material (S. baicalensis) extract.

Anti-inflammatory activity

Injury and infection could lead to inflammation, which plays a key role in the accelerated pathogenesis of immune-mediated disease^[40]. Tong et al.^[41], Zhou et al.^[42], and Zhao et al.^[43] found that S. baicalensis stem-leaf total flavonoid (SSTF) could inhibit acute exudative inflammation caused by xylene, glacial acetic acid, and egg white and also have a significant inhibitory effect on chronic inflammatory of granulation tissue hyperplasia. Wang et al.^[44] observed the effect of SSTF on the aerocyst synovitis of the rat model and found that it could reduce capillary permeability, reduce the aggregation of neutrophils and basophils in tissues, reduce histamine, bradykinin, and other substances that increase vascular permeability, which is conducive to the recovery of vascular permeability in inflammation. Studies have shown that the SSTF significantly inhibits specific and non-specific inflammatory responses and can regulate the body's cellular and humoral immune functions. The mechanism of action is closely related to the effective reduction of capillary permeability, inhibition of PGE2 and NO synthesis in vivo, reduction of TNF-α expression, and reduction of inflammatory exudation^[45,46]. SSTF (200 mg/kg) could balance the ${\text{CD}^+_4}$ Tlymphocyte subsets Th1/Th2 cells and the related cytokines IL-10 and IFN-γ in the rheumatoid arthritis model^[47]. SSTF (17.5, 35 and 70 mg/kg for 38 d) could significantly improve the impairment of relearning ability and retention ability on memory impairment and nerve inflammation in chronic cerebral ischemia rats, which might be due to the inhibition of the proliferation of astrocyte and balanced the expression of the inflammatory factors in the brain^[48]. Besides, the extract of S. baicalensis stem-leaf shows anti-inflammation effects both in vitro and in vivo. In cultured macrophage cells (RAW 264.7), the extract of S. baicalensis stem-leaf showed a strong anti-inflammation effect, which inhibited the expression of IL-1β. Similarly, it suppressed the LPS-induced transcriptional activity mediated by NF-κB in fish aquaculture^[49]. S. baicalensis stems and leaves (3, 6, and 12g /kg, gavage for 7 d, once per day) have anti-inflammatory effects on 2% carrageenan-induced acute pleurisy in rats, and the mechanism of action may be related to the reduction of the production of inflammatory factors and the down-regulation of TRPV1 signaling protein^[50]. The combination of S. baicalensis stems- Polygonum cuspidatum (3.5, 7, and 14 g/kg, gavage for 7 d) has a protective effect on lipopolysaccharide-induced acute lung injury rats, and its mechanism may be related to down-regulating the expression of TRPV1 and inhibiting the levels of TNF-α and IL-1β in inflammatory cells^[50]. It is also reported that S. baicalensis stem-leaf combined with Morus alba (4, 8, and 16 g/kg/d, gavage, 10 d) has a protective effect on rats with acute pneumonia induced by lipopolysaccharide, and the mechanism might be related to the reduction of inflammatory factors and the down-regulation of TRPV1 signaling pathway^[51]. Besides, the network pharmacology showed that S. baicalensis stem-leaf could prevent and control COVID-19 by intervening in 30 targets and 127 pathways, potentially preventing and treating inflammation caused by COVID-19^[52].

Based on the studies, S. baicalensis stem-leaf extract shows promising anti-inflammatory properties. These effects are likely mediated through a combination of factors, including the modulation of immune responses, reduction of inflammatory mediators, and potential interactions with signaling pathways like TRPV1. However, it's important to note that while these studies provide valuable insights, further research, including clinical trials, is needed to establish the full extent of its benefits and its potential for therapeutic applications in humans.

Anti-bacterial and antiviral activity

Scutellaria baicalensis stem and leaf aqueous extract exhibit different degrees of inhibition of 36 strains from 13 kinds of bacteria, such as Staphylococcus aureus, Staphylococcus, Streptococcus pneumoniae, alpha-hemolytic streptococcus, beta-hemolytic streptococcus and Escherichia coli. This shows that anti-bacterial activity against Staphylococcus aureus is strong (MIC₅₀ 0.94 g/L, MBC 0.94 g/L). In vivo (217 mg/kg), it protects against the death of mice infected by Staphylococcus aureus and shows a certain dose-dependence^[53]. Zhang et al.^[54] found that the stem and leaves of S. baicalensis against Staphylococcus aureus and Shigella dysenteriae with MIC values of 1 and 4 mg/mL, respectively. Besides, it is reported that the water extract of the aerial part of S. baicalensis could inhibit the growth of several common pathogenic bacteria in aquacultures, such as Aeromonas hydrophila, Edwardsiella tarda, Vibrio alginolyticus and V. harveyi^[49].

Zhao et al.^[55] found that the active part of the stem and leaf of S. baicalensis could inhibit the cytopathic effect caused by 10 kinds of viruses such as Coxsackie B virus, influenza virus, parainfluenza virus, adenovirus, respiratory syncytial virus, and herpes simplex virus. It is suggested that the active parts of the stem and leaf of S. baicalensis can be used for the prevention and treatment of influenza virus, parainfluenza virus, coxsackievirus, and other related infectious diseases.

These findings indicate that S. baicalensis stem and leaf extract possess anti-bacterial and antiviral properties, making it a potentially valuable natural resource for combating infections caused by various pathogens. However, while these results are promising, further research, including clinical trials, would be necessary to fully establish the effectiveness and safety of using S. baicalensis extract for preventing or treating bacterial and viral infections, including COVID-19.

Antipyretic and analgesic effect

In a series of studies, Tong et al.^[41] demonstrated that SSTF at a dosage of 20 mg/kg significantly reduced body temperature in rats with fever induced by subcutaneous injection of a 10% dry yeast suspension. Zhang et al.^[56] conducted research on the antipyretic effect of scutellarin, an extract from S. baicalensis stems and leaves, in febrile rabbits and observed an antipyretic substantial impact induced by pyrogen. Yang et al.^[57] conducted several animal experiments, where they discovered that intraperitoneal injection of effective doses of SSTF (42.2 and 84.4 mg/kg) exhibited a specific inhibitory effect on infectious fever in experimental animals. Moreover, intraperitoneal injection of appropriate SSTF doses (30.1, 60.3, and 120.6 mg/kg), as found in Yang et al.'s experiments^[58], effectively inhibited the pain response in experimental animals. Furthermore, Zhao et al.^[59] noted that SSTF exhibited a certain inhibitory effect on the pain response in experimental animals subjected to chemical and thermal stimulation.

These findings suggest that S. baicalensis stem and leaf extract may have antipyretic and analgesic effects, particularly its total flavonoid component. These effects could be beneficial for managing fever and providing pain relief. However, as with any natural remedy, further research, including controlled clinical trials in humans, is necessary to fully understand the effectiveness, safety, and optimal dosing of S. baicalensis extract for these purposes.

Neuroprotective effect

Amyloid protein (Aβ) has been widely recognized as the initiator of Alzheimer's disease (AD)^[60]. The SSTF can improve cognitive function and delay the process of dementia. SSTF has been found to exert neuroprotective effects in AD animal models through various mechanisms. Ye et al.^[61] demonstrated that oral administration of SSTF (50 mg/kg) could effectively improve cognitive function and reduce neuronal injury in Aβ_25-35-3s -induced memory deficit rats. The underlying mechanisms may involve inhibiting oxidative stress and decreasing gliosis^[62,63]. Furthermore, SSTF was shown to reduce Aβ-induced neuronal apoptosis by regulating apoptosis-related proteins Bax and Bcl-2^[64]. Subsequent studies further validated the neuroprotective effects of SSTF. Cheng et al.^[65] found that SSTF treatment inhibited neuronal apoptosis and modulated mitochondrial apoptosis pathway in composited Aβ rats. Ding & Shang^[66] found that the SSF improves neuroprotection and memory impairment in rats due to its inhibition of hyperphosphorylation of multilocus Tau protein in rat brains. SSTF has also been found to exert neurogenesis-promoting effects by regulating BDNF-ERK-CREB signaling^[12] and activating the PI3K-AKT-CREB pathway^[67].

In further studies, Ding et al.^[11] proposed that the effect of SSF on promoting neurogenesis and improving memory impairment may be related to the regulation of abnormal expression of Grb2, SOS1, Ras, ERK, and BDNF molecules in the BDNF-ERK-CREB signaling pathway. Zhang et al.^[68] found that SSF (25, 50, and 100 mg/kg) could significantly modulate okadaic-induced neuronal damage in rats, which provides a basis for evaluating SSF as a means to reduce tau hyperphosphorylation and Aβ expression in Alzheimer's disease. Cao et al.^[69] found that SSTF (100 mg/kg, 60 d) may alleviate tau hyperphosphorylation-induced neurotoxicity by coordinating the activity of kinases and phosphatase after a stroke in a vascular dementia rat model. Gao et al.^[70] demonstrated that the stems and leaves of S. baicalensis (SSF, 25, 50, and 100 mg/kg/d, 43 d) could inhibit the hyperphosphorylation of tau in rats' cerebral cortex and hippocampus induced by microinjection of okadaic acid, which may be related to the activities of protein kinase CDK5, PKA and GSK3β. Furthermore, Liu et al.^[67] demonstrated that SSF (35, 70, and 140 mg/kg/d, 43 d) improved composited Aβ-induced memory impairment and neurogenesis disorder in rats through activated the PI3K-AKT-CREB signaling pathway and up-regulated the mRNA and protein expression of TRKB, PI3K, AKT, CREB and IGF2. More recently, a new study demonstrated that SSF (35, 70, and 140 mg/kg) alleviated myelin sheath degeneration in composited Aβ rats, potentially modulating sphingomyelin metabolism^[71]. Collectively, these findings suggest that SSTF holds therapeutic potential for AD by targeting multiple Alzheimer's pathogenesis-related processes.

Li et al.^[72] confirmed that SSTF (5 mg/kg) could improve the behaviors and the numbers of dopaminergic neurons in the substantia nigra in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease in mice, and these beneficial activities appear to be associated with the reduction of the level of serum malondialdehyde.

These studies suggest that S. baicalensis stem and leaf extract have the potential to exert neuroprotective effects in various neurodegenerative conditions, including Alzheimer's disease and Parkinson's disease. These effects could be attributed to its ability to modulate oxidative stress, apoptosis, signaling pathways, and protein hyperphosphorylation. However, as with any potential therapeutic agent, further research is needed to establish the full extent of its benefits, optimal dosages, and mechanisms of action, as well as its potential applications in human patients.

Effects on cardiovascular and cerebrovascular diseases

In recent years, ischemic cerebrovascular disease has seriously threatened human health. Cerebral ischemia is one of the leading causes of death. It can occur in focal or global ischemia, with most cases associated with ischemic stroke^[73]. Neuronal protection against oxidative damage has been proposed as a potential therapeutic strategy to avoid damage during ischemic stroke^[74]. It is reported that SSTF can reduce neuronal apoptosis and free radical damage caused by heart and brain ischemia. Zhao et al.^[75] have found that the pretreatment of SSTF (100 mg/kg/d) can protect the ischemia-reperfusion myocardium by enhancing the activity of the anti-oxidative enzyme, inhibiting lipid peroxidation and attenuating the oxygen-free radicals-mediated damage to the myocardium in rats. In further studies, Zhao et al.^[76] proposed that SSTF (50, 100, or 200 mg/kg/d, 7 d) pretreatment could alleviate the neuronal damage incurred by ischemia-reperfusion, demonstrating a neuroprotective effect in focal ischemia-reperfusion rat model, which may involve the prohibition of the apoptosis of the neurons. Yu et al.^[77] confirmed that SSTF (17.5, 35, and 70 mg/kg/d, 7 d) could attenuate cardiomyocyte apoptosis during ischemia reperfusion injury by down-regulating the protein expression of the JAK2 gene. Qin et al.^[78] found that SSF (17.5, 35, and 70 mg/kg/d, 38 d) can decrease the expression of the NMDAR in hippocampus, and increase the expression of VEGF in the cerebral cortex of chronic cerebral ischemia rats.

Focal cerebral ischemia-reperfusion can result in neuronal loss but strongly promotes activation and proliferation of hippocampal glial cells. Losing hippocampal neurons is considered one of the basic pathological mechanisms of cognitive impairment^[79]. Zhao et al.^[79] found that the pretreatment with SSTF (100 and 200 mg/kg) could improve neurological function after focal cerebral ischemia-reperfusion injury, with preventive and protective effects. Shang et al. found flavonoids from S. baicalensis (35−140 mg/kg) could attenuate neuron injury and improve learning and memory behavior in rats with cerebral ischemia/reperfusion^[80]. In further studies, Kong et al.^[81] found that the mechanisms of the protective effects on the brain against cerebral ischemia/reperfusion injury of SSTF may involve decreasing the content of brain water, increasing microvascular recanalization, reducing the apoptosis of hippocampal neurons, and attenuating free radical damage. Bai et al.^[82] proposed that SSTF (100 mg/kg/d, 7 d) could protect the neurological function in rats following I/R injury by alleviating the damage to the ultrastructure of cerebral cortex neurons and synapse. Yan et al.^[83] found that SSTF (100 mg/kg/d, 7 d) pretreatment can exert preventive, protective effects on cerebral tissue by relieving brain edema, decreasing neural damage, promoting microvascular repatency, and increasing enzyme activity. It has been reported that the SSTF may protect neurons and their synaptic structures in multiple ways, but whether this mechanism enhances the resistance of neurons to damage or increases the repair function remains to be further explored.

Essential hypertension is a common chronic cardiovascular disease, which can lead to multiple target organ damage, such as heart, brain, and blood vessels. It is a risk factor for coronary heart disease, heart failure, and other cardiovascular diseases. It is reported that SSTF (17.5, 35.0, and 70 0 mg/kg, 8 weeks) can inhibit myocardial remodeling in primary hypertensive rats, and the medium dose exerts the best inhibitory effect, and the mechanism may be related to inflammatory response induced by inhibiting the NF-κB signaling pathway^[84].

S. baicalensis stem and leaf extract have the potential to provide neuroprotective effects in conditions related to ischemic cerebrovascular disease and hypertension. Its ability to modulate oxidative stress, inflammation, and apoptotic pathways appears to contribute to its beneficial effects. However, further research is needed to fully understand the mechanisms and optimal usage of SSTF for these therapeutic purposes.

Anti-aging effects

Aging is associated with the deterioration of physiological function and the decline of cognitive ability^[85]. It is reported that the alcohol extracts from roots, stems, leaves, and flowers of S. baicalensis (400 mg/kg, 7 weeks) could regulate the content of differential metabolites in urine samples of D-gal-induced aging-model rats to different degrees and play a certain role in improving the metabolic disorders of aging rats^[7]. A further study investigated the anti-aging effects and potential mechanisms of S. baicalensis leaves and flower extract. S. baicalensis leaves (400 and 800 mg/kg, 7 weeks) have an anti-aging effect, which can improve the acquired alopecia, slow response, and other characteristics of aging rats, increase the spontaneous activity of aging rats, and reduce the damage of lipid peroxidation and glycosylation induced by D-galactose^[86]. The S. baicalensis flowers extract (400 and 800 mg/kg, 7 weeks) could effectively reverse the cognitive decline and oxidative stress injury and alleviate liver pathological abnormalities in the D -galactose-induced aging rats, which are involved in the glutamine-glutamate metabolic pathway^[85].

S. baicalensis extracts, particularly those from leaves and flowers, may have anti-aging properties by regulating metabolic disorders, improving cognitive function, reducing oxidative stress, and alleviating aging-related physiological abnormalities. However, further research is necessary to fully understand the mechanisms underlying these effects and to determine the potential of these extracts for human applications in addressing age-related issues.

Others

The SSTF (200 mg/kg d, 35 d) can reduce the joint damage of collagen-induced arthritis mice and balance the ${\text{CD}^+_4}$ T lymphocyte subsets Th17 and Treg cells^[87]． Besides, on the multiple sclerosis model, the SSTF (100, 200 mg/kg d, 16 d) displayed a protective effect on experimental autoimmune encephalomyelitis rats through a balance of the ${\text{CD}^+_4}$ Tlymphocyte subsets Th17 and Treg cells^[88]. Zhang et al.^[89] have found that SSTF attenuated EAE disease severity, accompanied by enhanced Treg frequency and level of Treg-associated cytokines (IL-10 and TGF-β), as well as downregulated Th17 frequency and expression of Th17-related cytokines (IL-17 and IL-23).

It is reported that the essential oils from the aerial parts of S. baicalensis showed toxicity against booklice (Liposcelis bostrychophila) with an LC50 of 141.37 μg/cm². The components of myristate, caryophyllene, eugenol, and caryophyllene oxide displayed dramatic toxicity against the L. bostrychophila, with LC₅₀ values of 290.34, 104.32, 85.75, and 21.13 μg/cm², respectively^[31].

Guo & Xu^[90] have found that SSTF could inhibit the proliferation of Hela cells obviously (p< 0.01). Tang et al.^[10] have found that SSTF could play an anti-colon cancer role by up-regulated the expressions of Cleaved Caspase-3 and the ratio of Bax/Bcl-2 (p < 0.05 and 0.01) and significantly down-regulated the expressions of MMP-2 and MMP-9 in HCT116 cells (p < 0.05 and 0.01). Recently, Shen et al.^[6] studied the chemopreventive effects of HQT against AOM-induced preneoplastic colonic aberrant crypt foci in rats and found HQT inhibits AOM-induced aberrant crypt foci formation by modulating the gut microbiota composition, inhibiting inflammation and improving metabolomic disorders.

Cardiovascular disease is one of the most important threats to human health. Hyperlipidemia is a major risk factor for atherosclerosis, which can cause various cardiovascular and cerebrovascular diseases. Different doses of SSTF (50, 100, and 200 mg/kg) can effectively reduce the body weight increase of rats with hypertriglyceridemia, reduce the serum levels of triglyceride(TG), total cholesterol(TC), low-density lipoprotein cholesterol (LDL-C) and high-density lipoprotein cholesterol (HDL-C), which indicate that SSTF has the effect of regulating blood lipid^[91].

Oxidative stress is important in developing tissue damage in several human diseases^[92]. The antioxidant capacities of separated organs (flower, leaf, stem, and root) of S. baicalensis were conducted by DPPH, ABTS+, and RP methods, respectively. The results showed that the antioxidant activity of the root (66.9 ± 0.3, 121.6 ± 0.5, and 80.2 ± 0.4 μg/mL) was the highest, followed by the leaf (68.4 ± 1.3, 128.2 ± 2.1, and 135.8 ± 2.0 μg/mL), stem (127.8 ± 3.1, 199.2 ± 1.7, and 208.2 ± 8.3 μg/mL) and flower (129.8 ± 6.3, 285.7 ± 4.7, and 380.3 ± 14.2 μg/mL)^[93]. The antioxidant activities of the extracts of the aerial part of S. baicalensis and separated organs were conducted by DPPH assay and reducing power method with the antioxidant ability 7.73–8.83 mg TE/g DW and 51.48–306.09 mg TE/g DW, respectively. The content of total polyphenols and total flavonoids were significantly positively correlated with the reducing power^[94]. Liu et al.^[95] found that the flavonoids extracted from the stems and leaves of S. baicalensis (SSF, 18.98, 37.36, and 75.92 μg/mL) could protect rat cortical neurons against H₂O₂-induced oxidative injury in a dose-dependent manner. Cao et al. found that SSTF could alleviate the damage of human umbilical vascular endothelial cells injured by H₂O₂ and reduce their apoptosis, which may be related to the increasing level of Bcl-2^[96].

Preventive treatment with SSTF (50, 100, and 200 mg/kg) could significantly inhibit the blood glucose increase induced by alloxan in mice, and SSTF treatment could reduce the blood glucose level in diabetic mice. Both the prevention group and the treatment group could increase the activity of serum superoxide dismutase and decrease the content of malondialdehyde^[97]. Liu et al.^[98] found that SSTF (75 and 150 mg/kg) could significantly reduce blood glucose and blood lipid and improve insulin resistance in type 2 diabetic rats with hyperlipidemia.

Yang et al.^[99] found that SSTF (35 mg/kg/d, 8 weeks) could resist hepatic fibrosis by inhibiting the expression of α-smooth muscle actin in Hepatic Stellate Cells. In vivo, it is reported that SSTF (50, 100, and 200 mg/kg) could significantly reduce alanine transaminase activities in serum, increase the expression of superoxide dismutase and reduce the content of malondialdehyde in acute hepatic injury mice induced by carbon tetrachloride and ethanol^[100].

These findings suggest that S. baicalensis stem and leaf extract hold promise in promoting various aspects of health, including immune modulation, antioxidant activity, anti-tumor effects, cardiovascular health, oxidative stress protection, and more. However, further research, including clinical studies, is necessary to better understand the full therapeutic potential and safety of these effects in human applications.

Safety issues

Flavonoids are considered the main active components in HQT. As the active substance basis of HQT, the safety of SSTF has also been investigated. After 90 d of oral administration of SSTF (0.5, 1, and 2 g/kg) to rats, no abnormal changes were observed in all indexes, and no delayed toxic reactions or obvious toxic reactions were observed, indicating that the toxicity of SSTF is low^[101]. The LD₅₀ value of SSTF was 14.87 g/kg is equivalent to 68.5 times the maximum dose in the pharmacodynamic test of mice, and the experiment confirms the safety of oral administration of the SSTF. Intraperitoneal injection of SST showed certain toxicity in mice, with an LD₅₀ value of 732.11 mg/kg^[102]. Liu et al.^[103] conducted a systematic safety assessment experiment on the aqueous extract of S. baicalensis stem and leaves based on the China National Standard 'Guidelines for the Safety Evaluation of Food Toxicology (GB15193-2014)'. The results indicated that S. baicalensis stem and leaves are non-toxic, non-teratogenic, and non-mutagenic. Acute toxicity tests in mice revealed a Maximum Tolerated Dose of 15.0 g/kg. A 90-d feeding trial showed no changes in toxicological damage in animals, even at a high dosage of 8.333 g/kg (equivalent to 100 times the recommended human daily intake), suggesting the safety and non-toxicity of consuming S. baicalensis stem and leaves. In addition, HQT has long been used in folklore, and no toxicity has been reported.

These findings collectively indicate that HQT is generally safe for consumption. However, as with any herbal product, it's important to follow recommended dosages and consult healthcare professionals, especially for individuals with pre-existing health conditions or medications.

Conclusions and future perspectives

In recent years, HQT, a non-Camellia tea with a long history in China, has attracted attention due to its diverse pharmacological activities. Among various Scutellaria species, S. baicalensis is the most extensively studied and cultivated source for HQT. The aerial parts, including flowers, stems, and leaves, serve as the principal source of HQT preparation. HQT are rich in flavonoids and volatile components with various beneficial effects. To date, about 295 compounds have been identified from HQT, including approximately 54 flavonoid compounds and 145 volatile components identified online. The current research on the activity of HQT primarily focuses on flavonoid compounds, with limited studies on the larger quantity of volatile oil compounds.

Additionally, the processing and brewing techniques used to prepare HQT may influence the bioactivity of its flavonoid content, although few studies have investigated this. More research is necessary to optimize the processing and brewing techniques to maximize the health benefits of HQT. Comparative studies reveal that the aerial parts of S. baicalensis, while sharing similarities with the roots, contain varying flavonoid compositions. Limited research on S. scordifolia, S. amoena, and S. viscidula, indicates the presence of comparable flavonoid compounds in their aerial parts. Although individual flavonoids like baicalin, wogonin, and scutellarin have demonstrated various therapeutic properties, it is essential to consider the synergistic effects of these compounds when consumed together in the form of tea. These findings contribute to laying the groundwork for quality assessment of HQT and offer insights into potential health benefits.

HQT is mainly derived from the aerial parts of S. baicalensis. Recent studies have increasingly recognized the pharmacological value of the aerial parts of S. baicalensis. Preliminary pharmacological studies have shown that the aerial parts of S. baicalensis may possess beneficial activities in antioxidant, anti-tumor, antiviral, anti-bacterial, protection of ischemia-reperfusion injured neural function, neuroprotective effects against brain injury, and blood lipid regulation. These findings suggest that the value of using HQT may be attributed to these pharmacological activities. Although HQT is generally safe for consumption, further investigation is required to understand its safety profile, particularly in special populations such as pregnant or lactating women, children, and individuals with pre-existing medical conditions. Additionally, potential interactions between the flavonoids in HQT and conventional medications must be examined to ensure their safe and effective use with pharmaceutical treatments. In addition, although the safe dose of HQT on rodents has been studied, the safe dose for humans has yet to be determined.

In conclusion, these initial research results support the potential health benefits of HQT and encourage more in-depth studies on its raw materials. Further studies are necessary to elucidate the synergistic effects of the flavonoids in HQT, optimize the processing and brewing techniques for maximum bioactivity, and investigate the safety profile and potential interactions with conventional medications. A comprehensive understanding of HQT will contribute to developing evidence-based recommendations for promoting health and well-being.

Author contributions

The authors confirm contribution to the paper as follows: Conceptualization and writing: Quan Y, Li Z, Meng X, Li P, Shen J; Figure and table modification: Quan Y, Li Z, Meng X, Li P; review and editing: Wang Y, He C, Shen J. All authors reviewed the results and approved the final version of the manuscript.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgments

This research was funded by the Shandong Provincial Natural Science Foundation, China (ZR2022QH147, ZR2022QH165) and the Innovation Team and Talents Cultivation Program of National Administration of Traditional Chinese Medicine (No. ZYYCXTD-D-202005).

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions
Copyright: © 2024 by the author(s). Published by Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.

References

[1]	Iqbal S, Xu J, Gui H, Bu D, Alharbi SA, et al. 2024. Interactive effects of microplastics and typical pollutants on the soil-plant system: a mini-review. Circular Agricultural Systems 4:e007 doi: 10.48130/cas-0024-0008 CrossRef Google Scholar
[2]	Hu Y, Wang J, Yang Y, Li S, Wu Q, et al. 2024. Revolutionizing soil heavy metal remediation: cutting-edge innovations in plant disposal technology. Science of The Total Environment 918:170577 doi: 10.1016/j.scitotenv.2024.17057 CrossRef Google Scholar
[3]	Lin H, Wang Z, Liu C, Dong Y. 2022. Technologies for removing heavy metal from contaminated soils on farmland: a review. Chemosphere 305:135457 doi: 10.1016/j.chemosphere.2022.135457 CrossRef Google Scholar
[4]	Hashem A, Abd Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, et al. 2016. Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi Journal of Biological Sciences 23(2):272−81 doi: 10.1016/j.sjbs.2015.11.002 CrossRef Google Scholar
[5]	Amna, Ali N, Masood S, Mukhtar T, Kamran MA, et al. 2015. Differential effects of cadmium and chromium on growth, photosynthetic activity, and metal uptake of Linum usitatissimum in association with Glomus intraradices. Environmental monitoring and assessment 187:311 doi: 10.1007/s10661-015-4557-8 CrossRef Google Scholar
[6]	Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, et al. 2016. Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicology and Environmental Safety 126:138−46 doi: 10.1016/j.ecoenv.2015.12.031 CrossRef Google Scholar
[7]	Buendía-González L, Orozco-Villafuerte J, Cruz-Sosa F, Barrera-Díaz CE, Vernon-Carter EJ. 2010. Prosopis laevigata a potential chromium (VI) and cadmium (II) hyperaccumulator desert plant. Bioresource Technology 101(15):5862−67 doi: 10.1016/j.biortech.2010.03.027 CrossRef Google Scholar
[8]	Liu L, Li W, Song W, Guo M. 2018. Remediation techniques for heavy metal-contaminated soils: principles and applicability. Science of the Total Environment 633:206−19 doi: 10.1016/j.scitotenv.2018.03.161 CrossRef Google Scholar
[9]	Manoj SR, Karthik C, Kadirvelu K, Arulselvi PI, Shanmugasundaram T, et al. 2020. Understanding the molecular mechanisms for the enhanced phytoremediation of heavy metals through plant growth promoting rhizobacteria: A review. Journal of Environmental Management 254:109779 doi: 10.1016/j.jenvman.2019.109779 CrossRef Google Scholar
[10]	Luo Y, Zhang Y, Xiong Z, Chen X, Sha A, et al. 2024. Peptides used for heavy metal remediation: a promising approach. International Journal of Molecular Sciences 25(12):6717 doi: 10.3390/ijms25126717 CrossRef Google Scholar
[11]	Xiao CW, Luo XY, Tian Y, Lu XY. 2013. Research progress of bioremediation of heavy metal cadmium pollution. Chemistry & Bioengineering 30:1−4 Google Scholar
[12]	Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, et al. 2017. Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710−21 doi: 10.1016/j.chemosphere.2016.12.11 CrossRef Google Scholar
[13]	Adiloğlu S, Adiloğlu A, Açıkgöz FE, Yeniaras T, Solmaz Y. 2016. Phytoremediation of cadmium from soil using patience dock (Rumex patientia L.). Analytical Letters 49(4):601−6 doi: 10.1080/00032719.2015.1075132 CrossRef Google Scholar
[14]	Bokhari SH, Ahmad I, Mahmood-Ul-Hassan M, Mohammad A. 2016. Phytoremediation potential of Lemna minor L. for heavy metals. International Journal of Phytoremediation 18(1):25−32 doi: 10.1080/15226514.2015.1058331 CrossRef Google Scholar
[15]	Li JT, Gurajala HK, Wu LH, van der Ent A, Qiu RL, et al. 2018. Hyperaccumulator plants from China: a synthesis of the current state of knowledge. Environmental Science & Technology 52(21):11980−94 doi: 10.1021/acs.est.8b01060 CrossRef Google Scholar
[16]	Medina-Díaz HL, López-Bellido FJ, Alonso-Azcárate J, Fernández-Morales FJ, Rodríguez L. 2024. A new hyperaccumulator plant (Spergularia rubra) for the decontamination of mine tailings through electrokinetic-assisted phytoextraction. Science of the Total Environment 912:169543 doi: 10.1016/j.scitotenv.2023.169543 CrossRef Google Scholar
[17]	Huang R, Wu Z, Zhao X, Li F, Wang W, et al. 2022. Pfaffia glomerata is a hyperaccumulator candidate: Cd and Zn tolerance, absorption, transfer, and distribution. Ecotoxicology and Environmental Safety 246:114196 doi: 10.1016/j.ecoenv.2022.114196 CrossRef Google Scholar
[18]	He QX. 2013. Research progress of screening cadmium hyperaccumulators. Environmental Protection and Circular Economy 33:46−49 Google Scholar
[19]	Yang J, Huang Y, Zhao G, Li B, Qin X, et al. 2022. Phytoremediation potential evaluation of three rhubarb species and comparative analysis of their rhizosphere characteristics in a Cd- and Pb-contaminated soil. Chemosphere 296:134045 doi: 10.1016/j.chemosphere.2022.134045 CrossRef Google Scholar
[20]	Li X, Chen D, Li B, Yang Y. 2021. Cd accumulation characteristics of Salvia tiliifolia and changes of rhizospheric soil enzyme activities and bacterial communities under a Cd concentration gradient. Plant and Soil 463:225−47 doi: 10.1007/s11104-021-04905-0 CrossRef Google Scholar
[21]	Li X, Li B, Zheng Y, Luo L, Qin X, et al. 2022. Physiological and rhizospheric response characteristics to cadmium of a newly identified cadmium accumulator Coreopsis grandiflora Hogg. (Asteraceae). Ecotoxicology and Environmental Safety 241:113739 doi: 10.1016/j.ecoenv.2022.113739 CrossRef Google Scholar
[22]	Liao Y, Jiang X, Xiao Y, Li M. 2020. Exposure of microalgae Euglena gracilis to polystyrene microbeads and cadmium: perspective from the physiological and transcriptional responses. Aquatic Toxicology 228:105650 doi: 10.1016/j.aquatox.2020.105650 CrossRef Google Scholar
[23]	Li X, Zhang X, Li B, Wu Y, Sun H, et al. 2017. Cadmium phytoremediation potential of turnip compared with three common high Cd-accumulating plants. Environmental Science and Pollution Research 24:21660−70 doi: 10.1007/s11356-017-9781-z CrossRef Google Scholar
[24]	Fadzil FNM, Mohamad MAN, Repin R, Harumain ZAS. 2024. Metal uptake and tolerance in hyperaccumulator plants: Advancing phytomining strategies. Rhizosphere 29:100836 doi: 10.1016/j.rhisph.2023.100836 CrossRef Google Scholar
[25]	Hu P, Yin YG, Ishikawa S, Suzui N, Kawachi N, et al. 2013. Nitrate facilitates cadmium uptake, transport and accumulation in the hyperaccumulator Sedum plumbizincicola. Environmental Science and Pollution Research 20:6306−16 doi: 10.1007/s11356-013-1680-3 CrossRef Google Scholar
[26]	Tang L, Yao A, Yuan M, Tang Y, Liu J, et al. 2016. Transcriptional up-regulation of genes involved in photosynthesis of the Zn/Cd hyperaccumulator Sedum alfredii in response to zinc and cadmium. Chemosphere 164:190−200 doi: 10.1016/j.chemosphere.2016.08.026 CrossRef Google Scholar
[27]	Liu H, Zhao H, Wu L, Liu A, Zhao FJ, et al. 2017. Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytologist 215(2):687−98 doi: 10.1111/nph.14622 CrossRef Google Scholar
[28]	Qiu W, Song X, Han X, Liu M, Qiao G, et al. 2018. Overexpression of Sedum alfredii cinnamyl alcohol dehydrogenase increases the tolerance and accumulation of cadmium in Arabidopsis. Environmental and Experimental Botany 155:566−77 doi: 10.1016/j.envexpbot.2018.08.003 CrossRef Google Scholar
[29]	Zhao H, Wang L, Zhao FJ, Wu L, Liu A, et al. 2019. SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola. Plant, Cell & Environment 42(4):1112−24 doi: 10.1111/pce.13456 CrossRef Google Scholar
[30]	Wu B, Shao B, Zhao H, Wang X, Lei M. 2017. Cd accumulation and tolerance characteristics of 11 species in Sedum sensu lato. Acta Scientiae Circumstantiae 37(5):1947−56 doi: 10.13671/j.hjkxxb.2016.0339 CrossRef Google Scholar
[31]	Guo JM, Lei M, Yang JX, Yang J, Wan XM, et al. 2017. Effect of fertilizers on the Cd uptake of two sedum species (Sedum spectabile Boreau and Sedum aizoon L.) as potential Cd accumulators. Ecological Engineering 106:409−14 doi: 10.1016/j.ecoleng.2017.04.069 CrossRef Google Scholar
[32]	Nedaee Ziabari SZ, Sedaghathoor S, Kaviani B, Baniasad M. 2024. Phytoremediation ability of three succulent ornamental plants; cactus (Opuntia humifusa), kalanchoe (Kalanchoe blossfeldiana) and bryophyllum (Bryophyllum delagoensis) under heavy metals pollution. Science of the Total Environment 947:174579 doi: 10.1016/j.scitotenv.2024.174579 CrossRef Google Scholar
[33]	Zhou Q, Guo JJ, He CT, Shen C, Huang YY, et al. 2016. Comparative transcriptome analysis between low- and high-cadmium-accumulating genotypes of pakchoi (Brassica chinensis L.) in response to cadmium stress. Environmental Science & Technology 50(12):6485−94 doi: 10.1021/acs.est.5b06326 CrossRef Google Scholar
[34]	Yu SJ, Gao SF, Qu YM, Chen YH, Wang G. 2014. Toxicity and its threshold of cadmium to tomato roots in different soils. Journal of Agro-Environment Science 33:640−46 Google Scholar
[35]	Jin C, Wei X, Yang S, Yao L, Gong G. 2017. Microwave-assisted extraction and antioxidant activity of flavonoids from Sedum aizoon leaves. Food Science and Technology Research 23(1):111−18 doi: 10.3136/fstr.23.111 CrossRef Google Scholar
[36]	Choppala G, Saifullah, Bolan N, Bibi S, Iqbal M, et al. 2014. Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Critical Reviews in Plant Sciences 33(5):374−91 doi: 10.1080/07352689.2014.903747 CrossRef Google Scholar
[37]	Ahmad Anjum S, Tanveer M, Hussain S, Shahzad B, Ashraf U, et al. 2016. Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environmental Science and Pollution Research 23:11864−75 doi: 10.1007/s11356-016-6382-1 CrossRef Google Scholar
[38]	Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BHN, et al. 2017. Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Frontiers in Plant Science 8:115 doi: 10.3389/fpls.2017.00115 CrossRef Google Scholar
[39]	Mansoor S, Ali A, Kour N, Bornhorst J, Alharbi K, et al. 2023. Heavy metal induced oxidative stress mitigation and ROS scavenging in plants. Plants 12(16):3003 doi: 10.3390/plants12163003 CrossRef Google Scholar
[40]	Song L, Wang J, Shafi M, Liu Y, Wang J, et al. 2016. Hypobaric treatment effects on chilling injury, mitochondrial dysfunction, and the ascorbate–glutathione (AsA-GSH) cycle in postharvest peach fruit. Journal of Agricultural and Food Chemistry 64(22):4665−74 doi: 10.1021/acs.jafc.6b00623 CrossRef Google Scholar
[41]	Møller IM. 2001. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Biology 52(1):561−91 doi: 10.1146/annurev.arplant.52.1.561 CrossRef Google Scholar
[42]	Zhang J, Zhang M, Shohag MJI, Tian M, Song H, et al. 2016. Enhanced expression of SaHMA3 plays critical roles in Cd hyperaccumulation and hypertolerance in Cd hyperaccumulator Sedum alfredii Hance. Planta 243(3):577−89 doi: 10.1007/s00425-015-2429-7 CrossRef Google Scholar
[43]	Liu H, Zhao H, Wu L, Xu W. 2017. A genetic transformation method for cadmium hyperaccumulator Sedum plumbizincicola and non-hyperaccumulating ecotype of Sedum alfredii. Frontiers in Plant Science 8:1047 doi: 10.3389/fpls.2017.01047 CrossRef Google Scholar
[44]	Peng JS, Wang YJ, Ding G, Ma HL, Zhang YJ, et al. 2017. A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola. Molecular Plant 10(5):771−74 doi: 10.1016/j.molp.2016.12.007 CrossRef Google Scholar
[45]	Chang S, Shu H. 2015. The inhibition analysis of two heavy metal ATPase genes (NtHMA3a and NtHMA3b) in Nicotiana tabacum. Bioremediation Journal 19(2):113−23 doi: 10.1080/10889868.2014.995372 CrossRef Google Scholar
[46]	Shao JF, Xia J, Yamaji N, Shen RF, Ma JF. 2018. Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. Journal of Experimental Botany 69(10):2743−52 doi: 10.1093/jxb/ery107 CrossRef Google Scholar
[47]	Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, et al. 2016. Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicology and Environmental Safety 126:111−21 doi: 10.1016/j.ecoenv.2015.12.023 CrossRef Google Scholar

About this article

Cite this article

Huang X, Li Y, Karel NNJ, Tang H, Hu N, et al. 2024. Theoretical phytoextraction rates evaluating the application potential of two Cd accumulators from Crassulaceae for cleaning Cd-contaminated farmland. Circular Agricultural Systems 4: e018 doi: 10.48130/cas-0024-0018

Huang X, Li Y, Karel NNJ, Tang H, Hu N, et al. 2024. Theoretical phytoextraction rates evaluating the application potential of two Cd accumulators from Crassulaceae for cleaning Cd-contaminated farmland. Circular Agricultural Systems 4: e018 doi: 10.48130/cas-0024-0018

Figures(4)

Download PDF

Article Metrics

Article views(796) PDF downloads(117)

Other Articles By Authors

on this site
on Google Scholar

HTML

Introduction

Environmental pollutants such as heavy metals, microplastics, and antibiotics have raised significant concerns about agricultural sustainability, ecosystem stability, and human health^[1] . Cadmium (Cd) contamination has attracted the most attention because of its high toxicity, widespread pollution area, and easy uptake by plants^[2]. Cd enrichment in soils can change soil physicochemical properties, and reduce soil fertility^[3]. As a nonessential element for organisms, Cd can influence the normal physiological function of most plants at low concentrations, leading to growth inhibition, metabolic dysregulation, and even plant death^[4]. Moreover, Cd can easily be absorbed by crops and vegetables to enter the food chain, ultimately endangering human health^[5,6].

To ensure agricultural food safety, remediation of heavy metal-polluted soil is necessary. To date, separate or combined biological, physical, and chemical methods have been developed to remediate contaminated soils^[7]. Physical‒chemical techniques are commonly applied in soil remediation because they have quick effects^[8]. However, most physical‒chemical techniques are expensive, easily introduce secondary pollution, or destroy soil properties; thus, they are difficult to apply widely and sustainably^[9]. In contrast, biological remediation, which decreases heavy metal concentrations or bioavailability in soils through the metabolic activities of organisms^[10], has the advantages of low cost, environmental friendliness, and easy management, thereby attracting much interest^[11].

Phytoremediation, especially the phytoextraction technique, has become one of the highly anticipated bioremediation methods in recent years because of its simple, environmentally friendly, and cost-effective feasibility^[12]. Phytoextraction is dependent on the abilities of plants, especially those hyperaccumulators, to absorb heavy metals and remove them^[13,14]. To date, hundreds of heavy metal hyperaccumulators have been discovered worldwide^[15] and new hyperaccumulators are being constantly reported^[16,17]. However, because heavy metal contents accumulated by plants are determined by both the heavy metal concentrations in plants and plant biomasses, quite a few heavy metal hyperaccumulators with slow growth rates, and low biomasses^[18] cannot be practically used for phytoremediation. Additionally, the shape of plants can determine the optimum planting density of plants in the field, thus affecting the removal efficiency of heavy metals, which is also worth paying attention to when screening or breeding plant resources for phytoextraction. To date, laboratory research has hardly simultaneously focused on these factors. In this study, Cd tolerance and accumulation capacities of two Crassulaceae species, Phedimus aizoon and Kalanchoe blossfeldiana were identified. On this basis, a new index, theoretical phytoextraction rate (TPR), integrating plant biomass, heavy metal accumulation capacity, and plant shape and size are proposed to perform a more referential evaluation of their application potential for Cd phytoextraction. This study is expected to provide new plant resources and theoretical methods for heavy metal phytoextraction.

Materials and methods

Plant culture and treatment

Uniform seedlings that were approximately 10 cm high of both P. aizoon and K. blossfeldiana were purchased from a horticultural company located in Yunnan Province, China. The seedlings were neatly transplanted into uniform ﬂowerpots according to the method of Yang et al.^[19]. The Cd-free soils and contaminated soils were obtained according to the methods of Li et al.^[20], with three replicates of each group. The flower pots were placed in a greenhouse with appropriate watering (500 ml each time, about once every 2 d, tap water without Cd) to avoid soil surface dryness.

Measurement of plant growth
After 3 months of growth, the plant size was measured before the plants were harvested. The diameter of the maximum amplitude and the diameter in the vertical direction were used to represent the plant size. After the roots were washed three times with deionized water, the root length was measured. The samples of leaves, stems, and roots were treated as described previously by Li et al.^[21].

Chlorophyll content measurement
Fresh leaves (top first to third) were harvested to measure the chlorophyll content. Fresh leaves (0.1 g) were soaked in 10 ml 80% acetone for 24 h under darkness. After centrifugation at 12,000 ×g for 10 min, the absorbance of the resulting supernatant was precisely measured at wavelengths of 645 and 663 nm via a spectrophotometer (Youke, Shanghai, China). The concentrations of chlorophyll a (Chla) and chlorophyll b (Chlb) were calculated via formulas described in a previous report by Liao et al.^[22].

Detection of reactive oxygen species (ROS)
The concentrations of superoxide anions (O₂⁻) and hydrogen peroxide (H₂O₂) were detected using their corresponding kits (Solarbio, Beijing, China) according to the instructions.

Antioxidant enzyme activity assay
The activities of superoxide dismutase (SOD) and peroxidase (CAT) were detected using their corresponding kits (Solarbio, Beijing, China) according to the instructions.

Cd concentration detection
The Cd concentrations in dry samples were measured via a previously described method by Li et al.^[23].

Index calculation

$\rm{B}ioconcentration\; factor\; (BCF)=\dfrac{\mathrm{S}\mathrm{a}\mathrm{m}\mathrm{p}\mathrm{l}\mathrm{e}\; \mathrm{ }\mathrm{C}\mathrm{d}\; \mathrm{ }\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}}{\mathrm{S}\mathrm{o}\mathrm{i}\mathrm{l}\; \mathrm{ }\mathrm{C}\mathrm{d}\; \mathrm{ }\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}}$

$\rm{T}ranslocation\; factor\; (TF)=\dfrac{\mathrm{L}\mathrm{e}\mathrm{a}\mathrm{f}\; \mathrm{ }\mathrm{o}\mathrm{r}\mathrm{ }\; \mathrm{s}\mathrm{t}\mathrm{e}\mathrm{m}\; \mathrm{ }\mathrm{C}\mathrm{d}\; \mathrm{ }\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}}{\mathrm{R}\mathrm{o}\mathrm{o}\mathrm{t}\; \mathrm{ }\mathrm{C}\mathrm{d}\; \mathrm{ }\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}}$

${ \rm TPR = \dfrac{\mathrm{C}\mathrm{d}\;\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{t}\mathrm{e}\mathrm{n}\mathrm{t}\;\mathrm{i}\mathrm{n}\;\mathrm{a}\mathrm{b}\mathrm{o}\mathrm{v}\mathrm{e}\mathrm{g}\mathrm{r}\mathrm{o}\mathrm{u}\mathrm{n}\mathrm{d}\;\mathrm{o}\mathrm{f}\;\mathrm{i}\mathrm{n}\mathrm{d}\mathrm{i}\mathrm{v}\mathrm{i}\mathrm{d}\mathrm{u}\mathrm{a}\mathrm{l}\;\mathrm{p}\mathrm{l}\mathrm{a}\mathrm{n}\mathrm{t}\;\times \;\mathrm{O}\mathrm{p}\mathrm{t}\mathrm{i}\mathrm{m}\mathrm{u}\mathrm{m}\;\mathrm{p}\mathrm{l}\mathrm{a}\mathrm{n}\mathrm{t}\mathrm{i}\mathrm{n}\mathrm{g}\;\mathrm{d}\mathrm{e}\mathrm{n}\mathrm{s}\mathrm{i}\mathrm{t}\mathrm{y}}{\mathrm{S}\mathrm{o}\mathrm{i}\mathrm{l}\;\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}\;\times \;(\mathrm{R}\mathrm{o}\mathrm{o}\mathrm{t}\;\mathrm{l}\mathrm{e}\mathrm{n}\mathrm{g}\mathrm{t}\mathrm{h}\;\times \;\mathrm{U}\mathrm{n}\mathrm{i}\mathrm{t}\;\mathrm{a}\mathrm{r}\mathrm{e}\mathrm{a}\;\times \;\mathrm{S}\mathrm{o}\mathrm{i}\mathrm{l}\;\mathrm{d}\mathrm{e}\mathrm{n}\mathrm{s}\mathrm{i}\mathrm{t}\mathrm{y})}} \times\; \mathrm{100}{\text{%}}$

$\begin{split} & \rm{O}ptimum\; planting\; density=\dfrac{\mathrm{U}\mathrm{n}\mathrm{i}\mathrm{t}\; \mathrm{a}\mathrm{r}\mathrm{e}\mathrm{a}}{\mathrm{P}\mathrm{l}\mathrm{a}\mathrm{n}\mathrm{t}\; \mathrm{s}\mathrm{i}\mathrm{z}\mathrm{e}}= \\ &\quad\dfrac{\mathrm{U}\mathrm{n}\mathrm{i}\mathrm{t}\; \mathrm{a}\mathrm{r}\mathrm{e}\mathrm{a}}{\mathrm{D}\mathrm{i}\mathrm{a}\mathrm{m}\mathrm{e}\mathrm{t}\mathrm{e}\mathrm{r}\; \mathrm{o}\mathrm{f}\; \mathrm{m}\mathrm{a}\mathrm{x}.\; \mathrm{a}\mathrm{m}\mathrm{p}\mathrm{l}\mathrm{i}\mathrm{t}\mathrm{u}\mathrm{t}\mathrm{e}\; \times \; \mathrm{D}\mathrm{i}\mathrm{a}\mathrm{m}\mathrm{e}\mathrm{t}\mathrm{e}\mathrm{r}\; \mathrm{i}\mathrm{n}\; \mathrm{v}\mathrm{e}\mathrm{r}\mathrm{t}\mathrm{i}\mathrm{c}\mathrm{a}\mathrm{l}\; \mathrm{d}\mathrm{i}\mathrm{r}\mathrm{e}\mathrm{c}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}} \end{split}$

Statistical analysis

Bar charts were drawn using SigmaPlot 10.0 software (Systat, San Jose, CA, USA). Significant difference was analysed by SPSS 18.0 software (IBM, New York, NY, USA).

Discussion

High Cd accumulation capacities of P. aizoon and K. blossfeldiana

Heavy metal phytoextraction efficiency largely depends on high tolerance and accumulation capacities of plants; thus, numerous studies have focused on screening and identifying high-heavy metal-accumulating species, especially hyperaccumulators^[24]. In Crassulaceae, Sedum alfredii, and S. plumbizincicola have been identified as zinc/Cd hyperaccumulators^[25], and their physiological and molecular mechanisms underlying Cd tolerance and uptake have attracted much interest^[26−29]. These findings have prompted scientists to screen novel Cd accumulators or hyperacccumulators from other Crassulaceae species. For example, Wu et al. analysed the Cd accumulation characteristics of 11 generalized Sedum species^[30], which included Sedum aizoon (namely, P. aizoon in this study). The results showed that P. aizoon could tolerate 100 mg·kg⁻¹ but succumb to 200 or 400 mg·kg⁻¹ soil Cd. Additionally, both the BCF in the aboveground part and the TF were < 1^[30], which value is the threshold for determining whether a species belongs to hyperaccumulators^[17]. However, in another study, both the shoot BCF and TF of P. aizoon were > 1 when treated by low Cd concentrations^[31]. Interestingly, P. aizoon used in this study met all the threshold values (i.e., aboveground part Cd concentration > 100 mg·kg⁻¹, BCF > 1, and TF > 1) for Cd hyperaccumulators under 50 mg·kg⁻¹ soil Cd treatment (Fig. 3), indicating that it may be a potential Cd hyperaccumulator. For K. blossfeldiana, the results of Cd accumulation characteristics (Fig. 3) indicate it can be considered a high-Cd-accumulating species, which is superior to the Cd accumulation capacity of K. blossfeldiana reported in a recent study^[32]. The distinct results from different studies may be attributed to multiple factors, including plant genotype^[33], soil property^[34], and Cd treatment time. Overall, both P. aizoon and K. blossfeldiana genotypes used in this study are high-Cd-accumulating species, which can thus be considered for the phytoextraction of Cd-polluted soils.

Additionally, Phedimus aizoon has often been used as a medicinal vegetable by some people in China, as it contains many medicinal ingredients^[35]. The present results thus suggest that appropriate attention should be paid to the safety of P. aizoon consumption because of the risk of Cd intake.

Cd tolerance mechanism in P. aizoon and K. blossfeldiana
To improve phytoextraction efficiency via genetic engineering or other strengthening measures, understanding the physiological and molecular mechanisms by which plants tolerate and accumulate heavy metals is important^[33,36]. In this study, although P. aizoon and K. blossfeldiana accumulated a large amount of Cd in their leaves, their physiological activities (e.g., chlorophyll synthesis) were not harmed. These results suggest that these two plants provide effective protection strategies against Cd stress.

Previous studies have demonstrated that plants usually involve a trade-off between the accumulation and elimination of ROS under Cd stress^[37,38]. The accumulation of ROS (e.g., O₂⁻, H₂O₂, and •OH) can cause damage to DNA, proteins, and lipids when stress occurs^[39]. However, plants have evolved effective mechanisms to regulate ROS homeostasis^[40]. Antioxidant systems, including antioxidant enzymes (e.g., SOD, CAT, and peroxidase) and nonenzymatic antioxidants are responsible for adjusting ROS homeostasis^[41]. Specifically, SOD catalyzes the dismutation of O₂⁻ to produce O₂ and H₂O₂ in cells, whereas H₂O₂ can be further catalyzed to decompose into O₂ and H₂O by CAT^[41]. In this study, the induced activities of SOD and CAT and the steady concentrations of O₂⁻ and H₂O₂ fully illustrate that P. aizoon and K. blossfeldiana can effectively start the antioxidant system to control ROS accumulation to avoid oxidative damage.

Recently, S. plumbizincicola and S. alfredii have gradually become model species for investigating the mechanisms of Cd tolerance and accumulation in plants^{[26,28,29,42−44]}. Several important genes have been found to participate in Cd detoxification or transport in them. For example, Liu et al. reported that the tonoplast-localized SpHMA3 protein could transport Cd into vacuoles for compartmentalization to reduce Cd toxicity in the shoots of S. plumbizincicola^[43]. Zhao et al. reported that the SpHMA1 protein can export Cd from chloroplasts to protect against photosynthesis^[29]. Most of these genes have also been reported in other species with similar functions^[29,45,46]. To date, owing to the lack of whole-genome information, few unique tolerance and accumulation mechanisms have been identified in S. plumbizincicola, which has higher Cd tolerance and accumulation capacities than most Cd hyperaccumulators^[25]. Crassulaceae species have unique crassulacean acid metabolism pathways; thus, it is of interest to explore whether these metabolic processes contribute to Cd detoxification in high-Cd-accumulating Crassulaceae species. For P. aizoon and K. blossfeldiana, more work should be conducted to analyse their physiological and molecular mechanisms in response to Cd.

Phytoextraction potential of P. aizoon and K. blossfeldiana for Cd-polluted soils
Heavy metal accumulators or hyperaccumulators are the preferred resources for phytoextraction. However, studies have also indicated that plant biomass and growth rate are important for phytoextraction efficiency^[11,47]. Indeed, for many reported heavy metal accumulators or hyperaccumulators, their actual phytoextraction potential has not been well analysed by combining factors such as growth rate or biomass accumulation. In this study, although P. aizoon and K. blossfeldiana presented high Cd accumulation capacities, their growth rates were relatively mediocre. For example, the dry weight biomasses of 3-month-old P. aizoon and K. blossfeldiana were approximately equal to those of 2-month-old turnip, rape, and Phytolacca americana reported previously^[23] under similar soil conditions. However, the high biomass of individual plants of certain species does not mean that higher total biomass yields can be harvested in a unit area. The shape and size of different plants determine their optimum planting densities in the field, thus affecting the total biomass yields in a unit area. Generally, upright-type plants (e.g., K. blossfeldiana) can have higher optimum planting densities than scatted-type species (e.g., P. aizoon). This can increase the total biomass yield of upright-type plants per unit area, which is confirmed by the present estimation results for P. aizoon and K. blossfeldiana. On the whole, we believe that the ultimate phytoextraction efficiency will depend on the capacity of a plant to accumulate pollutants and biomass yield, as well as planting density determined by plant shape and size.

In this study, the TPR index was introduced, which integrates all of the above mentioned factors, to evaluate the Cd phytoextraction potentials of P. aizoon and K. blossfeldiana. The results revealed the Cd extraction rates by P. aizoon and K. blossfeldiana from the soil layer at a depth of approximately 25 cm (root length) per unit area under the appropriate planting density for 3 months of growth. Interestingly, the TPR value of K. blossfeldiana was markedly greater than that of P. aizoon, although Cd accumulation in the aboveground part of individual P. aizoon plant was much greater than that of individual K. blossfeldiana plant. This finding highlights the importance of plant shape on phytoextraction rates when screening and breeding hyperaccumulating plant resources. The TPR index provides a bridge between experimental research (e.g., pot experiments) and actual phytoextraction efficiency in the field. However, it is necessary to verify the reliability of this theory in combination with practical phytoextraction work in the future.

Contents

Policies

Services

Partnerships

Theoretical phytoextraction rates evaluating the application potential of two Cd accumulators from Crassulaceae for cleaning Cd-contaminated farmland

Abstract

Introduction

Chemical components of Huangqin Tea

Flavonoids

Essential oils

Others

Functional properties

Anti-inflammatory activity

Anti-bacterial and antiviral activity

Antipyretic and analgesic effect

Neuroprotective effect

Effects on cardiovascular and cerebrovascular diseases

Anti-aging effects

Others

Safety issues

Conclusions and future perspectives

Author contributions

Data availability

Acknowledgments

Conflict of interest

Rights and permissions

References

About this article

Cite this article

Article Metrics

Access History

Other Articles By Authors