Hydrothermal deglycosylation and deconstruction effect of steam explosion: Application to high-valued glycyrrhizic acid derivatives from liquorice

Food Chemistry 307 (2020) 125558

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Hydrothermal deglycosylation and deconstruction effect of steam explosion: Application to high-valued glycyrrhizic acid derivatives from liquorice Wenjie Suia,b,c,1, Mengjia Zhoua,b,1, Yi Xua,b, Guanhua Wangd, Huan Zhaoa,b, Xiaoling Lva,b,

T

⁎

a

State Key Laboratory of Food Nutrition and Safety, Tianjin University of Science & Technology, Tianjin 300457, China Key Laboratory of Food Nutrition and Safety, Ministry of Education, Tianjin University of Science & Technology, Tianjin 300457, China c Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU), Beijing 100048, China d Tianjin Key Laboratory of Pulp and Paper, College of Paper Making Science and Technology, Tianjin University of Science and Technology, Tianjin 300457, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Steam explosion Hydrothermal conversion Glycyrrhizic acid Liquorice Kinetics Thermodynamics

In this work, steam explosion (SE) was exploited as a green and facile process to deconstruct liquorice’s structure and deglycosylate glycyrrhizic acid (GL) to improve conversion and diffusion efficacy of GL and its hydrolyzed products. Results showed SE induced auto-hydrolysis of GL into glycyrrhetic acid 3-O-mono-β-D-glucuronide (GAMG) and glycyrrhetinic acid (GA), by which 30.71% of GL conversion, 5.24% and 21.47% of GAMG and GA formation were obtained. GL hydrolytic pathways were revealed by reaction kinetics and thermodynamics, which possessed complex consecutive and parallel reactions with endothermic, non-spontaneous and entropydecreasing features. SE referred to cause cleavage of the β-1,3 glycosidic bond in GL which was hydrolyzed to GA as a main product and GAMG and glucuronic acids as minor products. Diffusion of hydrolyzed products was accelerated by raising the diffusion coefficient and shortening the equilibrium time by over 90%. This work provides a sustainable and efficient route for product conversion and function enhancement of bioactive components.

1. Introduction Triterpenoid saponins are an important class of natural plant products with a wide range of biological activities. They are crucial to human health, which have been broadly used in confectioneries, beverages and cosmetics (Xu, Cai, Gao, & Liu, 2016; Zhao & Li, 2018). Triterpenoid saponins have useful medicinal benefits, including antiviral, antimicrobial, anti-cancer and anti-pathogen activities (Xu et al., 2015; Zhao & Li, 2018). They generally exist in the form of glycosides, which are more easily absorbed through transformation to aglycon by enzymatic degradation in the absorption process of human body. The deglycosylation of different triterpenoid glycosides represents a necessary step in food and pharmaceutical technology for raising bioactivity, attenuating toxicity, accelerating absorption, de-bittering and clarifying fruit juices (Chen & Chen, 2011; Hsiao & Hsieh, 2011; Ruen-ngam, Quitain, Tanaka, Sasaki, & Goto, 2012; Zhang, Sun, Gu, & Du, 2017). Glycyrrhizic Acid (GL) is the major bioactive triterpene glycoside of licorice root (Glycyrrhiza Radix) extracts, composing of one molecule of glycyrrhetinic acid (GA) as aglycone and two molecules of glucuronic acid (Amin, El-Menoufy, El-Mehalawy, & Mostafa, 2011; Shabkhiz,

Eikani, Sadr, & Golmohammad, 2016). It has been proven to possess a wide range of pharmacological properties (Bai et al., 2018; Shabkhiz et al., 2016; Xu et al., 2016). As its sweetness is 150 times greater than that of sucrose, GL is also commercially available world-wide as a sweetener or as a functional additive in tobacco, food and confectionery products (Xu et al., 2016). However, GL is not an optimal molecule for easy absorption in the bloodstream and interferes with ionic metabolic balance in numerous organisms, which can create the side-effect of edema and hypertension (Fan et al., 2016). With cleavage of one terminal glucuronic acid by hydrolysis, GL can be transformed into glycyrrhetic acid 3-O-mono-β-D-glucuronide (GAMG). Compared with GL, GAMG has more pleasant sweetness (about 5–20 times greater than GL), better safety (MLD50 of GAMG was 5000 g/kg bw while that of GL was 805 mg/kg bw in acute toxicity tests), higher bioavailability and lower caloric value (Amin et al., 2011; Chen, Kaleem, He, Liu, & Li, 2012). Therefore, GAMG is thought to be a potential substitute for GL as a promising functional sweetener and therapeutic agent with high sweetness and safety (Hu, 2008). Glycyrrhetinic acid (GA), is the hydrolyzed aglycone of GL by cleavage of both glucuronic acids. It can be hydrolyzed completely by intestinal bacteria and enter into the

⁎

Corresponding author at: State Key Laboratory of Food Nutrition and Safety, Tianjin University of Science & Technology, Tianjin 300457, China. E-mail addresses: [email protected] (W. Sui), [email protected] (X. Lv). 1 These authors contributed to the work equally and should be regarded as co-first authors. https://doi.org/10.1016/j.foodchem.2019.125558 Received 11 April 2019; Received in revised form 14 September 2019; Accepted 16 September 2019 Available online 30 September 2019 0308-8146/ © 2019 Elsevier Ltd. All rights reserved.

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broken down, which helps to enhance the reactant or solvent accessibility. As compared with other pretreatment technologies, SE offers several attractive features, including lower environmental impact without adding chemical catalysts, lower equipment and energy investment, and better feasibility at industrial scale development (Alvira, Tomás-Pejó, Ballesteros, & Negro, 2010; Auxenfans, Crônier, Chabbert, & Paës, 2017). Several studies investigating the SE process of fibrous materials originating from food and medicinal herbs have reported the following conclusions. On one hand, its explosion effect resulted in the disruption and degradation of solid residues from bundles to individual fibers and even to the cell wall level that easing the solutes’ diffusion behaviour (Sui & Chen, 2014; Sun et al., 2015). SE technology has been proven for achieving increasing extraction efficiency of wheat bran, ginkgo leaf, sumac fruit, radix astragali and pine needles, etc (Sui & Chen, 2014; Sui et al., 2018). On the other hand, during the steaming stage, structural and active components were auto-hydrolyzed by organic acids as released from acetyl or other functional groups from feedstock (Liu, Qin, Liu, Jin, & Bai, 2015). Notably, such hydrothermal atmosphere caused the auto-hydrolysis of glycosidic bonds for prompting the exploitation and utilization of highly active aglycones. This deglycosylation effect has been applied in the quercetin preparation from sumac fruit, the diosgenin preparation from Radix Curcumae Longae, and the resveratrol preparation from Polygonum Cuspidatum (Chen & Chen, 2011; Chen & Peng, 2012; Chen & Sui, 2014; Sui et al., 2018). In this work, SE technology was exploited to deconstruct the liquorice’s structure and deglycosylate the triterpene glycoside GL in situ to improve the conversion and extraction of GL and its high-valued hydrolyzed products. Hydrothermal deconstruction of liquorice was comparatively investigated using multiple characterization techniques on compositional, morphological and porous properties after SE. Hydrothermal degradation of GL within liquorice under SE at temperatures up to 480 K and steaming times up to 30 min were explored, concentrating on the elucidation of reaction mechanism, kinetics and thermodynamics of product formation. Diffusion kinetics of GL and its hydrolyzed products were evaluated to interpret the extraction enhancing effect of SE. This work allows us to understand the hydrothermal deglycosylation and deconstruction effect of SE and thus offer new insights to apply SE technology in the food and medicinal processing field. It also has positive significance for the efficient preparation, product development and functional enhancement of triterpenoid saponins in bioresources.

systematic circulation of the human body (Fan et al., 2016). Although it loses the sweetness, GA has been revealed to exhibit similar or stronger pharmacological properties to GL (Graebin, 2018; Hussain et al., 2018). Some research has shown the effective dose of GA was only 2.5% of GL to generate an equal effect for inhibiting the proliferation of hepatoma carcinoma cells and it has a greater impact on in vitro anti-platelet aggregation (Fan et al., 2016). GA and its derivatives, as potential therapeutic agents for several viral diseases, including chronic hepatitis and AIDS, have gained extensive attention recently (Graebin, 2018; Hussain et al., 2018). Considering the vital significance and expanding market of GAMG and GA, methodologies are required for their efficient conversion and large-scale production. Traditional chemical methods mainly refer to mineral acid-catalyzed hydrolysis of GL at high temperature over 10 h (Fan et al., 2016). This method usually has low selectivity for glycosidic linkages and forms aglycones as the main product, so it is difficult to selectively remove one of the glucuronic acids. Biotransformation of GL mainly includes microbial, enzymatic and intestinal bacteria transformation, and plant tissue cell culture (Amin et al., 2011; Liu, Wang, & Guo, 2010; Shen, Huang, Wang, & Xu, 2009; Xu et al., 2016). Their essence is under the catalytic action of β-D-glucuronidase that can hydrolyze the glycosidic bond between carbohydrates or between carbohydrate and non-carbohydrate moieties (Amin et al., 2011). It was reported that GAMG conversion rate was 23.7% and 10% by glucuronidase hydrolysis and liquid fermentation (Liu et al., 2010; Shen et al., 2009). However, low water solubility of both GL and GAMG at normal pressure made them incompletely in contact with the biocatalyst, greatly limiting the large-scale biotransformation efficiency (Amin et al., 2011; Chen et al., 2012). Researchers hence prompted the conversion efficiency by reaction media optimization or enzyme immobilization (Liu et al., 2010; Shen et al., 2009). Some of them used whole-cell biocatalysts to perform the hydrolysis of GL to GAMG in a system containing non-conventional solvents (Amin et al., 2011; Chen et al., 2012; Zhao & Li, 2018). The transformation of GL by Penicillium purpurogenum in an ionic liquid ([Bmim]PF6)/buffer and aqueous/organic biphasic system was studied, and a GAMG yield of 70–80% was achieved after 60 h (Chen et al., 2012). While, the process of biocatalysis is difficult to realize in industrial scale production hindered by the low enzyme productivity and activity. Besides, several measures for the improvement of enzyme stability and reactant solubility have operational complexity and high cost. Also, it was reported that subcritical water was applied as a novel medium for hydrothermal conversion of GL into GAMG and GA, by which 95% of GL conversion, 25% and 37% of GAMG and GA formation were obtained at optimal parameters (Fan et al., 2016). However, the above conversion process took GL as a direct substrate, so the purity of GL through several separation and purification steps certainly has an impact on its conversion efficiency. In this respect, the introduction of a green and efficient conversion approach of GL appears as a promising research line for the high-value utilization of its hydrolyzed products. Steam explosion is one of the most widely employed physico-chemical pretreatments for lignocellulosic biomass. It is a hydrothermal pretreatment in which materials are exposed to high-pressure saturated steam for a period of time and then undergo an explosive decompression. This treatment combines chemical effects and mechanical forces. The auto-hydrolysis of acetyl groups present in hemicellulose took place to promote the formation of acetic acids, and the decrease of water pKw at high temperature, which jointly promotes the formation of a mild acidic environment. High temperature and acidic conditions facilitated a series of hydrothermal reactions: easy hydrolysis and solubilization of hemicellulose, some removal and redistribution of lignin, partial exposure of cellulose crystalline region, etc (Ruiz, RodríguezJasso, Fernandes, Vicente, & Teixeira, 2013; Rodríguez, Sanchez, & Parra, 2017; Ruiz, Thomsen, & Trajano, 2017; Sui, Xie, Liu, Wu, & Zhang, 2018). The mechanical effects are caused because the pressure was suddenly reduced and fibers were separated, porous matrix was

2. Materials and methods 2.1. Materials Liquorice, the roots of Glycyrrhiza uralensis Fisch., was purchased from Beijing Qiancao Herbal Pieces Co., Ltd. (Beijing, China). Glycyrrhizic acid (≥98%, lot No. PO4N7F24311), 18β-glycyrrhetinic acid (≥98%, lot No. HM0327KA14), Glycyrrhetinic acid 3-O-mono-βD-glucuronide (≥98%, lot No. W04SBK42699) were purchased from Tianjin Dingguo Biotechnology Co., Ltd. (Tianjin, China). All reagents (HPLC-grade) and chemical and solvents (analytical-grade) were purchased from Sinopharm Chemical Reagent Co., Ltd. (Tianjin, China). 2.2. Steam explosion process SE treatment was performed in a 5 L batch vessel (Weifang Derui Biotechnology Co., Ltd., China) which was composed of a reaction retort, a receiving tank and a saturated steam generator. During treatment, 500 g liquorice was top-loaded into the reaction retort and possessed at a certain saturated steam pressure of 0.8 MPa (443 K), 1.0 MPa (452 K), 1.3 MPa (464 K), 1.5 MPa (471 K) and 1.8 MPa (480 K) until reaching the desired time of 2, 5, 10, 20, 30 min, respectively. And the retention time was started after the reaction retort was heated to the 2

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settled pressure. The steaming period terminated with a swift decompression by the ball valve and materials were exploded into the receiving tank. After SE, the samples were naturally cooled and dried at room temperature for 24 h, and then stored at 277 K for further use and regarded as SE samples.

rGL =

−d [GL] = k1 [GL] + k3 [GL] dt

rGAMG =

rGA =

2.3. Physicochemical property characterization of steam exploded liquorice

(1)

d [GAMG] = k1 [GL] − k2 [GAMG] dt

(2)

d [GA] = k3 [GL] + k2 [GAMG] dt

(3)

where rGL is the degradation rate of GL (g/s), rGAMG and rGA represents the conversion rate of GAMG (g/s) and the formation rate of GA (g/s); [GA], [GL] and [GAMG] represents the mass of GA, GL and GAMG (g), respectively; k1, k2 and k3 are the kinetic constants (/s) of reactionGL→GAMG, reactionGAMG→GA and reactionGL→GA, and t is the reaction time (s). Eq. (1) was integrated and expressed as,

The identified chemical composition, including water extracts, ethanol extracts, cellulose, hemicellulose, acid-soluble lignin (ASL), acid-insoluble lignin (AIL) and ash of raw and SE liquorice, were determined according to the Laboratory Analytical Procedures of the National Renewable Energy Laboratory (NREL). The Fourier transform infrared spectroscopy (FTIR) study of liquorice samples was measured by IS50 FTIR spectroscopy (Nicolet, Thermo Fisher, America). Each sample was prepared according to the potassium bromide technique. The region between 4000 and 400 cm−1 were recorded with a resolution of 4 cm−1 and 40 scans. The scanning electronic microscopy (SEM) observation of liquorice samples was obtained using A JEOL JSM–6700F system (JEOL, Japan) to get SEM images (100×, 200×, 300× and 500× magnification). Before measurement, samples were frozen in liquid nitrogen and dried in a vacuum freeze-dryer. Then, they were coated with a thin layer of gold using a sputter-coater (Hitachi Science Systems, Tokyo, Japan). The porous property characterization was measured by nitrogen adsorption and desorption isotherms on a Beshide 3H-2000PS2 sorption analyzer (BeiShiDe Instrument, China). The samples were degassed in a vacuum at 353 K for 6 h before measurement. The specific surface area in the relative pressure range between 0.04 and 0.16 was calculated by the multipoint BET method. The total pore volume at a relative pressure of 0.99 was estimated according to the BJH method. The median pore diameter was calculated as 4 V/A by the BET method. Pore size distribution was calculated according to the BJH method from the desorbed amount of liquid nitrogen.

[GL] = [GL]0 e (−k1 t − k3 t )

(4)

To calculate the differential form of GAMG and GA, Eq. (4) was substituted into Eq. (2) and Eq. (2) which governed the mass variation of GAMG and GA:

d [GAMG] + k2 [GAMG] = k1 [GL]0 e (−k1 t − k3 t ) dt

(5)

d [GA] dt = k3 [GL]0 e (−k1 t − k3 t ) + k2 [GL]0 ×

k1 e (−k1 t − k3 t ) − e (−k2 t ) k2 − (k1 + k3)

[

] (6)

Eqs. (4), (5) and (6) were integrated to get the final variations in yields of GL, GAMG and GA:

yGL =

[GL] = e (−k1 t − k3 t ) [GL]0

yGAMG = 2.4. Extraction and determination of glycyrrhizic acid and its hydrolytic products

yGA =

25 g SE liquorice was extracted with 500 ml 70% ethanol in a flask and placed in an ultrasound water bath (Kunshan Ultrasonic Instrument Co., Ltd., China) for 18 h (ultrasonic processing 30 min per hour). The ultrasonic frequency was 40 kHz and input power was settled at 250 W. After ultrasonic-assisted extraction, the samples were stored at 277 K for further analyses. Chromatographic separation of extracts was performed using a ZORBAX SB-C18 column (4.6 mm × 250 mm i.d., 5 μm) with an SPDM20A UPLC system (Agilent, America). Gradient elution was performed at 1 ml/min and 303 K using 0.1% phosphoric acid solution (A) and 100% acetonitrile (B) as mobile phases with a total run time of 41 min. The method applied in the following gradient elution order: 38–50% B at 0–3 min, 50–52% B at 3–10 min, 52%~58% B at 10–20 min, 85–90% B at 20–30 min, 90%~38% B at 30–35 min, 38% B at 35–41 min. The UV absorbance wavelength was set at 254 nm and injection volume of the sample was 20 µl. High resolution mass spectrometry was carried out using a MicroTOF-Q II Bruker Daltonic system (Bruker, Germany). ESI negative ionization mode was performed with the following settings; mass range: 50–3000 m/z, capillary voltage: 2600 V, drying gas: 6 L/min at 180 °C, nebulizer pressure: 200 kPa.

(7)

[GAMG] k1 = e (−k1 t − k3 t ) − e (−k2 t ) [GL]0 k2 − (k1 + k3)

(

[GA] k3 = [GL]0 k2 × (k1 + k3)

)

(8)

[ (k1 + k3) e(−k t ) − k2 e(−k t−k t ) ] 2

1

3

(9)

Thermal dynamic parameters of GL hydrolysis were determined as follows (Huang et al., 2016; Khan et al., 2016; Tizazu & Moholkar, 2018): Activation energy (Ea) was calculated from Arrhenius law expressed as:

ln k g = −

Ea + ln A RT

(10)

where kg is the kinetic constant, A represents the pre-exponential factor, T is the steaming temperature (K) and R is the gas constant (8.31451 J/ mol/K). Enthalpy change (ΔH) of hydrolysis is related to activation energy as: (11)

ΔH = Ea − RT

The entropies (ΔS) in hydrolysis are calculated according to the Eyring equation, which use the values of reaction rate constants (kg) and enthalpies change as:

ΔS h ⎞ ⎛ k g ⎞ + ΔH = ln ⎛⎜ ⎟ + ln R k B RT g ⎝T ⎠ ⎝ ⎠ ⎜

2.5. Reaction kinetic and thermodynamic analysis

⎟

(12)

where, h represents Plank’s constant (6.6260755 × 10−34 J·s) and B represents the Boltzman constant (1.380658 × 10−23 J/K). The Gibbs free energy (ΔG) for hydrolysis can be estimated by:

According to the fundamental chemical reaction kinetics theory of homogeneous reactions, the rate equations for the three compounds are expressed below:

ΔG = ΔH − T ΔS 3

(13)

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3.1. Physicochemical property analysis of SE liquorice

mono-saccharides by organic acids, such as acetic acids, which were produced from acetyl or other functional groups released from feedstock (Liu et al., 2015; Liu et al., 2017). Further degradation of sugars into furfural and hydroxymethylfurfural (5-HMF) might also take place during SE owing to thermal-acidic conditions (Sui & Chen, 2016). ASL and AIL contents after SE were mostly less than raw samples, while ASL decreased and AIL increased with the increase of steaming temperature. SE was also reported to induce the melting of lignin and its partial depolymerization through the homolytic cleavage of the predominant β-O-4′ ether and other acid-labile hemicellulose-lignin linkages (Liu et al., 2015; Rodríguez et al., 2017). The increased AIL content could be attributed to the generation of “pseudo-lignin”, defined as aromatic compounds yielding a positive klason lignin value not derived from native lignin (Hu, Jung, & Ragauskas, 2012). These compounds were generally generated following the polymerization or aggregation of carbohydrate macromolecules and by-products (such as furans) formed during SE. The reduction of cellulose content was owing to the fact that the treatment at high severity led to a reorganization of the paracrystalline and amorphous regions in cellulose of liquorice. As a result, SE treated samples exhibited an effective relative enrichment in water extracts and ethanol extracts, which were maximally increased by 0.24 folds and 3.24 folds, respectively. To further investigate the chemical modifications of liquorice by SE, a functional group analysis of liquorice samples was undertaken using FTIR spectroscopy. In Fig. S1, there is a decrease or a disappearance in the intensity of peaks at 1733 and 1236 cm−1, which were associated with the ester linkages C]O of the acetyl groups in hemicelluloses, were detectable in SE liquorice (Auxenfans et al., 2017; Sui & Chen, 2014; Sun et al., 2015). And it should be because of the removal of hemicelluloses from liquorice, confirming the chemical composition analyses (Table 1). The region between 1300 and 1600 cm−1 is largely contributed from the aromatic skeletal vibrations of lignin (Auxenfans et al., 2017). The bands at 1488 and 1436 cm−1 were reported to be the deformation of CeH within the methoxyl groups and C]C stretching of the aromatic rings in lignin (Sun et al., 2015). As steaming temperature increased, the intensity of two bands increased in the treated liquorice, which reflected an enrichment in condensed and cross-linked G-type lignin structures. The hydrogen bond intensity (HBI) is defined as the ratio of the intensity of the bands at 3400 cm−1 (OeH stretching, Hbonds between molecules) and 1360 cm−1 (CH rocking vibration of the glucose ring). It is closely associated with the crystal region and the degree of intermolecular regularity, i.e. crystallinity and the amount of bound water (Auxenfans et al., 2017). The HBI showed higher values for the treated samples (0.80 at SE condition of 480 K, 10 min) compared to the untreated materials (0.45), suggesting a more ordered cellulose structure after SE. In addition, the bands at 877–819 cm−1 were dominated by the β-(1 → 4)-glycosidic bond (C1-O-C4) and were cleaved by SE treatment (Sun et al., 2015). Overall, these results demonstrated that SE removed the structural components and increased the content of non-structural components, both of which might improve the exposure of intracellular glycyrrhizic acids and their accessibility to extraction solvents. Besides, the formation of a thermal-acid atmosphere through the above chemical reactions may exacerbate the GL transformation behaviour to some extent.

3.1.1. Chemical composition The chemical composition of liquorice samples was investigated and compared, as illustrated in Table 1. Results showed that SE obviously decreased the cellulose, hemicellulose, and ASL contents. Notably, about 61.18% of the hemicellulose fraction was removed under the most severe SE condition and this impact was higher as the severity of SE treatment increased. As confirmed in previous studies, the major physicochemical changes of lignocellulosic feedstock during SE process were ascribed to hemicellulose removal, lignin transformation and cellulosic amorphous region deconstruction (Sui & Chen, 2016; Sui et al., 2018). The hemicelluloses were easily hydrolyzed to oligo- and

3.1.2. Morphological and porous properties The ultrastructure of SE liquorice as observed through optical and SEM imaging indicated a large variation in liquorice morphology after SE (Fig. S2). According to Fig. S2a-c, SE led to an overall reduction in the particle size and a browning in the colour of liquorice samples. The observed darkening of SE liquorice could be related to the successive degradation of carbohydrate structures to acetic, formic acids and other pyroligneous acids, as well as the polymerization of furans (or aromatic rings) and other sugar degradation products, which ultimately led to the production of char at severe SE conditions (Rodríguez et al., 2017). The treatment led to the delamination of phloem and xylem, the

2.6. Extraction kinetic analysis The extraction kinetics were analyzed based on Fick’s second law. Mass transfer of bioactive compounds in the matrix follows (Sui & Chen, 2014):

∂ [cg ] ∂te

= Dg

∂2 [cg ] ∂r 2

(14) ∂ [cg ]

Boundary condition (1): ∂r = 0 at r = 0 for all te Boundary condition (2): [cg ] = [cg ]i = 0 at r = R for all te > 0 Initial condition: [cg ] = [cg ]0 at te = 0 for r < R where subscript g represents one of GL, GAMG and GA, cg0 is their initial concentration in the particle, R is the particle radius. Under any initial conditions, if the sphere is maintained at a uniform concentration c0 and the surface concentration remained constant at cgi = 0, the solution becomes:

[cg ] − [cg ]0 [cg ]i − [cg ]0

=1+

2R πr

∞

∑ n=1

Dg n2π 2te ⎞ (−1)n nπr sin exp ⎜⎛− ⎟ n R R2 ⎠ ⎝

(15)

The correcting factor A is introduced in order to avoid the concentration error resulting from unstable factors in the initial extraction procedure. The total amount of diffusing compounds entering or leaving the sphere is given by:

[cg (te )] [cg ]∞

=1−A

6 π2

∞

∑ n=1

Dg n2π 2te ⎞ 1 exp ⎜⎛− ⎟ 2 n R2 ⎠ ⎝

(16)

All terms except the first become negligible after a short period. Since the mass transferred from the sphere at time t is equal to the mass [C ] in the solution [Cg], the determined data points of g versus t can be [Cg ]∞

described by a typical exponential equation (which is calculated for 6 A 2 = 1) with sufficient accuracy: π

[Cg ] [Cg ]∞

= 1 − exp(−Hte )

(17)

where H is an empirical adjustable constant. So the diffusion coefficient is deduced:

Dg =

HR2 π2

(18)

2.7. Statistical analysis All the experiments were performed in triplicate with the average value being reported on the dry basis. The differences between variables were tested for significance using ANOVA and Duncan’s multiple range test. Differences between means were considered significantly different at P < 0.05 (SPSS for Window 24.0). 3. Results and discussion

4

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Table 1 Composition (g/100 g of raw material) of raw liquorice and SE liquorice. Steaming Temperature (K)

Steaming time (s)

Raw liquorice 443 K 464 K 480 K 464 K 464 K 464 K

600 600 600 120 600 1200

Water extracts (%)

Ethanol extracts (%)

Cellulose (%)

Hemicellulose (%)

Acid soluble lignin (%)

Acid insoluble lignin (%)

Ash (%)

43.33 53.84 53.69 52.93 49.22 53.69 53.58

1.35 3.79 3.56 5.72 3.43 3.56 3.80

18.78 17.67 12.11 15.16 11.37 12.11 11.88

7.29 5.34 3.17 3.46 3.64 3.17 2.83

2.16 1.54 1.28 1.02 1.49 1.28 1.09

11.72 ± 0.67 7.43 ± 0.04 9.80 ± 0.12 10.97 ± 0.21 10.60 ± 0.02 9.77 ± 0.11 12.79 ± 0.58

0.13 0.27 0.37 0.27 0.27 0.40 0.27

± ± ± ± ± ± ±

0.76 2.97 1.44 1.57 0.98 1.44 1.03

± ± ± ± ± ± ±

0.82 1.34 1.02 1.54 0.37 1.02 0.79

± ± ± ± ± ± ±

0.37 0.25 1.01 0.5 1.06 1.01 0.66

disentangling and exposure of fibrous strands, as well as the loosening of the fibrous network occurring progressively with increasing steaming temperature and time. SEM images of SE samples presented a disorganized, rugged and rough morphology, which could be elucidated by the coupling effect of the hydrolytic chemical reactions and intense shearing forces of SE process. The apparent separation and unloosening of fiber bundles were obtained after SE accompanied with structural distortions in parenchyma. Another feature was the disappearance of starch droplets that often existed in parenchyma cells as a result of starch gelatinization in the high temperature of SE, seen as the appearance of melted sample surfaces. To better understand the significant influence of SE on the porous structure of liquorice, the pore distribution characteristics of SE liquorice were investigated by the N2 adsorption method (Fig. S3). Within the valid range of pore size tested (1.795–418.695 nm), compared with untreated liquorice, the median pore diameter increased from 55.36 nm to 112.49 nm and the total volume of pores increased by 64% after SE, leading to a reduction of surface area. This suggested that nanopores among fibrils in the cell wall were unblocked or new nanopores were formed. According to the pore size distribution calculated from dV/dd and dS/dd, both the volume and area of pores smaller than 10 nm decreased after the treatment. The reason could be that the hemicellulose and lignin of the interwoven wrapped cellulose crystalline structure were broken and the mutually binding force between holocellulose and lignin was weakened by SE under different explosion pressures. This is contrary to SE polar and corn stover where the pores of 5–9 nm increased (Zhao & Chen, 2013), but new pores were gradually formed above 75 nm (Fig. S3B), suggesting the transformation of small pores into large pores. The small particle size and large pore diameter of SE liquorice should facilitate the mass transfer process of GL and its hydrolyzed products.

± ± ± ± ± ± ±

0.29 0.05 0.31 0.13 0.35 0.31 0.25

± ± ± ± ± ± ±

GL

Extraction yield (mg/g)

A

0.15 0.02 0.06 0.07 0.04 0.06 0.04

GAMG

± ± ± ± ± ± ±

Total proportion (%) 0.01 0.01 0.02 0.03 0.01 0.03 0.04

84.74 90.87 83.97 89.53 80.02 83.97 86.24

± ± ± ± ± ± ±

3.07 6.48 3.97 4.05 2.84 3.97 3.39

GA

36 34 32 30 28 26 24 22 20

6 4 2 0

Raw

443 K

452 K

464 K

471 K

480 K

Steaming temperature (K)

Extraction yield (mg/g)

B

3.2. Reaction kinetic and thermodynamic analysis of GL hydrolysis during SE process

36 34 32 30 28 26 24 22 20

6 4 2

3.2.1. Effects of SE conditions on the GL hydrolysis process Fig. 1 shows the effects of SE steaming temperature and time on GL, GAMG and GA contents of liquorice. With the increase in temperature and time, results showed that GL content declined from 33.96 mg/g to 23.53 mg/g. This meant that GL was hydrolyzed by 30.71%. The GAMG content was generated up to 1.78 mg/g by the cleavage of distal glycosidic bonds in GL and the removal of monomolecular glucuronide. And then it slightly reduced because of its decomposition to produce GA. The glucoside bonds were susceptible to thermal processing owing to their weak stability in aqueous solutions. The maximum conversion rate, 5.24% of GAMG, was reached at the SE condition of 1.0 MPa, 10 min. As a result, the GA content increased correspondingly from 0.14 mg/g to 7.43 mg/g, reaching the highest conversion rate of 21.47%. According to some literature (Fan et al., 2016), higher temperatures would lead to further degradation of GA and result in its decreased tendency, which were not observed in this work. In the SE process, hydrolytic reactions tended to be carried out at high temperatures under mild acidic conditions. The acidic environment largely

0

Raw

2 min

5 min

10 min 20 min

30 min

Steaming time (min) Fig. 1. The effect of steaming temperature (A) and retention time (B) on the conversion ratio of GL and formation ratios of GAMG and GA. A: the hydrolysis reactions were carried out at steaming time of 10 min for different temperatures; B: the hydrolysis reactions were carried out at steaming temperature of 464 K for different times.

came about from the decreased pKw of water with increased steaming temperature and the further release of organic acids from structural components (Bai et al., 2018). The acetyl groups became an in situ source of acetic acids that subsequently catalyzed GL hydrolysis. Results showed that positive energy could be provided for the cleavage of glucosidic bonds to form GAMG and GA, under high temperature and pressure, as well as acidic conditions. As is well-known, both the 5

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[GL]/[GL]0 vs. t (Fig. 3A). Linear relationships of the plots suggest good estimates of irreversible consecutive first-order theoretical models using Eqs. (7)–(9) within the steaming time. Similar results were reported in previous research (Fan et al., 2016; Ruen-ngam et al., 2012), the general approach for kinetic analysis of GL hydrolysis could be performed based on the first order reaction. The estimated kinetic parameters are depicted in Fig. 3B. Based on these parameters, GA concentration profiles with time were calculated through the theoretical model. Their comparisons with the experimental results for each temperature are depicted in Fig. 3D. Fig. 3D shows deviations within a 20% range, suggesting that the proposed model and kinetic parameters fit well with the obtained experimental data. As seen from Fig. 3B, k2 and k3 values for most hydrolysis temperatures are higher than k1 values. This essentially indicates that the cleavage of β-1,3 glucosidic bond is easier than β-1,2 glucosidic bond. And k2 values are larger than k1 values, implying that GAMG hydrolysis is much faster than its formation, which is adverse to GAMG for accumulation. The direct formation of GA is predominant according to the above results. This is analogous to literature, which reported that GA is the main product and GAMG is the minor product during GL hydrolysis in subcritical water (Fan et al., 2016). Besides, the kinetic parameters are a strong function of hydrolysis temperature. With the rise in temperature, k1 and k2 increased at first and decreased later, but k3 progressively increased. It suggested that high temperature caused the hydrolysis of GL. A possible explanation to this result can be given as follows: intuitively, as temperature increased, molecules started to move faster and as molecules moved faster they were likely to collide and therefore reacted with each other (Swati, Haldar, Ganguly, & Chatterjee, 2013). The time for producing GAMG and GA by SE was much shorter than that of other biosynthesis methods that lasted for several dozens of hours. It is concluded that SE technology for the conversion of GL is efficient.

steaming temperature and time directly influence reaction equilibrium and rate constants, thus are principal factors to control chemical reactions. A similar result was reported by Fan et al. (2016) who showed the interaction between reaction temperature and time on the hydrolytic reaction of glycosides. At lower temperatures, GL needed more time to accumulate energy to be hydrolyzed; while at higher temperatures, GL was hydrolyzed completely in a shorter time. It has also been reported that SE could change the physicochemical characteristics and induce the deglycosylation conversion of some glycosidic structures, e.g. quercitrin, the dominant flavonoid in sumac fruits, which was deglycosylated and converted into quercetin by SE treatment (Chen & Chen, 2011). Compared with other technologies, the steaming time is shorter and the conversion is carried out in situ without the addition of acid or enzyme in the SE process. The concentration behaviour indicates a complicated reaction mechanism for GL hydrolysis. There are two parallel reactions. One is a consecutive reaction via an intermediate product, GAMG, following its degradation to GA. The other one is the direct cleavage of β-1,3 glycosidic bond of GL to form GA. Glucuronic acids are the main by-products of the hydrolysis reaction and their formation from the reaction has been observed elsewhere (Chen et al., 2012; Fan et al., 2016). A hydrothermal reaction would break both glycosidic bonds in GL, thereby obtaining GAMG and GA. The possible mechanism should be that: protonation of the CeOeC glucosidic bond followed by a cyclic carbanion formation and the aglycon part elimination by the scission of corresponding bonds. And it is indicated that the reaction is mainly triggered by the attacking of proton ions decomposed from liquorice structural carbohydrates. So the GL hydrolysis reaction is a multi-step process, including four steps listed as follows (Fig. 2): a) Diffusion of protons through the liquorice matrix. The protons were generated from the breakage of bonds between hemicellulose and lignin under high temperature and pressure of SE. Hemicellulose was broken to form pentoses, hexoses and acetic acids, and the noncrystalline region of cellulose was degraded to form glucose (Liu et al., 2017; Sui et al., 2018). As the proton concentration increased, the degradation products such as glucose and xylose were further degraded to 5-HMF and furfural under thermal-acid catalysis; and as the temperature increased, 5-HMF and furfural continued to be degraded to form formic acids and levulinic acids (Ramli and Amin, 2018; Sui & Chen, 2016; Wang, Chang, Ma, Sun, & Wu, 2015). b) The oxygen atom in the glycosidic bond was attacked by hydrogen protons, resulting in its rapid protonation and the formation of oxonium ion (Qiao, Teng, Zhai, Na, & Zhu, 2018). The most likely case was that, both oxygen atoms were protonated with the position of the scission depending upon electronic density distribution on the intermediate carbanion. c) The instability of the oxonium ion led to the breakage of glycosidic bond. The positive electrical charge was transferred to C1 of glucuronic acid, and thus the intermediates, which appeared in the glycosyl carbemum ion and half-chair structure were formed, accompanied by the removal of aglycon (Fan et al., 2016). In fact, a slight rotation of the ring constitutive groups can give rise to the mandatory half-chair conformation of the cyclic carbanion. And the energy required for this step is dependent on the electronic density distribution on the intermediate carbanion (Belkacemi, Abatzoglou, Overend, & Chornet, 1991). d) The carbemum ion on intermediates reacted with water, forming dissociative glucuronic acids and releasing hydrogen protons, which participated in the circle of glycosidic bond hydrolysis. Meanwhile, the reaction products were back diffused from the liquorice matrix in a liquid phase micro-environment (Tizazu & Moholkar, 2018).

3.2.3. Thermodynamic analysis of GL hydrolysis reaction Activation energy (Ea) and pre-exponential factors (A) were calculated from Arrhenius plots (lnkg versus 1/T) according to Eq. (10), based on the slope and y-intercept of the estimated linear lines connecting the point, respectively (Fig. 3C). The calculated results are shown in Table 2. The change of Ea shows the energy differences between the activated complex and the reagents. This kinetic parameter is of vital importance to reveal the activation energy which is needed to keep the chemical reaction going (Huang et al., 2016; Maia & de Morais, 2016). It is favoured to form an activated complex if this energy difference is slight, indicating the low potential energy barrier. And A reflected the frequency of molecular collisions, a higher A value indicated more possibility of an effective collision, which might imply the occurrence of a chemical reaction (Swati et al., 2013). According to Table 2, the value of Ea1 (14.30 kJ/mol) is lesser than Ea2 (63.64 kJ/ mol) and Ea3 (42.91 kJ/mol). The lower values of Ea1 meant that the energy barrier for the cleavage of β-1,2 glucosidic bond could be lower than β-1,3 glucosidic bond, leading to the easier hydrolysis of GL to GAMG. Similar variation was also observed in the report of Fan et al. (2016). They attributed this variation to the stronger steric interactions (intramolecular and intermolecular van der Waals repulsions). The steric hindrance would delay attacks on the carbocation by H+ selfdissociated of water. While the A1 value is lesser than A2 and A3, implying the lower effective collision frequency of reactionGL→GAMG. Therefore, the lower energy barrier of reactionGL→GAMG made substrates easier to be activated, but once activated, the reaction proceeded slowly, as presented by the low value of k1. And the Ea3 value is less than Ea2, therefore lower energy is needed to overcome the energy barrier of reactionGL→GA, inferring that it could easily reach the transition state in a quicker hydrolysis, as presented by k3﹥k2. The obtained values for activation energy (14.30–63.64 kJ/mol) are lower than the range of those reported from the hydrothermal hydrolysis of GL in subcritical water (36.51–129.52 kJ/mol), the possible reason is that the

3.2.2. Kinetic analysis of GL hydrolysis reaction The overall hydrolysis reactions of GL were considered to follow a first-order rate kinetics. The reaction order was verified by plotting ln 6

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Fig. 2. Proposed major reaction pathways and mechanism of GL hydrolysis.

and ΔS3 (−0.235 kJ/K·mol). The higher value of ΔS2 means that GAMG are more activated, disordered and have more degrees of freedom of rotation, as well as vibration. Under this circumstance, the reactivity is high, and the system could react faster to produce the activated complex, resulting in the shortened reaction time and the accelerated mass loss rate that was observed. The increase in disorderness of GAMG suggests correlation with their lower thermal stabilities. Gibb’s free energy (ΔG) is an important state function used to conclude the degree and spontaneity of chemical reactions. It is a comprehensive evaluation of the heat flow and disorder change. A higher value of ΔG indicates a lower favourability of reaction (Khan et al., 2016; Tizazu & Moholkar, 2018). As illustrated in Table 2, all reactions had positive ΔG values. It reveals that these reactions are endergonic and non-spontaneous. And the thermodynamical favourability order of reactions is the following: reactionGL→GA﹥reactionGAMG→GA﹥reactionGL→GAMG. In terms of ΔG, reactionGL→GA had the smallest energy barrier and absorbed the least amount of heat in most temperatures, and it increased the disorder of the system compared to other reactions, and hence, it had the highest favourability. This result is in agreement with the calculated results of kinetic parameters. In addition, ΔG of the three reactions increased with the increase of reaction temperature. The result emphasizes the importance of the high temperature to accelerate the hydrolytic reaction for overcoming the non-spontaneity of the process.

reactivity of activated molecules were stronger under the high pressure of saturated steam. Table 2 shows thermodynamic parameters (ΔH, ΔS and ΔG), which were calculated from Eqs. (11) to (13). The enthalpy (ΔH) value is the energy difference between the reagent and the activated complex, which ascertains that the reaction will be endothermic or exothermic (Huang et al., 2016; Khan et al., 2016). All three reactions showed the positive ΔH values, which meant that the hydrolysis of GL was endothermic. The conversion of reactants into their transition state required an external source of energy to raise their energy level. Based on the obtained calculated value, the variation in the enthalpy change (ΔH2﹥ΔH3﹥ΔH1) is consistent with the change of activation energy. The smaller difference corresponds to the need of lower energy for the formation of activated complex and thermal decomposition, indicating a more reactive system. The value of ΔS is associated with the degree of order in the transition state. A positive ΔS demonstrates that the disorder of the system would be increased by the reaction, and thus, the reaction is favourable (Huang et al., 2016; Khan et al., 2016; Tizazu & Moholkar, 2018). It is found that the entropy of the three reactions has negative values, which indicate that the structure at transition state is more orderly than that of reactant. A similar trend in entropy change of GL hydrolysis was also observed in the report of Fan et al. (2016). The ΔS2 of reactionGAMG→GA varied from −0.191 kJ/K·mol to −0.186 kJ/ K·mol and showed higher average value than ΔS1 (−0.300 kJ/K·mol) 7

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Fig. 3. A: Plots of ln([GL]/[GL]0) vs. t for evaluation of overall rate constants for GL hydrolysis; B: Plots of estimated kinetic parameters of GL hydrolysis in SE process; C: Eyring plots of hydrolytic reaction at different steaming temperatures; D: Comparison between calculated and experimental values of GA concentrations.

were extracted in a larger amount. The extraction yields of all three compounds were significantly increased until 2 hours and then remained constant, which implied their extraction equilibrium was faster to reach. While the extracting process of raw samples showed the trend towards equilibrium at the end of extraction for over 18 h. In combination with the analysis in Section 3.1.2, it can be concluded that SE effectively promoted the diffusion of GL and its converted products through the reconstruction of multi-scale porous network. This phenomenon is in accordance with many previous reports (Chen & Chen, 2011; Sui & Chen, 2014). Table 3 lists the estimated results of maximum extraction concentration C∞ and diffusion coefficient D for GL, GAMG and GA. The decomposition of GL in the SE process led to the reduction of C∞, and correspondingly, C∞ values of GAMG and GA were increased. As the temperature rose, there occurred the conversion of GAMG to GA, as presented by a decrease in C∞ of GAMG and an increase in C∞ of GA. It is worth noting the D values of GL and GA are significantly increased after SE, which are 3.07 folds and 1.53 folds than untreated liquorice. The physic-chemical changes of SE liquorice including the degradation of cell wall components, the destruction of tissue structure and the magnification of pore diameters in Section 3.1, are all bound to improve the mass transfer pathway of solutes and weaken the internal diffusion resistance, which can be reflected by the increase of D. Above results indicate that SE not only facilitates GL conversion, but also improves the extraction efficiency of its converted products, aiming to promote their valuable utilization.

Table 2 Estimated reaction kinetic and thermodynamic parameters of GL hydrolysis at different temperatures. Temperature (K)

Reaction

A (s−1)

Ea (kJ/mol)

R2

443 ~ 480

1 (GL → GAMG) 2 (GAMG → GA) 3 (GL → GA)

0.00168 2999.86 14.4100

14.30 63.64 42.91

0.8523 0.7978 0.8742

Temperature (K)

Reaction 1 (GL → GAMG) 2 (GAMG → GA) 3 (GL → GA)

△S (kJ K−1 mol−1) −0.310 −0.191 −0.235

△G (kJ)

443

△H (kJ/ mol) 10.61 59.95 39.22

Temperature (K)

Reaction 1 (GL → GAMG) 2 (GAMG → GA) 3 (GL → GA)

△S (kJ K−1 mol−1) −0.308 −0.186 −0.234

△G (kJ)

464

△H (kJ/ mol) 10.43 59.77 39.04

Temperature (K)

Reaction 1 (GL → GAMG) 2 (GAMG → GA) 3 (GL → GA)

△S (kJ K−1 mol−1) −0.311 −0.192 −0.235

△G (kJ)

480

△H (kJ/ mol) 10.30 59.64 38.82

148.19 144.83 143.27

153.75 146.63 147.75

159.72 152.14 151.97

3.3. Extraction kinetic analysis of GL and its hydrolytic products after SE The concentration profiles with extraction time for GL and its hydrolyzed products at SE conditions of 443–480 K and 10 min are shown in Fig. S4. The breaking points indicate the measured values and the continuous lines represent the fits with the exponential function from Eq. (17). According to Fig. S4, with the comparison to raw liquorice, the extraction yield of GL after SE was lower and its hydrolyzed products

4. Conclusions In summary, SE removed the structural components in cell wall of liquorice by maximally 61.18% of hemicellulose, 39.46% of cellulose 8

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Table 3 Extraction kinetic parameters of GL, GAMG and GA from raw and SE liquorice. SE condition

GL

GAMG

Steaming temperature (K)

C∞ (mg/g)

D (10

Raw liquorice 443 K 464 K 480 K

31.22 21.85 22.67 21.50

0.29 0.95 0.91 1.18

−9

2

m /s)

R

2

0.9965 0.9494 0.9512 0.9454

C∞ (mg/g)

D (10

0.188 2.03 1.48 1.58

0.50 1.02 1.93 2.16

2

m /s)

R

C∞ (mg/g)

D (10−9m2/s)

R2

0.8164 0.9096 0.9140 0.9570

0.14 4.34 4.30 5.83

1.31 1.73 2.27 3.32

0.8767 0.8292 0.9201 0.9608

2

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and 35.37% of lignin, and restructured the multi-scale porous network of liquorice by increasing 1.03-fold median pore diameter and 0.64-fold pore volume, both of which facilitated the formation of thermal-acid atmosphere and the accessibility to reaction and dissolution reagents. SE was thus applied as a new method for in situ hydrothermal autohydrolysis of GL into GAMG and GA, by which 30.71% of GL conversion, 5.24% and 21.47% of GAMG and GA formation were obtained. The concentration behaviour suggested multistep reaction mechanism for GL hydrolysis with endothermic, non-spontaneous and entropy-decreasing features. And SE was inclined to induce the cleavage of β-1,3 glycosidic bond with low energy barrier in GL, leading to GA as the main product and GAMG and glucuronic acids as minor products. Extraction kinetics indicated that SE effectively promoted the diffusion of GL’s hydrolyzed products by raising the diffusion coefficient D and shortening the equilibrium time by 90% at least. It was concluded that SE provided a potential way to improve the conversion and extraction of GL and its high-value hydrolyzed products, which has positive significance to apply SE technology for product development and functional enhancement in the food and medicinal processing field. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper Acknowledgements The work was supported financially Program of China (2016YFD0400803), Foundation of China (21808171), Tianjin (18JCQNJC84100) and Beijing Advanced Nutrition and Human Health, Beijing University (BTBU).

GA −9

by the National Key R&D National Natural Science Natural Science Foundation Innovation Center for Food Technology and Business

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B. (2015). A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nature Genetics, 47, 784–792. Xu, G., Cai, W., Gao, W., & Liu, C. (2016). A novel glucuronosyltransferase has an unprecedented ability to catalyse continuous two-step glucuronosylation of glycyrrhetinic acid to yield glycyrrhizin. New Phytologist, 212, 123–135. Zhang, H. X., Sun, G., Gu, J. L., & Du, Z. Z. (2017). New sweet-tasting oleanane-type triterpenoid saponins from “Tugancao”(Derris eriocarpa How). Journal of Agricultural and Food Chemistry, 65, 2357–2363. Zhao, J., & Chen, H. (2013). Correlation of porous structure, mass transfer and enzymatic hydrolysis of steam exploded corn stover. Chemical Engineering Science, 104, 1036–1044. Zhao, Y. J., & Li, C. (2018). Biosynthesis of plant triterpenoid saponins in microbial cell factories. Journal of Agricultural and Food Chemistry, 66, 12155–12165.

10