Characterization of Lentinus edodes β-glucan influencing the in vitro starch digestibility of wheat starch gel

Food Chemistry 224 (2017) 294–301

Contents lists available at ScienceDirect

Food Chemistry journal homepage: www.elsevier.com/locate/foodchem

Characterization of Lentinus edodes b-glucan influencing the in vitro starch digestibility of wheat starch gel Haining Zhuang a, Zhongqiu Chen b, Tao Feng b,⇑, Yan Yang a, Jingsong Zhang a, Guodong Liu c, Zhaofeng Li c, Ran Ye d a Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, Key Laboratory of Edible Fungi Resources and Utilization (South), Ministry of Agriculture, National Engineering Research Center of Edible Fungi, National R&D Center for Edible Fungi Processing, Shanghai 201403, PR China b School of Perfume and Aroma Technology, Shanghai Institute of Technology, Shanghai 201418, PR China c School of Food Science and Technology, Jiangnan University, Wuxi 214122, PR China d Roha USA, 5015 Manchester Ave, St. Louis, MO 63110, USA

a r t i c l e

i n f o

Article history: Received 15 October 2016 Received in revised form 20 December 2016 Accepted 22 December 2016 Available online 24 December 2016 Chemical compounds studied in this article: Iodine (PubChem CID: 807) Sodium acetate (PubChem CID: 517045) Acetic acid (PubChem CID: 176) Sodium hydroxide (PubChem CID: 14798) Potassium iodide (PubChem CID: 4875) Sodium nitrate (PubChem CID: 71309218) Monosodium Phosphate (PubChem CID: 23672064) Trifluoroacetic Acid (PubChem CID: 6422) Ethanol (PubChem CID: 702)

a b s t r a c t Lentinus edodes b-glucan (abbreviated LEBG) was prepared from fruiting bodies of Lentinus edodes. The average molecular weight (Mw) and polydispersity index (Mw/Mn) of LEBG were measured to be 1.868
106 g/mol and 1.007, respectively. In addition, the monosaccharide composition of LEBG was composed of arabinose, galactose, glucose, xylose, mannose with a molar ratio of 5:11:18:644:16. After adding LEBG, both G0 and G00 of starch gel increased. This is mainly because the connecting points between the molecular chains of LEBG and starch formed so that gel network structures were enhanced. The peak temperature in the heat flow diagram shifted to a higher temperature and the peak area of the endothermic enthalpy increased. Furthermore, LEBG can significantly inhibit starch hydrolysis. The predicted glycemic index (pGI) values were reduced when starch was replaced with LEBG at 20% (w/w). It might indicate that LEBG was suitable to develop low GI noodle or bread. Ó 2016 Elsevier Ltd. All rights reserved.

Keywords: LEBG (LEBG) Rheological properties Thermal properties In vitro starch digestibility

1. Introduction Mushroom is the spore-bearing fruiting body of a fungus, typically appeared above ground depending on food resources. Fresh and preserved mushrooms are consumed in many countries as a delicacy, particularly for their specific aroma and texture (Pavel, 2013). Mushrooms have been playing important roles in several

⇑ Corresponding author at: School of Perfume and Aroma Technology, Shanghai Institute of Technology, No. 100 Hai Quan Road, Shanghai 201418, PR China. E-mail addresses: [email protected] (H. Zhuang), czq594915620@163. com (Z. Chen), [email protected] (T. Feng), [email protected] (Y. Yang), [email protected] (J. Zhang), [email protected] (G. Liu), zfli@jiangnan. edu.cn (Z. Li), [email protected] (R. Ye). http://dx.doi.org/10.1016/j.foodchem.2016.12.087 0308-8146/Ó 2016 Elsevier Ltd. All rights reserved.

aspects of human health. It is well-known that mushrooms contain a very large variety of nutritional biomolecules (Ahmad, Anjum, Zahoor, Nawaz, & Dilshad, 2012; Lindequist, Niedermeyer, amp, lich, & WolfDieter, 2005; Poucheret, Fons, & Rapior, 2006). Among the family of mushroom, Lentinus edodes are the main cultivated edible mushroom in the world. Lentinus edodes have been applied into many Asian cuisines, because of not only their unique flavour characteristics, but also because of their known medicinal and nutritional properties, including decreasing the risk of developing hypertension, hypercholesterolaemia, diabetes mellitus and cancer (Her, Min, Kim, & Lee, 2015). Due to these properties, mushrooms have been recognized as functional foods, and as a natural source for the development of medicines, nutraceuticals, and cosmeceuti-

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301

cals (Zhu, Du, Bian, & Xu, 2015). b-glucan is one of the most potential components (Ren, Perera, & Hemar, 2012). b-Glucan is a polysaccharide of d-glucose monomers linked by b-glycosidic bonds. It is a kind of dietary fibre in cereals, yeasts, mushrooms, some bacteria and seaweeds (Du, Bian, & Xu, 2014). The biological activities of b-glucan are presented in immunological activity (Borchers, Keen, & Gershwin, 2004), antitumor activity (Lindequist et al., 2005), radioprotective properties (Pillai & Devi, 2013), antioxidant activity (Deng et al., 2012), cardiovascular properties (Wasser & Weis, 1999), hypoglycaemic activity (Beattie et al., 2010) and hepatoprotective activity (Zhang et al., 2013). Diabetes mellitus (DM) is a debilitating and life-threatening metabolic syndrome characterised by inappropriate hyperglycaemia caused by a relative or absolute deficiency of insulin or by a resistance to the action of insulin at the cellular level. According to the International Diabetes Federation, 387 million people have diabetes worldwide. It has been become one of the world’s main killers. The inhibition of starch digestion is highly concerned because 40–50% of the body’s daily energy is provided by starch which is widely present in food (Zhao, Wu, Yang, Liu, & Huang, 2015). According to the rate and extent of its digestion, starch is generally classified into rapidly digestible starch (RDS), slowly digestible starch (SDS), and resistant starch (RS) (Englyst, Kingman, & Cummings, 1992). The glycemic index (GI) concept was introduced to classify different carbohydrate-rich foods with respect to their effect on post-meal glycaemia. Therefore, foods can be classified into three classes: low GI, medium GI and high GI. The low GI foods can prevent and control diabetes (Atkinson, Fosterpowell, & Brandmiller, 2002) . Ingestion of high RDS food will cause the increases of GI, negatively affecting human health. RS is not absorbed in the small intestine and can improve sensitivity to insulin and regulate blood sugar balance of the body (Kapelko, Zieba, Pietrzak, & Gryszkin, 2016). Moreover, it also could improve the postprandial satiety and reduces calorie intake of the body. In addition, it could also prevent the occurrence of intestinal diseases, diabetes, obesity and other chronic diseases. Intake of high level of SDS will not produce hyperglycemia and insulin response (Kendall, Emam, Augustin, & Jenkins, 2004). The efficacy of b-glucan as a potential bioactive hypoglycemic component is related to its structure, solubility, molecular weight (MW) and rheological characteristics (Cleary, Andersson, & Brennan, 2007). Some studies have shown that the soluble fibre b-glucan could slow the rate of starch digestion. Cleary (Cleary et al., 2007) illustrated that barley b-glucan (BBG) was incorporated into starch at 2.5, 5, 7.5 and 10% (w/w). Incorporation of the BBG to starch attenuated sugar release during starch digestion in vitro. In a study of Wu (Jia & Xie, 2011), it was demonstrated that the hypoglycemic effect of oat b-glucan was greatly related to its viscosity. The viscosity of starch and b-glucan mixed systems depended on the solid concentration and pasting properties. Since b-glucan and starch formed the viscous gel in the intestinal. The viscous gel could delay the absorption of glucose leading to the decreases in postprandial blood glucose. Most studies have been focused on b-glucan of oats and other cereals to inhibit in vitro starch digestion. However, little attention has been paid on the effects of LEBG on in vitro starch digestibility. In this study, LEBG was applied to prepare mixed gels with wheat starch followed by enzymatic hydrolysis. Rheological properties and thermal properties of mixed gels were also measured. Therefore, the aim of this study is to explore the impact of LEBG on wheat starch digestion in vitro. This study will provide valuable information for future research on the development of hypoglycemic food with LEBG and wheat starch.

295

2. Materials and methods 2.1. Materials LEBG was prepared by ourselves according to the schematic in Fig. 1 and the purity of LEBG is up to 70.62% (w/w). Wheat starch was purchased from Shandong Qufeng Food Tech Co., Ltd, China. a-amylase type VI-B (EC 3.2.1.1, 19.6 units/mg) from porcine pancreas, amyloglucosidase (EC 3.2.1.3, 21.1 units/mg) from Rhizopus mold, pepsin (EC 3.4.23.1, 51 units/mg) from porcine stomach mucosa, pancreatin (EC 3.4.4.4, 100 units/mg) from porcine pancreas and invertase (EC 3.2.1.26, 300 units/mg) were purchased from Sigma Chemical Co. (St. Louis, MO, USA). Glucose assay reagents were bought from Nanjing Jiancheng Bioengineering Institute, China. 2.2. High performance size exclusion chromatography analysis All samples were dissolved in solutions (2 mg/mL) to analyze the purity and molecular weight by high performance size exclusion chromatography (HPSEC). The system was consisted of Waters 2695 HPLC system equipped with multiple detectors: a refractive index detector (RI). The column was a TSK-GEL G6000PWXL filtration column which was eluted with phosphate buffer (abbreviated PB) (0.15 mol/L NaNO3 and 0.05 mol/L NaH2PO4, pH = 7) at a flow rate of 0.5 mL/min. The calibration of the refractive index detector was done with Pullulan shodex standard (p-82, Sigma). Astra software (Version 6.1, Wyatt Technology Co., Ltd. USA) was utilized for data acquisition and analysis. Columns temperature and RI detector temperature were maintained at 35.1 °C. The molecular weight was calculated according to the method as previously described by Zhang (Zhang, 2010). 2.3. Monosaccharide composition analysis of LEBG The composition of LEBG was measured according to the preceding study by Liu (Liu et al., 2013). Three fractions (2 mg) were hydrolyzed with 4 mL 2 mol/L trifluoroacetic acid (TFA) at 110 °C for 3 h. The monosaccharide composition was determined by high performance anion exchange chromatography (HPAEC) using a Dionex LC 30 equipped with a CarboPacTM PA20 column (3 mm
150 mm). The column was eluted with 2 mmol/L NaOH (0.45 mL/min) followed by 0.05 to 0.2 mol/L NaAc and the monosaccharides were monitored using a pulsed amperometric detector (Dionex, company name, state name, USA). Monosaccharide components were characterized and determined using d-Gal, d-Glc, d-Ara, l-Rha, d-Man and d-Xyl standards (Sigma-Aldrich).

2.4. Infrared spectra analysis of LEBG The infrared spectra analysis of LEBG was determined based on the method described by Tie (Mei et al., 2008). After LEBG was mixed with KBr tablet, the infrared spectrometer scan analysis was made with resolution of 4 cm1 and accumulated 32 times. Air background was deducted before scanning, and then scanning range was from 4000 cm1 to 400 cm1. 2.5. Differential scanning calorimetry of LEBG/starch gel systems Differential scanning calorimetry (DSC, TA-Instruments, model Q2000, USA) was used to determine thermal transitions associated with starch gelatinization. The mixture of LEBG and wheat starch was weighed into a DSC aluminum pan. The mixture of LEBG and

296

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301

Fig. 1. Extraction Process of LEBG.

wheat starch is 2 mg. And the ratio of LEBG is 0, 2.5, 5, 10, 20%(w/ w), respectively. Distilled water (4 mL) was added, and pans were hermetically sealed. Sample pans were equilibrated for 12 h prior to testing at room temperature. Starch dispersions were gelatinized from 20 to 100 °C at a heating rate 10 °C/min. An empty pan was used as a reference, and the system was calibrated with indium.

2.6. Rheological property measurement of LEBG/starch gel systems Wheat starch with LEBG (0%, 2.5%, 5%, 10% and 20% based on dry weight of starch) was first cooked at 135 °C for 2 h to make the starch be completely gelatinized. To measure the viscoelastic property of mixed wheat starch gel affected by LEBG, a strain sweep test on starch paste was first performed from 0.1 to 1% strains at 1 Hz and 25 °C to identify the linear viscoelastic region. Then, the frequency sweep procedure for the samples were run from 0.1 to 10 Hz in their corresponding linear strain range at 25 °C, and the storage modulus G0 and loss modulus G00 were recorded to show their viscoelastic properties.

2.7.2. In vitro digestion properties Gel samples were added to 50 mL glass tube, followed by addition of 4 mL pepsin/phosphor acid buffer solution (5 mg/mL). The tubes were incubated at 37 °C for 30 min. Six glass beads and 2 mL sodium acetate buffer (0.5 mol/L, pH = 5.2) were added, and the tubes were vortexed and then slanted in a 37 °C water bath with 160 rpm shaking for 25 min. The dispersion was then mixed with an enzyme solution (2 mL) consisted of pancreatin extract, amyloglucosidase, and invertase. The hydrolyzed glucose content was measured using the glucose oxidase method at different times (0, 15, 30, 60, 90, 120, 180 and 240 min). Values for the digested starch fractions are expressed as milligrams of glucose multiplying 0.9. Values for RDS, SDS, and RS were calculated from the G20 and G120 values, using the follow equations (Englyst et al., 1992).

C ð%Þ ¼ ðGt  G0 Þ
0:9=TS
100 RDS ð%Þ ¼ ðG20  G0 Þ
0:9=TS
100 SDS ð%Þ ¼ ðG120  G0 Þ
0:9=TS
100 RS ð%Þ ¼ ½TS  ðRDS þ SDSÞ=TS
100

2.7. Gel preparation and in vitro starch digestion 2.7.1. Preparation of mixed system Wheat starch was replaced with LEBG at 0%, 2.5%, 5%, 10%, 15% and 20% by weight. The mixtures (2 g) of wheat starch and LEBG were dispersed in distilled water (2 ml). The suspensions were stirred continuously for 30 min, and then heated in a water bath at 95 °C for 20 min with continuous stirring. The starch gels were prepared for starch digestibility analysis. Wheat starch without LEBG was prepared as a control gel.

where c is ratio of starch digestibility, t is sampling time points, Gt is the glucose content of the digest at sampling time points, G0 is the content of free glucose contained in the system before digest, G20 is the glucose content of starch released contained in the system after 20 min, G120 is the glucose content of starch released contained in the system after 120 min and TS is total dry mass of wheat starch. 2.7.3. Predicted glycemic index (pGI) The digestion kinetics and pGI of mixed powder of LEBG and wheat starch were plotted and determined according to the proce-

297

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301

dure established by Granfeldt (Granfeldt, Björck, Drews, & Tovar, 1992). The hydrolysis index (HI) was derived from the ratio between the area under the hydrolysis curve (0–180 min) of each samples and the corresponding area of the starch digest curve expressed as a percentage over the same period. The predicted glycemic index (pGI) was calculated using the equation: pGI = 8.198 + 0.862
HI (Granfeldt et al., 1992).

a 70 65

1

60 55 50 45

3

40

2.8. Statistical analysis

35

All analyses were performed at least in triplicate and their values were expressed as mean ± standard deviation. Statistical analyses were carried out with Tukey’s multiple range test (p < 0.05) using statistical software SPSS (Version. 17.0 software, Chicago, IL, USA).

4

2

30

5

6

25 20 15 10 5 0 5

3. Results and discussion

10

20

b

3.1. Characterization of LEBG The HPSEC profiles (Fig. 2) indicate that LEBG was a single symmetrical peak. No absorption in 260 nm and 280 nm was detected in UV spectrum of LEBG, revealing that LEBG did not contain nucleic acid and protein. I2–KI reaction of LEBG was negative, indicating no starch was detected. The molecular weight of LEBG was determined with HPSEC. The weight average molecular weight (Mw) and polydispersity index (Mw/Mn) of LEBG in PB buffer were estimated to be 1.868
106 g/mol and 1.007, respectively. It was indicated that the LEBG had a relatively high purity. This result showed some differences from a previous study, concluding that the average molecular weight (Mw) of the three polysaccharides from the fruits bodies of Lentinus edodes were determined to be 4.02 x 104, 2.16 x l05, 8.93 x 105, respectively. It was speculated that differences in Mw may mainly reflect the differences of extraction methods. Fig. 3 (a, b) shows the monosaccharide in LEBG consisted mainly of glucose with traces of galactose, arabinose, xylose and mannose. The monosaccharide (Table 1) indicated the weight percentage of arabinose, galactose, glucose, xylose, mannose was 0.72%, 1.61%, 2.61%, 92.75%, 2.34% respectively. The molar ratio of arabinose, galactose, glucose, xylose, mannose is 5:11: 18: 644: 16. These results are similar to those from previous studies, in which polysaccharide was separated from the fruit body of Lentinula edodes. Chemical analyses demonstrated that polysaccharide consisted of glucose (87.5%), galactose (9.6%), and arabinose (2.8%) (Xu, Yan, & Zhang, 2012). 2.4x10-6 2.2x10-6 2.0x10-6 1.8x10-6 1.6x10-6

DelRIU

15

Minutes 60

5

55 50 45 40 35 30 25 20 15

4

2 3

10

6

5 0 5

10

15

20

Minutes Fig. 3. Monosaccharide analysis of LEBG. a is the standard monosaccharides; b is the one of monosaccharide hydrolyzed from LEBG. 1–6 are rhamnose, arabinose, xylose, mannose, glucose, galactose respectively. The same number in both figures represents one monosaccharide.

Table 1 Monosaccharide compositions of LEBG. Monosaccharide

Composition (%, w / w)

Rhamnose Arabinose Xylose Mannose Glucose Galactose

– 0.72 ± 0.01 1.61 ± 0.01 2.61 ± 0.01 92.75 ± 0.04 2.34 ± 0.02

Data expressed as mean ± S.D. of triplicate determinations. – means not detected.

1.4x10-6 -6

1.2x10

1.0x10-6 8.0x10-7 6.0x10-7 -7

4.0x10

2.0x10-7 0.0 02

10

20

30

40

50

Retention time (min) Fig. 2. The elution profiles of polysaccharide fractions of LEBG.

60

Infrared (IR) spectroscopy (Fig 4) showed absorption at 3321.82, 2924.31, 1647.67, 1199.20, 1073.40 and 889.20 cm1, corresponding to the stretching of the OAH, CAH, C@H, tertiary alcohol, CAOAC and pyranoside bond groups. Pyranoside bond groups revealed that LEBG belong to b-pyran polysaccharide. This result was identical to the result in literature, which concluded that the polysaccharide of Lentinus edodes was a polysaccharide containing pyranose ring.

298

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301

100

889.20

95 1741.95 1539.21 90

1199.20 1313.10

1371.36 1647.67 1423.71

85

80

%T

2924.31

75

70

65

1073.40

60

55

3321.82

50 4000

3500

3000

2500

2000

1500

1000

cm-1

Fig. 4. IR spectrum of LEBG.

3.2. Thermal properties of LEBG/Starch gel systems As shown in Fig. 5, with the increase of LEBG concentration in wheat starch, the peak temperature in the heat flow diagram shifted to the higher temperature, the peak area of the endothermic enthalpy was also increased. Comparison of the DSC values between five groups (Table 2) illustrated that pasting temperature and enthalpy increased with the increment of the amount of LEBG in wheat starch. Compared with the control group, the treatment group with 20% addition of LEBG, its T0, Tp, Tc were enhanced to 3.92, 4.18, 3.19 °C, respectively, and pasting enthalpy was increase to 2.90 J/g. LEBG can increase the pasting temperature as well as pasting enthalpy of wheat starch. As reported previously, bglucan can improve starch pasting temperature, thereby increasing the enthalpy of gelatinized starch (Funami et al., 2005).

a b Endothermic

c d

e

It may ascribe to the higher concentration of LEBG in starch system holding more moisture. It allowed for the gelatinization and the need of absorbing much more heat. In addition, because LEBG might inhibit the starch granule swelling, the starch system was gelatinized at a higher temperature when LEBG were added more (Zhou, Wang, Zhang, Du, & Zhou, 2008). 3.3. Rheological measurements of LEBG/Starch gel systems As the oscillation frequency increased in Fig. 6, G0 and G00 of LEBG/wheat starch gel systems were gradually increased, and G’ was always greater than G00 . It was indicated that as the oscillation frequency increases, the elastic modulus of mixed wheat starch gel was greater than the viscous modulus. After adding LEBG, G0 and G00 of wheat starch gel systems increased. This may be caused by the addition of LEBG which diluted wheat starch gels. LEBG and starch crosslinked with each other, the connection between the molecular chains of hybrid architecture was improved and the network structure of gel system is enhanced (Fig. 7). As reported in literature, the presence of Lentinus edodes powder can significantly alter the viscoelastic properties of wheat starch. Moreover, water absorption of mixed gel greatly improved after adding the Lentinus edodes powder. Meanwhile, the polysaccharide of Lentinus edodes powder and starch were cross-linked, resulting in the increase in the degree of cross-linking of molecules mixed system. The gel system network architecture enhance (Zhou, Tang, & Nan, 2014). 3.4. In vitro starch digestibility of LEBG/Starch gel systems

20

40

60

80

100

120

Temperature (䉝㻕 Fig. 5. DSC thermograms of wheat starch containing different LEBG concentration. (a:control;b:2.5% LEBG;c:5% LEBG;d:10% LEBG;e:20% LEBG).

The effects of LEBG on starch digestion in vitro in wheat starch gels were investigated by measuring the hydrolysis rate during starch digestion. Fig. 8 describe the starch hydrolysis curves which were compared with those of the control and different ratios of LEBG. All of the materials used in this study could inhibit starch hydrolysis by restraining digestive enzymes, compared with the control gel. The rate and extent of starch digestion were the

299

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301 Table 2 Pasting temperature and enthalpy of wheat starch with different content of LEBG. Treatments

T0 (°C)

TP (°C) bc

a (0%) b (2.5%) c (5%) d (10%) f (20%)

60.33 ± 0.45 61.36 ± 0.33b 62.37 ± 0.57b 62.53 ± 0.51b 64.25 ± 0.20a

DH (J/g)

TC (°C) d

66.16 ± 0.22 67.24 ± 0.06c 67.94 ± 0.35c 69.04 ± 0.14b 70.34 ± 0.41a

c

10.64 ± 0.03c 11.52 ± 0.49bc 12.52 ± 0.33ab 12.75 ± 0.18a 13.54 ± 0.32a

76.77 ± 0.34 77.91 ± 0.10bc 78.63 ± 0.69ab 79.19 ± 0.25ab 79.96 ± 0.25a

Means in the same row with different letters are significantly different (p < 0.05) according to Duncan’s multiple range test. Data expressed as mean ± S.D. of triplicate determinations.

G'0% G'2.5% G'5% G'10% G'20% G''0% G''2.5% G''5% G''10% G''20%

6500 1200

6000 5500

1000

5000 4500

G' (Pa)

3500 600

3000 2500

G'' (Pa)

800

4000

400

2000 1500

200

1000 500 0 -5

0

5

0 10 15 20 25 30 35 40 45 50 55 60 65 70

Frequency (rad/s) Fig. 6. Storage modulus (G0 ) and loss modulus (G00 ) LEBG and wheat starch mixed system changing with angular frequency. Each datum is the representative one from duplicate measurements.

Wheat starch

LEBG

Water

Hydrogen bond Fig. 7. Gel network formed between LEGB and wheat starch.

300

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301

0% 2.5% 5% 10% 20%

70 60

Hydrolysis (%)

50 40 30 20 10 0

0

30

60

90

120

150

180

210

240

270

300

Time (min) Fig. 8. Effects of different LEBG ratios on the Hydrolysis rate curves of wheat starch gels.

Table 3 In vitro starch digestibility (rapidly digestible starch, RDS; slowly digestible starch, SDS; resistant starch, RS; pGI, predicted glycemic index) in control and LEBG for wheat flour at 0, 2.5, 5, 10, 20% (w/w).

Control 2.5% 5% 10% 20%

RDS (%)

SDS (%)

RS (%)

pGI

39.25 ± 0.28a 33.81 ± 0.43ab 31.90 ± 0.23ab 27.92 ± 0.19b 27.42 ± 0.27b

10.15 ± 0.19a 15.55 ± 0.14b 16.50 ± 0.35b 17.19 ± 0.22b 18.23 ± 0.16b

50.06 ± 0.17a 50.64 ± 0.28b 51.60 ± 0.47b 54.89 ± 0.41bc 54.95 ± 0.35c

86.94 ± 0.32a 77.66 ± 0.36b 73.62 ± 0.40b 68.08 ± 0.08b 56.43 ± 0.29b

Means in the same row with different letters are significantly different (p < 0.05) according to Duncan’s multiple range test. Data expressed as mean ± S.D. of triplicate determinations.

4. Conclusions In this study, LEBG was successfully isolated from the fruiting bodies of Lentinus edodes. The weight average molecular weight (Mw) and polydispersity index (Mw/Mn) of LEBG in PB buffer were measured to be 1.868
106 g/mol and 1.007, respectively. The monosaccharide composition of LEBG was identified as glucose, galactose, fructose, xylose and mannose. In addition, the molar ratio of arabinose, galactose, glucose, xylose, and mannose is 5:11: 18: 644: 16. DSC results showed that pasting temperature and enthalpy increased with increment of added amount of LEBG in wheat starch. The rheological properties of wheat starch containing LEBG, revealed the presence of the strong interactions between LEBG and wheat starch. After in vitro digestion, the concentrations of slowly digestible starch and resistant starch in mixed gel system increased with addition of LEBG, and the variance reached a significant level (P < 0.05). The content of slowly digestible starch and resistant starch of the treatment group with the 20% LEBG addition were 18.23% and 54.95% respectively, which were 1.80 times and 1.10 times of the control group, respectively. The predicted glycemic index decreased with the increasing amount of LEBG. The predicted glycemic index of 20% LEBG were 56.43. Compared with the control, it was reduced by 30.51 and the difference was significant (p < 0.05). Obviously, the concentration of LEBG had a significant impact on pasting, rheological properties and in vitro digestion of starch. Starch with LEBG could be used to manufacture low glycemic index foods. Funding This work was supported by the 2015 Youth Talent Development Plan of Shanghai Municipal Agricultural System, China (Grant No. 1-8). Acknowledgments

highest in the control, followed by 2.5%, 5%, 10% and 20% addition of LEBG, attributing to the network structure in the gel system. From the rheological results, LEBG enhanced the possibility of its entangling with wheat starch, and promoted the mutual gathering between the starch. There were some extent interactions with LEBG and wheat starch. And it reduced the contacting of amylase and starch (Zhou, Liu, Gu, & Hong, 2015). It has been reported that the swelling index of pasta added with mushroom beta-glucan fiber fraction is significantly higher than that of the control, and b-glucan, starch and protein form a network and starch granules are wrapped (Lu, Brennan, Serventi, Mason, & Brennan, 2016). Gao, Brennan, Mason, and Brennan (2016) showed that the addition of inulin to the muffins led to lower starch hydrolysis, and may be due to a decrease in starch content as the amount of inulin increases. The concentrations of RDS, SDS, and RS, and the pGI values in the gel samples were shown in Table 3. Compared to the control gel, the gels with LEBG exhibited lower levels of RDS and pGI. Also, the gels with LEBG contained the higher amounts of SDS and RS. The calculated pGI values of the wheat starch gels prepared with LEBG ranged from 77.66 to 56.43, which were significantly lower than that of the control (86.94) (p < 0.05). This result agreed with the results from the study by Regand (Regand, Chowdhury, Tosh, Wolever, & Wood, 2011) indicating that oat bglucans as a source of soluble dietary fiber can significantly lower the peak blood glucose response and the incremental area under the curve. Thus the blend ratio of LEBG and wheat starch acts as an important factor to retard glucose release during starch digestion within a specific range of wheat flour replacement.

The authors would like to extend a sincere gratitude for the supports of the 2015 Youth Talent Development Plan of Shanghai Municipal Agricultural System, China (Grant No. 1–8) and ‘‘Shu Guang” project which supported by Shanghai Municipal Education Commission and Shanghai Education Development Foundation. References Ahmad, A., Anjum, F. M., Zahoor, T., Nawaz, H., & Dilshad, S. M. (2012). Beta glucan: a valuable functional ingredient in foods. Critical Reviews in Food Science & Nutrition, 52(3), 201–212. Atkinson, F. S., Fosterpowell, K., & Brandmiller, J. C. (2002). International tables of glycemic index and glycemic load values: 2008. American Journal of Clinical Nutrition, 76(1), 5–56. Beattie, K. D., Rouf, R., Gander, L., May, T. W., Ratkowsky, D., Donner, C. D., ... Tiralongo, E. (2010). Antibacterial metabolites from Australian macrofungi from the genus Cortinarius. Phytochemistry, 71(8–9), 948–955. Borchers, A. T., Keen, C. L., & Gershwin, M. E. (2004). Mushrooms, tumors, and immunity: an update. Experimental Biology & Medicine, 229(5), 281–293. Cleary, L. J., Andersson, R., & Brennan, C. S. (2007). The behaviour and susceptibility to degradation of high and low molecular weight barley b-glucan in wheat bread during baking and in vitro digestion. Food Chemistry, 102(3), 889–897. Deng, C., Hu, Z., Fu, H., Hu, M., Xu, X., & Chen, J. (2012). Chemical analysis and antioxidant activity in vitro of a b-d-glucan isolated from Dictyophora indusiata. International Journal of Biological Macromolecules, 51(1–2), 70–75. Du, B., Bian, Z., & Xu, B. (2014). Skin health promotion effects of natural beta-glucan derived from cereals and microorganisms: A review. Phytotherapy Research, 28 (2), 159–166. Englyst, H. N., Kingman, S. M., & Cummings, J. H. (1992). Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition, 46(2), 33–50. Funami, T., Kataoka, Y., Omoto, T., Goto, Y., Asai, I., & Nishinari, K. (2005). Effects of non-ionic polysaccharides on the gelatinization and retrogradation behavior of wheat starchq. Food Hydrocolloids, 19(1), 1–13.

H. Zhuang et al. / Food Chemistry 224 (2017) 294–301 Gao, J., Brennan, M. A., Mason, S. L., & Brennan, C. S. (2016). Effect of sugar replacement with stevianna and inulin on the texture and predictive glycaemic response of muffins. International Journal of Food Science & Technology, 51, 1979–1987. Granfeldt, Y., Björck, I., Drews, A., & Tovar, J. (1992). An in vitro procedure based on chewing to predict metabolic response to starch in cereal and legume products. European Journal of Clinical Nutrition, 46(9), 649–660. Her, J. Y., Min, S. K., Kim, M. K., & Lee, K. G. (2015). Development of a spray freezedrying method for preparation of volatile shiitake mushroom (Lentinus edodes) powder. International Journal of Food Science & Technology, 50(10), 2222–2228. Jia, W. U., & Xie, B. J. (2011). The effect of oat b-glucan on a-amylase in vitro. Acta Nutrimenta Sinica, 33(6), 612–615. Kapelko-Zeberska, M., Zieba, T., Pietrzak, W., & Gryszkin, A. (2016). Effect of citric acid esterification conditions on the properties of the obtained resistant starch. International Journal of Food Science & Technology, 51(7), 1647–1654. Kendall, C. W., Emam, A., Augustin, L. S., & Jenkins, D. J. (2004). Resistant starches and health. Journal of AOAC International, 87(3), 769–774. Lindequist, Ulrike, Niedermeyer, Timo, amp, H. J., lich & WolfDieter (2005). The pharmacological potential of mushrooms. Evidence-based Complementary and Alternative Medicine, 2(3), 285–299. Liu, Y., Zhao, Y., Yang, Y., Tang, Q., Zhou, S., Wu, D., & Zhang, J. (2013). Structural characteristics and hypoglycemic activity of polysaccharides from Coprinus comatus. Bioactive Carbohydrates & Dietary Fibre, 2(2), 164–169. Lu, X., Brennan, M. A., Serventi, L., Mason, S., & Brennan, C. S. (2016). How the inclusion of mushroom powder can affect the physicochemical characteristics of pasta. International Journal of Food Science & Technology, 50, 1705–1717. Mei, T., Chuang, L. I., Fei, J. Y., Zhao, S. Y., Shi, X. F., Hua-Wei, L. I., & Zang, S. L. (2008). Study on the Purification and IR Spectroscopy of Se-polysaccharides in Selenium-enriched Flammulina Velutipes. Journal of Instrumental Analysis, 27 (2), 158–161. Pavel, K. (2013). A review of chemical composition and nutritional value of wildgrowing and cultivated mushrooms. Journal of the Science of Food & Agriculture, 93(2), 209–218. Pillai, T. G., & Devi, P. U. (2013). Mushroom beta glucan: Potential candidate for post irradiation protection. Mutation Research/fundamental & Molecular Mechanisms of Mutagenesis, 751(2), 109–115.

301

Poucheret, P., Fons, F., & Rapior, S. (2006). Biological and Pharmacological Activity of Higher Fungi: 20-Year Retrospective Analysis. Cryptogamie Mycologie, 27(4), 311–333. Regand, A., Chowdhury, Z., Tosh, S. M., Wolever, T. M. S., & Wood, P. (2011). The molecular weight, solubility and viscosity of oat beta-glucan affect human glycemic response by modifying starch digestibility. Food Chemistry, 129(2), 297–304. Ren, L., Perera, C., & Hemar, Y. (2012). Antitumor activity of mushroom polysaccharides: a review. Food Funct, 3(11), 1118–1130. Wasser, S. P., & Weis, A. L. (1999). Medicinal properties of substances occurring in higher basidiomycetes mushrooms: current perspectives (review). International Journal of Medicinal Mushrooms, 1(1), 31–62. Xu, X., Yan, H., & Zhang, X. (2012). Structure and immuno-stimulating activities of a new heteropolysaccharide from Lentinula edodes. Journal of Agricultural & Food Chemistry, 60(46), 11560–11566. Zhang, A. Q. (2010). Isolation and structural characterization of a water-soluble polysaccharide from Hericium erinaceus. Mycosystema, 29, 911–917. Zhang, Y., Xia, L., Pang, W., Wang, T., Chen, P., Zhu, B., & Zhang, J. (2013). A novel soluble b-1,3-D-glucan salecan reduces adiposity and improves glucose tolerance in high-fat diet-fed mice. British Journal of Nutrition, 109(2), 254–262. Zhao, C., Wu, Y., Yang, C., Liu, B., & Huang, Y. (2015). Hypotensive, hypoglycaemic and hypolipidaemic effects of bioactive compounds from microalgae and marine micro-organisms. International Journal of Food Science & Technology, 50 (8), 1705–1717. Zhou, S. S., Liu, G. D., Gu, Z. B., & Hong, Y. (2015). Effect of guar gum on the digestibility, pasting properties and water mobility of tapioca starch. Science & Technology of Food Industry, 36(9), 111–115. Zhou, J., Tang, X., & Nan, P. (2014). Effects of Lentinus edodes flour on the thermomechanical and dynamic rheological properties of wheat flour dough. Journal of the Chinese Cereals & Oils Association, 29(7), 7–11. Zhou, Y., Wang, D., Zhang, L., Du, X., & Zhou, X. (2008). Effect of polysaccharides on gelatinization and retrogradation of wheat starch. Food Hydrocolloids, 22(4), 505–512. Zhu, F., Du, B., Bian, Z., & Xu, B. (2015). Beta-glucans from edible and medicinal mushrooms: Characteristics, physicochemical and biological activities. Journal of Food Composition & Analysis, 41, 165–173.