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Food Chemistry 113 (2009) 578–584

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

Flavour components and antioxidant properties of several cultivated mushrooms


Shu-Yao Tsai a, Shih-Jeng Huang b, Sheng-Hua Lo c, Tsai-Ping Wu c, Pei-Ying Lian c, Jeng-Leun Mau c,*
a
Department of Health and Nutrition Biotechnology, Asia University, 500 Liufeng Road, Wufeng, Taichung 41354, Taiwan, ROC
b
Department of Nutrition and Health Science, Chungchou Institute of Technology, Yuanlin, Changhua 51003, Taiwan, ROC
c
Department of Food Science and Biotechnology, National Chung-Hsing University, 250 Kuokuang Road, Taichung 40227, Taiwan, ROC

a r t i c l e i n f o a b s t r a c t

Article history: Three mushrooms, Clitocybe maxima, Pleurotus ferulae and Pleurotus ostreatus grey strain were used to
Received 7 March 2008 study their flavour components and antioxidant properties. The volatile flavour components found com-
Received in revised form 2 June 2008 prised of six eight-membered carbon compounds and two aromatic compounds. The content total of sol-
Accepted 12 August 2008
uble sugars and polyols was 125–270 mg/g. The content of monosodium glutamate-like components was
1.76–8.89 mg/g. The contents of flavour 50 -nucleotides ranged from 1.89 to 7.59 mg/g. Based on the
results obtained, three mushrooms possessed highly intense umami taste. Ethanolic extracts were more
Keywords:
effective in the inhibition of conjugated diene and scavenging ability on 1,1-diphenyl-2-picrylhydrazyl
Mushrooms
Volatile components
radicals, whereas hot water extracts were more effective in the scavenging ability of hydroxyl radicals.
Taste components EC50 values were less than 14 and 30 mg/ml for ethanolic and hot water extracts, respectively, indicating
Antioxidant properties that the three mushrooms were relatively effective as they exhibited antioxidant properties, despite hav-
ing scavenging abilities for hydroxyl radicals. Phenols were the major antioxidant components and the
total contents were 5.10–11.1 mg gallic acid equivalents/g.
Ó 2008 Elsevier Ltd. All rights reserved.

1. Introduction tents of potential antioxidant components in these extracts were


also determined.
Edible mushrooms are commonly used as foods and food-fla-
vouring substances and also traditional Chinese medicines. Some 2. Materials and methods
edible mushrooms have also been reported as therapeutic foods
which are useful in preventing diseases such as hypertension, 2.1. Mushrooms
hypercholesterolaemia and cancer. These functional characteristics
are mainly due to chemical composition (Manzi, Aguzzi, & Pizzo- Three species of fresh mushrooms (C. maxima, P. ferulae and P.
ferrato, 2001). Mushrooms have become attractive as functional ostreatus) were obtained from Tatsuen Farm, Pushin, Chunghua
foods and a source of physiologically beneficial substances. County, Taiwan. Fruit bodies from each species were randomly di-
Recently, fresh fruit bodies of mushrooms from three species vided into six trays without cover, each containing about 200 g.
have become available in the market, including giant clitocybe (Cli- Immediately after sampling, three trays of fresh samples from each
tocybe maxima Gaertn. et G. Mey.: Fr., big cup mushroom), ferulae species were used for the analysis of volatile components. The
mushroom [Pleurotus ferulae (DC.: Fr) Quel.] and Japanese oyster other three trays of C. maxima were divided into three trays of caps
mushroom [Pleurotus ostreatus (Jacquin: Fries) Kummer (grey and three trays of stipes based on its separate and distinct morpho-
strain), grey tree oyster mushroom]. However, the volatile compo- logical appearance. All trays of mushrooms were then freeze dried
nents, non-volatile taste components and antioxidant properties of and ground using a mill (Retsch ultracentrifugal mill and sieving
C. maxima, P. ferulae and P. ostreatus are unknown. Therefore, our machine Haan, Germany) to obtain a coarse powder (24 opening/
objective was to examine the volatile and taste components cm).
including proximate compositions, soluble sugars, free amino acids
and 50 -nucleotides in these three mushrooms. The antioxidant 2.2. Extraction of volatile compounds
properties of the ethanolic and hot water extracts assayed included
inhibition of conjugated diene, reducing capability, scavenging A tray of mushrooms (200 g, about 100 g for C. maxima caps or
abilities of radicals and chelating abilities to metal ions. The con- stipes) was cut into small cubes and blended with 600 ml of 0.1 M
sodium phosphate buffer (pH 6.5, Wako Pure Chemical Co., Osaka,
* Corresponding author. Tel.: +886 4 2285 4313; fax: +886 4 2287 6211. Japan) containing 0.15% Tween 80 (Wako) and 1 ml of methanol
E-mail address: jlmau@dragon.nchu.edu.tw (J.-L. Mau). containing 1000 lg of 1-nonanol (Sigma Chemical Co., St. Louis,

0308-8146/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodchem.2008.08.034
S.-Y. Tsai et al. / Food Chemistry 113 (2009) 578–584 579

MO, USA) used as an internal standard. After 1 min of blending, the 38–40 min, and 0:100:0 for 40–43 min. The flow rate was
homogenate was mixed with 50 ml n-hexane (Mallinckrodt Baker, 1.2 ml/min.
Phillipsburg, NJ, USA), and centrifuged at 10,000g for 10 min at 50 -Nucleotides were extracted and analysed as described by
4 °C. The n-hexane layer was preconcentrated with a distillation Taylor, Hershey, Levine, Coy, and Olivelle (1981). Dried powder
apparatus at 40 °C and carefully reconcentrated to approximately (500 mg) was extracted with 25 ml of deionised water. This sus-
50 ll using a 0.2 mm i.d.  10 cm Vigreux column (Tung Kawn pension was heated to boiling for 1 min, cooled and then centri-
Glass Co., Hsinchu, Taiwan) at 40 °C. fuged at 22,200g for 15 min. The extraction was repeated once
with 20 ml of deionised water. The combined filtrate was then
2.3. Determination of volatile compounds using GC–MS evaporated, and filtered prior to HPLC injection in the same man-
ner as in the soluble sugar and polyol assays. The HPLC system
A HP 5890A Series II GC coupled to an HP 5972A MSD mass was the same as for sugar and polyol assay except for a Shimadzu
spectrometer was used. A fused silica column (0.32 mm  30 m, UV detector and a LiChrospher 100 RP-18 column (4.6  250 mm,
J&W, Folsom, CA, USA) coated with DB-Wax (1.0 lm thickness) 5 lm, Merck). The mobile phase was 0.5 M KH2PO4/H3PO4 (pH
was used. The oven temperature was programed from 50 to 4.3, Wako Pure Chemical Co., Osaka, Japan) at a flow rate of 1 ml/
200 °C at 2 °C/min. The operating conditions were as follows: injec- min and UV detection at 254 nm. Each sugar or polyol, amino acid
tor temperature, 250 °C; GC–MS interface temperature, 265 °C; he- and 50 -nucleotide was identified using an authentic sample (Sig-
lium carrier flow rate, 1.0 ml/min; electron multiplier voltage, ma) and quantified by its respective calibration curve.
1500 V; electron ionisation energy, 70 eV. Volatile components
were identified by comparing the mass spectral data with those 2.5. Extraction of antioxidant components
spectra available from the Wiley MS Chemstation Libraries (6th
edition, G1034, Rev. C.00.00, Hewlett–Packard) and GC retention For ethanolic extractions, a subsample (10 g) was extracted by
times of the components with those of authentic compounds, stirring with 100 ml of 95% ethanol at 25 °C at 20g for 24 h and
which were commercially available (Aldrich Chemicals Co., Mil- filtration through Whatman No. 1 filter paper. The residue was
waukee, WI, USA; Penta Manufacturing Co., Livingston, NJ, USA). then extracted with two additional 100 ml portions of ethanol as
Kovats retention indices of the volatile components were calcu- described above. The combined ethanolic extracts were then con-
lated with n-paraffin (C8–C25, Alltech Associates, Deerfield, IL, centrated under reduced pressure at 40 °C to dryness. For hot
USA) as references. The amount of each component was deter- water extractions, a subsample (10 g) was extracted by stirring
mined using an internal standard method and calculated from with 100 ml of boiling water at 100 °C at 20g for 10 min, centri-
the peak area of gas chromatogram. fugation at 5000g for 15 min and filtration through Whatman No.
1 filter paper. The residue was then extracted with two additional
2.4. Soluble sugar, polyol, free amino acid and 50 -nucleotide assays 100 ml portions of boiling water as described above. The combined
hot water extracts were then freeze dried. The dried extract was
Soluble sugars and polyols were extracted and analysed as de- used directly for analyses of antioxidant components or redis-
scribed by Ajlouni, Beelman, Thompson, and Mau (1995). Dried solved in water or ethanol to a concentration of 50 mg/ml and
powder (600 mg) was extracted with 50 ml of 80% aqueous ethanol stored at 4 °C for further use.
(95% pure, Taiwan Tobacco & Wine Monopoly Bureau, Taipei). This
suspension was shaken for 45 min at room temperature and fil- 2.6. Evaluation of antioxidant properties
tered through Whatman No. 4 filter paper. The residue was washed
five times with additional 25 ml portions of 80% ethanol. The com- The inhibition of conjugated diene was determined according to
bined filtrate was then concentrated under reduced pressure at the method of Lingnert, Vallentin, and Eriksson (1979). Each ex-
40 °C and redissolved in deionised water to a final volume of tract (0.5–20 mg/ml) in deionised water or ethanol (100 ll) was
10 ml. The aqueous extract was then passed through a filter unit mixed with 2 ml of 10 mM linoleic acid (Sigma) emulsion in
(13 mm, Lida, Corp., Kenosha, WI), and filtered using a 0.45 lm 0.2 M sodium phosphate buffer (pH 6.6, Wako) in test tubes and
CA non-sterile filter (Lida) prior to HPLC analysis. The HPLC system placed in the dark at 37 °C to accelerate oxidation. After incubation
consisted of a Hitachi L-6000 pump, a Rheodyne 7161 injector, a for 15 h, 6 ml of 60% methanol (Mallinckrodt Baker) in deionised
20 ll sample loop, a Hitachi D-2500 chromato-integrator, a Shima- water was added, and the absorbance of the mixture was measured
dzu RID-10A detector and a Phase Sep-NH2 column (4.6  250 mm, at 234 nm against a blank in a Hitachi U-2001 spectrophotometer.
5 lm, Phase Separation Inc., Norwalk, CT). The mobile phase was The inhibition of conjugated diene was calculated as follows:
acetonitrile (LC grade, Tedia Co., Fairfield, OH)/deionised water inhibitory ability (%) = [(DA234 of control  DA234 of sample)/
85:15 (v/v) at a flow rate of 1 ml/min. DA234 of control]  100%.
Free amino acids were extracted and analysed as described by The reducing capability was determined according to the meth-
Mau, Chyau, Li, and Tseng (1997). Dried powder (500 mg) was od of Oyaizu (1986). Each extract (0.5–20 mg/ml) in deionised
shaken with 50 ml of 0.1 N HCl (Union Chemical Co., Hsinchu, water or ethanol (2.5 ml) was mixed with 2.5 ml of 200 mM so-
Taiwan) for 45 min at ambient temperature and filtered through dium phosphate buffer (pH 6.6, Wako) and 2.5 ml of 1% potassium
Whatman No. 4 filter paper. The filtrate was then passed through ferricyanide (Sigma), and the mixture was incubated at 50 °C for
a filter unit (13 mm, Lida), and filtered using a 0.45 lm CA non- 20 min. After 2.5 ml of 10% trichloroacetic acid (Wako) was added,
sterile filter (Lida). This filtrate was mixed with o-phthalaldehyde the mixture was centrifuged at 200g for 10 min. The upper layer
reagent (Sigma) in an eppendorf tube, shaken to facilitate derivat- (5 ml) was mixed with 5 ml of deionised water and 1 ml of 0.1%
isation and then immediately injected onto the HPLC. The HPLC ferric chloride (Wako), and the absorbance was measured at
system was the same as for sugar analysis but included a Hitachi 700 nm against a blank.
L-7485 fluorescence detector with fluorescence excitation at Scavenging ability on 1,1-diphenyl-2-picrylhydrazyl (DPPH)
340 nm and emission at 450 nm and a LiChrospher 100 RP-18 col- radicals was determined according to the method of Shimada,
umn (4.6  250 mm, 5 lm, Phenomenex Inc., Torrance, CA). The Fujikawa, Yahara, and Nakamura (1992). Each extract (0.5–
mobile phases were A, 50 mM sodium acetate (pH 5.7) containing 20 mg/ml) in deionised water or ethanol (4 ml) was mixed with
0.5% tetrahydrofuran; B, deionised water; and C, methanol. The 1 ml of methanolic solution containing DPPH (Sigma) radicals,
gradient was A:B:C 80:0:20–33:0:67 for 0–38 min, 0:33:67 for resulting in a final concentration of 0.2 mM DPPH. The mixture
580 S.-Y. Tsai et al. / Food Chemistry 113 (2009) 578–584

was shaken vigorously and left to stand for 30 min in the dark and anol and the resulting mixture (100 ll) was added to 2 ml of 2%
the absorbance was then measured at 517 nm against a blank. The aqueous sodium carbonate (Wako) solution. After 3 min, 100 ll
scavenging ability was calculated as follows: Scavenging ability of 50% Folin-Ciocalteau phenol reagent (Sigma) were added to
(%) = [(DA517 of control  DA517 of sample)/DA517 of control]  100. the mixture. After 30 min standing, the absorbance was measured
The scavenging ability on hydroxyl radicals was determined at 750 nm against a blank. The content of antioxidant components
according to the method of Shi, Dalal, and Jain (1991). The hydro- was calculated on the basis of the calibration curve of the corre-
xyl radicals reacted with the nitrone spin trap 5,5-dimethyl pyrro- sponding authentic compounds and gallic acid for total phenols
line-N-oxide (DMPO, Sigma) and the resultant DMPO–OH adducts (Sigma).
were detected with an electron paramagnetic resonance (EPR)
spectrometer. The EPR spectrum was recorded 2.5 min after mix- 2.8. Statistical analysis
ing each extract (5–20 mg/ml) in deionised water or ethanol
(200 ll) with 200 ll of 10 mM H2O2 (Merck, Darmstadt, Germany), For each mushroom species, three samples were used for the
200 ll of 10 mM Fe2+ (Sigma) and 200 ll of 10 mM DMPO using a determination of every quality attribute. For each of ethanolic
Bruker EMX-10 EPR spectrometer at the following settings: 0.348 T and hot water extractions, three samples were prepared for assays
magnetic field, 1.0  104 T modulation amplitude, 0.5 s time con- of every antioxidant attribute and component. The experimental
stant and 200 s scan period. The scavenging ability was calculated data were subjected to an analysis of variance for a completely ran-
by subtracting the relative EPR signal intensity from 100. The rela- dom design to determine the least significant difference amongst
tive EPR signal intensity was calculated as follows: Relative EPR means at the level of 0.05.
signal intensity (%) = [hDH2 (sample)/hDH2 (control)]  100; h is
the width of the peak, DH is the length of the peak. 3. Results and discussion
The chelating ability was determined according to the method
of Dinis, Madeira, and Almeida (1994). Each extract (0.5–20 mg/ 3.1. Volatile components
ml) in water or ethanol (1 ml) was mixed with 3.7 ml of methanol
and 0.1 ml of 2 mM ferrous chloride (Merck). The reaction was ini- Volatile flavour components found in the three mushrooms
tiated by the addition of 0.2 ml of 5 mM ferrozine (Sigma). After were six eight-membered carbon compounds and two aromatic
10 min at room temperature, the absorbance of the mixture was compounds (Table 1). Typical mushroom aroma was attributed to
determined at 562 nm against a blank. EC50 value (mg extract/ eight-membered carbon compounds, especially 1-octen-3-ol
ml) is the effective concentration at which the inhibition of conju- (Mau & Hwang, 1997). However, P. ostreatus showed much higher
gated diene was inhibited by 50%; the absorbance was 0.5 for concentrations of eight-membered carbon compounds (>1100 mg/
reducing capability; DPPH or hydroxyl radicals were scavenged kg). The major compound in C. maxima and P. ferulae was 1-octen-
by 50%; and ferrous ions were chelated by 50%, respectively. EC50 3-ol whereas for P. ostreatus was 1-octen-3-one. It seems that aro-
value was obtained by interpolation from linear regression matic compounds were insignificant in Pleurotus mushrooms, 6%
analysis. and 1% the major compound of aromatics was obtained for P. feru-
lae and P. ostreatus, respectively. However, in addition to the typi-
2.7. Determination of antioxidant components cal mushroom aroma, aromatic compounds in C. maxima might
give rise to an almond-like and fruity aroma (Arctander, 1969).
b-Carotene was extracted and analysed as described by Rundh- Volatile contents in Volvariella volvacea, Pleurotus eryngii and Agar-
aug, Pung, Read, and Bertram (1988). Each dried extract (100 mg) icus bisporus were 8.35–19.7 mg/kg (Mau et al., 1997), 17.8–
was extracted with 1 ml of ethanol, 2 ml of n-hexane containing 29.1 mg/kg (Mau, Lin, Chen, Wu, & Peng, 1998) and 53.0 mg/kg
BHA (25 lg/ml) and 1 ml of deionised water at 20g for 45 min
at room temperature and then centrifuged at 400g for 10 min.
After the removal of the n-hexane layer by N2 gas, the volume
was adjusted to 1 ml using n-hexane and filtered through a syr-
inge-driven filter unit (13 mm, Millipore, Billerica, MA) using a Table 1
0.45 lm PVDF non-sterile filter paper. Immediately after filtration, Content of volatile components in Clitocybe maxima, Pleurotus ferulae and Pleurotus
ostreatus
the filtrate was injected into a HPLC detector. The HPLC system was
the same as for the 50 -nucleotide assay. The mobile phase was Peak no. Compound RIa Content (mg/kg fresh weight)
75 ml methanol/25 ml toluene at a flow rate of 1.5 ml/min and [% total volatiles]b
UV detection was at 450 nm. C. maxima P. ferulae P. ostreatus
Tocopherols were extracted and analysed according to the 1 3-Octanone 1270 2.21 ± 0.33 Bc 3.49 ± 0.08 B 138 ± 43.9 A
method of Carpenter (1979). Each extract (50 mg) was suspended 2 1-Octen-3-one 1316 13.8 ± 3.79 B 1.13 ± 0.55 B 506 ± 34.9 A
in 6 ml of pyrogallol (6% in ethanol) and 4 ml of 60% aqueous 3 3-Octanol 1406 13.6 ± 3.50 B 0.94 ± 0.26 B 181 ± 19.4 A
4 1-Octen-3-ol 1472 65.4 ± 0.15 C 98.8 ± 5.25 B 254 ± 1.17 A
potassium hydroxide solution. The resulting mixture was saponi-
5 Benzaldehyde 1534 29.0 ± 0.84 A 0.85 ± 0.09 C 2.72 ± 0.23 B
fied at 70 °C for 20 min. Deionised water (15 ml) was added and 6 1-Octanol 1579 30.8 ± 2.20 A 5.28 ± 0.64 B 32.5 ± 2.06 A
the mixture was extracted with 15 ml of n-hexane. The organic 7 2-Octen-1-ol 1637 4.76 ± 0.98 B 0.52 ± 0.05 C 6.22 ± 0.30 A
layer was washed with deionised water until neutral, then dried 8 Benzyl alcohol 1893 30.7 ± 6.63 A 6.28 ± 0.40 C 12.9 ± 0.23 B
over anhydrous sodium sulfate, and concentrated under reduced Total 190 ± 9.39 B 117 ± 4.57 B 1130 ± 145 A
pressure to dryness (<40 °C). The residue was redissolved in 5 ml Eight carbon 131 [69] 110 [94] 1120 [99]
of n-hexane and filtered prior to HPLC injection in the same man- compounds
Aromatic 59.6 [31] 7.13 [6] 15.6 [1]
ner as in the b-carotene assay. The HPLC system was the same as
compounds
for the 50 -nucleotide assay. The mobile phase was acetonitrile/
a
methanol (85:15, v/v) at a flow rate of 1.0 ml/min and UV detection Linear retention index was determined on a DB-Wax column using n-paraffins
(C8–C25) as reference standards.
was at 295 nm. b
% total volatiles = (the content of eight-membered carbon or aromatic com-
The total phenol content was determined according to the pounds/total volatiles contents in each mushroom)  100%.
method of Taga, Miller, and Pratt (1984). Each extract (20 mg) c
Each value is expressed as mean ± SD (n = 3). Means with different letters
was dissolved in a solution of 5 ml of 3% HCl (Merck) in 60% meth- within a row are significantly different (P < 0.05).
S.-Y. Tsai et al. / Food Chemistry 113 (2009) 578–584 581

Table 2 As compared to other mushrooms, the total content of soluble


Content of soluble sugars and polyols in Clitocybe maxima, Pleurotus ferulae and sugars or polyols were found to be 349–457 mg/g in V. volvacea
Pleurotus ostreatus
(Mau et al., 1997), 205–320 mg/g in A. bisporus (Tseng & Mau,
Sugar or polyol Content (mg/g dry weight) 1999), 98.7–316 mg/g in Auricularia spp. and Tremella fuciformis
C. maxima cap C. maxima stipe P. ferulae P. ostreatus (Mau & Tseng, 1998), 150–225 mg/g in Agaricus blazei, A. cylindr-
Arabitol 3.60 ± 0.25 Ca ndb 24.1 ± 1.48 A 17.1 ± 1.35 B
acea and Boletus edulis (Tsai, Tsai, & Mau, 2007) and 6.96–
Fructose nd 4.55 ± 0.46 nd nd 20.8 mg/g in P. eryngii (Mau et al., 1998). It seems that the con-
Glucose 1.25 ± 0.05 C 1.29 ± 0.38 C 13.2 ± 0.68 A 11.5 ± 0.26 B tent of sugars and polyols in these three mushrooms were in
Mannitol 4.45 ± 0.45 D 12.9 ± 0.54 C 20.6 ± 1.22 B 31.6 ± 2.57 A the middle range. Soluble sugars contained in the mushroom con-
Myo-inositol nd 20.7 ± 0.77 C 34.0 ± 0.31 B 45.8 ± 2.58 A
tributed a sweet taste (Litchfield, 1967). Therefore, the high con-
Ribose 4.77 ± 0.42 nd nd nd
Sucrose 18.2 ± 0.72 nd nd nd tent of sugars and polyols would give rise to a moderately sweet
Trehalose 156 ± 3.89 B 231 ± 9.01 A 33.3 ± 1.15 C 32.8 ± 2.43 C taste perception.
Total 188 ± 4.58 B 270 ± 3.43 A 125 ± 3.02 D 139 ± 1.57 C
a
Each value is expressed as mean ± SD (n = 3). Means with different letters 3.3. Free amino acids and taste components
within a row are significantly different (P < 0.05).
b
Not detected. The contents of total free amino acids in the three mushrooms
ranged from 10.5 to 37.6 mg/g and were in the descending order
of C. maxima cap > C. maxima stipe > P. ostreatus > P. ferulae (Table
(Mau & Hwang, 1997), respectively. It seems that these three 3). Interestingly, the content of total free amino acids in C. maxima
mushrooms showed much stronger aroma than other mushrooms cap was 2-fold higher than that found in stipe and 3-fold higher
mentioned above. than that found in P. ostreatus and P. ferulae. In addition, the free
amino acid profiles of the three mushrooms were found to be con-
3.2. Soluble sugars and polyols siderably different. Surprisingly, c-aminobutyric acid (GABA), a
hypotensive agent (Kohama et al., 1987), was found in these three
The contents of total soluble sugars and polyols ranged from mushrooms. The GABA content ranged from 0.25 to 0.45 mg/g and
125 to 270 mg/g and in the descending order of C. maxima stipe > C. was in descending order of C. maxima cap  C. maxima stipe > P.
maxima cap > P. ostreatus > P. ferulae (Table 2). Stipes of C. maxima ferulae > P. ostreatus. Furthermore, Tsai et al. (2007) found that
contained much more sugars and polyols than caps and the other the content of GABA in A. blazei, A. cylindracea and B. edulis was
two mushrooms. Obviously, C. maxima stipe was the energy reser- 0.36, 0.21 and 0.11 mg/g, respectively. Since GABA is a biologically
voir for the cap. Mannitol and trehalose, which were the major active compound, the presence of GABA in these three mushrooms
mushroom polyol and sugar, respectively (Mau et al., 1997), were would be beneficial to humans in addition to their palatable taste
found in these three mushrooms. High amounts of trehalose were and other therapeutic effects.
found in C. maxima stipe and cap (156 and 230 mg/g, respectively) In Table 3, free amino acids were divided into several classes on
whereas those in P. ferulae and P. ostreatus were relatively low the basis of their taste characteristics, as described by Komata
(33.3 and 32.8 mg/g, respectively). The profiles of Pleurotus mush- (1969). Aspartic and glutamic acids were the monosodium gluta-
rooms were similar and consisted of arabitol, glucose, mannitol, mate-like (MSG-like) components, which gave the most typical
myo-inositol and trehalose. mushroom taste, the umami taste or palatable taste that was the

Table 3
Content of free amino acids and taste components in Clitocybe maxima, Pleurotus ferulae and Pleurotus ostreatus

Amino acid Content (mg/g dry weight)


C. maxima cap C. maxima stipe P. ferulae P. ostreatus
L-Alanine 5.00 ± 0.10 Ac 2.46 ± 0.01 B 1.30 ± 0.07 C 1.14 ± 0.03 D
L-Arginine 2.48 ± 0.11 A 0.35 ± 0.04 D 1.30 ± 0.06 B 1.13 ± 0.08 C
L-Aspartic acid 1.48 ± 0.07 A 0.65 ± 0.01 B 0.36 ± 0.02 C 0.58 ± 0.01 B
GABAa 0.45 ± 0.03 A 0.42 ± 0.01 A 0.31 ± 0.02 B 0.25 ± 0.02 C
L-Glutamic acid 7.41 ± 0.43 A 4.55 ± 0.03 B 1.40 ± 0.09 C 1.56 ± 0.02 C
Glycine
+ L-Threonine 0.68 ± 0.03 B 0.50 ± 0.01 C 0.80 ± 0.01 B 2.27 ± 0.13 A
L-Histidine 11.78 ± 0.35 A 3.84 ± 0.03 B 0.39± 0.04 D 1.27 ± 0.07 C
L-Isoleucine 0.72 ± 0.07 B 0.27 ± 0.05 C 0.72 ± 0.06 B 1.09 ± 0.03 A
L-Leucine 0.06 ± 0.01 B 1.01 ± 0.33 A 0.32 ± 0.01 B 0.83 ± 0.03 A
L-Lysine 1.92 ± 0.09 A 0.73 ± 0.02 C 0.75 ± 0.02 C 0.86 ± 0.03 B
L-Methionine 0.23 ± 0.02 B 0.14 ± 0.01 BC 1.04 ± 0.11 A 0.11 ± 0.01 C
L-Phenylalanine 0.28 ± 0.03 B 0.46 ± 0.14 A 0.42 ± 0.09 AB 0.44 ± 0.02 AB
L-Serine 2.82 ± 0.12 A 1.26 ± 0.02 B 0.59 ± 0.07 C 0.12 ± 0.01 D
L-Tyrosine 0.89 ± 0.04 A 0.32 ± 0.01 D 0.73 ± 0.03 B 0.51 ± 0.08 C
L-Valine 1.44 ± 0.11 A 0.64 ± 0.08 B 0.05 ± 0.01 D 0.36 ± 0.01 C
Taste componentb
Bitter 17.0 ± 0.04 A 6.71 ± 0.35 B 4.24 ± 0.15 D 5.23 ± 0.06 C
MSG-like 8.89 ± 0.08 A 5.20 ± 0.18 B 1.76 ± 0.09 D 2.14 ± 0.03 C
Sweet 8.50 ± 0.37 A 4.22 ± 0.59 B 2.69 ± 0.11 D 3.53 ± 0.09 C
Tasteless 3.26 ± 0.20 A 1.47 ± 0.19 C 1.79 ± 0.01 B 1.62 ± 0.15 BC
Total 37.6 ± 1.05 A 17.6 ± 1.76 B 10.5 ± 0.09 D 12.5 ± 0.16 C
a
GABA, c-aminobutyric acid.
b
Bitter, Arg + His + Ile + Leu + Met + Phe + Val; MSG-like, monosodium glutamate-like, Asp + Glu; sweet, Ala + Gly + Ser + Thr; tasteless, Lys + Tyr + GABA.
c
Each value is expressed as mean ± SD (n = 3). Means with different letters within a row are significantly different (P < 0.05).
582 S.-Y. Tsai et al. / Food Chemistry 113 (2009) 578–584

characteristic taste of MSG and 50 -nucleotides (Yamaguchi, Yoshik- Table 4


awa, Ikeda, & Ninomiya, 1971). The contents of MSG-like compo- Content of 50 -nucleotides in Clitocybe maxima, Pleurotus ferulae and Pleurotus ostreatus

nents ranged from 1.76 to 8.89 mg/g and their order was the 50 -Nucleotidea Content (mg/g dry weight)
same as that of the content of total free amino acid. For three C. maxima C. maxima P. ferulae P. ostreatus
mushrooms, the content of bitter components was higher than cap stipe
the contents of MSG-like components. 50 -AMP 0.17 ± 0.02 0.32 ± 0.01 C 1.48 ± 0.02 1.39 ± 0.02
Chen (1986) conducted a series of sensory evaluations on syn- Dc A B
thetic mushroom extracts prepared by omitting and adding soluble 50 -CMP 0.90 ± 0.10 B 2.96 ± 0.23 A 0.32 ± 0.01 0.72 ± 0.06
components and found that alanine, glycine and threonine (sweet), C B
50 -GMP 0.03 ± 0.01 D 0.11 ± 0.01 C 0.58 ± 0.02 0.61 ± 0.01
and aspartic and glutamic acids (MSG-like) were taste-active ami-
B A
no acids in A. bisporus, whereas none of the bitter components was 50 -IMP 0.22 ± 0.02 C 0.20 ± 0.02 C 0.69 ± 0.02 0.74 ± 0.03
found to be taste-active. The bitterness from the bitter components B A
0
in three mushrooms could probably be masked by the sweetness 5 -UMP 0.28 ± 0.04 D 0.77 ± 0.07 C 1.94 ± 0.01 1.05 ± 0.01
A B
from sweet components and mainly the high amount of soluble
50 -XMP 0.29 ± 0.04 D 3.23 ± 0.24 A 1.78 ± 0.04 1.13 ± 0.02
sugars and polyols. Therefore, MSG-like and sweet components B C
would be responsible for the natural taste of these three Flavour 50 - 0.54 ± 0.08 D 3.54 ± 0.02 A 3.05 ± 0.01 2.48 ± 0.01
mushrooms. nucleotideb B C
With regard to the contents of MSG-like components in A. bisp- Total 1.89 ± 0.61 D 7.59 ± 0.13 A 6.79 ± 0.11 5.64 ± 0.14
B C
orus (22.7–47.1 mg/g; Tseng & Mau, 1999), these three mushrooms
a
possessed comparable content of MSG-like components. Further- 50 -AMP, 50 -adenosine monophosphate; 50 -CMP, 50 -cytosine monophosphate;
more, Tsai et al. (2007) found that contents of MSG-like compo- 50 -GMP, 50 -guanosine monophosphate; 50 -IMP, 50 -inosine monophosphate; 50 -UMP,
50 -uridine monophosphate; 50 -XMP, 50 -xanthosine monophosphate.
nents in A. blazei, A. cylindracea and B. edulis were 8.97–14.9 mg/ b
Flavour 50 -nucleotide, 50 -GMP + 50 -IMP + 50 -XMP.
g. Yang, Lin, and Mau (2001) found that contents of MSG-like com- c
Each value is expressed as mean ± SD (n = 3). Means with different letters
ponents in Lentinula edodes, Flammulina velutipes strain white, within a row are significantly different (P < 0.05).
Pleurotus cystidiosus and P. ostreatus), ranged from 0.84 to
1.93 mg/g. Mau, Lin, Ma, and Song (2001a) found that contents of
MSG-like components in Dictyophora indusiata, Grifola frondosa, P. ostreatus were in the high range whereas those in C. maxima
Hericium erinaceus and Tricholoma giganteum ranged from 0.68 to cap were in the middle range.
1.09 mg/g. Yang et al. (2001) also found that that in the yellow 50 -GMP gave the meaty flavour, and is a much stronger flavour
strain of F. velutipes was 7.06 mg/g of MSG-like components. How- enhancer than MSG (Litchfield, 1967). The synergistic effect of fla-
ever, Mau, Lin, and Chen (2001b) found that contents of MSG-like vour 50 -nucleotides with MSG-like components might greatly in-
components in Ganoderma lucidum, Ganoderma tsugae and Coriolus crease the umami taste of mushrooms (Yamaguchi et al., 1971).
versicolor were in the range of 0.17–0.50 mg/g. Yang et al. (2001) Using the equation derived from sensory evaluation (Yamaguchi
divided contents of MSG-like components into three ranges: low et al., 1971), the equivalent umami concentrations (EUC) were
(<5 mg/g), middle (5–20 mg/g) and high (>20 mg/g). Based on the 46.3, 139, 56.8 and 60.4 g MSG per 100 g dry weight for C. maxima
previous results, contents of MSG-like components in C. maxima cap and stipe, P. ferulae and P. ostreatus, respectively. Mau (2005)
cap and stipe were in the middle range, but those in P. ostreatus reported that EUC values could be grouped into four levels: first le-
and P. ostreatus were in the low range. vel of >1000 g per 100 g dry matter, second level of 100–1000 g per
100 g, third level of 10–100 g per 100 g, and fourth level of <10 g
3.4. 50 -Nucleotides per 100 g. Therefore, EUC value of C. maxima stipe was at the sec-
ond level, and C. maxima cap, P. ferulae and P. ostreatus were at the
The contents of total 50 -nucleotides in C. maxima stipe, P. ferulae third level. In other words, the umami intensity of 1 g of C. maxima
and P. ostreatus (5.64–7.59 mg/g) were higher than that in C. cap and stipe, P. ferulae and P. ostreatus was equivalent to the uma-
maxima cap (Table 4). Flavour 50 -nucleotides, which also gave the mi intensity given by 0.46, 1.39, 0.57 and 0.60 g of MSG.
umami or palatable taste, were found to be 50 -guanosine mono- Based on the results obtained, C. maxima cap and stipe, P. ferulae
phosphate (50 -GMP), 50 -inosine monophosphate (50 -IMP) and and P. ostreatus possessed a highly intense umami taste in addition
50 -xanthosine monophosphate (50 -XMP) (Chen, 1986). Contents to its pharmacological properties. The sensory EUC values of three
of flavour 50 -nucleotides in three mushrooms ranged from 1.89 mushrooms might be beneficial for its use as foods or food-flavour-
to 7.59 mg/g and in the descending order of C. maxima stipe > P. ing materials or in the formulation of nutraceuticals and functional
ferulae > P. ostreatus > C. maxima cap. foods with a palatable umami taste.
The contents of flavour 50 -nucleotides were found to be 4.19–
6.13 mg/g in A. bisporus (Tseng & Mau, 1999) and 1.63–4.89 mg/g 3.5. Antioxidant properties
in P. eryngii (Mau et al., 1998). In addition, Yang et al. (2001) found
that contents of flavour 50 -nucleotides in F. velutipes white strain, P. The yields extracted by ethanol were in the descending order
cystidiosus and P. ostreatus, ranged from 5.52 to 8.60 mg/g. Mau of P. ferulae (18.9%) > P. ostreatus (15.3%) > C. maxima cap
et al. (2001b) found that contents of flavour 50 -nucleotides in D. (11.2%) > C. maxima stipe (5.89%). The yields extracted by hot
indusiata, G. frondosa, H. erinaceus and T. giganteum were 9.04, water were in the descending order of P. ferulae (57.2%) > P. ostre-
0.64, 0.62 and 13.6 mg/g, respectively. The contents of flavour atus (44.5%) > C. maxima stipe (39.2%)  C. maxima cap (38.3%).
50 -nucleotides in G. lucidum, G. tsugae and C. versicolor were 1.18– The yields of the hot water extracts were higher than those of
5.65 mg/g (Mau et al., 2001a). The contents of flavour 50 -nucleo- the ethanolic extracts. The use of hot water to extract soluble
tides in A. blazei, A. cylindracea and B. edulis were 2.01–5.15 mg/g components from three mushrooms was to simulate the making
(Tsai et al., 2007). Yang et al. (2001) reported that the contents of of Chinese medicine and the brewing of herbal tea. Therefore,
flavour 50 -nucleotides could be divided into three ranges: low as compared to other solvent extraction, the information obtained
(<1 mg/g), middle (1–5 mg/g) and high (>5 mg/g). Therefore, the by use of hot water would be more valuable for these extracts
content of flavour 50 -nucleotides in C. maxima stipe, P. ferulae and used in human diets.
S.-Y. Tsai et al. / Food Chemistry 113 (2009) 578–584 583

The antioxidant properties assayed herein were summarised in they are additives and used or present in milligram levels in foods.
Table 5 and the results were normalised and expressed as EC50 val- However, C. maxima cap and stipe, P. ferulae and P. ostreatus could
ues (mg dry weight of various extracts per ml) for comparison. be used in gramme levels as food or a food ingredient. Therefore,
Effectiveness of antioxidant properties inversely correlated with these three mushrooms might serve as possible protective agents
their EC50 values. Generally, ethanolic extracts were more effective in human diets to help human reduce oxidative damage.
than hot water extracts in the inhibition of conjugated diene and
scavenging ability on DPPH radicals; whereas hot water extracts 3.6. Antioxidant components
were more effective in the scavenging ability on hydroxyl radials
as evidenced by their lower EC50 values. EC50 values were less than Naturally occurring antioxidant components, including b-caro-
14 and 30 mg/ml for ethanolic and hot water extracts, respectively, tene, tocopherols and total phenols, were found in two extracts
indicating that the three mushrooms were relatively effective in of three mushrooms (Table 6). However, ascorbic acid was not de-
antioxidant properties, except for scavenging ability on hydroxyl tected in two extracts and b-carotene was not detected in hot
radicals. water extracts. Total phenols were the major naturally occurring
Amongst the ethanolic extracts, P. ferulae and P. ostreatus were antioxidant components found in the range of 5.51–9.66 mg gallic
more effective than C. maxima cap and stipe in antioxidant activi- acid equivalents/g and 5.10–11.1 mg gallic acid equivalents/g for
ties and chelating ability on ferrous ions. In contrast, C. maxima cap ethanolic and hot water extracts, respectively. Contents of total
and stipe were more effective in scavenging ability on DPPH radi- phenols were similar for both extracts of C. maxima cap and stipe
cals. However, none of the ethanolic extracts were effective in their whereas for P. ferulae and P. ostreatus, contents of total phenols
scavenging ability on hydroxyl radicals. The ethanolic extract from were higher in hot water extracts than in ethanolic extracts.
P. ostreatus was more effective in the inhibition of conjugated diene
and chelating ability on ferrous ions whereas C. maxima cap was
more effective in reducing capability and scavenging ability on
DPPH radicals. Table 6
Like ethanolic extracts, hot water extracts from P. ferulae and P. Contents of b-carotene, tocopherols and total phenols in ethanolic and hot water
ostreatus were more effective than C. maxima cap and stipe in anti- extracts from Clitocybe maxima, Pleurotus ferulae and Pleurotus ostreatus
oxidant activities. However, the effectiveness in reducing capabil- Contenta (mg/g dry weight)
ity was in the descending order of C. maxima cap > C. maxima
C. maxima cap C. maxima stipe P. ferulae P. ostreatus
stipe > P. ferulae > P. ostreatus. Only hot water extracts from P. fer-
Ethanolic
ulae and P. ostreatus showed scavenging ability on DPPH radicals.
b-Carotene 0.05 ± 0.01 A 0.04 ± 0.01 A ndb nd
The hot water extract from C. maxima cap was more effective in a-Tocopherol b 0.01 ± 0.00 D a 0.04 ± 0.02 C a 0.31 ± 0.03 B 0.50 ± 0.02 A
its chelating ability on ferrous ions compared to the water extract c-Tocopherol a 0.09 ± 0.02 B 0.18 ± 0.01 A 0.19 ± 0.01 A 0.17 ± 0.03 A
from P. ferulae, but lower those from C. maxima stipe and P. ostre- d-Tocopherol a 0.01 ± 0.00 C 0.39 ± 0.02 A 0.08 ± 0.01 B 0.03 ± 0.01 C
Total phenols a 9.66 ± 0.03 A a 5.51 ± 0.02 D b 6.71 ± 0.29 C b 7.11 ± 0.24 B
atus. In scavenging ability on hydroxyl radicals, the effectiveness
was in the descending order of P. ferulae > P. ostreatus > C. maxima Hot-water
b-Carotene nd nd nd nd
cap whereas C. maxima stipe was not effective. However, amongst
a-Tocopherol a 0.04 ± 0.01 A a 0.01 ± 0.00 B b 0.01 ± 0.00 B nd
antioxidant properties assayed, the hot water extract from P. ostre- c-Tocopherol a 0.06 ± 0.00 nd nd nd
atus was slightly more effective. Overall, for both extracts, P. ostre- d-Tocopherol b 0.02 ± 0.00 nd nd nd
atus was more effective amongst antioxidant properties assayed Total phenols a 9.71 ± 0.05 B b 5.10 ± 0.01 D a 7.73 ± 0.23 C a 11.1 ± 0.25 A
than C. maxima and P. ferulae. a
Each value is expressed as mean ± SD (n = 3). Means with different capital let-
Although BHA and a-tocopherol showed good inhibitory ability ters within a row are significantly different (P < 0.05). Means with different small
on lipid oxidation, reducing capability and scavenging ability on letters within a column are significantly different (P < 0.05).
b
DPPH radicals and EDTA was excellent for chelating ferrous ions, Not detected.

Table 5
EC50 values of ethanolic and hot water extracts from Clitocybe maxima, Pleurotus ferulae and Pleurotus ostreatus in antioxidant properties

EC50 valuea (mg extract/ml)


C. maxima cap C. maxima stipe P. ferulae P. ostreatus
Ethanolic
Inhibition of conjugated diene b 12.9 ± 0.19 Ab b 13.2 ± 0.42 A b 0.74 ± 0.04 B b 1.16 ± 0.29 B
Reducing capability b 0.59 ± 0.02 D b 2.92 ± 0.19 C a 8.40 ± 0.17 A a 6.76 ± 0.34 B
Scavenging ability on DPPH radicals 0.81 ± 0.02 D 1.68 ± 0.08 C b 4.55 ± 0.04 B b 5.58 ± 0.24 A
Scavenging ability on OH radicals –c –c –c –c
Chelating ability on ferrous ions a 5.73 ± 0.03 A a 5.03± 0.02 B b 4.85 ± 0.15 C b 3.42 ± 0.08 D
Hot-water
Inhibition of conjugated diene a 17.6 ± 1.06 B a 29.5 ± 0.19 Ad a 15.2 ± 0.27 C a 9.86 ± 0.25 D
Reducing capability a 1.99 ± 0.06 C a 4.43 ± 0.54 A b 2.86 ± 0.09 B b 4.01 ± 0.03 A
Scavenging ability on DPPH radicals –c –c a 22.9 ± 0.03 Ad a 14.8 ± 0.49 B
Scavenging ability on OH radicals 55.1 ± 0.78 Ad –c 11.7 ± 0.55 C 21.3 ± 0.51 Bd
Chelating ability on ferrous ions a 6.40 ± 0.79 B b 3.22 ± 0.08 C a 10.9 ± 0.84 A a 4.22 ± 0.13 C
a
EC50 value: the effective concentration at which the inhibition of conjugated diene was inhibited by 50%; the absorbance was 0.5 for reducing capability; 1,1-diphenyl-2-
picrylhydrazyl (DPPH) or hydroxyl (OH) radicals were scavenged by 50%; and ferrous ions were chelated by 50%, respectively. EC50 value was obtained by interpolation from
linear regression analysis.
b
Each value is expressed as mean ± SD (n = 3). Means with different capital letters within a row at a specific antioxidant attribute significantly different values (P < 0.05).
Means with different small letters within a column are significantly different (P < 0.05).
c
No effect.
d
Obtained by extrapolation from linear regression analysis.
584 S.-Y. Tsai et al. / Food Chemistry 113 (2009) 578–584

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