Journal of Chemistry
Volume 2015 (2015), Article ID 372152, 7 pages
http://dx.doi.org/10.1155/2015/372152

Research Article

Variations in Element Levels Accumulated in Different Parts of Boletus edulis Collected from Central Yunnan Province, China

Xue-Mei Wang,¹ Ji Zhang,² Tao Li,³ Jie-Qing Li,¹ Yuan-Zhong Wang,² and Hong-Gao Liu¹

¹College of Agronomy and Biotechnology, Yunnan Agricultural University, Kunming 650201, China
²Institute of Medicinal Plants, Yunnan Academy of Agricultural Sciences, Kunming 650200, China
³College of Resources and Environment, Yuxi Normal University, Yuxi 653100, China

Received 9 December 2014; Revised 17 January 2015; Accepted 24 January 2015

Academic Editor: Yuangen Yang

Copyright © 2015 Xue-Mei Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

ICP-AES and microwave assisted digestion were applied to determine P, Mg, Ca, Zn, Na, Cu, Ba, Ni, V, Cd, Sr, Co, and Li in the caps and stipes of Boletus edulis collected from six spatially distant sites in Yunnan province, China. Fruiting bodies of King Bolete are abundant in P, Mg, Ca, Zn, Cu, and Na, followed by Ba, Cd, Ni, V, Li, Sr, and Co. Contents of P, Mg, Zn, and Cu are more abundant in caps than in stipes of King Bolete. However, elements such as Na, Ba, Cd, Ni, V, Li, Sr, and Co prefer to accumulate in stipes of mushrooms from Yaoan, Chuxiong. The results of this study indicate that spatial variations of elements between caps and stipes are mainly related to different bedrock soil geochemistry and enrichment capability for various elements.

1. Introduction

Edible wild-grown mushrooms are traditionally consumed as delicacy in lots of countries and many are also used in traditional Chinese medicine [1–4]. This would be due to the abundant sources of protein, carbohydrates, dietary fibre and certain vitamins, and minerals as well as bioactive components [5–7]. Reports suggested that edible wild-grown mushrooms have many pharmacological effects such as antioxidant, antitumor, and hypoglycaemic effect and boosting the immune system [8, 9]. In Yunnan province, the main wild edible and medicinal fungi are Boletus, Tricholoma, Termitomyces, Aphyllophorales, and Tuber [10].

King Bolete (Boletus edulis Bull. Fr.) is famous for its nutrition, flavor, taste, appearances, and medicinal value worldwide [11]. In China, they are mainly distributed in Yunnan, Sichuan, Fujian, Shanxi, and Guizhou province and usually grow up under the pine forest and broad-leaved forest [12]. Some alkaloid substances such as adenine, choline, and putrescine are produced by King Bolete, which are one of the ingredients of traditional Chinese medicine—Shujin Pill [11]. Besides, studies have indicated that inhibition rate of King Bolete extract for Sarcoma-180 is 100% and 90% for ehrlich ascites carcinoma [13, 14]. These functional characteristics are, as suggested by Qi et al., mainly due to the type and content of trace element but other active compounds seem also to take part [15].

Edible wild-grown mushrooms have a very effective mechanism to accumulate extremely high concentrations of macro- and microelements from soil [16–19]. Recognized factors influencing the bioaccumulation of trace elements in fungi are bedrock geochemistry, fungal lifestyle, environmental pollution, specific species, and element [20–24]. Fruiting bodies of King Bolete are naturally abundant in certain essential elements including P, K, Ca, Mg, Zn, Fe, Cu, and Se, but also in Hg, Cd, Pb, Ag, and Ni which are hazardous to human [25–29].

Central Yunnan province is one of the most wild edible mushrooms resource-rich and largest production regions in China. The main species are Boletus, Leccinum, Xerocomus, Tricholoma matsutake, Termitomyces, and Thelephora ganbajun [10]. Data published on element concentration of King Bolete did indicate the considerable variation between the sites, years, and reports [30, 31]. There is scarcity of data on minerals composition variation of King Bolete collected from China. In addition, due to the presence of hymenophore with generative spores in caps, distribution of elements is unevenly within the fruiting body of mushroom [32]. It is necessary to ascertain elements variation of King Bolete in China through knowledge of the concentrations of many essential and toxic elements. The objective was to examine and evaluate the distribution disparity in elements concentration (P, Mg, Ca, Zn, Na, Cu, Ba, Ni, V, Cd, Sr, Co, and Li) of caps and stipes of King Bolete collected from central Yunnan province, China.

2. Materials and Methods

2.1. Mushrooms Sampling

King Bolete (Boletus edulis Bull.: Fr.) samples were collected during summer and autumn in 2011 from six spatially distant sites in central Yunnan province, China (Figure 1). The specific site and number of specimens used in this study are given in Table 1. Fresh fruiting bodies were cleaned up with a plastic knife from visible plant or substrate debris and next separated to two parts (cap and stipe). Each sample was washed with deionized water and dried in an electrically heated oven at 65°C to constant weight. Dried samples were pulverized with a muller and stored in sealed polyethylene bag in dry condition for analysis.

Table 1: Locations and numbers of Boletus edulis samples collected from central Yunnan in 2011.

Code
Location
Number of samples

BE1
Baofeng, Jinning, and Kunming
11

BE2
Yulu, Nanhua, and Chuxiong
7

BE3
Pubei, Yimen, and Yuxi
12

BE4
Longchuan, Nanhua, and Chuxiong
10

BE5
Qianchang, Yaoan, and Chuxiong
8

BT6
Shaqiao, Nanhua, and Chuxiong
8

Figure 1: Localization of the sampling sites (dot) of Boletus edulis in central Yunnan, China.

2.2. Reagents and Apparatus

Deionized water and nitric acid solution were used to prepare all aqueous solutions and clean or soak the glassware. Nitric acid solution (HNO₃ 65%) and hydrogen peroxide (H₂O₂ 30%) were used for digestion of samples in automatic microwave digestion system. The contents of the minerals in King Bolete were determined using inductively coupled plasma atomic emission spectrophotometer (ICP-9000, Shimadzu, Japan).

2.3. Analysis

0.5 g of dried and powdered sample was mixed with 4 mL HNO₃ (65%), 2 mL H₂O₂ (30%), and 3 mL deionized water in polytetrafluoroethylene (PTFE) pressure vessels and digested in microwave digestion system. Ultimate digest was transferred to 25 mL colorimetric cylinder using deionized water for constant volume and subjected to instrumental analysis. Concentration of all elements in caps and stipes was determined using inductively coupled plasma atomic emission spectrophotometer and for blank solutions and certified reference material (GBW07605) as well. Discrepancies between certified values and concentrations quantified were all below 10%.

3. Results and Discussion

Data on the parameters determined for caps and stipes of King Bolete are presented in Table 2. The element concentrations vary significantly not only among the collection sites but also within morphological parts of a particular fruiting body. Samples of King Bolete collected from different sites show rich content in P, Mg, Ca, Zn, Cu, and Na which accumulate both in cap and in stipe, followed by Ba, Cd, Ni, V, Li, Co, and Sr. Meanwhile, prominent differences in the concentrations of these elements are also found in the caps and in the stipes of King Bolete.

Table 2: Elements content of Boletus edulis collected from central part of Yunnan province in 2011 (mg/kg dm, mean, SD, range).

Elements
BE1
BE2
BE3
BE4
BE5
BE6

P

    Cap
5523 ± 1070
9013 ± 2328
5528 ± 705
6021 ± 1044
4356 ± 1146
5420 ± 1410

1429–13588
11620–13010
4451–6406
3970–7381
1285–5655
2339–7256

    Stipe
3022 ± 535
3891 ± 965
2150 ± 406
3616 ± 1577
2668 ± 668
3348 ± 1229

1614–6086
2635–5008
1595–2794
1679–7179
1285–3435
3966–5730

    Qc/s
1.83
2.32
2.57
1.67
1.63
1.62

Mg

    Cap
1221 ± 64
1447 ± 137
935 ± 184
1138 ± 185
1028 ± 163
918 ± 173

332–3071
2116–2334
737–1404
782–1416
365–1397
580–1136

    Stipe
705 ± 42
710 ± 143
442 ± 59
939 ± 261
620 ± 48
636 ± 156

406–1771
462–889
339–523
607–1393
653–645
761–942

    Qc/s
1.73
2.04
2.12
1.21
1.66
1.44

Ca

    Cap
212 ± 15
249 ± 64
656 ± 126
635 ± 114
339 ± 104
367 ± 149

34–260
303–476
199–2435
353–1118
189–487
204–924

    Stipe
209 ± 11
236 ± 72
239 ± 68
952 ± 202
144 ± 59
373 ± 121

26–279
115–338
125–349
151–1632
67–259
170–750

    Qc/s
1.01
1.06
2.74
0.67
2.35
0.98

Zn

    Cap
128 ± 69
534 ± 122
204 ± 72
113 ± 26
54 ± 16.6
86 ± 21

29–299
426–1370
102–652
79–167
16–71
38–103

    Stipe
65 ± 13
332 ± 82
60 ± 24
66 ± 12
35 ± 9.3
47 ± 23

38–134
61–512
39–120
27–176
16–45
26–84

    Qc/s
1.97
1.61
3.4
1.71
1.54
1.83

Na

    Cap
19.3 ± 5.8
35.2 ± 16.7
15.3 ± 9.9
100 ± 21
63 ± 6.7
2.9 ± 0.4

5.8–57.2
5.2–134
3.8–89
38–156
55–74
1.3–5.8

    Stipe
19.6 ± 6.2
27.5 ± 5
23.5 ± 8.1
129 ± 34
95 ± 17
148 ± 47

3.9–73.0
2.1–41.1
5.8–102
69–202
62–143
16–242

    Qc/s
0.98
1.28
0.65
0.77
0.66
0.02

Cu

    Cap
33.6 ± 1.8
884 ± 63
40.3 ± 17
53.4 ± 44
17 ± 5.7
26.8 ± 8

11.5–81.3
57–3025
22–79
19–202
5.4–23.5
17.3–41

    Stipe
19.2 ± 2.3
703 ± 49
20.4 ± 11
32 ± 21
8.6 ± 2.7
13.9 ± 3.8

10.6–52.3
24–1496
9–54
14–87
5.4–13
9–20

    Qc/s
1.75
1.26
1.98
1.67
1.98
1.93

Ni

    Cap
2.7 ± 0.8
5.2 ± 1.1
2.1 ± 0.35
5.2 ± 1.8
2.4 ± 0.7
63.7 ± 14

1.27–4.33
3–9.9
1.5–2.6
2.1–7.9
1.2–3.2
49–83

    Stipe
1.7 ± 0.6
2.3 ± 0.42
1.1 ± 0.22
5.1 ± 3.1
16.7 ± 8
42.9 ± 16

1.05–2.66
1.86–2.96
0.77–1.54
2.3–15.2
1.2–25.7
25–62

    Qc/s
1.59
2.26
1.91
1.02
0.14
1.48

Co

    Cap
1.0 ± 0.34
0.8 ± 0.36
1.1 ± 0.39
0.9 ± 0.21
0.4 ± 0.1
8.4 ± 2.7

0.53–1.61
0.29–1.64
0.55–1.79
0.54–1.36
0.19–0.49
4–13.6

    Stipe
0.9 ± 0.25
0.5 ± 0.15
1.0 ± 0.61
0.8 ± 0.18
4.6 ± 1.7
6.3 ± 2.4

0.34–2.13
0.27–0.67
0.38–2.04
0.31–2.56
0.39–5.9
2.5–8.7

    Qc/s
1.11
1.6
1.1
1.13
0.09
1.33

Ba

    Cap
8.1 ± 1.1
9.7 ± 3.4
6.6 ± 1.9
9.9 ± 4
4.8 ± 1.5
66.7 ± 32

2.59–12.0
3.96–20.3
3.44–9.13
4.5–18.2
2.7–6.9
26–136

    Stipe
5.3 ± 0.58
4.4 ± 1.37
2.7 ± 0.7
9.6 ± 3.4
65.5 ± 20
41.1 ± 13

3.27–7.81
2.62–6.85
1.78–3.84
5.4–25.1
3.4–73
25–63

    Qc/s
1.53
2.2
2.44
1.03
0.07
1.62

V

    Cap
1.7 ± 0.56
3.9 ± 0.86
1.2 ± 0.34
3.7 ± 0.8
1.6 ± 0.7
27.3 ± 10.5

0.6–2.85
1.24–8.75
0.65–1.64
0.98–7.29
0.7–2.82
12.5–46.6

    Stipe
1.1 ± 0.34
1.4 ± 0.41
0.5 ± 0.02
3.4 ± 1.1
15.3 ± 4.8
15.8 ± 7.5

0.45–1.93
1.02–2.11
0.33–0.92
1.5–11.1
0.9–23.9
8–30

    Qc/s
1.55
2.79
2.4
1.09
0.1
1.73

Cd

    Cap
2.1 ± 0.3
5.3 ± 1.9
1.2 ± 0.35
1.4 ± 0.67
1.6 ± 0.6
24.8 ± 5.6

0.48–5.37
1.2–13
0.74–2.05
0.76–2.99
0.41–2.6
11.8–36.5

    Stipe
0.9 ± 0.25
1.5 ± 0.03
0.5 ± 0.1
0.9 ± 0.72
5.1 ± 1.9
10.1 ± 2.3

0.35–1.95
0.96–2.23
0.31–0.82
0.19–4.45
0.5–9.1
4–16.5

    Qc/s
2.33
3.53
2.4
1.56
0.31
2.46

Sr

    Cap
4.4 ± 0.32
1.5 ± 0.1
1.5 ± 0.4
2.1 ± 0.57
0.9 ± 0.3
11.5 ± 5.9

0.5–23.5
0.45–3.34
0.92–2.5
1.13–2.89
0.56–1.54
6.7–24.8

    Stipe
1.4 ± 0.5
0.9 ± 0.2
1.0 ± 0.37
1.9 ± 1
9.7 ± 3.1
9.9 ± 2.6

0.78–2.14
0.59–1.09
0.64–1.82
0.53–4.26
0.59–15.4
6.8–12.9

    Qc/s
3.14
1.67
1.5
1.11
0.09
1.16

Li

    Cap
0.6 ± 0.03
1.6 ± 0.2
0.3 ± 0.05
1.6 ± 0.85
1.2 ± 0.45
5.9 ± 1.3

0.37–1.02
0.57–3.68
0.18–0.36
0.29–3.27
0.7–2.1
1.2–8.7

    Stipe
0.4 ± 0.02
0.6 ± 0.17
0.2 ± 0.08
1.4 ± 1.1
3.1 ± 1.13
4.3 ± 1.26

0.06–0.91
0.42–0.88
0.07–0.33
0.57–3.96
0.87–4.1
0.3–3.89

    Qc/s
1.5
2.67
1.5
1.14
0.39
1.37

Qc/s is the ratio of the element concentration in cap to stipe.

Qc/s value is a quotient between the minerals concentrations in caps and stipes, which is used to express the elements distribution within the fruiting body of the mushrooms. Significant differences have been suggested in loads of accumulated elements between caps and stipes, and some were caused by the site or year of mushroom collection [30, 31, 33]. In this study, multivariate Qc/s values are obtained between the elements and collection sites (Table 2). Minerals such as P, Mg, Zn, and Cu prefer to accumulate in the cap of King Bolete collected of all sites in this study. Except for the prevailing elements P, Mg, Zn, Ca, and Cu, Qc/s values for other elements in King Bolete collected from BE5 are <1. Consequently, these different distributions of elements between caps and stipes are mainly related to different bedrock soil geochemistry and ability to accumulate various elements.

3.1. Essential Elements: P, Mg, Ca, Zn, Na, Cu, Ni, and Co

P is the essential element that nearly participates in all physiological chemical reactions such as forming the bones, teeth, and nucleic acid, maintaining balance of ATP metabolism, and regulating acid-base balance. Rich concentrations are found in King Bolete and with the range of 4356–9013 mg kg⁻¹ and 2150–3891 mg kg⁻¹ dm for cap and stipe, respectively. So contents in caps are higher than in stipes, and Qc/s values vary between 1.62 and 2.57 (Table 2). King Bolete collected from mountain area of Liaoning province in China with 4995 mg kg⁻¹ dm agreed with this study [11]. P value in fruiting body (cap and stipe) and Qc/s of King Bolete is insufficient.

Caps of King Bolete contain Mg at 918–1447 mg kg⁻¹ dm, which are higher than for stipes (442–939 mg kg⁻¹ dm). Lower values of 590–960 mg kg⁻¹ dm were obtained for caps of King Bolete collected from Poland [31, 33, 34]. However, in the study by Liu et al. [23], elevated contents of Mg (1100–1500 mg kg⁻¹ dm) were got in wild-grown mushroom such as Catathelasma ventricosum, Laccaria amethystina, and Stropharia rugoso-annulata.

Ca is the activator of more than 200 kinds of enzymes in the human body, which can make each organ function well. Na concentration values distribution in King Bolete varies depending on the sites (Table 2). Qc/s values for Ca vary between 0.67 and 2.74, and contents of stipes for BE4 (0.67) exceed that of caps, and opposite feature could be observed for BE3 (2.74) and BE5 (2.35), while they are similar for BE1 (1.01), BE2 (1.06), and BE6 (0.98).

Zinc contents were reported at between 28 and 140 mg kg⁻¹ dm for edible wild-grown mushrooms collected from China [7]. Meanwhile, higher concentration was also reported showing its physiological importance to mushroom. The examples are as follows: 190 mg kg⁻¹ dm (cap) [34], 240 mg kg⁻¹ dm (cap) [35], and 580 mg kg⁻¹ dm (whole fruiting body) [30]. As shown in Table 2, stipes of King Bolete are half or even less than caps in essential Zn, and value of Qc/s for Zn in this study is 1.54–3.4, which extremely agrees with literature data previously reported [16]. Nevertheless, a higher value (Qc/s = 4.6) was reported in fruiting body of King Bolete collected from Xichang in Sichuan province, China [36].

Na content for caps is between 2.9 and 100 mg kg⁻¹ dm and for stipes between 19.6 and 148 mg kg⁻¹ dm. Higher values were determined in cultivated and some preserved mushrooms and content was 860, 1000, and 16000–25000 mg kg⁻¹ dm for Agaricus bisporus (whole), Lentinula edodes, and Agaricus bisporus (preserved), respectively [37–39]. Na is present higher in concentrations in stipes than in caps, except for samples collected from BE2 (Yulu, Nanhua) with the value of 1.28 (Table 2). Published data in stipes of King Bolete are about twice more abundant in Na than the caps [16]. Report also suggested the similar Qc/s value (0.45) for sodium in parasol mushroom Macrolepiota procera [40].

Cu is an essential element, and a large variation of values is noted; they ranged, respectively, between 17–884 and 8.6–703 mg kg⁻¹ dm for caps and stipes (Table 2). Cu in this study is more abundant in caps than stipes of King Bolete, and Qc/s value varies between 1.26 and 1.98. Higher Qc/s value of 2.8 was obtained for King Bolete collected from Pbocka Dale in Poland [34]. In addition, Cu contents in caps of Leccinum mushrooms from Poland were half or even less than in stipes [41].

Published data on Ni and Co in caps and stipes of King Bolete is few and relatively insufficient. Ni content of King Bolete at six sites varied between 2.1 and 63.7 mg kg⁻¹ dm in caps and between 1.1 and 42.9 mg kg⁻¹ dm in stipes. The mean Co concentrations were 0.4–8.4 and 0.5–6.4 mg kg⁻¹ for caps and stipes, respectively. Published data on Co contents were usually below or around 0.5 mg/kg DM, which were lower than the results in this study [42]. Contents in caps are somewhat higher than those in stipes except sample collected from BE5; that is, Qc/s value is 1.02–2.26 and 1.1–1.6 for Ni and Co, respectively.

3.2. Ba, V, Cd, Sr, and Li

As shown in Table 2, Ba, V, Cd, Sr, and Li contents in samples from BE6 are obviously higher than those from other regions, which is most probably depending on the geological bedrock in this site. Arithmetic mean of Qc/s for these elements is 1.03–3.53; nevertheless, for certain site (BE5) the Qc/s value is <1.

Ba content is in the range of 4.8–66.7 and 2.7–65.5 for caps and stipes, respectively, and these values are particularly higher than the reference data previously reported, which were 0.2–1.5 mg kg⁻¹ dm for caps and 0.36–1.4 mg kg⁻¹ dm for stipes [30, 31, 33, 34].

Reports on V contents on King Bolete were very few, and literature data were 0.02–0.09 mg kg⁻¹ dm in caps, 0.03 mg kg⁻¹ dm in stipes, and 1.27 mg kg⁻¹ dm in whole fruiting body [27, 31]. King Bolete in this study contains V at elevated concentrations; for caps it is 1.2–27.3 mg kg⁻¹ dm and for stipes at 0.5 to 15.8 mg kg⁻¹ dm, Qc/s value is 0.1–2.79.

Cd is toxic metallic element is found in edible mushrooms and can leach out of fruiting bodies during boiling. Tolerance limit is 2 μg/g dm for cultivated mushroom, and no such tolerances exist for edible wild-grown fungi [43]. Apart from the highest value (24.8 mg kg⁻¹ dm) of cap from EB6, other values are relatively low, which is consistent with the results of earlier studies [16].

King Bolete contains Sr at 0.9–11.5 mg kg⁻¹ dm in caps and at 0.9–9.9 mg kg⁻¹ dm in stipes, which is higher value than for samples from Poland. Most of the sites surveyed caps, when compared to stipes containing higher content of Sr, and opposite feature was found in earlier reports [30, 31, 33, 34].

The lithium salt, Li₂CO₃, is considered as a therapeutic for neurodisorders. Li is a trace element in fungi, and content is relatively low [16]. Li content of King Bolete from Italy was between 0.04 and 0.9 mg kg⁻¹ dm [44]. Higher results are determined in present study: mean value of Li is from 0.3 to 5.9 mg kg⁻¹ dm in caps and from 0.2 to 4.3 mg kg⁻¹ dm in stipes.

4. Conclusion

King Bolete collected from central Yunnan province contained high content of elements such as P, Mg, Ca, Zn, Na, and Cu, next for Ba, Ni, V, Cd, and Sr, and the least for Co and Li. Distribution of elements in different parts of King Bolete was unevenly, mainly depending on the hymenophore in the caps. In addition, spatial variations of Qc/s value were noted for King Bolete from different sites, which seem to be due to variations in local soil substrate geochemistry. Our results indicated that there is a close relationship between element concentrations and hymenophore in cap and bedrock soil geochemistry.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgments

This study has been supported by the National Natural Science Foundation of China (31460538, 31260496, and 31160409), the Special Project on the Countryside Comprehensive Reform (2014NG007-18), and the Science Foundation of the Yunnan Province Department of Education (2013Z074).

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