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. 2024 Mar 15;22:101288. doi: 10.1016/j.fochx.2024.101288

Formation of special odors driven by volatile compounds during the growth and maturation in edible fungi (Phallus impudicus)

Huijuan Liu a, Zhifei Cheng b, Jiao Xie a,⁎
PMCID: PMC10957454  PMID: 38524779

Highlights

  • •

    Volatile changes in edible fungi are affected by the growth stage.

  • •

    Changes in volatiles during the growth of Phallus impudicus were analyzed by GC–MS.

  • •

    A total of 102 volatile compounds were identified from the fruiting bodies.

  • •

    Growth stages of Phallus impudicus had significant effect on volatiles.

  • •

    PI stage was key turning point for synthesis and accumulation of volatile compounds.

Keywords: Edible fungi of Phallus impudicus, Volatile compounds, Growth stages, HS-SPME-GC–MS

Abstract

Composition and content of volatiles, the important factors in flavor formation of edible fungi, are affected by growth process. GC–MS was performed and a total of 102 volatiles were identified in Phallus impudicus. Almost all identified volatile compounds showed an obvious upward trend at four growth period, and reached the maximum at fourth stage (PIII), of which the transition from first stage (ZP) to second stage (PI) achieved a breakthrough for 88 volatile compounds from scratch. The PCA and HCA results showed that the four stages were completely separated and appeared different, among which third stage (PII) and PIII might be the two dramatic change nodes in aroma quality. In addition, the top 50 differential metabolites were screened by OPLS-DA and PLS-DA, and correlation analysis showed that 6-undecyl alcohol, α-terpine-7-al, 2, 4-decenol, and 2-cyano-2-ethyl-butanamide, might co-regulate the flavor formation of Phallus impudicus through synergistic action of other chemical components.

Introduction

Phallus impudicus (Phallus impudicus L. ex. Pers.), known as “Wuqunsun” in China, is a genus of edible fungus homologous to medicine that belongs to the family of Phallus, class of Phallaceae and oder of Phallales (Hosaka et al., 2006, Khan et al., 2020, Pudil et al., 2014, Shou, 2020). The mature fruiting body of Phallus impudicus consists mainly of three parts, namely pileus (covered with spores), volva and stipe (Pudil, Uvira & Janda, 2014). Of them, the commercially available product generally takes the stipe as edible part. Previous studies have shown that Phallus impudicus is rich in polysaccharides, polyphenols, flavonoids, and other bioactive substances, which have significant effects on immune regulation, anti-oxidation, lowering blood lipid and inhibiting tumor. (Gupta, Jayaprakash & Shinde, 2016; Khan et al., 2020, Kuznecova et al., 2007, Shou, 2020, Vyacheslav et al., 2019, Zhang, 2015). Thus, Phallus impudicus has good commercial value and social value.

At present, the Phallus impudicus was well known not only the high nutritional value but also its unique flavor (Gupta et al., 2016; Shou, 2020). Of them, flavors was strictly affected by the composition and abundance of volatile compounds (Gupta et al., 2016, Pudil et al., 2014). Currently, the most studies on volatile compounds have mainly focused on widely cultivated and consumed fungi such as Agaricus bisporus and Shiitake Mushrooms in the market (Cho et al., 2003, Feng et al., 2021; Li et al., 2022; Yao et al., 2023). For example, existing studies have pointed out that both eight carbon compounds (1-octanol, 3-octanol, 3-octanone, etc.) and some non-eight carbon compounds (N-nonanal, etc.) were important volatile components in these edible fungi (Feng et al., 2021). However, there are few studies on the changes of volatile components in Phallus impudicus. As a crucial factor for consumer preferences, the special flavor of edible fungi was also mainly affected by growth process (Aisala et al., 2019, Cao et al., 2023, Grosshauser and Schieberle, 2013, Tietel and Masaphy, 2018, Yao et al., 2023). In addition, the unique volatile compounds in each type of edible fungi contributed to the unique aroma and participated in the regulation of edible fungi growth (Aisala et al., 2019, Cao et al., 2023; Dickschat, Celik & Brock, 2018; Yao et al., 2023). Therefore, the factor of maturity can significantly affect the composition and abundance of volatile compounds (Cho et al., 2003, Feng et al., 2021, Hou et al., 2020, Pudil et al., 2014, Xie et al., 2023). All in all, the changes of volatile compounds during the development and maturation reflect the variations in flavor of edible fungi during this period, and these characteristic changes can be used as important indicators of maturity and optimal harvest time of edible fungi.

At present, previous studies have revealed that the flavor formation of edible fungi was affected by the development stage (Aisala et al., 2019, Cao et al., 2023; Dickschat et al., 2018; Grosshauser and Schieberle, 2013, Tietel and Masaphy, 2018, Yao et al., 2023). However, little is known about the effects of different developmental stages on volatile constituents related to flavor formation in the rare edible fungi, Phallus impudicus.. In this study, the samples of Phallus impudicus at four different developmental stages were collected, headspace solid-phase microextraction-gas chromatography-mass spectrometry (HS-SPME-GC–MS) was performed to analyze the stage-dependent changes of volatile constituents, and the key volatile compounds in the stipes of four growth stages were screened by combining orthogonal partial least squares-discriminant analysis (OPLS-DA) and partial least squares-discriminant analysis (PLS-DA). Through the in-depth study of the characteristic volatile constituents of Phallus impudicus, the theoretical basis for the chemical features behind the formation of the special flavor and the best harvest time of Phallus impudicus was provided.

Materials and methods

Plant materials

Phallus impudicus samples used in the present study originated from a under-forest planting field in Baiyun District, Guiyang City, Guizhou Province, China. The development period in this study was divided into four stages (Immature egg form for ZP, Shell breaking stage for PI, Rapid growth stage for PII and Mature stage for PIII) showed in Fig. 1. Five strains of Phallus impudicus were selected for each developmental stage, and fifteen stipes were collected. A total of three biological replicates were performed in this study. The samples used were the same size and appearance at the same developmental stage with free from pests or diseases as well as mechanical damage. After the sample collection, the volva, stipe and pileus were separated immediately to prevent the cross-contamination between different parts or the fuzzy stage division caused by the failure to terminate the growth in time. Of them, the stipes were immediately placed in liquid nitrogen, and then stored at −80 °C until extraction.

Fig. 2.

Fig. 2

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Types and multivariate statistical analysis of volatile compounds in Phallus impudicus at different development stage (ZP, PI, PII and PIII stage). (A) indicated Venn diagram; (B) exhibited the classification and relative content of volatile compounds; (C) meant the principal component analysis (PCA). (D) indicated the hierarchical cluster analysis (HCA).

Fig. 1.

Fig. 1

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Schematic diagram of Phallus impudicus at different developmental stages (ZP, PI, PII and PIII stage).

Chemicals and reagents

Sodium chloride was of analytical grade and was supplied by Sinopharm Chemical Reagent Co., Ltd (Shanghai, China). Chromatographic grade n-hexane was acquired from Merck Co (Darmstadt, Germany). The internal standard of [3,4,5,6-2H4]-Methyl 2-hydroxybenzoate and standards of 102 compounds listed in Table 1were all chromatographic grade, and part of them were purchased from BioBioPha/WAKO/Sigma-Aldrich (St Louis, MO, USA).

Table 1.

Volatile compounds of Phallus impudicus with various developmental stages.

NO. Compounds Identification of the volatile components Relative contents (μg/mL)
RRI RI CAS Q1 Q2 M (Da) IB ZP PⅠ PⅡ PⅢ
1 iminodiacetonitrile – 1108 628–87-5 94 68 95.05 MS 0.00 ± 0.00a 3.11 ± 0.28a 7.54 ± 1.49a 58.31 ± 10.72c
2 geranylacetone 1449 1453 3796–70-1 69 41 194.17 MS, CR 0.18 ± 0.01a 0.44 ± 0.03a 1.87 ± 0.12a 42.65 ± 10.90b
3 α-2-propenyl-benzenmethanol – 1244 936–58-3 107 79 148.09 MS 26.79 ± 0.02ab 26.48 ± 0.61a 26.59 ± 0.50a 28.18 ± 1.25b
4 pentamethylbenzene 1261 1260 700–12-9 133 148 148.13 MS, CR 0.00 ± 0.00a 8.69 ± 0.54b 20.64 ± 0.73c 94.09 ± 3.17d
5 β-terpenyl acetate 1272 1317 10198–23-9 93 68 196.15 MS, CR 0.00 ± 0.00a 0.40 ± 0.07a 13.21 ± 0.16b 31.57 ± 6.24c
6 (E, E)-2,4-decadienal 1322 1317 25152–84-5 81 41 152.12 MS, CR 0.00 ± 0.00a 1.27 ± 0.13a 82.26 ± 0.64b 225.54 ± 49.86c
7 verbenone 1228 1228 18309–32-5 107 91 150.10 MS, CR 0.00 ± 0.00a 9.19 ± 0.63b 31.09 ± 1.56c 130.01 ± 8.70d
8 α-muurolene 1499 1499 10208–80-7 105 161 204.19 MS, CR 8.83 ± 0.35a 9.95 ± 0.98a 11.18 ± 1.23a 19.57 ± 5.26b
9 o-xylorcinol – 1490 527–55-9 138 123 138.07 MS 12.19 ± 0.52a 13.33 ± 1.68a 16.78 ± 2.61a 33.55 ± 8.76b
10 (E)-6-nonenal – 1124 2277–20-5 41 55 140.12 MS 0.00 ± 0.00a 12.38 ± 1.11a 30.23 ± 6.66a 229.18 ± 41.60b
11 (Z)-3-nonen-1-ol 1156 1156 10340–23-5 55 68 142.14 MS, CR 0.00 ± 0.00 a 7.04 ± 0.52b 14.64 ± 0.33c 58.62 ± 3.11d
12 7-methyl-3-methyleneoct-6-enal 1147 1147 55050–40-3 69 41 152.12 MS, CR 0.00 ± 0.00a 5.45 ± 0.22b 11.43 ± 0.12c 49.21 ± 3.33d
13 3-ethyl-3-methyldecane – 1229 17312–66-2 57 85 184.22 MS 0.00 ± 0.00 a 0.39 ± 0.06ab 1.56 ± 0.03b 9.47 ± 1.27c
14 o-sec-butylphenol 1252 1289 89–72-5 121 150 150.10 MS, CR 0.00 ± 0.00a 4.71 ± 0.24b 9.09 ± 0.59c 38.56 ± 2.87d
15 chavicol 1258 1255 501–92-8 134 133 134.07 MS, CR 0.00 ± 0.00a 1.00 ± 0.05b 2.47 ± 0.07c 10.66 ± 0.88d
16 (Z)-2-decenal 1250 1252 2497–25-8 41 55 154.14 MS, CR 0.00 ± 0.00a 1.23 ± 0.10a 3.09 ± 0.05b 14.22 ± 1.44c
17 (E)-2-dodecenal 1468 1468 20407–84-5 41 70 182.17 MS, CR 0.00 ± 0.00a 0.15 ± 0.04a 0.68 ± 0.08a 16.27 ± 3.90b
18 3,4-dimethyl-2,4,6-octatriene 1132 1121 57396–75-5 121 136 136.13 MS, CR 0.00 ± 0.00a 3.21 ± 0.20a 8.00 ± 1.76a 62.18 ± 11.78b
19 citronellal 1153 1153 106–23-0 154 95 154.14 MS, CR 0.00 ± 0.00a 20.30 ± 1.03b 42.48 ± 1.03c 173.31 ± 10.33d
20 γ-muurolene 1477 1477 30021–74-0 161 105 204.19 MS, CR 3.59 ± 0.30a 3.99 ± 0.13a 4.28 ± 0.24a 6.99 ± 1.94b
21 (3E)-3-nonen-1-ol 1143 1143 10339–61-4 55 41 142.14 MS, CR 0.00 ± 0.00a 7.03 ± 0.42b 14.63 ± 0.32c 59.13 ± 3.60d
22 hexyl-2-methylbutanoate 1236 1236 10032–15-2 103 57 186.16 MS, CR 0.00 ± 0.00a 1.24 ± 0.05b 3.94 ± 0.18c 16.31 ± 1.11d
23 methyl geranate 1326 1323 2349–14-6 69 41 182.13 MS, CR 0.00 ± 0.00a 6.86 ± 0.63a 345.52 ± 1.17b 956.79 ± 186.85c
24 (E)-carvone 1243 1242 99–49-0 82 54 150.10 MS, CR 11.57 ± 0.06a 11.46 ± 0.12a 11.51 ± 0.42a 11.90 ± 0.34a
25 4-vinylguaiacol 1312 1316 7786–61-0 135 150 150.07 MS, CR 0.00 ± 0.00a 0.28 ± 0.04a 11.56 ± 0.23b 31.78 ± 6.71c
26 4-pentenyl propionate 978 974 30563–30-5 57 68 142.10 MS, CR 8.91 ± 4.09a 29.08 ± 4.21b 95.06 ± 14.27c 23.90 ± 1.62b
27 4, 8-dimethyl-1, 3, 7-nonadiene 1117 1116 19945–61-0 69 41 150.14 MS, CR 0.00 ± 0.00a 43.28 ± 3.86a 106.24 ± 24.24a 824.59 ± 155.89b
28 isoxylaldehyde 1208 1208 5779–94-2 134 133 134.07 MS, CR 0.00 ± 0.00a 0.64 ± 0.03ab 2.38 ± 0.08b 12.50 ± 1.90c
29 piperitone oxide 1259 1256 5286–38-4 69 55 168.12 MS, CR 0.00 ± 0.00a 2.20 ± 0.11b 5.29 ± 0.09c 24.11 ± 1.25d
30 bornyl formate 1220 1226 7492–41-3 95 121 182.13 MS, CR 0.00 ± 0.00a 2.80 ± 0.31ab 11.39 ± 0.38b 74.67 ± 10.29c
31 3-formylphenol 1267 1327 100–83-4 122 121 122.04 MS, CR 0.00 ± 0.00a 0.25 ± 0.04a 7.01 ± 0.24b 17.43 ± 3.54c
32 α-zingiberene 1495 1495 495–60-3 119 93 204.19 MS, CR 9.18 ± 0.20a 10.05 ± 1.12a 11.60 ± 1.35a 20.86 ± 5.60b
33 α-cyclocitral 1116 1116 432–24-6 81 123 152.12 MS, CR 0.00 ± 0.00a 9.28 ± 0.69a 22.70 ± 5.23a 180.25 ± 34.07b
34 o-methylnitrobenzene 1155 1161 88–72-2 120 65 137.05 MS, CR 0.00 ± 0.00a 5.11 ± 0.32b 10.71 ± 0.19c 47.26 ± 3.52d
35 trans-chrysanthenyl acetate 1238 1239 50764–55-1 119 134 194.13 MS, CR 0.00 ± 0.00a 2.33 ± 0.12b 7.87 ± 0.46c 33.56 ± 2.11d
36 perillyl alcohol – 1312 18457–55-1 68 79 152.12 MS 0.00 ± 0.00a 0.60 ± 0.04a 32.18 ± 0.20b 87.16 ± 17.30c
37 α-terpinen-7-al 1282 1283 1197–15-5 79 107 150.10 MS, CR 0.00 ± 0.00a 166.88 ± 9.00b 316.35 ± 18.80c 1217.01 ± 73.75d
38 propyl benzeneacetate 1331 1331 4606–15-9 91 92 178.10 MS, CR 0.00 ± 0.00a 0.23 ± 0.02a 14.38 ± 0.05b 34.98 ± 6.51c
39 α-caryophyllene 1451 1454 6753–98-6 93 80 204.19 MS, CR 0.30 ± 0.02a 0.46 ± 0.05a 0.97 ± 0.10a 15.19 ± 3.94b
40 butylbenzene 1053 1054 104–51-8 91 92 134.11 MS, CR 0.00 ± 0.00a 9.67 ± 1.48a 9.46 ± 1.06a 433.33 ± 39.38b
41 geranyl nitrile – 1231 31983–27-4 69 41 149.12 MS 0.00 ± 0.00a 2.20 ± 0.08a 8.23 ± 0.23b 45.85 ± 5.01c
42 linalyl acetate 1256 1257 115–95-7 93 80 196.15 MS, CR 0.00 ± 0.00a 2.12 ± 0.13b 4.64 ± 0.16c 21.56 ± 1.88d
43 decanol 1272 1272 112–30-1 70 55 158.17 MS, CR 0.00 ± 0.00a 4.30 ± 0.23b 8.51 ± 0.52c 33.27 ± 1.90d
44 2, 4-decadienol 1295 1274 14507–02-9 41 55 154.14 MS, CR 0.00 ± 0.00a 127.52 ± 6.97b 268.70 ± 12.11c 1216.42 ± 100.20d
45 2-cyano-2-ethyl-butyramide – 1287 18705–38-9 82 97 140.10 MS 0.00 ± 0.00a 434.70 ± 28.65a 1040.56 ± 36.81b 6154.87 ± 640.47c
46 car-3-en-5-one 1314 1314 81800–50-2 107 150 150.10 MS, CR 0.00 ± 0.00a 0.90 ± 0.10a 35.78 ± 0.82b 94.95 ± 19.74c
47 phenol 981 980 108–95-2 94 66 94.04 MS, CR 5.01 ± 0.22a 6.51 ± 0.33a 11.65 ± 1.81b 17.98 ± 0.36c
48 adamantane 1117 1116 281–23-2 136 79 136.13 MS, CR 0.00 ± 0.00a 1.00 ± 0.09a 2.33 ± 0.53a 17.94 ± 3.27b
49 cinnamaldehyde 1278 1274 104–55-2 131 132 132.06 MS, CR 0.00 ± 0.00a 4.76 ± 0.22ab 10.72 ± 0.28b 65.12 ± 7.58c
50 panaxene 1314 1314 871660–95-6 121 105 204.19 MS, CR 0.00 ± 0.00a 0.33 ± 0.02a 9.09 ± 0.18b 23.93 ± 5.00c
51 p-hydroxyacetophenone 1442 1455 99–93-4 121 136 136.05 MS, CR 0.00 ± 0.00a 0.14 ± 0.02a 0.38 ± 0.03a 9.60 ± 2.49b
52 isopropyl benzoate 1223 1217 939–48-0 105 77 164.08 MS, CR 0.00 ± 0.00a 12.93 ± 0.83b 43.89 ± 1.96c 190.55 ± 12.82d
53 veratrol 1147 1148 91–16-7 138 95 138.07 MS, CR 0.00 ± 0.00a 3.69 ± 0.22b 14.43 ± 1.90c 33.85 ± 0.57d
54 trans-limonene oxide 1139 1139 6909–30-4 94 108 152.12 MS, CR 0.00 ± 0.00a 12.65 ± 0.70b 26.49 ± 0.57c 115.45 ± 7.05d
55 p-acetylethylbenzene 1274 1277 937–30-4 133 148 148.09 MS, CR 0.00 ± 0.00a 159.26 ± 12.03b 292.87 ± 19.26c 823.65 ± 47.62d
56 dihydromethyl cinnamate 1279 1279 103–25-3 104 91 164.08 MS, CR 0.00 ± 0.00a 13.19 ± 0.76b 22.17 ± 1.58c 67.79 ± 3.35d
57 p-vinylanisole 1155 1156 637–69-4 134 91 134.07 MS, CR 0.00 ± 0.00a 6.65 ± 0.34b 14.17 ± 0.40c 64.95 ± 4.91d
58 borneo camphor 1146 1145 76–22-2 95 41 152.12 MS, CR 0.00 ± 0.00a 1.73 ± 0.11b 5.23 ± 0.48c 15.68 ± 0.70d
59 p-hydroquinone 1241 1283 123–31-9 110 81 110.04 MS, CR 0.00 ± 0.00a 1.43 ± 0.12b 2.67 ± 0.14c 10.28 ± 0.80d
60 trans-anethole 1281 1283 4180–23-8 148 147 148.09 MS, CR 0.00 ± 0.00a 182.37 ± 12.71b 330.10 ± 19.21c 947.02 ± 63.83d
61 d-camphor 1144 1144 464–49-3 95 81 152.12 MS, CR 0.00 ± 0.00a 1.78 ± 0.12b 5.24 ± 0.54c 16.24 ± 0.40d
62 2-ethylhexyl acetate 1144 1129 103–09-3 70 43 172.15 MS, CR 0.00 ± 0.00a 2.55 ± 0.24a 6.36 ± 1.59a 49.99 ± 9.59b
63 (E)-myroxide 1143 1141 28977–57-3 79 81 152.12 MS, CR 0.00 ± 0.00a 81.27 ± 4.47b 168.96 ± 3.29c 720.78 ± 46.07d
64 4-methylpentyl-2-methylbutyrate 1201 1143 35852–40-5 103 57 186.16 MS, CR 0.00 ± 0.00a 10.80 ± 0.66b 22.26 ± 0.51c 95.19 ± 5.84d
65 camphenone 1149 1114 55659–42-2 93 108 150.10 MS, CR 0.00 ± 0.00a 2.79 ± 0.15a 7.22 ± 1.07a 48.62 ± 7.87b
66 nerol oxide 1151 1154 1786–08-9 68 67 152.12 MS, CR 0.00 ± 0.00a 1.64 ± 0.13b 3.49 ± 0.14c 15.07 ± 0.96d
67 2-oxocineole 1217 1217 107598–08-3 82 43 168.12 MS, CR 0.00 ± 0.00a 0.90 ± 0.08a 3.74 ± 0.15b 21.85 ± 2.54c
68 trans-carveole 1219 1217 1197–07-5 109 84 152.12 MS, CR 0.00 ± 0.00a 2.45 ± 0.17ab 10.38 ± 0.13b 68.87 ± 10.15c
69 8, 9-dehydrothymol 1221 1221 18612–99-2 148 105 148.09 MS, CR 0.00 ± 0.00a 6.82 ± 0.43b 23.25 ± 1.13c 90.84 ± 4.42d
70 cumaldehyde 1236 1239 122–03-2 133 105 148.09 MS, CR 0.00 ± 0.00a 7.79 ± 0.49b 27.09 ± 1.29c 117.59 ± 8.12d
71 5-methyl-5-propylnonane – 1229 17312–75-3 71 57 184.22 MS 0.00 ± 0.00a 1.51 ± 0.07ab 6.27 ± 0.12b 40.94 ± 5.59c
72 anisole 916 921 100–66-3 108 78 108.06 MS, CR 0.00 ± 0.00a 2.65 ± 0.14b 2.03 ± 0.06b 9.56 ± 0.64c
73 benzoic aldehyde 961 960 100–52-7 77 106 106.04 MS, CR 1.78 ± 0.19a 2.26 ± 0.28a 1.03 ± 0.29a 33.67 ± 2.34b
74 albene 1167 1159 38451–64-8 95 94 162.14 MS, CR 0.00 ± 0.00a 1.77 ± 0.14b 5.16 ± 0.53c 16.01 ± 0.42d
75 β-ocimene 1037 1037 13877–91-3 93 91 136.13 MS, CR 0.00 ± 0.00a 0.16 ± 0.03a 0.14 ± 0.02a 7.38 ± 0.62b
76 durene 1108 1115 95–93-2 119 134 134.11 MS, CR 0.00 ± 0.00a 0.56 ± 0.04a 1.17 ± 0.19a 7.70 ± 1.28b
77 β-linalool 1101 1099 78–70-6 71 93 154.14 MS, CR 4.06 ± 0.33a 3.83 ± 0.03ab 4.24 ± 0.12b 5.76 ± 0.22c
78 filifolone 1108 1108 4613–37-0 80 79 150.10 MS, CR 0.00 ± 0.00a 1.71 ± 0.13a 4.01 ± 0.77a 30.03 ± 5.39b
79 2-furanacrolein 1111 1111 623–30-3 65 122 122.04 MS, CR 0.00 ± 0.00a 1.65 ± 0.05a 5.26 ± 0.59a 34.67 ± 5.92b
80 p-tolyl-acetaldehyde 1120 1120 104–09-6 105 77 134.07 MS, CR 0.00 ± 0.00a 1.48 ± 0.14ab 3.51 ± 0.40b 22.15 ± 3.42c
81 chrysanthenone 1121 1123 473–06-3 107 91 150.10 MS, CR 0.00 ± 0.00a 7.68 ± 0.58a 18.80 ± 4.07a 142.57 ± 25.63b
82 allo- neoocimene 1144 1144 3016–19-1 121 79 136.13 MS, CR 0.00 ± 0.00a 1.16 ± 0.09b 2.49 ± 0.01c 10.39 ± 0.78d
83 α-phenylacrolein 1152 1152 4432–63-7 103 77 132.06 MS, CR 0.00 ± 0.00a 10.72 ± 0.51b 22.39 ± 0.52c 95.61 ± 5.92d
84 tetralin 1155 1155 3 104 132 132.09 MS, CR 0.00 ± 0.00a 6.83 ± 0.45b 13.76 ± 0.43c 59.76 ± 3.19d
85 phellandral 1273 1276 21391–98-0 109 41 152.12 MS, CR 0.00 ± 0.00a 7.19 ± 0.28b 14.51 ± 0.91c 55.12 ± 3.25d
86 3-o-tolylpentane 1239 1240 54410–74-1 105 133 162.14 MS, CR 0.53 ± 0.02a 1.13 ± 0.08ab 1.99 ± 0.15b 10.14 ± 1.00c
87 allyl benzoate 1254 1254 583–04-0 105 77 162.07 MS, CR 0.00 ± 0.00a 9.40 ± 0.90b 22.40 ± 1.14c 94.13 ± 6.00d
88 cis-anethole 1252 1254 25679–28-1 148 147 148.09 MS, CR 0.00 ± 0.00a 11.93 ± 0.92a 28.35 ± 0.93b 132.96 ± 12.89c
89 perilla aldehyde 1276 1274 2111–75-3 68 79 150.10 MS, CR 0.00 ± 0.00a 16.95 ± 0.97b 37.37 ± 1.45c 186.45 ± 15.88d
90 5-undecanol 1376 1288 37493–70-2 69 55 172.18 MS, CR 0.00 ± 0.00a 43.46 ± 2.99b 80.38 ± 4.97c 278.38 ± 15.47d
91 2-phenylcrotonaldehyde 1274 1276 4411–89-6 117 146 146.07 MS, CR 0.00 ± 0.00a 47.55 ± 3.01b 81.40 ± 6.01c 248.65 ± 12.74d
92 6-undecanol 1281 1277 23708–56-7 83 55 172.18 MS, CR 0.00 ± 0.00a 358.67 ± 17.99b 592.02 ± 24.48c 1822.92 ± 151.10 d
93 2-hexylpyridine – 1284 1129–69-7 93 106 163.14 MS 0.00 ± 0.00a 146.21 ± 7.04b 258.97 ± 17.84c 806.51 ± 35.95d
94 terephthaladehyde 1166 1284 623–27-8 134 133 134.04 MS, CR 0.00 ± 0.00a 19.52 ± 0.86b 35.74 ± 2.48c 104.11 ± 5.71d
95 camphoroquinone – 1319 10373–78-1 95 69 166.10 MS 0.00 ± 0.00a 0.20 ± 0.02a 11.37 ± 0.13b 30.11 ± 5.91c
96 isobutyl benzoate 1331 1321 120–50-3 105 123 178.10 MS, CR 0.00 ± 0.00a 0.24 ± 0.02a 6.84 ± 0.19b 16.85 ± 3.06c
97 nerolic acid 1347 1344 4613–38-1 69 41 168.12 MS, CR 0.00 ± 0.00a 0.00 ± 0.00a 0.00 ± 0.00a 23.31 ± 5.60b
98 (E, Z)-3,6-nonadienol 1156 1156 56805–23-3 67 93 140.12 MS, CR 0.00 ± 0.00a 10.31 ± 0.67b 21.41 ± 0.44c 88.58 ± 4.98d
99 eremophilene 1486 1494 10219–75-7 107 161 204.19 MS, CR 8.72 ± 0.24a 9.74 ± 0.92a 10.95 ± 1.17a 19.62 ± 5.43b
100 guaiacol 1090 1089 90–05-1 109 124 124.05 MS, CR 0.00 ± 0.00a 13.04 ± 0.64b 20.66 ± 2.82c 82.97 ± 1.54d
101 dipropyl disulfide 1098 1107 629–19-6 150 108 150.05 MS, CR 0.00 ± 0.00a 7.55 ± 0.62a 18.72 ± 4.33a 151.14 ± 29.10b
102 furfuryl methyl disulfide 1226 1226 57500–00-2 81 53 160.00 MS, CR 0.00 ± 0.00a 3.00 ± 0.20a 11.47 ± 0.40b 65.91 ± 7.94c
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Extraction of volatile components

The extraction method was referred to the study of Hou, Liang and Wang (2020) on volatile compounds of navel orange and modified. The stipe samples of the four developmental stages taken out from the refrigerator at −80 °C was immediately placed in liquid nitrogen and ground into powder. Approximately 500 mg of powder sample was extracted by 2 mL of saturated sodium chloride solution with 10 µL of [3,4,5,6-2H4]-Methyl 2-hydroxybenzoate (50 µg/mL) as internal standard were added. Subsequently, the volatile compounds from the stipe of Phallus impudicus were extracted using the Headspace-Solid Phase Microextraction (HS-SPME), i.e., the HS vial with mixed liquor was shaken at 60 °C for 5 min, then extraction was conducted using a 120 µm DVB/CWR/PDMS fiber at the same temperature for 15 min.

GC–MS analysis

The volatile compounds were separated on a DB-5MS column (30 m × 0.25 mm × 0.25 μm film thickness; Agilent J&W Scientific, Folsom, CA, USA) at splitless mode installed on an Agilent 8890 gas chromatograph equipped with a Agilent 7000D mass spectrometer (Santa Clara, CA, USA). The GC–MS system was controlled and operated using an Agilent Mass-hunter. Helium (99.999 %) was selected as the carrier gas at a linear velocity of 1.2 mL/min. The temperatures of 250 °C were set for the injector. To ensure the complete desorption of volatile components, the SPME fiber need to be inserted into the heated GC injector after sampling and maintained at 250 °C for 5 min. The temperature program of column was set as follows: first, the initial column temperature was maintained at 40 °C for 3.5 min, followed by a ramp of 10 °C/min to 100 °C, then a ramp of 7 °C/min to 180 °C, finally increased to 280 °C at a rate of 25 °C/min, and held at 280 °C for 5 min. For MS, selected ion monitoring (SIM) mode was used for the identification and quantification of analytes. The ionization voltage was 70 eV, and the temperatures of ion source, quadrupole mass detector and transfer line were 230, 150 and 280 °C, respectively. The total ionic chromatogram (TIC) with m/z range of 50–450 was obtained (Supplementary Fig. 1).

Identification and quantification of volatile components

In this study, Agilent MassHunter software was used for the initial processing and analysis of raw mass spectrometry data. Automated mass spectral deconvolution and identification system (AMDIS) software was used to achieve chromatographic peak deconvolution (Huang et al., 2022). Volatile compounds in the stipe of Phallus impudicus during the growth period were identified by comparing retention index (RI) and mass spectra with reference standards, literatures or NIST Chemistry WebBook (https://webbook.nist.gov/chemistry and NIST 2020). Of them, the literature RI values were obtained from the NIST database. In addition, for the mass spectrum of the sample after deducting the background, if the retention time detected was close to the standard reference, it was determined to be the substance (Yuan et al., 2022). The relevant indicators for the identification of each identified compound were shown in Table 1. The [3,4,5,6-2H4]-Methyl 2-hydroxybenzoate was used as an internal standard for semi-quantitative analysis of the identified volatile compounds. Assuming that C, Cis, Ac and Ais represent the relative content of analyte, the final content of internal standard in sample, the peak area of analyte and the peak area of internal standard, respectively, the relative content of analyte C can be calculated according to the formula below: C = (Ac / Ais) × Cis (Shen et al., 2023). The relative contents of volatile compounds were expressed as µg/mL, and three biological replicates were conducted for all samples.

Statistical analysis

All data were analyzed statistically using IBM SPSS Statistics 22.0, and graphic production was conducted using GraphPad Prism 7 and Photoshop 6.0. Principal component analysis (PCA) was completed with the help of R Software (R i386 ver. 3.3.3). The relative quantitative values were presented as mean ± standard deviation of three biological replicates. Duncan's multiple comparisons were used to analyze the spatiotemporal dynamic changes of volatile compounds in the stipe of Phallus impudicus during different growth stages. The OPLS-DA was carried out according to the reference of Thévenot et al. (2015). Metabolites satisfying the criteria for both variable importance in projection (VIP) > 1 and P value < 0.05 that obtained by the method of OPLS-DA and PLS-DA were differential metabolites. Correlation heatmap with signs was constructed with the R software package (R version 3.6.3), and the relationship between different developmental stages and the different volatile compounds were proved by Pearson correlation coefficient. P < 0.05 was recognized as statistical significance.

Result and discussion

Identification and quantitative descriptive analysis of volatile compounds

Regarding the Gómez et al. (2022) and Tagkouli et al. (2021) for the method of determining edible fungi, volatile compounds in the stipe of Phallus impudicus at four different developmental stages were measured by headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry (HS-SPME-GC–MS). The identification information of all the volatile compounds was summarized in Table 1, 102 metabolites were identified successfully based on the MS information and RI. Obviously, the identified compounds in samples showed the same change tendency during the whole developmental period, that was, the metabolites accumulated continuously over time. For most of the volatile compounds found in the stipe of Phallus impudicus, there were significant differences in the relative content of the four different developmental stages, especially for the latter three stages. The volatile compounds with the highest relative content were 2-cyano-2-ethyl-butyramide and 6-undecanol, followed by α-terpinen-7-al, 2, 4-decadienol and methyl geranate, from shell breaking stage to mature stage, ranging from 434.70 to 6154.87, 358.67–1822.92, 166.88–1217.01, 127.52–1216.42 and 6.86–956.79, respectively. Of them, the 2-cyano-2-ethyl-butyramide had not been reported in other edible fungi, which might be the characteristic volatile component of Phallus impudicus. In addition, trans-anethole, p-acetylethylbenzene, 2-hexylpyridine, (E)-myroxide, (E, E)-2,4-decadienal, verbenone, (E)-6-nonenal, citronellal, 4, 8-dimethyl-1, 3, 7-nonadiene, α-cyclocitral, butylbenzene, isopropyl benzoate, chrysanthenone, cis-anethole, perilla aldehyde, 5-undecanol and 2-phenylcrotonaldehyde with relative content range of 1.27–947.02 were also key contributors to the volatile composition and flavor formation of Phallus impudicus. The lowest relative volatile component content observed in the stipe of Phallus impudicus at the latter three stages was β-linalool and γ-muurolene, followed by β-ocimene, durene, 3-ethyl-3-methyldecane, anisole and p-hydroxyacetophenone, ranging from 3.83 to 5.76, 3.99–6.99, 0.16–7.38, 0.56–7.70, 0.39–9.47, 2.65–9.56 and 0.14–9.60, respectively. According to the semi-quantitative results obtained, except for a small amount of accumulation of 14 metabolites (eremophilene, 3-o-tolylpentane, β-linalool, benzoic aldehyde, phenol, α-caryophyllene,α-zingiberene, 4-pentenyl propionate, (E)-carvone, γ-muurolene, α-muurolene, o-xylorcinol, geranylacetone and α-2-propenyl-benzenmethanol) at the budding stage, the remaining 88 metabolites were not detected at this stage, which indicated that the production, accumulation and release of volatile compounds mainly occurred after the shell was broken by the thallus of mushroom. The dimethyl oligosulfides (including dimethyl disulfide, dimethyl trisulfide) were the main reason for the special flavor of ripe body (Gupta, Jayaprakash & Shinde, 2016; Pudil, Uvira & Janda, 2014). It is worth mentioning that the sulfide did not form at ZP stage in this study, and the sulfide increased significantly until the mature stage of PIII, which was consistent with the characterization results of Pudil, Uvira and Janda (2014) in identified sulfide from the Phallus impudicus L. Ex Pers at mature stage. Taken together, these findings indicated that adequate growth can improve the overall content of volatile compounds in the stipe of Phallus impudicus, which largely determined the quality and nutritional value of this regional characteristic edible fungus. Furthermore, the types and concentrations of volatile compounds in the edible mushroom of Phallus impudicus were mainly dependent on the growth stage, which was consistent with the research results of Cho, Seo and Kim (2003) and Feng et al. (2021).

Analysis profiles of volatile compounds

Existing studies have shown that 3 % of volatile compounds had odor activity, which had the greatest impact on the overall aroma or flavor of food (Dunkel et al., 2014). Phallus impudicus had a special odor and unique flavor, which was related to the complex mixture of compounds belonging to the different chemical categories. In this study, 102 volatile compounds were identified from the stipe of Phallus impudicus by SPME-GC–MS, which has been described in section 3.1. The data thus obtained were subjected to further analysis. Fig. 2A showed that 13 of the 102 volatile compounds were common in samples at four developmental stages. According to their different types, the identified 102 volatile compounds can be divided into nitrogen compounds, ether, hydrocarbons, phenol, heterocyclic compounds, ketone, ester, aromatics, aldehyde, terpenoids, alcohol and amine. Among them, amine, alcohol, aldehyde and terpenoids were the main components of aroma, and the total content of those four compounds accounted for about 70.47 % of the total volatile compounds at PIII stage (Fig. 2B). To further analyze the effect of growth stage on the aroma of Phallus impudicus fruit-body, multivariate statistical analysis was performed on 102 volatile compounds obtained qualitatively and semi-quantitatively, as shown in Fig. 2. In view of the complexity of the data, principal component analysis (PCA) was used to display the distribution and variation of data points visually and intuitively (Granato, Santos, Escher, Ferreira & Maggio, 2018). It can be clearly seen from Fig. 2C that the volatile compounds changed significantly during the whole growth process. The PCA score plot (13 samples, 102 volatile compounds) indicated that the Phallus impudicus at different growth stages can be well separated by the first two principal components, and the first two components could account for 97.52 % of the total variability, of which PC1 explained 95.49 % and PC2 explained 2.07 % (Fig. 2C). In addition, the samples can be intuitively divided into different groups or clusters by hierarchical cluster analysis (HCA). As shown in Fig. 2D, a total of 13 samples from four stages were classified into three categories by hierarchical cluster analysis, among which ZP and PI were one category, PII and PIII were one category respectively. Based on the results of PCA and HCA, it was speculated that the Phallus impudicus underwent a dramatic change in aroma quality at the rapid growth stage (PII) and mature stage (PIII).

OPLS-DA results

OPLS-DA can be used to filter out the orthogonal variables that are not related to the categorical variables in the metabolites, and the analysis of non-orthogonal variables and orthogonal variables can be carried out without interference to each other, so as to obtain the inter-group differences of metabolites with high reliability and the correlation degree information of experimental groups (Bao, Mu & Wang, 2023). The Fig. 3A showed the OPLS-DA score diagram of the four different developmental stages of Phallus impudicus. As shown in Fig. 3A, the 12 samples were all within the confidence intervals, and the four stages of samples were well distinguished, and the differences between the groups were significant. The above information indicated that the growth stage had a significant effect on the volatile metabolites of Phallus impudicus. In addition, there was no overlap between the samples, and the separation degree was high. The clustering of samples in the budding stage, the shell breaking stage and the rapid growth stage was strong, but the clustering of samples at the mature stage was poor. This might be because although the volatile components of these samples at mature stage were highly similar, the degree of accumulation varied greatly, and the influence of internal and external factors on different growth stages was different. The permutation test results of the OPLS-DA model were presented in Fig. 3B, and each group of models had two principal components (PCs). The cumulative values of R2X, R2Y and Q2 were equal to 0.985, 0.994 and 0.96, respectively. The S-plot of OPLS-DA presented multiple metabolites as shown Fig. 3C. Obviously, the permutation test results demonstrated that the OPLS-DA model was realistic and reliable, and there was no over-fitting phenomenon.

Fig. 3.

Fig. 3

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The results of OPLS-DA. OPLS-DA, orthogonal partial least squares-discriminant analysis; PCs, principal components. (A) indicated the scores of OPLS-DA plot; (B) meant the model validation diagram of OPLS-DA; (C) indicated the S-plot of OPLS-DA.

Identification of differential metabolites

In this study, the statistical method PLS-DA was used for supervised discriminant analysis. The VIP value was obtained to evaluate the strength and explanatory power of the expression pattern of each metabolite on the categorical discrimination of each group of samples, so as to effectively screen for biologically significant differential metabolites, also known as marker metabolites (Li, Zuo & Wang, 2022). The greater the VIP value of the metabolite, the greater the decisive effect on the sample discrimination. The VIP values of the first two principal components obtained by OPLS-DA model were applied to the screening of marker metabolites. As shown in Table S1 and Fig. 4, the top 50 differential metabolites with the highest VIP value were screened out from the four different developmental stages based on VIP > 1 and P < 0.05, which mainly included alcohol, aldehyde, ether, ketone, phenol, and other secondary metabolites. This result was agreed with Feng et al. (2021) that the differential volatile metabolites in edible fungi of Agaricus bisporus at growth stages were mainly composed of alcohols, aldehydes, ketones, etc. Specifically, the 50 differential metabolites screened included 1 amine (2-cyano-2-ethyl-butyramide), 7 alcohols (6-undecanol, 5-undecanol, 2, 4-decadienol, (E, Z)-3,6-nonadienol, (Z)-3-nonen-1-ol, (3E)-3-nonen-1-ol and decanol), 8 aromatics (trans-anethole, anisole, α-phenylacrolein, tetralin, p-vinylanisole, o-methylnitrobenzene, pentamethylbenzene and veratrol), 4 phenols (guaiacol, o-sec-butylphenol, p-hydroquinone and 8, 9-dehydrothymol), 1 ether (cis-anethole), 8 aldehydes (2-phenylcrotonaldehyde, α-terpinen-7-al, terephthaladehyde, perilla aldehyde, 7-methyl-3-methyleneoct-6-enal, cinnamaldehyde, (E)-6-nonenal and α-cyclocitral), 12 terpenoids ((E)-myroxide, citronellal, phellandral, (+)-trans-limonene oxide, 4, 8-dimethyl-1, 3, 7-nonadiene, verbenone, d-camphor, borneo camphor, cumaldehyde, nerol oxide, linalyl acetate and allo-neoocimene), 1 hydrocarbon (albene), 2 ketones (p-acetylethylbenzene and piperitone oxide), 1 heterocyclic compound (2-hexylpyridine) and 5 esters (dihydromethyl cinnamate, 4-methylpentyl-2-methylbutyrate, allyl benzoate, isopropyl benzoate and 4-pentenyl propionate). According to the synthesis pathway of precursors, most of the above volatiles belonged to the category of isoprenoid-, amino acid- and fatty acid-derived volatile compounds, which were similar to the composition of volatile substances in plants (Dombrowski et al., 2019, Mostafa et al., 2022, Shen et al., 2023).

Fig. 4.

Fig. 4

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The top 50 volatile metabolites of Phallus impudicus with the highest VIP value at different developmental stages obtain by the PLS-DA method. VIP, variable importance in projection; PLS-DA, partial least squares-discriminant analysis. Both the value of VIP > 1 and the P < 0.05 was considered as a significant difference.

Correlation analysis of different stages and differential metabolites

In order to intuitively represent the correlation between different developmental stages and the change patterns of 50 differential metabolites at developmental stages, heatmap analysis was used in this study, and the results were shown in Fig. 5. From the Fig. 5A, it showed that the correlation coefficients of the latter three stages were all greater than 0.5, while the correlation between the first stage and the latter three stages was not strong. Obviously, the shell breaking of Phallus impudicus fruiting bodies was the promoter for the synthesis and accumulation of volatile compounds. It was worth noting that the contents of 50 volatile compounds all showed a significant upward trend throughout the growth period, and the maximum accumulation was all obtained at the maturity stage, except for 4-pentenyl propionate (the highest value at rapid growth stage) (Fig. 5B). In other words, among the 50 kinds of representative differential metabolites, a large amount of volatile compounds were absent or extremely low in all samples (the blue region of circus-heatmap, Fig. 5B), which demonstrated that the growth stages affected the synthesis and accumulation of volatile compounds. The concentration of key aroma compounds was the highest at mature stage and the lowest at the beginning of growth, which was contrary to the results of Feng et al. (2021) on the volatile profiles of Agaricus bisporus at different growth stages. Furthermore, the studies had identified 11 key aroma compounds in button mushroom, such as 2-octenal, 1-octen-3-one, (E)-2-octen-1-ol, etc., which were completely different from the main aroma compounds identified in this study (Feng et al., 2021, Sun et al., 2020). The inconsistency of the results might be due to the different types of edible fungi or the different separation and determination methods of volatile compounds, but it also once again proved the uniqueness of the flavor of Phallus impudicus. Nevertheless, the conclusion that the change of key aroma mainly depended on the growth stage in this study was the same with the Agaricus bisporus (Feng et al., 2021), which also showed the importance of growth stage for the flavor formation in edible fungi.

Fig. 5.

Fig. 5

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The correlation analysis based on the top 50 volatile metabolites of Phallus impudicus with the highest VIP value. (A) indicated the correlation heatmap among the different development stage; (B) meant the circus-heatmap among the top 50 volatile metabolites of Phallus impudicus with the highest VIP value.

In order to further understand how the 50 volatile compounds with the highest VIP obtained by PLS-DA were coordinated during the development of Phallus impudicus, a correlation heatmap was constructed to investigate the potential relationships between these stage-dependent differential metabolites. Interestingly, as shown in Supplementary Fig. 2, except for 4-pentenyl propionate, the other 49 volatile compounds, including 1 amine, 7 alcohols, 8 aromatics, 4 phenols, 1 ether, 8 aldehydes, 12 terpenoids, 5 esters, 1 hydrocarbon, 2 ketones and 1 heterocyclic compound, were strongly correlated with each other, and the correlations between these metabolites tended to be significantly positive. There was no significant correlation between 4-pentenyl propionate and the other 49 differential metabolites, which corresponded to the different stage-dependent distribution characteristics of this compound compared to other compounds (as shown in Fig. 5B). In addition, among the top 5 compounds with relatively high content (Table 1), only 6-undecanol, α-terpinen-7-al, 2, 4-decadienol and 2-cyano-2-ethyl-butyramide with high VIP values were screened as differential metabolites (Fig. 5B), which indicated that the four volatile compounds above might mainly contribute the flavor formation. The above information indicated that volatile compounds (mainly 6-undecanol, α-terpinen-7-al, 2, 4-decadienol and 2-cyano-2-ethyl-butyramide) might regulated the flavor formation of fruiting bodies in Phallus impudicus during the growth stage through the synergistic interaction with other volatiles. Moreover, the above results further confirmed that volatile compounds, a variety of secondary metabolites, were the main contributors to the unique flavor of edible fungi (Sun et al., 2022).

Conclusions

A total of 102 volatile compounds were identified from the fruiting bodies of Phallus impudicus after shell breaking. According to PC1 and PC2 in the PCA plot, they accounted for 95.49 % and 2.07 % of the total variance of volatile compounds, respectively. The volatile compounds in the stipes of Phallus impudicus at growth stages could be separated and exhibited significant differences. The differential volatile metabolites were obtained by the method of OPLS-DA and PLS-DA, among which the top 50 metabolites with the largest VIP value was clearly distinguished at the four different growth stages, especially from the rapid growth stage to the mature stage, where almost all metabolites had the highest content at the mature stage. The Changes in volatile compounds were significantly dependent on the growth stage and increased with the growth stage. It was worth noting that the shell breaking of the fruiting body was the critical turning point for the synthesis and accumulation of volatile compounds. In addition, volatile compounds, mainly containing 6-undecyl alcohol, α-terpine-7-al, 2, 4-decenol, and 2-cyano-2-ethyl-butanamide, might co-regulate flavor formation of Phallus impudicus during growth stage through the synergistic action of other chemical components.

CRediT authorship contribution statement

Huijuan Liu, literature collection, manuscript written-review, editing and supervision; Zhifei Cheng, sample collection, language check and manuscript supervision; Jiao Xie, sample collection and carried out the experiment, had fund acquisition and manuscript revise and supervision.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research was supported by Guizhou Provincial Science and Technology Projects (ZK [2022] 365 and ZK [2022] 391); High-level talents start-up fund project of Guizhou Medical University ([2021] 007).

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.fochx.2024.101288.

Appendix A. Supplementary data

The following are the Supplementary data to this article:

Supplementary data 1
mmc1.docx (1.7MB, docx)

Data availability

Data will be made available on request.

References

  1. Aisala H., Sola J., Hopia A., Linderborg K.M., Sandell M. Odor-contributing volatile compounds of wild edible nordic mushrooms analyzed with HS-SPME-GC-MS and HS-SPME-GC-O/FID. Food Chemistry. 2019;283:566–578. doi: 10.1016/j.foodchem.2019.01.053. [DOI] [PubMed] [Google Scholar]
  2. Bao G.F., Mu L.Q., Wang Y. Effect of different accumulative temperate zones in Heilongjiang on glycine soja metabolites as analyzed by non-target metabolomics. Molecules. 2023;28(8):3296. doi: 10.3390/molecules28083296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cao L.P., Zhang Q., Miao R.Y., Lin J.B., Feng R.C., Ni Y.Q., Zhao X. Application of omics technology in the research on edible fungi. Current Research in Food Science. 2023;6 doi: 10.1016/j.crfs.2022.100430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cho D.B., Seo H.Y., Kim K.S. Analysis of the volatile flavor compounds produced during the growth stages of the shiitake mushrooms (lentinus edodes) Journal of Food Science & Nutrition. 2003;8(4):306–314. [Google Scholar]
  5. Dickschat J.S., Celik E., Brock N. Volatiles from three genome sequenced fungi from the genus Aspergillus. Beilstein Journal of Organic Chemistry. 2018;14:900–910. doi: 10.3762/bjoc.14.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dombrowski J.E., Kronmiller B.A., Hollenbeck V.G., Rhodes A.C., Henning J.A., Martin R.C. Transcriptome analysis of the model grass Lolium temulentum exposed to green leaf volatiles. BMC Plant Biology. 2019;19:222. doi: 10.1186/s12870-019-1799-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dunkel A., Steinhaus M., Kotthoff M., Nowak B., Krautwurst D., Schieberle P., Schieberle T. Nature' s chemical signatures in human olfaction: A foodborne perspective for future biotechnology. An gewandte Chemie International Edition. 2014;53(28):7124–7143. doi: 10.1002/anie.201309508. [DOI] [PubMed] [Google Scholar]
  8. Feng T., Yang M.Y., Ma B., Zhao Y., Zhuang H.N., Zhang J.S., Chen D. Volatile profiles of two genotype Agaricus bisporus species at different growth stages. Food Research International. 2021;140 doi: 10.1016/j.foodres.2020.109761. [DOI] [PubMed] [Google Scholar]
  9. Gómez I., Laveg González R., Tejedor-Calvo E., Pérez Clavijo M., Carrasco J. Odor profile of four cultivated and freeze-dried edible mushrooms by using sensory panel, electronic nose and GC-MS. Journal of Fungi. 2022;8(9):953. doi: 10.3390/jof8090953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Granato D., Santos J.S., Escher G.B., Ferreira B.L., Maggio R.M. Use of principal component analysis (PCA) and hierarchical cluster analysis (HCA) for multivariate association between bioactive compounds and functional properties in foods: A critical perspective. Trends in Food Science & Technology. 2018;72:83–90. [Google Scholar]
  11. Grosshauser S., Schieberle P. Characterization of the key odorants in panfried white mushrooms (Agaricus bisporus L.) by means of molecular sensory science: Comparison with the raw mushroom tissue. Journal of Agricultural and Food Chemistry. 2013;61(16):3804–3813. doi: 10.1021/jf4006752. [DOI] [PubMed] [Google Scholar]
  12. Gupta A., Jayaprakash, Shinde B. Immunopharmacological activity of medicinal plants against Aristolochia bracteolate and Phallus impudicus. Journal of Biomedical and Pharmaceutical Research. 2016;5(5):9–15. [Google Scholar]
  13. Hosaka K., Bates S.T., Beever R.E., Castellano M.A., Colgan-III W., Domínguez L.S., Trappe J.M. Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass phallomycetidae and two new orders. Mycologia. 2006;98(6):949–959. doi: 10.3852/mycologia.98.6.949. [DOI] [PubMed] [Google Scholar]
  14. Hou J.X., Liang L., Wang Y.X. Volatile composition changes in navel orange at different growth stages by HS-SPM-GC-MS. Food Research International. 2020;136 doi: 10.1016/j.foodres.2020.109333. [DOI] [PubMed] [Google Scholar]
  15. Huang W.J., Fang S.M., Wang J., Zhou C., Luo Y.H., Yu Y.L., Ning J.M. Sensomics analysis of the effect of the withering method on the aroma components of Keemun black tea. Food Chemisty. 2022;395 doi: 10.1016/j.foodchem.2022.133549. [DOI] [PubMed] [Google Scholar]
  16. Khan A.R., Fiaz M., Khan R.A., Wahab Z., Khan J.B., Khan I., Jan-Khan M.W. Anti-oxidant and hypoglyceamic potential of phallus impudicus (l. ex pers) (stink horn) mushroom in alloxan induced diabetic rats. Journal of Critical Reviews. 2020;7(18):4180–4185. [Google Scholar]
  17. Kuznecova G., Jegina K., Kuznecovs S., Kuznecovs I. P151 Phallus impudicus in thromboprophlyaxis in breast cancer patients undergoing chemotherapy and hormonal treatment. The Breast. 2007;16:S56. [Google Scholar]
  18. Li W., Li R., Chen W.C., Feng J., Wu D., Zhang Z., Yang Y. The anabolism of sulphur aroma volatiles responds to enzymatic and non-enzymatic reactions during the drying process of shiitake mushrooms. Food Chemistry. 2022;371 doi: 10.1016/j.foodchem.2021.131123. [DOI] [PubMed] [Google Scholar]
  19. Li L., Zuo Z.T., Wang Y.Z. Practical qualitative evaluation and screening of potential biomarkers for different parts of Wolfiporia cocos using machine learning and network pharmacology. Frontiers in Microbiology. 2022;13 doi: 10.3389/fmicb.2022.931967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mostafa S., Wang Y., Zeng W., Jin B. Floral scents and fruit aromas: Functions, compositions, Biosynthesis, and regulation. Frontiers in Plant Science. 2022;13 doi: 10.3389/fpls.2022.860157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pudil F., Uvira R., Janda V. Volatile compounds in stinkhorn (phallus impudicus l. Ex pers.) at different stages of growth. European Scientific Journal. 2014;10(9):163–171. [Google Scholar]
  22. Shen S.S., Wu H.T., Li T.H., Sun H.R., Wang Y.J., Niang J.M. Formation of aroma characteristics driven by volatile components during long-term storage of an tea. Food Chemistry. 2023;411 doi: 10.1016/j.foodchem.2023.135487. [DOI] [PubMed] [Google Scholar]
  23. Shou, K.X. (2020). Constituents analysis, activity evaluation of Phallus Impudicus L. and purification, structural properties of its polysaccharides. Master Thesis, Guizhou Medical University, the China. 4-5pp, pp. 12.
  24. Sun L.B., Zhang Z.Y., Xin G., Sun B.X., Xu H.R. Advances in umami taste and aroma of edible mushrooms. Trends in Food Science & Technology. 2020;96:176–187. [Google Scholar]
  25. Sun T., Jiang H., Yang K., Li X.K., Wang S.Y., Yao H.Y., Sun D.F. Nutritional function and flavor evaluation of a new soybean beverage based on Naematelia aurantialba fermentation. Foods. 2022;11(3):272. doi: 10.3390/foods11030272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tagkouli D., Bekiaris G., Pantazi S., Anastasopoulou M.E., Koutrotsios G., Mallouchos A., Kalogeropoulos N. Volatile profiling of Pleurotus eryngii and Pleurotus ostreatus mushrooms cultivated on agricultural and agro-industrial by-products. Foods. 2021;10(6):1287. doi: 10.3390/foods10061287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Thévenot E.A., Roux A., Xu Y., Ezan E., Christophe J. Analysis of the human adult urinary metabolome variations with age, body mass index, and gender by implementing a comprehensive workflow for univariate and OPLS statistical analyses. Journal of Proteome Research. 2015;14(8):3322–3335. doi: 10.1021/acs.jproteome.5b00354. [DOI] [PubMed] [Google Scholar]
  28. Tietel Z., Masaphy S. True morels (morchella)-nutritional and phytochemical composition, health benefits and flavor: A review. Critical Reviews in Food Science and Nutrition. 2018;58(11):1888–1901. doi: 10.1080/10408398.2017.1285269. [DOI] [PubMed] [Google Scholar]
  29. Vyacheslav B., Alexey B., Aliaksandr A., Valentina M., Tatyana P., Aliaksandar K., Mikolaj T. Polysaccharides of mushroom Phallus impudicus mycelium: Immunomodulating and wound healing properties. Modern Food Science and Technology. 2019;35(9):30–37. [Google Scholar]
  30. Xie J., Cao Q., Wang W.J., Zhang H.Y., Deng B. Understanding changes in volatile compounds and fatty acids of Jincheng orange peel oil at different growth stages using GC-MS. Journal of Integrative Agriculture. 2023;22(7):2282–2294. [Google Scholar]
  31. Yao F., Gao H., Yin C.M., Shi D.F., Fan X.Z. Effect of different cooking methods on the bioactive components, color, texture, microstructure, and volatiles of Shiitake Mushrooms. Foods. 2023;12(13):2573. doi: 10.3390/foods12132573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yuan H., Cao G., Hou X., Huang M., Du P., Tan T., Luo J. Development of a widely targeted volatilomics method for profiling volatilomes in plants. Molecular Plant. 2022;15(1):189–202. doi: 10.1016/j.molp.2021.09.003. [DOI] [PubMed] [Google Scholar]
  33. Zhang S. Study on the antimicrobial preservative effect of Dictyophora echinovlvata and Phallus impudicus. Master Thesis, Zhejiang Agriculture & Forestry University, the China. 2015;3:pp. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary data 1
mmc1.docx (1.7MB, docx)

Data Availability Statement

Data will be made available on request.

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