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Review

Review of the Structural Characteristics and Biological Activities of Tricholoma Secondary Metabolites (2018–2023)

by
Meili Zhao
1,
Shiqin Yuan
1,
Zhiming Li
1,
Chengwei Liu
1,* and
Ruiying Zhang
2,*
1
Key Laboratory for Enzyme and Enzyme-Like Material Engineering of Heilongjiang, College of Life Science, Northeast Forestry University, Harbin 150040, China
2
State Key Laboratory of Efficient Utilization of Arid and Semi-Arid Arable Land in Northern China, The Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China
*
Authors to whom correspondence should be addressed.
Molecules 2024, 29(19), 4719; https://doi.org/10.3390/molecules29194719
Submission received: 6 September 2024 / Revised: 3 October 2024 / Accepted: 3 October 2024 / Published: 5 October 2024
(This article belongs to the Special Issue Bioelements and Bioactive Metabolites of Natural Origin—Health-Promoting Applications—Volume II)
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Abstract

:
Tricholoma are significant medicinal and edible mushrooms within Basidiomycota. Known for their various medicinal properties such as anti-tumor, immune regulation, and antioxidant effects, they are regarded worldwide as health foods of the 21st century. Tricholoma species produce various types of secondary metabolites, which have been extensively studied by the scientific community. In 2018, Clericuzio et al. summarized the structures, biosynthesis, and biological activities of over one hundred different secondary metabolites isolated from the fruiting bodies of 25 Tricholoma species. Building on this, the present article reviews the research progress on Tricholoma secondary metabolites from 2018 to 2023, identifying a total of 101 compounds, 46 of which were newly discovered. These secondary metabolites include a wide range of chemical categories such as terpenoids, steroids, and alkaloids, demonstrating broad biological activities. This article aims to provide in-depth scientific insights and guidance for researchers in this field by summarizing the chemical and biological properties of these secondary metabolites, promoting further applications and development of Tricholoma fungi in the pharmaceutical and food industries.

1. Introduction

In recent years, with the increasing demand for health and nutrition, more and more mushrooms have gained attention in the food and medical fields. Tricholoma, an ancient and important edible mushroom, has been used as a medicinal material by humans since ancient times. Tricholoma is a fungus classified under the Basidiomycota class, the Tricholomataceae family, and the Tricholoma genus. It is particularly notable for its abundance of secondary metabolites, including polysaccharides, alkaloids, and phenolic compounds [1,2]. These secondary metabolites not only confer unique biological activities to Tricholoma, but also exhibit broad application potential. For example, Tricholoma polysaccharides have been found to possess whitening effects [3], Tricholoma peptides show immunomodulatory activity [4], and Tricholoma sterols demonstrate good anti-acetylcholinesterase (AchE) activity [5]. Although the secondary metabolites of Tricholoma have attracted widespread attention, research is still at a stage that requires further investigation. As the understanding of Tricholoma secondary metabolites continues to grow, the potential of these metabolites within an important medicinal and edible fungus will be better explored and utilized.
Tricholoma contains a rich array of metabolites, sparking extensive exploration by scientists. In 1968, German scientists first discovered that Tricholoma species produce an unpleasant odor. Using thin-layer chromatography, they preliminarily isolated and identified indole as the main component responsible for the bitter smell in Tricholoma fruiting bodies [2]. With advances in research techniques and methods, more secondary metabolites from Tricholoma have been discovered. In 2018, Italian scientist Clericuzio and colleagues summarized 112 secondary metabolites isolated from Tricholoma fruiting bodies (excluding mycelium) [1]. Since then, a large number of secondary metabolites have continued to be discovered in Tricholoma. Based on this, the present review summarizes the secondary metabolites of Tricholoma identified between 2018 and 2023, that is, a total of 101 compounds discovered, including 46 novel compounds. This article provides a comprehensive summary of the isolation, structural characteristics, and biological activities of these chemical substances. Table 1 lists the secondary metabolites found in Tricholoma from 2018 to 2023 and their biological activities.

2. Secondary Metabolites of Tricholoma

2.1. Terpenoids

Terpenoids are the largest and most structurally diverse class of natural products among secondary metabolites [6]. These compounds are based on isoprene units (C5 units) as their fundamental building blocks, resulting in rich structural diversity and widespread distribution. In the past five years, 73 terpenoid compounds have been identified from the genus Tricholoma, including triterpenes, diterpenes, and, less commonly, sesquiterpenes and C17 compounds. It is noteworthy that while sesquiterpenes are quite common in other species, they are rarely reported in Tricholoma. This suggests that Tricholoma may have unique evolutionary strategies in its secondary metabolic pathways.

2.1.1. Triterpenes and Sterols

Triterpenes are a class of secondary metabolites widely found in nature, typically derived from the acyclic precursor squalene [7]. Fungi are significant sources of triterpenes and steroid compounds. These compounds not only possess diverse pharmacological activities but are also crucial for new drug discovery. In the past five years, a total of 64 steroid or triterpene compounds have been identified from Tricholoma.
Lanostanes are a class of tetracyclic triterpenes with a core structure consisting of 30 carbon atoms. In this structure, the methyl group at C(13) is in the β-configuration, while the methyl group at C(14) is in the α-configuration, and the C(17) position is connected to a β-configured side chain [8]. Lanosterol is one of the most representative compounds among lanostanes, playing a critical role in triterpene biosynthesis as an important intermediate for the synthesis of sterol compounds such as ergosterol and stigmasterol. Ergosterol is a crucial component of the cell membranes of most fungi and serves as a precursor for vitamin D2 [9], playing an essential role in maintaining fungal life activities. Stigmasterol has cholesterol-lowering, antioxidant, and potential anti-cancer properties [10].
Zhang et al. [11] isolated eight novel lanostane-type triterpenes, named pardinols A–H (1–8), along with a known compound saponaceol B (9) from the fruiting bodies of the fungus T. pardinum. These compounds have a characteristic lanostane triterpene skeleton, and the A-ring contains a 3-hydroxy-3-methylglutaryl (HMG) group [12]. This structural feature is uncommon among triterpenes in other species. The authors elucidated the structures of these compounds through extensive spectroscopic analyses, including nuclear magnetic resonance (NMR) and mass spectrometry (MS), and applied alkaline methanolysis to reveal further structural details. The final structural and stereochemical configurations were successfully established using time-dependent density functional theory (TDDFT) and electronic circular dichroism (ECD) calculations, completing comprehensive structural identification [11]. Gozzini et al. [13] isolated three lanostane triterpenes from the ethyl acetate extract of T. saponaceum fruiting bodies, including a newly discovered compound, saponaceol D (10), and two previously reported compounds from T. pardinum, pardinol B (2) and pardinol D (4). The structures of these compounds were determined through spectrometric analysis [11,13]. Gilardoni et al. isolated three compounds, tricholidic acids B (11), C (12), and tricholidic acid (13) from the ethyl acetate extract of T. ustaloides fruiting bodies collected from Italian beech wood. Compounds 11 and 12 were identified for the first time [14]. Zhang et al. isolated three lanostane triterpenes (14–16) from the fruiting bodies of T. imbricatum, including two novel compounds, tricholimbrins A (14) and B (15). It is worth noting that 11–15 are all pentacyclic triterpenoids containing unique 5,5-cis-fused γ-lactone structures to the D ring [15] (Figure 1).
Ergostane-type compounds are natural products whose biosynthesis originates from lanosterol. This conversion process involves several key steps: first, the removal of three methyl groups from the C(14) and C(4) positions of lanosterol, followed by the introduction of a new methyl group at the C(24) position, forming the basic skeleton of ergostane [8]. These compounds are widely distributed in the fungal. Ergosterol can undergo various reactions such as oxidation, carbon-carbon bond cleavage, ring expansion, or ring contraction to produce new derivatives.
Zhang et al. identified a total of 29 ergostane compounds from the fruiting bodies of T. imbricatum, including 26 previously reported compounds (17–42) and three newly discovered ergosterol derivatives: tricholimbrins C, D, and E (43–45). These new compounds include a ring-rearranged ergosterol derivative, a highly conjugated ergosterol, and a novel ergosterol derivative. The discovery of these compounds provides new insights into the biosynthesis and metabolic pathways of ergosterol [15].
Jin et al. isolated four unique ergosterol derivatives from the fruiting bodies of T. terreum, named tricholosterols A–D (46–49), among these, compound 46 exhibited a rare D-ring open ergosterol skeleton, while 47–49 were identified as rare degraded ergosterols. These characteristics are extremely uncommon among known ergosterol derivatives. This was the first report of such compounds from this species, marking a significant breakthrough in the study of steroid components in T. terreum [16]. Kaplaner et al. isolated two novel compounds from the acetone extract of T. anatolicum, anatoluin A (50) and anatoluin B (51). The study confirmed that the -OH substituent at the 6-position has an α-configuration in 50 and a β-configuration in 51. These compounds belong to a new class of natural ergosterol derivatives. Additionally, three previously reported ergosterols (52–54) were also isolated [17].The structures of these compounds are shown in Figure 2.
Tricholoma triterpenoids are a unique class of triterpenoid natural products produced by the fungi of the genus Tricholoma. These structures include a central methylene cyclohexane ring connected to two heterocycles, along with a γ-lactone substituent and a spiroketal carbon shared by the pyran and bridged heterocyclic system [18,19]. Gozzini et al. [13] isolated a new triterpenoid compound, saponaceolide T (55), from the ethyl acetate extract of T. saponaceum fruiting bodies, along with the previously reported C-30 terpenoid compounds, saponaceolides A–D (56–59), F (60), and H (61). The structures of these compounds were determined through spectrometric analysis [13]. Compounds 56–59 possess an unprecedented C-30 terpenoid skeleton, which may be assembled through a novel biosynthetic pathway that does not involve the classical cyclization of oxidosqualene to triterpene precursors. Instead, they are composed of two C15 units connected via a C(11′)-C(2) bond, and are more accurately described as sesquiterpene dimers. Gilardoni et al. discovered two previously reported triterpenoid compounds, saponaceolides F (60) and J (62), in T. ustaloides [14]. Chen et al. isolated two novel triterpenoid compounds, tricholopardin C (63) and D (64), from T. pardinum [18]. These compounds feature four separate rings and exhibit a novel linear structure, which might possess potential biological activities. The structures of these compounds are shown in Figure 3.

2.1.2. Diterpenoids

Diterpenoids, as a representative class of terpenoids, are widely present in plants but rarely appear in higher fungi. Among large fungi, the most abundant diterpenoids are cyathane-type diterpenoids, which possess a unique 5–6–7 tricyclic carbon skeleton with a trans 6–7 ring junction [20]. The genus Cyathus (Nidulariaceae) is a significant producer of cyathane-type diterpenoids [21]. In the past five years, four compounds identified as novel diterpenoids have been discovered in the fruiting bodies of Tricholoma. These compounds exhibit a rare and unique rearranged terpenoid skeleton, expanding the diversity of known diterpenoids produced by Basidiomycetes [22].
Gilardoni et al. was the first to isolate and identify four novel diterpenoid compounds, tricholomalides D–G (65–68), from the fruiting bodies of T. ustaloides. The absolute configurations of these compounds were determined through detailed analysis of MS, NMR, and circular dichroism (CD) spectrometric data. Compounds 65, 66, and 68 feature a γ-lactone ring fused in a cis manner at C-2 and C-7 to the central cycloheptene ring of the second steroidal skeleton, while tricholomalide F (67) has the γ-lactone ring fused in a cis manner at C-7 and C-8 to the cycloheptene ring [23]. This characteristic is extremely rare among natural products (Figure 4A).

2.1.3. Sesterterpenoids and C17 Compounds

Sesterterpenoids, as a rare class of terpenoid natural products, have garnered significant attention due to their unique biological activities, such as anti-inflammatory [24], antibacterial [25], and anti-cancer properties [26]. However, these compounds constitute less than 2% of the total number of terpenoids [27], making them some of the rarest terpenoid compounds to date [28], with only about 1500 compounds formally reported [29]. Most sesterterpenoid compounds have been successfully extracted and isolated from sponges [30]. Notably, only one sesterterpenoid has been discovered from Tricholoma and, during this process, a rare C17 compound was also unexpectedly found.
Feng et al. [31] isolated a novel C25 sesterterpenoid compound, tricholopardin A (69) from the fruiting bodies of T. pardinum (Figure 4B). Additionally, they isolated a C17 compound, tricholopardin B (70), which is quite uncommon in fungi (Figure 4C). This suggests that Tricholoma may possess unique biosynthetic pathways. The structures of these compounds were determined using spectroscopic methods, electronic circular dichroism, and optical rotatory dispersion calculations [31].

2.2. Alkaloids

Alkaloids are a class of nitrogen-containing organic compounds that are widely distributed in nature and possess significant bioactivity [32]. Based on their core chemical structures, alkaloids are classified into several types, including isoquinoline, quinoline, indole, and piperidine alkaloids [33]. The chemical structures of alkaloids are diverse and complex, and they exhibit numerous pharmacological activities, including anti-inflammatory [34], antibacterial [35] and anti-cancer properties [36]. They are widely found in traditional Chinese medicinal herbs, with their medicinal functions gradually being elucidated. In recent years, four alkaloid compounds have been discovered in Tricholoma, two of which are newly identified.

2.2.1. Diketopiperazine

Diketopiperazine alkaloids (DKPs) are a unique class of compounds formed by the cyclization of two amino acids into cyclic dipeptides [37]. As an important component of alkaloids, DKPs are relatively common in the fermentation broths of higher fungal species but are quite rare in the fruiting bodies [37,38].
Zhao et al. isolated two novel diketopiperazine compounds, matsudipeptides A (71) and B (72) [39], from the fruiting bodies of T. matsutake. Both compounds contain a peroxide group (O-O), with 71 featuring a peroxide bridge structure. In this structure, two oxygen atoms are connected by sharing one oxygen atom, forming a bridge that links two carbon atoms, an unusual structure related to the biosynthesis of cyclic dipeptides. Natural products containing endoperoxide are not very common and the structure types containing endoperoxide are always terpenoids, polyketides, or ergosterols [39,40]. Notably, this is the first report of a diketopiperazine with peroxy groups [39]. This study enhanced the chemical diversity of diketopiperazines derived from mushrooms (Figure 5A).

2.2.2. Indole Derivatives

The main components responsible for the bitter odor produced by the fruiting bodies of Tricholoma species are indole derivative compounds [1]. Clericuzio et al. isolated two previously reported indole compounds, 73 and 74 [41], from the mushroom T. pardinum. Compound 73 was previously found in T. sulphureum and T. matsutake [1], while 74 was isolated from Agrocybe cylindracea [42]. The unpleasant odor emitted by many Tricholoma fruiting bodies is likely due to their significant abundance of indole derivatives, which exhibit monomeric and dimeric structural characteristics [43]. Similar odors have been detected in T. album and T. sulphureum [1,41] (Figure 5B).

2.3. Other Compounds

2.3.1. γ-Glutamine Derivative

In 1990, Eizenhofer et al. isolated the compound lascivol (75) from the MeOH extract of freeze-dried fruiting bodies of T. lascivum [44]. Until 2020, the absolute configuration of the hydroxyl group at the C3 position of 75 was not confirmed and was re-determined by Oba et al. using an improved Mosher method [45]. Lascivol is a new representative of γ-glutamine derivatives commonly found in Basidiomycetes [44].

2.3.2. Amide Derivatives

Amide derivative compounds play an important role in natural products. For example, β-lactam antibiotics, such as penicillin compounds, inhibit bacterial cell wall synthesis, making them widely used in the medical field to treat bacterial infections [46]. Zhang et al. isolated two new amide compounds, tricholomines A (76) and B (77), from the dried fruiting bodies of T. bakamatsutake. The absolute configuration of these compounds was confirmed by single-crystal X-ray diffraction analysis [47]. In 2023, the same research team isolated another new amide compound, tricholomine C (78) [48] (Figure 6B).

2.3.3. Acetylene Compounds

In nature, alkynyl compounds are composed of molecules containing one, two, or more triple bonds, and these naturally occurring compounds are often referred to as acetylene compounds [49]. Their distinctive feature is the presence of an alkynyl group (-C≡C-), which can be part of linear or cyclic structures. Alkynyl compounds have a broad range of sources, and various alkynyl metabolites have been isolated and identified from plants, fungi, and other organisms [50].
Gilardoni et al. isolated a previously reported alkynyl compound, tricholomenyn C (79) from T. ustaloides [14]. Compound 79 is a fragile compound that easily decomposes in solutions containing trace inorganic acids. It is also the first naturally occurring dimeric enynylcyclohexenone [51]. Clericuzio et al. isolated four unprecedented acetylenic alcohols from T. pardinum: (Z)-non-7-en-5-yn-1,2,4-triol (80), (Z)-non-7-en-5-yn-1,4-diol (81), (Z)-1,2-dihydroxynon-7-en-5-yn-4-one (82), and (Z)-1-hydroxynon-7-en-5-yn-4-one (83) [41]. These compounds feature a nine-carbon linear alkynyl chain, with terminal hydroxyl modifications. The structures, names, and sources of these compounds are shown in Figure 6C and Table 1.

2.3.4. Polyketide Compounds

Yang et al. [52] isolated four polyketide amino acid derivatives, pardinumones A–D (84–87) from T. pardinum. These compounds feature a combination of a C10 polyketide unit and an amino acid (or its derivative) unit, which is uncommon in natural sources. The structures and absolute configurations of these compounds were determined through spectral data analysis, including electronic circular dichroism (ECD) and nuclear magnetic resonance (NMR) analysis [52].
Kaplaner et al. isolated a previously reported polyketide compound, 3,5-dihydroxyfuran−2(5H) −one (88), from T. anatolicum [17]. Zhang et al. isolated a new 4−chromanone (89) from the fruiting bodies of T. imbricatum [15]. Compound 89 was identified as a chromanone derivative containing hydroxyl, methyl, and ester groups, with a structure formed by connecting a benzene ring and a cyclohexane ring to form a cyclopentyl ketone (chromanone) scaffold. The chroman-4-one framework belongs to oxygen-containing heterocyclic structures and is a major component of a large class of medicinal compounds, exhibiting a variety of notable biological and pharmacological activities [53]. Their structures are displayed in Figure 6D.

2.3.5. Volatile Compounds

Murray et al. [54] analyzed the wild mushroom T. magnivelare, which has a unique aroma, using solvent-assisted flavor evaporation and aroma extract dilution analysis techniques. They detected 12 active components (90–101). The study showed that hexanal (90), 1-octen-3-one (91) or 1-octen-3-ol (93), (2E,4E)-non-2,4-dienal (95), (E)-methyl cinnamate (98), and linalool (101) are crucial for the aroma of T. magnivelare, and that the content of other active compounds is low. Chiral chromatography showed that alpha-pinene (100) is a mixture of 34% (R)-(+)- and 66% (S)-(–)-enantiomers, while 1-octen-3-ol (93) is a mixture of 95% (R)-( −)- and 5% (S)-(+)-enantiomers and linalool (101) is a mixture of 96% (R)-(–)- and 4% (S)-(+)-enantiomers. These findings lay the groundwork for further studies on the aroma chemistry of other Tricholoma compounds [54]. The structures of these compounds are shown in Figure 6E.

3. Biological Activity

Tricholoma, one of the most renowned higher fungi, is rich in bioactive compounds. Extracts from Tricholoma contain various active components with antioxidant, anti-inflammatory, and antibacterial properties [1]. Among the numerous secondary metabolites in Tricholoma, anatoluin A (50) and B (51) exhibit multiple bioactive functions. The majority of compounds found in Tricholoma have demonstrated anti-cancer properties. The biological activities of the secondary metabolites of Tricholoma are shown in Table 1 and Figure 7A.

3.1. Antibacterial Activity

The polyketide–amino acid derivatives 84–87 exhibit moderate antibacterial activity against Staphylococcus aureus, Staphylococcus epidermidis, and Escherichia coli, with MIC values ranging from 6.25 to 50 μg/mL [52].
Similarly, the most abundant volatile compound in Tricholoma, 93, can alter cell membrane permeability and exhibits strong antibacterial activity against various bacteria, including S. aureus, Bacillus subtilis, S. epidermidis, and E. coli [55,56].
Karakas et al. determined the significant antibacterial potential of the methanol crude extract of T. terreum against S. epidermidis, Serratia marcescens, and Proteus vulgaris using the disk agar diffusion method (Kirby-Bauer method) [57].
Additionally, experiments by Li et al. demonstrated that 40 possesses antibacterial activity against S. aureus, B. subtilis, Pseudomonas aeruginosa, S. epidermidis, and E. coli, but it had a more significant inhibitory effect on S. aureus and B. subtilis [58].

3.2. Anti-Cancer Activity

Compounds 2, 5–8, 26, 32, 41, and 42 inhibited the growth of human tumor cell lines HL-60, SMMC-7721, A-549, MCF-7, and SW480, with IC50 values all being below 40 μM [11,15]. Compounds 29 and 30 showed selective cytotoxicity against HL-60 and A-549, while 40 and 16 exhibited selective toxicity against A-549 and MCF-7. Notably, 29 and 30 had IC50 values below 10 μM against HL-60, while 40 and 42 showed IC50 values below 10 μM against A-549, demonstrating significant inhibitory effects. Structure–activity relationship analysis revealed that triterpenoids and ergosteroids with conjugated systems, such as 26, 32, and 40–42, exhibited cytotoxicity, providing new insights for anti-cancer drug development [15].
Compounds 50–53 demonstrated significant cytotoxic activity against four different cancer cell lines (MCF7, HT29, H1299, and HeLa). Based on the cytotoxicity results, compounds 50, 51, and 52 selectively inhibited MCF-7 and H1299 cancer cells, while compounds 50, 52, and 53 selectively inhibited HT29 cancer cells, exhibiting good cytotoxic activity. Compound 50 showed the strongest toxicity against the HeLa cell line (with the lowest IC50 of 14.3 ± 1.7 μg/mL), and relatively weaker toxicity against the H1299 cell line (IC50 of 34.3 ± 1.1 μg/mL). Compound 51 also exhibited good cytotoxic activity similar to 50. Compounds 50–54 displayed almost no toxicity to normal or healthy cell lines (such as PDF and L929) even at high concentrations (e.g., >100 μg/mL or IC50 of 93.2 ± 2.5 μg/mL), indicating they do not cause significant harm to these cells [17]. However, 53 exhibited toxicity to PDF and L929 cells, with IC50 values of 52.8 ± 0.5 and 65.6 ± 2.2 μg/mL, respectively [17].
Compounds 56, 57, 60, and 62 exhibited IC50 values ranging from 0.3 to 1.5 μM against HL-60 cells, demonstrating significant cytotoxic effects on these cells. Additionally, these compounds showed notable inhibitory effects on A-549, Hep G2, Caki-1, and MCF-7 cells, further confirming their potential in cancer treatment [14]. Compounds 55, 56, 58, 60, and 61 displayed strong antiproliferative effects on A549, Hep G2, Caki-1, MCF-7, and WISH cells, particularly surpassing the inhibitory effects of the well-known cytotoxic agent shikonin on A549 and Hep G2 cells. Among these, 56, 60, and 61 exhibited the most significant cytotoxicity, highlighting their potential application in the development of anticancer drugs [13].
Tricholopardin C (63) and 64 exhibited cytotoxicity against MCF-7 and HeLa cell lines. Notably, 63 shows a potent inhibitory effect on MCF-7 cells with an IC50 value of 4.7 μM [18]. Research indicates that caspases play a crucial role in tricholopardin C-induced apoptosis. Compared to the control group, activation of caspase-3 and caspase-9 was observed. The activated caspase-3 subsequently promotes the cleavage of PARP protein, leading to apoptosis. Figure 7B reveals the mechanism by which tricholopardin C induces tumor cell death through apoptosis [18].

3.3. Anti-Inflammatory Activity

The anti-inflammatory activity of several compounds was evaluated by inhibiting nitric oxide (NO) production in lipopolysaccharide (LPS)-induced RAW264.7 macrophages. Compounds 46 and 49 exhibited moderate inhibitory activity against NO production with IC50 values of 27.6 and 31.8 μM, respectively [16]. Compounds 2 and 5–8 exhibited stronger inhibitory effects, with IC50 values ranging from 5.3 to 14.70 μM [11]. Compound 69 showed potent NO inhibition with an IC50 value of 0.08 μM, indicating significant anti-inflammatory activity, while compound 70 displayed moderate anti-inflammatory activity with an IC50 value of 16.2 μM [31].

3.4. Antioxidant Activity

The antioxidant activity was determined using lipid peroxidation inhibitors and ABTS•+ scavenging activity. Compounds 50–54 exhibited very close activities in both acetone and methanol extracts. Among them, 50 was the most active compound in lipid peroxidation inhibitory activity, followed by 51, 52, 53, and 54, respectively. In the ABTS assay, the IC50 values of 50–54 were all more than 100 μg/mL, indicating relatively weak antioxidant activity [17]. Meanwhile, fungal studies on antioxidant activity suggest that T. ustale has a high free radical scavenging effect [59].
Table 1. The secondary metabolites of Tricholoma, discovered during 2018–2023.
Table 1. The secondary metabolites of Tricholoma, discovered during 2018–2023.
NumbersNamesSpeciesBioactivitiesReferences
Lanostane triterpenoids
1pardinol AT. pardinum-[11]
2pardinol BT. pardinumAnti-inflammatory activity; Anti-cancer activity[11]
3pardinol CT. pardinum-[11]
4pardinol DT. pardinum-[11]
5pardinol ET. pardinumAnti-inflammatory activity; Anti-cancer activity[11]
6pardinol FT. pardinumAnti-inflammatory activity; Anti-cancer activity[11]
7pardinol GT. pardinumAnti-inflammatory activity; Anti-cancer activity[11]
8pardinol HT. pardinumAnti-inflammatory activity; Anti-cancer activity[11]
9saponaceol BT. pardinum-[11]
10saponaceol DT. saponaceum-[11]
11tricholidic acid BT. ustaloides-[14]
12tricholidic acid CT. ustaloides-[14]
13tricholidic acidT. ustaloides-[14]
14tricholimbrin AT. imbricatum-[15]
15Tricholimbrin BT. imbricatum-[15]
16(25S)-(+)-12α-hydroxy-3α-methylcarboxyacetate-24-methyllanosta-8,24(31)-diene-26-oic acidT. imbricatumAnti-cancer activity[15]
Ergostane triterpenoids
173β,5α-dihydroxy-6β-methoxyergosta-7,22-dieneT. imbricatum-[15]
18(22E,24R)-5α,6α-epoxyergosta-8,22-T. imbricatum-[15]
19dien-3β,7α-diolT. imbricatum-[15]
20(22E,24R)-ergosta-7,22-diene-3β,5α,6β,9α-tetraolT. imbricatum-[15]
21(22E,24R)-ergosta-8,22-diene-3β,5α,6β,7α-tetrolT. imbricatum-[15]
(22E,24R)-ergosta-8,22-diene-3β,5α,6β,7α-tetrolT. imbricatum-[15]
22(22E,24R)-ergosta-8(14),22-diene-3β,5α,6β,7α-tetrolT. imbricatum-[15]
233β,5α,6β-trihydroxy-(22E,24R)-ergost-22-en-7- oneT. imbricatum-[15]
243β-hydroxy-(22E,24R)-ergosta-5,22- dien-7-oneT. imbricatum-[15]
253β-hydroxy-(22E,24R)-ergosta-5,22- dien-7-oneT. imbricatum-[15]
26isocyathisterolT. imbricatumAnti-cancer activity[15]
27(22E)-ergosta-4,6,8,22-tetraen-3-oneT. imbricatum-[15]
28(22E,24R)-ergosta-4,6,8(14),22-tetraen-3-oneT. imbricatum- [15]
293β-hydroxyl-(22E,24R)-ergosta-5,8,22-trien-7,15-dioneT. imbricatumAnti-cancer activity[15]
303β-hydroxyl-(22E,24R)-ergosta-5,8,22-trien-7-oneT. imbricatumAnti-cancer activity[15]
313β-hydroxyl-(22E,24R)- ergosta-5,8,14,22-tetraen-7-oneT. imbricatum-[15]
323β,15α-dihydroxyl-(22E,24R)-ergosta-5,8(14),22-trien-7-oneT. imbricatumAnti-cancer activity[15]
333β,15β-dihydroxyl-(22E,24R)-ergosta-5,8(14),22-trien-7-oneT. imbricatum-[15]
343β-hydroxyl-(22E,24R)-ergosta-5,8(14),22-trien-7,15-dioneT. imbricatumAnti-cancer activity[15]
355α,6α-epoxy-(22E,24R)-ergosta-8,22-diene-3β,7β-diolT. imbricatumAnti-cancer activity[15]
365α,6α-epoxy-(22E,24R)-ergosta-8(14),22-diene-3β,7α-diolT. imbricatum-[15]
375α,6α-epoxy-(22E,24R)-ergosta-8(14),22-diene-3β,7β-diolT. imbricatum-[15]
385α,6α-epoxy-(22E,24R)-ergosta-8(14),22-diene-3β,7β-diolT. imbricatum-[15]
395α,8α-epidioxy-(22E,24R)-ergosta-6,22- dien-3β-olT. imbricatum-[15]
40chaxine CT. imbricatumAntibacterial activity;
Anti-cancer activity		[15,58]
41demethylincisterol A3T. imbricatumAnti-cancer activity[15]
42volemolideT. imbricatumAnti-cancer activity[15]
43tricholimbrin CT. imbricatum-[15]
44tricholimbrin DT. imbricatum-[15]
45tricholimbrin ET. imbricatum-[15]
46tricholosterol AT. terreumAnti-inflammatory activity[16]
47tricholosterol BT. terreum-[16]
48tricholosterol CT. terreum-[16]
49tricholosterol DT. terreumAnti-inflammatory activity; Cytotoxic against human cancer cell lines[16]
50anatoluin AT. anatolicumAntioxidant activity; Cytotoxic against human cancer cell lines[17]
51anatoluin BT. anatolicumAntioxidant activity; Cytotoxic against human cancer cell lines[17]
525α,6α-epoxy-ergosta-7,22-dien,3β-olT. anatolicumAntioxidant activity; Cytotoxic against human cancer cell lines[17]
53ergosterol-endoperoxideT. anatolicumAntioxidant activity;
Cytotoxic against human cancer cell lines		[17]
54ergosterol,3β-olT. anatolicum-[17]
Triterpenoids
55saponaceolide TT. saponaceumCytotoxic against human cancer cell lines[13]
56saponaceolide AT. saponaceumCytotoxic against human cancer cell lines[13]
57saponaceolide BT. saponaceumCytotoxic against human cancer cell lines[13]
58saponaceolide CT. saponaceumCytotoxic against human cancer cell lines[13]
59saponaceolide DT. saponaceum-[13]
60saponaceolide FT. saponaceumCytotoxic against human cancer cell lines[13,14]
61saponaceolide HT. saponaceumCytotoxic against human cancer cell lines[13]
62saponaceolide JT. ustaloidesCytotoxic against human cancer cell lines[14]
63tricholopardin CT. pardinumCytotoxic against human cancer cell lines[18]
64tricholopardin DT. pardinumCytotoxic against human cancer cell lines[18]
Diterpenoids
65tricholomalide DT. ustaloides-[23]
66tricholomalide ET. ustaloides-[23]
67tricholomalide FT. ustaloides-[23]
68tricholomalide GT. ustaloides-[23]
Sesterterpenoid
69tricholopardin AT. pardinumAnti-inflammatory activity[31]
C17 compound
70tricholopardin BT. pardinumAnti-inflammatory activity[31]
Diketopiperazines
71matsudipeptide AT. matsutake-[39]
72matsudipeptide BT. matsutake-[39]
Indole derivatives
731H-indole-3-carbaldehydeT. lascivum-[45]
746-hydroxy-1H-indole-3-carbaldehydeT. pardinum-[41]
γ-glutamine derivative
75lascivolT. pardinum-[41]
Amide derivatives
76tricholomine AT. bakamatsutake-[47]
77tricholomine BT. bakamatsutake-[47]
78tricholomine CT. bakamatsutake-[48]
Acetylene compounds
79tricholomenyn CT. ustaloides-[14]
80(Z)-non-7-en-5-yn-1,2,4-triolT. pardinum-[41]
81(Z)-non-7-en-5-yn-1,4-diolT. pardinum-[41]
82(Z)-1,2-dihydroxynon-7-en-5-yn-4-oneT. pardinum-[41]
83(Z)-1-hydroxynon-7-en-5-yn-4-oneT. pardinum-[41]
Polyketide compounds
84pardinumone AT. pardinumAntibacterial activity[52]
85pardinumone BT. pardinumAntibacterial activity[52]
86pardinumone CT. pardinumAntibacterial activity[52]
87pardinumone DT. pardinumAntibacterial activity[52]
883,5-dihydroxyfuran-2(5H)-oneT. anatolicum-[17]
894-chromone derivativeT. imbricatum-[15]
Volatile compounds
90hexanalT. magnivelare-[54]
911-octen-3-oneT. magnivelare-[54]
92(E)-oct-2-enalT. magnivelare-[54]
931-octen-3-olT. magnivelareAntibacterial activity[55,56]
94linaloolT. magnivelare-[54]
95(2E,4E)-nona- 2,4-dienalT. magnivelare-[54]
96ethyl 3-phenylpropanoateT. magnivelare-[54]
974-methoxybenzaldehydeT. magnivelare-[54]
98methyl (E)-3-phenylprop-2-enoateT. magnivelare-[54]
993,4-dimethoxybenzaldehydeT. magnivelare-[54]
100α-pineneT. magnivelare-[54]
101linaloolT. magnivelare-[54]

4. Conclusions and Prospect

In recent years, with the increasing demand for health and nutrition, mushrooms have garnered significant attention as valuable resources for both medicinal and culinary purposes. Mushrooms are not only popular on dining tables for their taste and nutritional value but also widely used in the medical field due to their various medicinal properties. For instance, Ganoderma lucidum is extensively used in health supplements and traditional Chinese medicine because of its notable immune-modulating and anti-cancer effects [60]. Hericium erinaceus is renowned for its protective gastric and neuro-regulatory functions, and is commonly used in both traditional medicine and dietary supplements [61,62]. Lentinula edodes and Agrocybe are known for their rich polysaccharides and alkaloids, which exhibit anti-cancer, antiviral, and immune-regulating effects [42,63]. Similarly, Tricholoma has also attracted widespread attention.
This review summarizes the rich research achievements in the field of secondary metabolites of Tricholoma from 2018 to 2023. Up to 101 compounds have been isolated and identified, including 46 novel compounds. Most of these compounds are extracted from the fruiting bodies of Tricholoma mushrooms, exhibiting diverse structures that highlight the complex metabolic pathways that have evolved in these fungi as products of natural evolution. Of particular interest are compounds such as triterpenes, diterpenes, and rare C17 compounds, which possess unprecedented chemical scaffolds and unique biosynthetic pathways. These findings not only expand our understanding of fungal secondary metabolism mechanisms but also offer possibilities for enhancing the production and diversity of these secondary metabolites through rational modification of host organisms or de novo synthesis methods.
From a biological activity perspective, the secondary metabolites from Tricholoma have properties including anti-cancer, anti-inflammatory, anti-microbial, and antioxidant, and demonstrate potential applications in pharmaceutical research. Additionally, crude acetone extracts of T. pardinum mushrooms exhibit strong acaricidal activity against dangerous crop pests from the Acarinae family [41], offering new solutions for agricultural biocontrol. In today’s advancing technology landscape, our understanding of mushrooms and natural products continues to deepen, expanding their potential applications in drug development and beyond. The diversity and bioactivity of the Tricholoma secondary metabolites represent a significant resource for pharmaceutical research and agricultural biocontrol, providing a foundation for the development of new drugs and effective biocontrol strategies.

Author Contributions

M.Z., S.Y. and C.L. conceived and designed the research. M.Z., C.L. and R.Z. surveyed the scientific literature. M.Z., Z.L. and S.Y. analyzed data and wrote the draft manuscript. M.Z., Z.L. and C.L. interpreted the data and reviewed the manuscript. C.L. and R.Z. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (No. 32370069 and U22A20369), the Natural Science Foundation of the Heilongjiang Province of China (No. LH2023C035), and the Chinese Agriculture Research System (CARS-20).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Informed consent has been obtained from the subjects to publish this paper.

Conflicts of Interest

The authors declare no conflicts of interest.

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Molecules 29 04719 g001
Figure 1. Chemical structures of the lanostane triterpenoids.
Figure 1. Chemical structures of the lanostane triterpenoids.
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Figure 2. Chemical structures of the ergostane triterpenoids.
Figure 2. Chemical structures of the ergostane triterpenoids.
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Figure 3. Chemical structures of the triterpenoids.
Figure 3. Chemical structures of the triterpenoids.
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Figure 4. Chemical structures of the diterpenoids (A), sesterterpene (B), and the C17 compound (C).
Figure 4. Chemical structures of the diterpenoids (A), sesterterpene (B), and the C17 compound (C).
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Figure 5. Chemical structures of the diketopiperazine derivatives (A) and indole derivatives (B).
Figure 5. Chemical structures of the diketopiperazine derivatives (A) and indole derivatives (B).
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Figure 6. Chemical structures of the γ-glutamine derivative (A), amide derivatives (B), acetylene compounds (C), polyketide compounds (D), and volatile compounds (E).
Figure 6. Chemical structures of the γ-glutamine derivative (A), amide derivatives (B), acetylene compounds (C), polyketide compounds (D), and volatile compounds (E).
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Figure 7. Biological activities of some of the compounds (A) from Tricholoma and the proposed model of Tricholopardin C induced apoptosis (B).
Figure 7. Biological activities of some of the compounds (A) from Tricholoma and the proposed model of Tricholopardin C induced apoptosis (B).
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Zhao, M.; Yuan, S.; Li, Z.; Liu, C.; Zhang, R. Review of the Structural Characteristics and Biological Activities of Tricholoma Secondary Metabolites (2018–2023). Molecules 2024, 29, 4719. https://doi.org/10.3390/molecules29194719

AMA Style

Zhao M, Yuan S, Li Z, Liu C, Zhang R. Review of the Structural Characteristics and Biological Activities of Tricholoma Secondary Metabolites (2018–2023). Molecules. 2024; 29(19):4719. https://doi.org/10.3390/molecules29194719

Chicago/Turabian Style

Zhao, Meili, Shiqin Yuan, Zhiming Li, Chengwei Liu, and Ruiying Zhang. 2024. "Review of the Structural Characteristics and Biological Activities of Tricholoma Secondary Metabolites (2018–2023)" Molecules 29, no. 19: 4719. https://doi.org/10.3390/molecules29194719

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