Secrets of Flavonoid Synthesis in Mushroom Cells: History
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Contributor:
Jan Pukalski
,
Dariusz Latowski

Flavonoids are chemical compounds that occur widely across the plant kingdom. They are considered valuable food additives with pro-health properties, and their sources have also been identified in other kingdoms. Especially interesting is the ability of edible mushrooms to synthesize flavonoids. Mushrooms are usually defined as a group of fungal species capable of producing macroscopic fruiting bodies, and there are many articles considering the content of flavonoids in this group of fungi. Whereas the synthesis of flavonoids was revealed in mycelial cells, the ability of mushroom fruiting bodies to produce flavonoids does not seem to be clearly resolved. This entry, as an overview of the latest key scientific findings on flavonoids in mushrooms, outlines and organizes the current state of knowledge on the ability of mushroom fruiting bodies to synthesize this important group of compounds for vital processes. Putting the puzzle of the current state of knowledge on flavonoid biosynthesis in mushroom cells together, a universal scheme of studies to unambiguously decide whether the fruiting bodies of individual mushrooms are capable of synthesizing flavonoids that was proposed.

  • mushrooms
  • fruiting bodies
  • mycelia
  • flavonoids
  • biosynthesis

1. Introduction

Fungal cells are known to produce a variety of biological compounds. They are a source of medicinal substances, such as antibiotics [1][2][3], anticancer drugs [4][5] and even psychoactive compounds such as psilocybin, the application of which is controversial but postulated by some scientists to be useful in mental disorder treatments [6]. Fungal cells are also capable of synthesizing large polymers such as melanins [7][8] and chitosan [9], which are considered promising biomaterials [10][11][12], and notably, whole-mycelium-based composites are intensively studied as, among others, eco-friendly building materials [11][13]. A diverse group of fungal metabolites is the sesquiterpenes, which may be characterized by antifungal, antibacterial, cytotoxic, anti-inflammatory and anticancer properties [14]. As sesquiterpenes can be non-volatile or volatile [15], fungal volatile organic compounds (fVOCs) constitute another large group of ecologically important compounds, which is well described in Inamdar et al.’s [16] and Guo et al.’s [17]] articles. Fungal cells are also a rich source of pigments, including not only the previously mentioned melanins but also oxopolyenes, quinones, anthraquinones, naphthoquinones, hydroxyanthraquinones and azaphilones [18]. Some pigments may also be valuable food ingredients, for example, carotenoids and flavonoids [19][20]. Fungi are considered a promising source of nutrients. Barzee et al. [21] stated that even microscopic filamentous fungi such as Fusarium venenatum, Aspergillus oryzae and Rhizopus oligosporus mycelia, after their proper preparation, may be consumed and become foods of the future. Interestingly, the mentioned fungi are characterized by high protein contents, with 48.0, 45.7 and 49.7 g per 100 g of dried weight, respectively. They also contain all essential amino acids required by humans and are a source of dietary fiber, unsaturated fatty acids, carbohydrates, macroelements such as calcium, potassium, and phosphorus and microelements involving, i.a., zinc, of which an especially rich source is F. venenatum, with 30.4 mg/100 g of dried weight [21]. However, today, as has been the case for centuries, more attractive to consumers are edible mushrooms such as Agaricus bisporus, Pleurotus sajor-caju or Pleurotus giganteus, the fruiting bodies of which are characterized by relatively high protein–fat ratios of 14.1:2.2, 37.4:1.0 and 17.7:4.3, respectively, and are a familiar, accepted form [22]. Moreover, nowadays, mushroom fruiting bodies are intensively studied as food sources, and detailed information about edible species, nutrient compositions, the digestibility of particular components and taste attributes can be found elsewhere [23][24][25].

2. Flavonoids and Mushrooms

Flavonoids are mainly considered plant secondary metabolites [26][27] that play protective roles against UV radiation [28] and reactive oxygen species (ROS) [29]. They are essential in plant–pollinator interactions [30] and protect the plant-host cells from pathogenic microbes, among which plant–fungi interactions and the antifungal properties of flavonoids are especially well described [31][32][33][34][35][36][37][38][39][40]. Thus, flavonoids, despite the positive role that they play in plant interactions with mycorrhizal fungi [41][42], are generally described as harmful to fungal cells. However, scientists are still focused on searching for fungi that produce flavonoids, especially mushrooms that evolve edible fruiting bodies [43][44][45], due to the health-promoting properties of these compounds [46][47][48][49][50][51][52][53][54][55]. Additionally, from the scientific point of view, the role of flavonoids in fruiting bodies is exceedingly interesting due to the fact that, except for hypogeous species, fruiting body cells are exposed to biotic and abiotic stresses that differ from those of mycelia located in the soil or touchwood.

Due to the term ‘mushroom’, which is defined as a group of species producing mycelia and macroscopic fruiting bodies or as macroscopic fruiting bodies only, what was mentioned for example on the official website of The Microbiology Society (https://microbiologysociety.org/why-microbiology-matters/what-is-microbiology/fungi.html access: 20.10.2022), there may be some linguistic problems with answearing the question whether mushrooms are capable of producing flavonoids. In the opinion the first definition better captures the nature of mushrooms and the researchers used it to construct the article ‘Secrets of Flavonoid Synthesis in Mushroom Cells’. From the scientific point of view, essential is whether mycelia as well as large fruiting bodies growing from it, are capable to synthesize flavonoids. Thus, the researchers used terms ‘mushroom mycelia’ and ‘mushroom fruiting bodies’ to emphasize that metabolites profiles may differ in the mentioned structures produced by species of macrofungi [56][57].

3. Are Mushrooms Capable of Producing Flavonoids?

The discussion of the capability of mushroom cells to produce flavonoids has been ongoing for years. In 2016, Gil-Ramírez et al. [58] published an important article showing the analysis of 24 mushroom species, and their conclusion was that the mentioned fungi are not capable to synthesize or absorb flavonoids. In addition, searching in bioinformatic databases has shown no mushrooms with the gene sequences of all three enzymes which were postulated as essential for flavonoid biosynthesis, which are phenylalanine ammonia-lyase (Pal), chalcone synthase (Chs) and chalcone isomerase (Chi). However, the statement that mushrooms do not contain flavonoids seems to be unnecessarily extended to all species and strains. In the researchers opinion, the valuable publication by Gil-Ramírez et al. [58] started the discussion of whether mushroom cells are capable of synthesizing flavonoids and the methods that should be used or avoided to verify this issue. The results of applying colorimetric analyses [58] led to the conclusion that more sophisticated methods, such as those using HPLC systems, should be involved instead of UV-Vis measurements only. Other papers, such as the article by Mohanta [59], which was a response to Gil-Ramírez et al.’s [58] paper, provided interesting information about mushrooms and fungi in general in the case of flavonoid synthesis, but they did not prove flavonoid synthesis inside the cells of mushroom fruiting bodies. Meng et al. [60] and Wang et al. [61] used both instrumental methods and gene expression analyses to study Auricularia cornea and Sanghuangporus baumii mushrooms respectively. The briliant results provided by the two mentioned Chinese teams proved that mushrooms mycelia are capable of synthesizing flavonoids, however fruiting bodies were not studied. The results provided by Liu et al. [62] proved that the fruiting bodies of some strains of Sanghuangporus sanghuang collected as environmental samples contained flavonoids, but there was no information on whether the genes associated with flavonoid biosynthesis were expressed; thus, the detected compounds could be synthesized by the mushroom or absorbed from the host mulberry tree. On the other hand, studies conducted by Shao et al. [63] revealed that genes engaged in flavonoid biosynthesis were expressed in the developmental stages of fruiting bodies of Sanghuangporus sanghuang KangNeng cultivated in the lab, and the lack of confirmation of flavonoid presence in fruiting body cells is the only reason why the synthesis of flavonoids in the analyzed mushroom strain was not fully proven. However, the results obtained by Liu et al. [62], Wang et al. [61] and Shao et al. [63] make the cells of the fruiting bodies of some strains of the Sanghuangporus genus highly probable flavonoid producers. Studies of Mohanta [59], Meng et al. [60], Wang et al. [61] and Shao et al. [63] showed that chs genes were absent in genomes of analysed fungi what suggests the presence of an alternative flavonoids synthesis pathway in comparison to plants. Other works, such as Alam et al. [64], revealed flavonoid content in mushroom fruiting bodies but did not provide information about the culture media and culture conditions; thus, similarly to environmental samples, the absorption of the compounds by fungal cells cannot be excluded. In conclusion, as can be found in the cited articles, although many researchers have been close to resolving the mystery of flavonoid synthesis in mushroom fruiting body cells, to the best of the knowledge, the veil of the mystery over this issue has not been fully lifted yet.

Studying the problem is technically challenging; nevertheless, the researchers propose factors that should be taken into consideration to conduct experiments to provide credible results. Firstly, one particular strain/isolate should be studied. Secondly, exclusively fruiting bodies, not mycelia, should be analyzed. Thirdly, if mushroom fruiting bodies can be cultivated on media with a well-defined composition, instrumental analyses, for example HPLC analysis, would be sufficient to prove flavonoid synthesis. When fruiting bodies are environmental samples, a combined analysis using instrumental methods and gene expression studies should be applied. The suggestions made are clear signposts on the paths leading to the definitive verification of the ability of mushroom fruiting body cells to synthesize flavonoids, and the goal itself already seems very close to being reached.

This entry is adapted from the peer-reviewed paper 10.3390/cells11193052

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