A review on the edible mushroom as a source of special flavor: Flavor categories, influencing factors, and challenges
Chunping Jiang, Xiaoyu Duan, Lin Lin, Wenjuan Wu, Xiaolin Li, Zhen Zeng, Qingying Luo, Yuntao LiuFirst published: 03 June 2023https://doi.org/10.1002/fft2.263Citations: 2
Chunping Jiang and Xiaoyu Duan contributed equally to this article.
Abstract
Edible mushrooms are highly valued for both their culinary and medicinal properties. Unlike traditional condiments, the complex flavor of mushrooms is not determined by a single component, but rather by the potential synergistic actions of several different components and chemical interactions. However, only a limited number of edible mushroom flavor compounds have been examined in detail, leading to an incomplete understanding of their overall flavor profile. To address this knowledge gap, it is necessary to conduct further scientific research on edible mushroom flavors to maximize their utilization. This review aims to provide a comprehensive overview of the flavor substances found in edible mushrooms, including both volatile and nonvolatile compounds, as well as the mechanisms by which various processing methods affect flavor. Additionally, we will explore the various factors that hinder the development of edible mushroom flavors and recommend strategies to further advance the technological and theoretical understanding of these unique and valuable food ingredients. In summary, by enhancing our understanding of the complex and unique flavor profile of edible mushrooms, we can better leverage their full potential as a valuable culinary and medicinal resource.
1 INTRODUCTION
Based on archeological evidence, mushrooms have been part of the human diet for thousands of years. Mushrooms are biologically distinct from plants and animals and are important decomposers of breaking down dead material (Sarikurkcu et al., 2020). Compared with plants and animals, limited research has been reported on mushrooms. We searched for literature using the terms “mushroom,” “plant,” and “animal” on the Web of Science and retrieved 40,599, 3,796,699, and 18,960,497 articles, respectively. This is a huge gap and there are about 20,000 species of mushrooms found in the world, while there are about 1.5 million known animals on Earth. However, in those existed research, a growing body of evidence suggests mushrooms (as food or extracts) are a rich source of various nutraceutical compounds, including carbohydrates, proteins, dietary fiber, vitamins, and minerals. Besides, they are low in calories, fat, and cholesterol. What's more, there are many bioactive substances in mushrooms and these compounds have biological functions, like antioxidation, reduce blood lipids, and enhance body immunity (Roncero-Ramos & Delgado-Andrade, 2017). For instance, mushroom polysaccharides exert health benefits through their effects on digestion and intestinal microbial fermentation (Liu et al., 2020b). A multifunctional protein (BEAP) isolated from Boletus edulis has antitumor and antimetastasis effects (Zhang et al., 2021). Taken together, these findings show that edible mushrooms improve health through their biological activity and bioaccumulation, like phenolic compounds, indole derivatives, sterols, ergothioneine, and B group vitamins in mushrooms with great prohealth effects (Krakowska et al., 2020).
In addition to their diverse bioactive compounds and high nutritional value, mushrooms possess attractive aroma, taste, texture, making it an ideal cooking ingredient. Flavor is a special characteristic component of food and is made up of many compounds that give food its aroma, making food flavor very complex. Nonetheless, the content of flavor compounds in mushrooms and their release during cooking and digestion vary by strain, cultivation conditions, cooking process, and storage methods (Liu et al., 2021a, 2020a; Pérez-Montes et al., 2021). Mushroom flavor is not only composed of a single substance, but is caused by volatile compounds (including acids, ketones, aldehydes, and esters) and nonvolatile components (including free amino acids and flavoring nucleotides and peptides). Umami and flavor are the primary characteristics of mushrooms, which becoming one of the most important parameters for consumers to choose various mushrooms (Sun et al., 2020b). Flavor research for the use of edible or medicinal mushrooms and understanding the composition characteristics and influencing factors of mushroom flavor are essential to maximize the benefits of mushroom consumption. This paper reviews the flavor compounds of edible mushrooms, their impact on metabolism, the influence of processing methods on mushroom flavor, and the current understanding of mycelia flavor and factors that hinder the development of edible mushroom flavors.
2 THE FLAVOR COMPONENTS OF EDIBLE MUSHROOMS
In addition to being rich in nutrients, mushrooms possess biological activity, aroma, and umami, making them a good source of cooking materials. Tricholoma matsutake and boletus are delicious and rich; Termitornyces albuminosus is fresh and crispy; and Craterellus cornucopioides is fresh, salty, and slightly sweet. Different structural characteristics give mushrooms different taste, but the difference in flavor composition makes mushrooms have different sensory attribute. Edible mushrooms produce various 8-carbon compounds, including 1-octanol, 3-octanol, 3-octanone, 1-octen-3-ol, and 1-octen-3-one, which are predominantly volatile organic compounds (Aisala et al., 2019). The tastes of various peptides, amino acids, and nucleotides have different effects on the overall mushroom taste and aroma. However, few studies have comprehensively compared the flavors or flavor components of various mushrooms. Here, we summarize current research on the flavor compounds and flavors of edible mushrooms and compare the flavors of substances present in edible mushrooms. This knowledge can help guide the fine division of the edible mushroom processing industry for application, lead to accurate utilization, and help the deep processing of edible mushrooms grow and improve in the future.
2.1 Research progress on edible mushroom flavor
We searched for literature using the terms “flavor” and “mushroom” on the Web of Science and retrieved 884 articles published before April, 2023. The search revealed that studies on this topic have increased annually, indicating a growing interest in mushroom flavor. Most of the articles were on food science technology (80.656%), nutrition dietetics (49.321%), agriculture (46.719%), biochemistry molecular biology (43.213%), and chemistry (42.986%). Medical subject headings (MeSH) mainly included the terms taste (11.538%), humans (11.425%), odorants (11.312%), agaricales (10.294%), and gas chromatography-mass spectrometry (8.484%). Further analysis revealed that MeSH subheadings mainly contain words chemistry (25.679%), analysis (19.796%), metabolism (10.068%), methods (8.484%), and pharmacology (6.222%). As a result, compared with the food field in previous years, research on edible mushrooms has been steadily increasing, and the research database on the varieties, nutrition, and flavor of edible mushroom is also gradually improving. As a source of special flavor, different mushrooms show different tastes and flavors due to the differences in metabolites or tastants (content and type). According to the research of various edible mushrooms, we summarized the flavor of them (Table S1). Some mushrooms exhibit pleasing sweet, umami, and mushroom flavors (like Agaricus bisporus (A. bisporus), Agrocybe cylindracea, Hypsizygus tessulatus and Lentinula edodes (fresh)), while others exhibit sour, astringent, and bitter flavors (like Auricularia auricular, Boletus edulis, Grifola frondose, and Pleurotus ostreatus). It is because of these different characteristics that the variety of edible mushrooms is so diverse, and it has also become a significant factor in mushroom identification and selection.
2.2 Volatile flavor components of edible mushrooms
With improving living standards, people are prioritizing food nutrition and flavor. Edible mushrooms have unique flavors. Databases containing data on the Gas Chromatograph—Ion Mobility Spectrometer (GC-IMS), Headspace solid phase microextraction combined with gas chromatography-mass spectrometry (HS-SPME-GC-MS) with 2014 National Institute of Standards and Technology (NIST), or IMS identify a variety of volatile compounds in edible mushrooms, including aldehydes, alcohols, acids, ketones, esters, pyrazines, phenols, sulfur compounds, hydrocarbon, and alkanes (Fang et al., 2019; Hou et al., 2021; Lin et al., 2017; Liu et al., 2021b; Wang et al., 2021; Xun et al., 2020; Zhuang et al., 2020). Volatile compounds provide flavor by stimulating human olfactory receptors. Edible mushrooms contain various volatile compounds, including alcohols, aldehydes, esters, and ketones (Figure 1a, Table S2). They also contain many alcohol compounds and relative levels of saturated as well as unsaturated alcohols, along with their unique odors, hence giving different mushrooms unique aromas including fruit, vegetable, floral, fat, and roasted flavors. Moreover, 1-octanol, 3-octanol, 3-octanone, 1-octen-3-ol, and 1-octen-3-one have typical raw mushroom odors, including mushroom-like, mushroom-like/buttery, and mushroom-like/chemical odors (Cho et al., 2006).
Studies have shown that aldehydes with a low threshold are mainly produced via the oxidation of polyunsaturated fatty acid double bonds. Aldehydes are a key component of mushroom flavor compounds and have been detected in Tuber aestivum, Cantharellus cibarius, Tricholoma matsutake, Boletus edulis, Boletus aereu, Boletus rubellus Krombh, Boletus auripes Pk, and Lentinula edodes (L. edodes) (Hou et al., 2021; Xun et al., 2020; Zhuang et al., 2020). Aldehyde compounds have extensive flavors, including fruit, vegetable, floral, roasted, and caramel flavors. However, the pentanal or furfural detected in Boletus and L. edodes has a strong, acrid, pungent smell (Hou et al., 2021; Zhuang et al., 2020).
Ketones, which are variants of aldehydes and alcohols, are rich in the odors of both compounds. Studies indicate that aldehydes are mainly present in Tuber aestivum, Boletus edulis, Cantharellus cibarius, L. edodes, Tricholoma matsutake, and Agaricus bernardii (Hou et al., 2021; Wang et al., 2021; Xun et al., 2020). The most abundant esters in Agaricus bernardii and L. edodes, including ethyl caproate, isoamyl butyrate, ethyl caprylate, hexyl acetate, butyl acetate, isoamyl acetate, ethyl butanoate, and ethyl propanoate have various fruit aromas (Hou et al., 2021; Wang et al., 2021). Ester gives a very pleasant flavor that potentially explains why Agaricus bernardii and L. edodes are preferred by consumers.
The flavor of edible mushrooms is also affected by acids, sulfur compounds, pyrazines, phenols, and alkanes (Li et al., 2019). For instance, phenols have smoky, roasted, or pungent odors. Pyrazines, which are primarily derived from -hydroxyamino amino acids, serine, and threonine, produce a variety of flavors such as meat, chocolate, peanuts, and popcorn. Sulfur compounds, which are formed by lentinic acid polymerization to produce dithiolane intermediates via glutamate transpeptidase activity influence the overall smell of mushrooms. Although passing dried edible mushrooms through sulfur smoke can improve flavor, this is prohibited since the resulting sulfur dioxide may exceed the standard level. In summary, mushroom smell depends on their numerous compounds, elative ratios, and thresholds.
2.3 Nonvolatile flavor components of edible mushrooms
In addition to the flavor produced by volatile components, the mushroom flavor is affected by nonvolatile substances, including soluble sugars, polyols, tasteful peptides, amino acids, and nucleotides (Figure 1b). Edible mushroom contain a wide range of soluble sugars and polyols, including mannitol, trehalose, raffinose, galactose, glucose, fructose, and xylose, which impart sweetness to edible mushroom (Kalac, 2013). However, the sweetness varies with the variety, maturity stage, and content of edible mushroom. For instance, the soluble sugar content in fresh Volvariella volvacea is 346.63 mg/g DW, most of which is trehalose (337.83 mg/g DW) (Fang et al., 2019). A study of the nonvolatile taste components of two strains of Hypsizigus marmoreus from Taiwan discovered that mannitol (18.19-22.59 mg/g DW) and trehalose (9.84-44.79 mg/g DW) are the primary polyol and sugar, respectively (Lee et al., 2009). Higher levels of mannitol may confer a more refreshing sweet taste (Litchfield, 1967). The sweetness of trehalose is 45% that of sucrose without leaving an aftertaste (Barros et al., 2007). They have similar expressions in various mushrooms, including Volvariella volvacea, Pleurotus eryngii, Agrocybe cylindracea, A. bisporus, Pleurotus cystidiosus, Agaricus blazei, and Coprinus comatus (Li et al., 2014; Mau et al., 1997; Mau et al., 1998a; Mau & Tseng, 1998b; Tseng & Mau, 1999). However, studies have shown that arabinose is the most abundant soluble sugar in Stropharia rugoso-annulata (60.10-119.14 mg/g DW) (Hu et al., 2020), white Flammulina velutipes (187 mg/g), and yellow Flammulina velutipes (190 mg/g) (Yang et al., 2001). Analysis of sugar and polyol levels in fruit bodies indicates that sucrose (7.08 mg/g) and trehalose (7.45 mg/g) levels are high in A. bisporus; ribose (5.07 mg/g) and trehalose (5.86 mg/g) levels are high in Volvariella volvacea; arabinose (11.48 mg/g) levels are high in Flammulina velutipes. However, according to Chiang's research, all of the soluble sugar and polyol contents are low (Chiang et al., 2006). The differences in the levels of sugar and polyol reported by different groups are potentially due to the use of different processing methods or strains. Summarily, differences in the type and content of soluble sugars or polyols affect the taste of edible mushroom, such as the sweetness of the mushrooms.
Amino acids mainly produce ammonia, hydrocarbons, nitriles, carbon dioxide, and other volatile and nonvolatile substances through reactions like deamination, decarboxylation, and oxidation. Most peptides that contain hydrophobic amino acids, including phenylalanine, tryptophan, leucine, isoleucine, histidine, valine, proline, alanine, tryptophan, glycine, arginine, and methionine have a bitter taste. Sour-taste peptides are generally associated with the taste of umami. The presence of free glutamic and aspartic acids gives rise to a sour and briny / umami taste. The alanine, glycine, serine, and threonine have a pure sweet taste, whereas lysine and tyrosine are unflavored (Pei et al., 2014). Several studies have shown that the levels of free amino acid in mushrooms vary by geographic location, maturity stage, cultivation conditions, mushroom type, and storage and drying conditions (França et al., 2022; Hou et al., 2021; Zhao et al., 2021). As such, the free amino acid content in mushrooms varies widely, and the combination of amino acids seems to determine the natural taste of mushrooms.
Taste peptides have molecular masses of <3000 Da and are generated via enzymatic hydrolysis or amino acid synthesis. Such peptides interact with specific taste receptors (including the heterodimeric T1R1/T1R3, and the taste-type metabolic glutamate receptors mGluR1and mGluR4) on taste buds, resulting in their characteristic tastes (Chen et al., 2022). However, some taste peptides (e.g., umami peptides) do not trigger taste after binding to taste receptors but only enhance flavor. Peptide can interact with other flavor substances in food and obviously change the original flavor. The unique taste properties of peptides in foods, such as sour, sweet, bitter, salty, and fresh tastes, result from differences in peptide chain length, amino acid composition, and arrangement structure. Taste peptides in food improve or conceal the sensory characteristics of foods that contain various tastants, thereby influencing flavor (Kong et al., 2019). So far, research on edible mushroom flavoring substances has primarily focused on flavoring amino acids, nucleotides, and carbohydrates; however, research on edible mushroom umami peptides and umami-enhancing peptides is limited (Kong et al., 2019). Asp and Glu are similar to monosodium glutamate (MSG), which confers the typical umami taste of mushrooms (Hu et al., 2020). Dipeptides or tripeptides containing Asp (Chen et al., 2022), Glu (Yu et al., 2018), and Gly (Kong et al., 2019) promote the unique taste of umami. Chen et al. (2022) isolated and identified five umami peptides from Stropharia rugoso-annulata mushroom, followed by EPLCNQ (Glu-Pro-Leu-Cys-Asn-Gln, Mw = 702.32, threshold value = 0.178 mmol/L), SGCVNEL (Ser-Gly-Cys-Val-Asn-Glu-Leu, Mw = 720.33, threshold value = 0.174 mmol/L), PHEMQ (Pro-His-Glu-Met-Gln, Mw = 640.28, threshold value = 0.390 mmol/L), SEPSHF (Ser-Glu-Pro-Ser-His-Phe, Mw = 702.31, threshold value = 0.356 mmol/L), and ESCAPQL (Glu-Ser-Cys-Ala-Pro-Gln-Leu, Mw = 746.34, threshold value = 0.167 mmol/L). These results affirm that Glu, Ser, and His might improve the taste of umami by strengthening the hydrogen-bond interactions between umami peptides and their taste receptor, T1R3. A study by Xu et al. showed that tasty peptides ASNMSDL (Ala-Ser-Asn-Met-Ser-Asp-Leu, threshold values = 10.19 mmol/L, umami enhance threshold on MSG = 13.58 mmol/L) and YYGSNSA (Tyr-Tyr-Gly-Ser-Asn-Ser-Ala, threshold values = 12.63 mmol/L, umami enhance threshold on MSG = 18.95 mmol/L) from Volvariella volvacea retain and enhance umami taste (Xu et al., 2019). However, in mushrooms, bitterness is perceived less strongly, indicating that various components, including soluble sugars, polyols, taste amino acids, and taste peptides effectively mask the bitterness of mushrooms, giving them a unique, natural taste.
Edible mushrooms are also rich in nucleic acids, which can be enzymatically degraded into corresponding nucleotides and 5′-nucleotides (5′-GMP, 5′-IMP, 5′-XMP, and 5′-AMP), which contribute to the taste of umami and the palatableness of mushrooms (Mau et al., 2001). Studies have found that relative umami intensities reduce in the order of 5′-GMP > 5′-IMP > 5′-XMP > 5′- 5AMP (Yamaguchi et al., 1971). With other mushroom components, the content and type of 5′-nucleotides varies across species, fruiting body parts, and growing environment (Sun et al., 2020a; Zhang et al., 2013; Zhao et al., 2021). 5′-CMP, 5′-AMP, 5′-GMP, and 5′-IMP have been detected in fresh A. bisporus, with a total 5′-nucleotide content of 5.35 mg/g DW (Beluhan & Ranogajec, 2011). A study on 5′-nucleotides in 10 popular Croatian wild edible mushroom species found the contents of flavor 5′-nucleotides and total 5′-nucleotides to be 0.52-13.88 mg/g DW and 2.01-35.36 mg/g DW, respectively (Beluhan & Ranogajec, 2011). However, the content of flavor 5′-nucleotides in most mushroom species is less than that of amino acids. Flavor analysis found that in most edible mushroom, MSG-like amino acids are the primary umami components, followed by flavor 5′-nucleotides. What's more, free amino acids and nucleotides have synergistic effects to make mushrooms more delicious.
Other mushroom components, such as unsaturated fatty acids (linoleic and arachidonic acids), vitamins, and inorganic ions (Na+ and K+), promote the umami taste of edible mushroom. Organic acids are associated with the metabolic processes of synthetic phenols, amino acids, esters, and aromatic substances. Such components directly or indirectly affect the flavor of edible mushroom due to the differences in their types and contents. The higher the content, the stronger the determining effect on the flavor of edible mushroom, but some flavor components with low content will also affect the final flavor. Inorganic ions, including Na+ and glutamic acid form sodium glutamate, and sodium succinate is also formed if succinic acid is present. Sodium glutamate and sodium succinate are both important modulators of flavor. However, because they are rich in nutrients and water content, fresh edible mushrooms are easily colonized by microorganisms, leading a change in flavor. Four different microorganism species were selected to ferment the pileus and stipe of Lentinus edodes, and it was found that Lactobacillus plantarum was the best species for fermentation providing the strongest umami flavor (Chen et al., 2021). In addition, nucleotide enzymes secreted by microorganisms during fermentation can promote the production of flavors (Sun et al., 2020b). Thus, understanding the composition of edible mushrooms can reveal their nutritional and pharmacological effects, as well as the mechanisms regulating their taste.
3 INFLUENCING FACTORS OF EDIBLE MUSHROOMS FLAVOR
During their growth phase, edible mushrooms accumulate various secondary metabolites, leading to flavor diversity. The flavors of edible mushrooms are determined by volatile and nonvolatile compounds and are important determinants of the quality and public acceptance of edible mushrooms (Fang et al., 2021). However, mushroom quality and flavor deteriorate rapidly after harvest (Fang et al., 2021; Zhang et al., 2018b). Flavor variation in mushrooms is a dynamic process influenced by factors including storage time, preservation method, microbial spoilage, metabolic changes after harvest, and processing method (e.g., enzymatic hydrolysis, Maillard reaction, drying, and cooking) (Fang et al., 2019; Lin et al., 2017).
3.1 Effect of physiological metabolism on the flavor of edible mushrooms
Because flavor is an important quality of agricultural products, producers regulate it using various strategies to maximize the production or retention of flavor, including breeding, cultivation, and postharvest processing (Nicolaï et al., 2008). Several factors affect the volatile and nonvolatile components of fresh products, including species, respiration, maturation stage, enzymatic activity, and external factors, that is, storage time, preservation method, ambient temperature, and microbial growth (Zhang et al., 2013). Notably, mushrooms have a higher respiration rate than other fresh products. Their endogenous metabolic enzymes, including deoxyribonucleases, proteases, and ribonucleases are activated upon harvest, leading to the hydroxylation of MSG-like amino acids and the release of free 5′-nucleotides from proteins (Hu et al., 2020; Liu et al., 2014). Packing mushrooms together with 1-methylcyclopropene (1-MCP) slows down mushroom respiration in different headspace compositions and the best effect is achieved by combining 1-MCP and medium permeable film, which ensures gas concentration levels of < 0.1% O2 and 5-10% CO2 (Sun et al., 2020a). This alters the process of flavor nucleotide formation, thereby improving the umami taste of mushrooms (Figure 2A).
Storage of fresh produce in changed atmospheres, for example, a controlled atmosphere (CA), can induce metabolic changes in flavor compounds (Nicolaï et al., 2008). Over a 19-day storage period, storing Agaricus bernardii in a controlled and equilibrium-modified atmosphere changed the varieties and contents of its volatile compounds quantitatively and qualitatively. Specifically, the content of alcohols, aldehydes, hydrocarbons, and esters increases during storage, whereas the levels of ketones decrease (Wang et al., 2021). Furthermore, lower O2 (15%) levels limited metabolic activities in mushrooms, while CO2 (5%) accumulation in the packing protected them from decay reactions (Gholami et al., 2017). Figure 2B showed a study on the button mushroom that high CO2 package treatment maintained levels of 1-octen-3-ol, increased its antioxidant capacity, and reduced the browning index (Lin et al., 2017), which preserved the appearance and flavor of button mushrooms during postharvest storage. Finally, negative air ions improve the contents of ATP and ADP, maintain a relatively stable energy charge level, promote energy utilization, and improve the quality of L. edodes during storage (Zhang et al., 2021). In addition to modified atmospheric packaging, packaging materials prepared with natural or chemical ingredients have a greater impact on the flavors of edible mushrooms. Coating fresh shiitake mushrooms with a polysaccharide isolated from Oudemansiella radicata (ORWP) improved their nutritional value and increased the contents of key monosodium glutamate-resembling amino acids, umami 5′-nucleotides, and 1-octen-3-ol (Liu et al., 2021b). The use of polyethylene glycol diglycidyl ether (PGDE) as a cross-linking agent to prepare γ-polyglutamic acid (γ-PGA) hydrogels after coating the surface of shiitake mushrooms enhanced the good sensory qualities (Tao et al., 2021).
Nanocomposite-based packaging (NP) technology is a potential alternative for active packaging associated with low respiration rates and slow metabolic processes (Shi et al., 2018). NP treatment reduces the physiological obstacles caused by anaerobic respiration and inactivates key enzymes to prevent excess oxidation or degradation of flavor components (Yang et al., 2019). Due to the antibacterial properties of active nanoparticles, the presence of nanosilver and nanotitanium dioxide in NP materials also inhibits microbial growth in the late stages of mushroom storage and also affected the content of flavor substances to a certain extent (de Azeredo, 2013). As a result of the developed NP postharvest treatment for Volvariella volvacea, browning issues and respiration rate were reduced (Figure 3Aa). In contrast with the control, straw mushrooms treated with NP better retained their flavors (Figure 3A) (Fang et al., 2019). In a previous study, NP-treated Flammulina velutipes similarly maintained higher levels of 5′-nucleotide and reduced the loss of umami to a certain extent during storage at 4 ± 1°C (Fang et al., 2016). Moreover, Nano-PM regulated oxygen and carbon dioxide levels, inhibited microbial growth, and beneficially decreased the metabolism rates of postharvest mushrooms, maintaining a good sensory attributes, and preventing physiologic changes. Fang et al. (2021) showed that NP maintained the relatively high umami taste compared with the control of Flammulina filiformis (Figure 3B). This might be because NP provided an adequate supply of energy during cold storage in postharvest mushrooms, contributing to a better umami taste (Li et al., 2021; Zhang et al., 2019).
Plant cells require sufficient energy levels to delay senescence, and maintain their quality and important physiological functions. Therefore, cellular energy levels play an important role in maintaining the quality of fruits, vegetables, or mushrooms and in extending postharvest storage and shelf life (Lin et al., 2018). Yan et al. (2020) reported that major taste components of white Hypsizygus marmoreus (H. marmoreus), including 5′-nucleotides (5′-GMP and 5′-IMP), succinic acid, and mannitol, maintained their higher levels in nanocomposite-based packaging materials. NP caused mitochondrial microstructure breakdown and ATPase activity to decrease, resulting in inadequate energy supply to maintain higher energy status by hydrolyzing ATP. In other words, NP effectively maintained the taste components of white H. marmoreus by regulating postharvest energy metabolism.
Moreover, microorganisms metabolize substances in food, conferring the corresponding fermented food a unique taste and flavor, and even having multiple effects on human health (Ding et al., 2019; Lao et al., 2020). Chen et al. (2021) analyzed and compared umami substances in fermentation liquid and found that all four species (Saccharomyces cerevisiae, Aspergillus oryzae, Aspergillus niger, and Lactobacillus plantarum) improved the flavor substances of the shiitake mushroom. L. plantarum had the greatest influence on the flavor of L. edodes.
In summary, postharvest preservation methods of mushrooms significantly affect their flavor, which is depicted in their physiological effects, respiration rates, energy metabolism, and microbial activities.
3.2 Effects of different processing or chemical reactions of edible mushrooms on flavor
Regarding food quality, food flavor is a key reference point for consumers. However, excess intake of monosodium glutamate with sodium glutamate as the main umami substance can cause obesity and diabetes by engaging the same purine nucleotide degradation pathway also activated by fructose and salt consumption (Andres-Hernando et al., 2021). Because of its unique culinary flavor and unparalleled medicinal value, the edible mushrooms has attracted huge market attention. At present, the naturalization, nutrition, and functionalization of condiments using edible mushrooms as raw materials pose a challenge to traditional eating habits. Dietary concept reforms are an inevitable consequence of social development. Edible mushroom seasoning products have recently emerged. They are nutritious, delicious, and have excellent polysaccharide, protein, and other nutrient levels, as well as good water solubility and stability. Mushroom functional compound condiments have occupied a relatively important position in the current condiment market, which is widely consumed and has a good effect and prospect in condiments and food, due to their natural, delicious, and healthy characteristics. Although the number of edible mushroom seasoning products on the market is increasing, most are crudely processed. They cannot release the flavor and taste of edible mushroom with simple processes. As a consequence of the premature research and processing technologies, it is easy to introduce an unpleasant taste to consumers. Some products contain lignified ingredients, with poor water solubility and low quality. Therefore, a comprehensive analysis of the influence of different processing technologies or chemical reactions (including drying, cooking, enzymatic hydrolysis, and Maillard reactions among others) on edible mushroom flavor will inform advances in technology and standardization of the mushroom industry.
3.2.1 Drying treatment
Similar to other perishable foods, mushrooms readily deteriorate during storage, a phenomenon attributed to their high moisture content (about 90% wet basis). To overcome this challenge and improve the sensory qualities as well as characteristic flavors, drying, convenient and effective procedures in the food industry are currently applied to mushrooms (Boy et al., 2019; Li et al., 2019; Liu et al., 2019). Zhang et al. (2018a) observed that drying increases the complexity of volatile compounds, thereby significantly changing the flavor profile of porcini. Dried samples exhibited more desirable roasted and seasoning-like flavors and fewer grass-like and earthy notes (Figure 4A).
Different drying techniques have vital effects on the flavor characteristics and sensory qualities of mushrooms. Hou et al. (2021) revealed that levels of C8 alcohols and C8 ketones of L. edodes markedly decreased after three drying treatments (hot air-drying (HD), vacuum freeze-drying (VFD), and VFD combined with HD (VFD-HD)). Specifically, hot air-drying (HAD) caused a significant loss of volatile compounds, reduced amounts of sweet FAAs and 5′-nucleotides (5′-AMP), as well as high amounts of bitter FAAs. Freeze-drying (VFD) and VFD combined with HD (VFD-HD) are beneficial for the retention of these volatile compounds. VFD-HD samples are strongly associated with umami, saltiness, and astringency. The umami intensities of VFD-HD mushrooms are comparable to those of HD samples and significantly higher than those of VFD ones (Figure 4B). According to another study (Luo et al., 2021), compared to mushrooms subjected to HAD and VFD, those subjected to air-impingement jet drying (AID) substantially increased their contents of volatile sulfides. Besides, AID increased sweet and umami amino acids to enhance the characteristic flavors of dried L. edodes by partially suppressing enzymatic and Maillard reactions (Figure 4C).
In a few studies, drying caused severe losses of alcohols, aldehydes, and ketones, possibly via thermal decomposition and oxidation (Misharina et al., 2010; Tian et al., 2016; Zhang et al., 2018a). On the other hand, several studies show that ketone and aldehyde levels increased in dried mushrooms (Misharina et al., 2010), which could be attributed to different drying periods throughout the process (Yang et al., 2016). In contrast with fresh mushrooms, the drying process also increases the varieties and quantities of nitrogen-containing and sulfur-containing compounds, particularly pyrazines, furans, and pyrroles (Misharina et al., 2010). This may be due to the chemical reactions of high amounts of the proteins and reducing sugars in edible mushrooms. Increased levels of Maillard reaction products, Strecker degradation products, and phenolic compounds and changes in alcohol, aldehyde, and ketone levels caused desirable roasted and seasoning-like aromas of dry edible mushrooms. In conclusion, flavor quality and overall aroma impressions of dried mushrooms by different drying methods were mainly evoked by different varieties of odorants, including volatile components, flavor profiles, aroma, and taste, which are important for edible mushroom sensory quality.
3.2.2 Cooking treatment
Mushroom consumption dates back to ancient times. From a culinary standpoint, mushrooms are part of most global cuisines either as main parts or as ingredients due to their taste components, aroma profiles, texture, and color properties (Selli et al., 2021). Mushrooms are an alternative to low-calorie and low-salt diets and contribute to flavors due to the presence of umami components (Mena García et al., 2021). Notably, taste compounds, or flavor precursors naturally occur in raw mushrooms. Multiple factors may affect the levels of taste compounds. The effects of cooking on flavor profiles vary depending not only on mushroom samples, but also on the methods of pretreatment (soaking in water), cooking (stir-frying, steaming, frying, boiling, and roasting), and storage (at room temperature or refrigerated). At certain temperatures (Figure 5), cooking promotes chemical reactions to varying degrees, such as the Maillard reactions of endogenic chemical components of sugars and amino acids.
Li et al. (2011) reported that the flavor of mushroom soup generated from button mushroom powder is dependent on the cooking method, with free amino acid and 5′-nucleotide levels in mushroom soup being higher in microwaved soup than in boiled or autoclaved soup. They also found a high number of aroma-active volatile compounds in the boiled mushroom soup. Analysis of the primary aroma-active compounds in mushroom soup revealed that boiled, autoclaved, and microwaved mushroom soup had 13, 10, and 9 aroma-active compounds, respectively. Besides, Sun et al. (2019) found that all four cooking methods (autoclaving, microwaving, sous vide, and stewing) increased polysaccharide, polyphenol, and amino acid levels in Hypsizygus marmoreus, compared with the uncooked soup. Stewing increased the crude protein contents, sous vide increased the nucleotide contents, whereas autoclaving generated the highest levels of polysaccharides (Sun et al., 2019). These variations in flavor factors resulted in characteristic effects on the properties of mushroom soup.
Studies on volatiles, color, key aromas or odorants, phenolics, and antioxidant properties of raw, boiled, and oven-cooked A. bisporus and Pleurotus ostreatus revealed that cooking is a crucial factor for key odorants in mushrooms. This is due to chemical reactions and modified volatiles produced by the evaporation of compounds and chemical reactions of aroma precursors after heat treatment (Selli et al., 2021). Overall, roasted mushrooms had higher intensities of roasted, dark meat, fried aroma, and potato aroma. Conversely, earthy contents and woody flavors decreased once mushrooms were roasted. For instance, A. bisporus (white, crimini, and portobello) from different producing areas showed that crimini lost more aroma and flavor intensities upon cooking, including mushroom and earthy aromas, earthy, hay, soybean, woody, and sulfur flavors, as well as sweetness. Roasted white and portobello mushrooms are also perceived to be saltier than raw, possibly due to moisture loss during roasting (Du et al., 2021).
Cooking mushrooms increases their umami taste and “meat-like” flavors. Mushroom addition enriches the composition of volatile substances in the beef paste. Due to the dilution of volatile compounds in mushrooms, not all volatile substances in meat increased with the addition of edible mushrooms (Qing et al., 2021). A study proposed a method for replacing lean pork meat with L. edodes from a sensory perspective, all modified sausages were considered acceptable (Wang et al., 2019). Also, freeze- or oven-dried winter mushroom powder is a partial substitute for phosphates in beef patties (Jeong et al., 2021). In general, interactions between meat and mushrooms modulate enrichments of volatile compounds in a mixture (Qing et al., 2021). After adding the mushroom toppings to an egg, before roasting and steaming, dominant sensory attributes shifted to mushroom-based flavor characteristics (Muniz et al., 2021). In brief, regardless of mushroom types, cooking has a significant impact on mushroom aroma and flavor sensory profiles.
3.2.3 Enzymatic hydrolysis and Maillard reactions
Mushrooms are highly consumed because of their flavors and tastes (Liu et al., 2021a; Liu et al., 2020a; Zhang et al., 2018c). Enzymatic hydrolysis is a fundamental technical point of the processing technology of edible mushroom seasoning products. Through enzymatic hydrolysis technology, the cell wall is destroyed to release the substances inside the cells, and the protein is hydrolyzed into amino acids. Through the Maillard reaction and other sequential processes, flavoring materials such as mushroom soy sauce and mushroom chicken essence are made with the fresh flavor of edible mushroom. However, the technical guidance for enzymatic hydrolysis of edible mushrooms has not been unified, and mushroom enzymatic hydrolysis flavor analysis has no uniform standard, which makes the development of the mushroom condiment industry difficult to scale and standardize.
Through enzyme-assisted extraction, studies have extracted the umami taste and total free amino acids from six different mushrooms. Enzyme-assisted extraction is a promising method for improving the recovery of MSG-like amino acids from mushrooms. The type of enzyme and various parameters are crucial (Figure 6A) (Poojary et al., 2017). Gao et al. (2021) reported that peptides below 3 kDa have the highest correlations with umami and salty flavors, whereas peptides in the range of 3-10 kDa are associated with bitterness and astringency (Figure 6B).
A relatively small number of studies have evaluated flavor as a whole, with most of them focusing on the optimization of enzymatic hydrolysis conditions as the main research direction. Comprehensive analysis is necessary to discuss the biological activity, potential biomass resources (such as solid biofuels), etc. (Chen et al., 2021; Chen et al., 2020; Mamimin et al., 2021). Enzymatic hydrolysis of edible mushrooms has a greater impact on flavor. Insufficient or excess hydrolysis easily introduces bad flavors, such as bitterness. Moreover, it might conceal the umami flavor rich in edible mushrooms. The specificity of enzymes with diverse cleavage sites and properties also leads to differences in the applicable enzymes of different mushrooms.
After enzymatic hydrolysis, the reducing sugars and amino acids produced by edible mushroom are susceptible to Maillard reactions (the amino-carbonyl reaction), generating O, N, and S heterocyclic compounds, including pyridines, pyrazine, furan, pyranne, and pyrrole compounds. They are responsible for thermal processing flavor and brown formation during processing and storage, thereby promoting the mushrooms to produce baked and roasted flavors (Lotfy et al., 2021). Maillard reaction products from mushroom hydrolysates produced by heating with d-xylose and l-cysteine have been extensively studied. MRP forms typical mushroom flavor compounds (including 1-octen-3-ol, 2-octen-1-ol, 3-phenylfuran, 2-octylfuran, nonanal, benzaldehyde, (+)−2-bornanone, 2-thiophenecarboxaldehyde, 2,5-thiophenedicarboxaldehyde, and 3-methylbutanal, etc.), significantly improves mushroom flavor intensities, and creates new flavor categories (Chen et al., 2018). In summary, flavor compounds can be highly enhanced by Maillard reactions relative to enzymatic hydrolysis. In addition, the Maillard reaction plays an important role in the production of flavor compounds.
4 EDIBLE MUSHROOM MYCELIUM FLAVORS
Mushroom fruiting bodies have been used as food and food flavoring materials for centuries because of their unique and subtle flavors. However, fruit body production via solid cultures requires a long period. Mycelium culture becomes a promising option for obtaining effective substances that can be successfully utilized in food production. They are even thought to be more efficient than solid culture propagation, as mycelium can be produced in a compact space and in a shorter time, and is less susceptible to outside contamination (Das et al., 2015). Based on the literature on the comparison of nutrition and nutritional value potential between mycelium and fruiting bodies, mycelium is known to have a high protein content (20-30%) (Ulziijargal & Mau, 2011). A comparison of the chemical constituents of fruiting bodies produced on cotton straw and mycelial pellets of Pleurotus ostreatus revealed several similarities in total nitrogen, protein, glycogen, fatty acids, RNA, and ash contents. Despite the similar total fatty acid contents, there are additional saturated fatty acids in the mycelium (Hadar & Cohen-Arazi, 1986). Further, higher content of total organic acid in the mycelium of Pleurotus eryngii and Lentinus edodes were found as compared to its fruiting bodies (Wang et al., 2016). But in some studies, due to the different fermentation methods of mycelia and fruiting bodies, relative to mycelia, fruiting bodies had higher levels of MSG-like free amino acids, flavor 5′-nucleotides, and the values of equivalent umami concentrations in three cultivated mushrooms (Pleurotus eryngii, Agrocybe aegerita, and L. edodes), respectively. Comparable findings were reported by Hsu et al. (2002), who studied Cordyceps militaris mycelium, and Lee et al. (2009), who studied Hypsizygus marmoreus. Fruiting bodies exhibited more taste characteristics than mycelia, which might be one of the factors restricting the development of the mycelial industry. In addition, mushrooms are mainly used as cooking materials in daily life, and the overall sense of mycelium is not as good as that of fruiting body. And most importantly, the aging and backward technology and equipment of agricultural product processing enterprises is an important factor restricting the rapid development of edible mushroom processing industry. In spite of this, mycelium still has a wide range of applications. Based on the above-mentioned mycelial characteristics and advantages, mycelium can be used to partially replace mushroom fruiting bodies to make products, which compensate for the shortcomings of the fruiting body. The development of valuable and effective cellular or extracellular substances from submerged mycelium culture can be used for the development of a variety of foods (Liu et al., 2020c; Rathore et al., 2019; Shih et al., 2007). Rathore et al. (2019) used discarded Cordyceps militaris (C. militaris) solid culture medium to ferment liquid vinegar instead of rice and found significantly improved vinegar flavor and quality. Moreover, meat analogs with mushroom mycelium have better textural properties, including higher hardness, springiness, chewiness, and preferable umami characteristics compared to meat analogs with soy proteins (Kim et al., 2011). A sweet and sour nutrient-rich fermented C. militaris beverage with less bitterness was obtained via enzymatic hydrolysis and fermentation (Lao et al., 2020). Ulziijargal et al. (2013) found that substituting 5% of the wheat flour in the bread formula with mushroom mycelium did not adversely affect the texture profile and organoleptic properties of bread. Highland barley was fermented with Cordyceps militaris, Stropharia rugoso-annulata, Morchella esculenta, Schizophyllum commune, and Tremella sanguinea mycelium, and it is found that fermentation with mushroom mycelium was able to change the flavor profile of highland barley, decreasing in hexanal, decanal, and 2-pentylfuran (the original strong grass flavor) and obtain new flavor (floral, sweet, and mushroom fragrance) (Wang et al., 2022). Therefore, incorporation of mycelium in the formulation of different conventional foods will provide beneficial effects. Better properties of the culture medium and autolysis when dissolved oxygen in the pellets drops below the critical limit enhance cell metabolism, resulting in a maximum synthesis of flavor compounds. Submerged fermentation of mushrooms ensures and enhances the production of biomass with high-value taste and aroma, which can be extracted from mycelium and used at the industrial level (Bakratsas et al., 2021; Rathore et al., 2019). Therefore, flavor components extracted from the mycelia of a few edible mushrooms have broad industrial application prospects.
5 CONCLUSION AND FUTURE PERSPECTIVES
Studies have evaluated the flavor substances of edible mushrooms, their mycelium, and their production mechanisms. We summarized the taste-producing substances of edible mushroom (volatile and nonvolatile flavor substances) and compared and analyzed the roles of various substances in the flavor of edible mushroom. The application of these key compounds and their effective regulation or release have always been a research hotspot in the development of edible mushroom flavors. In addition, the paper summarized the influence of different processing or chemical reactions on flavor. Drying, cooking, enzymatic hydrolysis, and the Maillard reaction would cause the loss of flavor or the generation of new substances. The identification of key flavor substances and flavor-influencing factors will help guide industrial development. Finally, some challenges to edible mushrooms flavor were introduced. Studies on edible mushroom flavors are associated with various limitations, including a small number of varieties. At present, there are many studies on wild edible mushroom, but the flavor utilization of some common mushroom is lower, and there is a lack of deep processing technologies. Therefore, there is no uniformly standardized processing method for mushrooms, which greatly restricts the development of mushroom utilization. The development of edible mushroom is likely to involve the following research directions: (1) Even though the content of flavoring substances in the mycelium of some edible mushroom is lower than that in fruiting bodies, the mycelium meets the requirements for modern industrialization of edible mushroom and has unparalleled advantages. Therefore, it is necessary to investigate and promote the applications of taste-producing substances in mycelium. (2) Edible mushroom are delicious. Whether fried or cooked, they exhibit different flavors. Is it possible to construct a fingerprint of the flavor of edible mushroom to further enhance the richness of the diet? That's a question for future research.
AUTHOR CONTRIBUTIONS
Chunping Jiang: methodology; formal analysis; visualization; writing – original draft. Xiaoyu Duan: methodology; formal analysis; visualization; writing – original draft. Lin Lin: conceptualization; methodology; funding acquisition. Wenjuan Wu: supervision. Xiaolin Li: resources. Zhen Zeng: validation; supervision. Qingying Luo: validation; conceptualization. Yuntao Liu: conceptualization; supervision; validation; funding acquisition.
ACKNOWLEDGMENTS
The authors thank Home for Researchers editorial team (www.home-for-researchers.com) for polishing and editing the article.
CONFLICT OF INTEREST STATEMENT
The authors declare that they have no known competing financial interests or personal relationships that could influence the work reported in this paper.