Healthy function and high valued utilization of edible fungi

Yanrong Zhang, Dawei Wang, Yuetong Chen, Tingting Liu Shanshan Zhang, Hongxiu Fan, Hongcheng Liu, Yu Li*

a School of Food Science and Engineering, Jilin Agricultural University, Changchun 130118, China

b Scientifi c Research Base of Edible Mushroom Processing Technology Integration of Ministry of Agriculture and Rural Affairs, Changchun 130118, China

c Engineering Research Center of Grain Deep-processing and High-effeciency Utilization of Jilin Province, Changchun 130118, China

d Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun 130118, China

Keywords:Edible fungi Functional components Processing and utilization High valued utilization

ABSTRACT Edible fungi are large fungi with high added value that can be utilized as resources.They are rich in high-quality protein, carbohydrate, various vitamins, mineral elements and other nutrients, and are characterized by high protein, low sugar, low fat and low cholesterol.In addition, edible fungi contain a variety of bioactive substances, such as polysaccharides, dietary fiber, steroids, polyphenols, and most of these compounds have antioxidant, anti-tumor and other physiological functions.This review comprehensively discusses the bioactive components and functional characteristics of edible fungi (such as antioxidant, anti-aging, hypolipidemic activities, etc.).Then the recent developments and prospect in the high-valued utilization of edible fungi are discussed and summarized.The objective of this review is to improve the understanding of health-promoting properties of edible fungi, and provide reference for the industrial production of edible fungi-based health products.

1.Introduction

Edible fungi are a kind of large fungus that can form large fl eshy or colloidal of fruit bodies or sclerotia tissues.They have long been used as food and folk medicine in different parts of the world due to their nutritional composition, pleasant taste and flavour [1,2].More than 2000 species of edible fungi exist in nature, and around 200 species are commercially or experimentally cultivated [3].20 species of them have been cultivated on an industrial scale, such asAgaricus bisporus,Lentinus edodes(shiitake),Pleurotusspp.(oyster mushrooms),Auricula auricula,Flamulina velutipes,Volvariella volvacea, etc.[4].Edible fungi can be divided into edible species and medicinal species according to their primary applications.For instance, shiitake,Flamulina velutipesand oyster mushroom are used in our daily diet, whileGanoderma Lucidum,Cordyceps sinensisare commonly used as herbal medicines [5].Edible fungi have a great nutritional value since they are rich resources of protein, dietary fiber, essential amino acids, vitamins and minerals and relatively low in fat and calories [6].Relevant studies confirmed that edible fungi contained a variety of biologically active compounds, such as polysaccharides [7], alkaloids [8], steroids [9], polyphenols [10], etc.M ost of these compounds are responsible for the biological activities of edible fungi including antioxidant [11], anticancer [12], anti-aging [13], hypolipidemic [14], immunoregulatory activities [7], as well as regulations of blood sugar and blood pressure [7,15].Nowadays more and more researchers indicated that there is not an easy distinction between edible and medical mushrooms because many of the common edible species have therapeutic properties and several used for medical purposes are also edible [14,16].

In recent years the consumption of edible fungi has increased as people become more aware that a healthy and balanced diet exerts a key role in normal body functioning and in sustaining health.As an estimate, the global mushroom market consumption is around 12.74 million tons in 2018, which is expected to reach up to 20.84 million tons by 2026 [17].The higher market growth rate of edible fungi is due to their increasing acceptability for nutraceutical and medicinal purposes.

With the expansion of the global edible fungus industry, the commercial production and distribution of edible fungi have increased significantly.Scholars have deepened the researches on the biologically active components and functional characteristics of edible fungi and their by-products.The high value-added utilization of edible fungi has become a new hot spot and new trend in recent years.However, a systematic and comprehensive review on the nutritional components and functional properties as well as the high-valued processing and utilization of edible fungi is still lacking.Therefore, the present review will present an overview in the active constituents and functional characteristics of edible fungi and recent developments in the high value-added utilization of edible fungi.The objective of this review is to provide theoretical reference for the applications of edible fungi in functional foods, pharmaceuticals, cosmetics or environmental-friendly materials.

2.Nutritional and functional components of edible fungi

Edible fungi are considered as a healthy food since they are rich in bioactive compounds including polysaccharides, dietary fibers, proteins, essential amino acids, vitamins, mineral elements, terpenoids, steroids, adenosine derivatives.These bioactive components have become popular sources of natural antioxidative, antitumor, anti-aging, hypolipidemic and immunomodulatory agents.Currently, edible fungi components of polysaccharide, triterpene, and adenosine are the top three efficacy components in the approved health foods [18].

2.1 Polysaccharide

Edible fungus polysaccharides are one of the promising health compounds with excellent nutritional and therapeutic properties.One of the main edible fungus polysaccharides isβ-glucan, in which the main chain is a comb-like structure and is composed ofβ-(1-3)-linked glucose groups, and theβ-(1-6) linked glucose groups randomly distributed along the main chain [19].The biological activities of edible fungi polysaccharides are found to be dependent on the type, molecular weight, branching, and structural conformation of polysaccharides, and these polysaccharides exert different biological activities through interactions with different receptors.Chen et al.[20]isolated edible fungus polysaccharides from 8 mushrooms includingFlammulina velutipes,G.lucidum,Hericium edodes,Pleurotusspp., shiitake,Pleurotus eryngii, etc.They found that all the polysaccharides in edible fungi had strong antioxidant activity, especially the polysaccharides inG.lucidumand shiitake.Zhang et al.[21]found that theTremella fuciformispolysaccharides extracted by hot water was mainly composed of mannose and uronic acid, and these polysaccharides could resist ultraviolet rays and prevent skin aging effect by inhibiting the protection of lipid peroxidation antioxidant enzymes.Zhang et al.[22]found that the lentinan polysaccharides could enhance the killing effect on tumor cells by regulating the immune function of the body.Polysaccharides extracted from black fungus, which was mainly composed of glucose (72%), fructose (10%), xylose (10%) and mannose (8%), could increase the blood and heart antioxidant enzyme activities and improve heart function parameters, e.g.left ventricle ejection fraction and left ventricular short axis fractional shortening [23].A new polysaccharide isolated fromG.lucidumnamed PSG-1, was shown to promote anti-tumor activity through mitochondrial-mediated apoptosis [24].Moreover, some studies demonstrated that edible fungus polysaccharides exerted anti-diabetic activity by preventing cell oxidative stress, promoting islet cell regeneration, increasing glucose consumption and glycogen biosynthesis, and preventing other complications related to diabetes [25-27].Other biological activities of edible fungi polysaccharides include treatment of arteriosclerosis, anti-inflammatory, painremoving, rheumatism dispelling, blood pressure lowering, cough relieving and detoxification [14,28-30].The functional properties of polysaccharides from common edible fungi are summarized in Table 1.Edible fungus polysaccharides are one of the most popular functional compounds mainly due to its wide variety of biological activity.Therefore, production and utilization, especially for food and nutraceuticals applications of edible fungus polysaccharides will have broad application prospect and large economic and social value.

Conventional extraction methods and a wide range of advanced extraction techniques are available nowadays for the extraction of these bioactive polysaccharides from edible fungi.Conventional edible fungi polysaccharide extraction methods generally involve the use of water or chemicals (alkalines or acids) as the extractant along with high temperature [31].Polysaccharides extracted from 4 edible fungi includingGanoderm lucidum,Grifola umbellate,Volvariella volvaceaandTremella fuciformisusing hot water extraction (HAE) had superoxide and hydroxyl radical scavenging activities [32].Alkaline- or acid-extraction are usually carried out after HAE to maximize the recovery of polysaccharides from edible fungi.Acid and alkaline treatments cause destruction and degradation of cell walls and coarse-fiber structure, allowing the release of intracellular polysaccharides and extraction of the acid- and the alkali-soluble fraction [31,33].Polysaccharides fromPleurotus ostreatuswere successively extracted with hot water and 1 mol/L sodium hydroxide/sodium borohydride solutions.The results showed that the yield of alkaline extraction step was higher than that of the hot water extraction, and the polysaccharide from the alkaline extraction step contained branchedβ-(1-3)/(1-6)-glucans with triple helix conformation [34].There has been a rapid development in advanced extraction technologies focusing on the extraction of polysaccharides from edible fungi, such as ultrasonic-assisted extraction (UAE), microwave-assisted extraction (MAE), ultrahigh pressure-assisted extraction (UPE), enzyme-assisted extraction (EAE), and electric field-assisted extraction (PEFAE) [31].These extraction technologies have the advantages of being environmentally friendly, less processing time and high extraction yield.Alzorqi et al.[35]extractedβ-D-glucan fromGanodermamushroom using HAE and UAE.The content ofβ-D-glucan by UAE extraction (44.42 mg/g) was higher than HWE (37.73 mg/g).In addition, the UAE process has a significantly lower energy consumption up to 12-fold (0.6 and 7.2 kWh) with a higher extraction rate due to much shorter operating time (1 and 16 h).Gil-Ramírez et al.[36]extracted polysaccharide-enriched fractions (PEF) from 13 mushrooms using MAE.The yields of obtained PEFs from the mushrooms includingAuricularia auricula,Agrocybe aegerita,Amanita caesarea,Boletus edulis,Cantharellus cibarius,Cantharellus cornucopioides,Cantharellus lutescens,Cantharellus tubaeformis,Hypsizygus marmoreus,Lactarius deliciosus,Morchella conica,P.eryngiiandPleurotus pulmonariusranged between 12.1% and 44.2%, and the polysaccharide content for these mushrooms were in the range of 51.1%-68.2%.Parniakov et al.[37]compared extracts ofA.bisporusobtained from different extraction methods: pressure extraction (PE), pressure extraction assisted by pulsed electric field (PEF) and HAE, and the results indicated that the combination of PE and PEF treatments seems to be rather promising for production of clear mushroom extracts with high colloid stability and high contents of fresh-like proteins and polysaccharides.It is expected that these advanced extraction technologies will be gradually used in extraction of mushroom polysaccharides in the near future, and the extracted edible fungi polysaccharides have a good prospect of application in health care foods and medicine.

2.2 Dietary fiber

Edible fungi are a rich source of dietary fiber (DF) that have various beneficial health effects.The DF of edible fungi was mainly composed ofβ-glucans, chitin, hemicellulose and mannans.β-Glucan is a major component in edible fungus DF and it exists in both soluble and insoluble edible fiber fractions.There is a large variation in the DF content of edible fungi among different species.Previous studies showed that the total DF contents ofPleurotus tuber-regium,grifolaandporiawere in the ranges of 79.9%-81.7%, 71.5%-85.9% and 96.3%-96.5%, respectively [66].Xue et al.[67]found that the total DF in shiitake account for 49.5% of the dry weight and it exhibited excellent water-holding capacity (5.7 g/g) and oil holding capacity (3.1 g/g).Consumption of edible fungi as part of our daily diet can easily provide 25% of the recommended dietary intake of DF.DF is one of the most important components in edible fungi and have a number of biological activities.The beneficial health effects of edible fungi DF that have been studied include immune-enhancing, antitumor activities as well as blood glucose, blood lipid and blood cholesterol attenuation [68-72].Zhang et al.[73]obtained edible fungi DF with hot alkali fromPleurotus tuber-regiumand they found that theedible fungi DF belongs toβ-glucan type, with average molecular weight ranging 1 × 104-42.2 × 104Da.In vitroexperiments showed that the alkaline-solubleβ-glucans were found to be effective in inhibiting tumor proliferation at 3 concentrations (50, 100, and 200 μg/mL) toward the tumor cell lines.Xue et al.[74]investigated the structure and hypolipidemic effects of 3 soluble DFs extracted fromLentinula edodes, and the result showed that at the concentrations of 50, 200 and 4000 mg/mL, the soluble DF was found to have effective inhibitory effect on lipids accumulation of HepG2 cells and on pancreatic lipase, which could provide theoretical guidance for obesity treatment.

Table 1 Biological activities of edible fungus polysaccharides.

The main dietary fiber preparation methods are the removal of non-DF components including protein and starch by enzymatic hydrolysis.Soluble dietary fiber (SDF) is extracted by water or by other aqueous solution, and the insoluble residue was recovered as insoluble dietary fiber (IDF) [66].Moreover, some physical processing techniques such as extrusion, high-pressure, microwaving, etc., cause the destruction of cell walls and degradation of dietary fiber structure, converting water IDF into water SDF [75,76].High pressure extraction was applied to extract SDF fromL.edodesbyproducts, and the SDF yield was 13.06%, which was higher than those fromA.bisporus(1.42%) andAgrocybe chaxingu(6.70%) [77].Xue et al.[75]reported that extrusion treatment improved the SDF content and changed the physicochemical and functional properties of DF fromL.edodes.The glucose adsorption capacity and bile acid retardation index of the extruded DF fromL.edodesincreased 0.46 mg/mg and 28%, respectively, suggesting that the DF ofL.edodesobtained with the extrusion treatment might be used as a potential ingredient in functional foods.Nowadays the DF of edible fungi is underutilized, given that many edible fungi species have not been studied.With advances in molecular biology, the structure and bioactivity of edible fungi DF, especially chitin, hemicellulose and mannans, will be elucidated more clearly.It is anticipated that industrial production of mushroom DF and high fiber products enriched with mushroom DF will be developed.

2.3 Protein and amino acids

Edible fungi are significant sources of proteins.The protein content of edible fungi is 19%-40% on dry basis, which is higher than that of most vegetables.During the past few years, a large number of proteins with interesting biological activities have been discovered and isolated from edible fungi, such as lectins [78], fungal immunomodulatory proteins (FIP) [79], ribosome inactivating proteins (RIP), antimicrobial or antifungal proteins, ribonucleases, and laccases [80,81].The frequently used protocol for isolating and purifying edible fungi proteins are as follows: edible fungi was extracted with buffer solutions, then the extracted crude protein was further purified by ammonium sulphate precipitation, ultrafiltration membranes, dialysis, ion exchange chromatography (DEAEcellulose, SP-Sepharose, etc.), affinity chromatography (Affi-gel blue gel, fetuin-Sepharose, etc.) and gel filtration chromatography [78,80,82,83].Although increasing reports are available for the isolation, purification and functions of edible fungi proteins, these isolation methods of protein usually take long time and is low yield and high cost.Thus it is very important to develop new methods for mass production of these bioactive proteins.

Edible fungus protein also contains all kind of amino acids, and the eight essential amino acids take up 25%-45% of the total amino acids.Previous studies showed that lysine and leucine were present in high amounts in edible fungi, whereas their contents in grains were low [84].Beluhan et al.[85]investigated the amino acids of 10 popular Croatian wild edible mushroom species, and they found that threonine (8.98 mg/g) and lysine (5.74 mg/g) represented the largest amount of amino acids.Song et al.[86]found that the free amino acid content inF.velutipeswas up to 20.23%, and the contents of lysine and arginine were significantly higher than those of other mushrooms.Lysine and arginine help to promote children’s physical health and intellectual development, thereforeF.velutipesis known as intelligence enhancing mushroom.Extraction and separation of free amino acids (FAA) from edible fungi are usually accomplished by water extraction or acid extraction methods, followed by methanol deproteinization and chromatography [84,87].Dong et al.[87]extracted FAA from shiitake mushrooms with water for 1 min at 80 °C.The extract was further purified by methanol deproteinization, and a LC-MS/MS method was developed for separation and identification of 20 FAAs in shiitake mushroom.Poojary et al.[88]reported that the highest recovery of FAAs was obtained when mushrooms were extracted with water at room temperature for 180 min.The total FAA contents of shiitake, oyster mushroom, tea tree mushroom, and white, brown and portobello champignons (A.bisporus) obtained by the optimum extraction conditions were 41.4, 77.62, 27.38, 70.30, 92.9 and 80.7 mg/g of dry matter sample respectively.

2.4 Vitamins

Edible fungi are also a good resource of vitamins with high levels of vitamin B2, B1, B12, C, and D, niacin, folates, ergosterol (provitamin D2) [89].The vitamin C content of edible fungi is similar to those of vegetables, and for straw mushroom andH.erinaceusthis value is higher [90].Some edible fungi such asChanterellesandArmillariacontain higher level of vitamin A.The fruiting body of edible fungi, either in their fresh or processed forms, is rich in sterols, which can be converted into vitamin D2by ultraviolet radiation.Some edible fungi includingA.bisporus,L.edodesandPleurotus cystidushave been reported to contain interesting level of vitamin D after exposure to ultraviolet [91].Morales et al.[92]extracted vitamin D-enriched compounds fromL.edodesby supercritical fluid extraction combined with UV-irradiation.The extract containing up to 18% (m/m) ergosterol and other ergosterol derivatives was obtained, and they can be transformed into vitamin D2and vitamin D4by UV light irradiation.Xiong et al.[93]investigated and analyzed the contents of vitamin B1and B2of six kinds of edible fungi collected from Yunnan province, China.They found that vitamin B1and B2are present in high amounts in both wild and cultivated edible fungi.

2.5 Other functional components

In addition to the above components, other bioactive compounds such as mineral elements, ganoderic acid, terpenoids, nucleosides have been identified on a wide variety of edible fungi, and their nutritional and antioxidant activities have been reported.Edible fungi are considered as product rich in mineral elements such as Ca, Fe, K, Mg, Mn, Na and Zn.For instance, the content of potassium inA.bisporuswas found to be 640 mg/100 g dry weight, which could be considered as a good source of potassium nutritious supplementary [94].Shiitake,Agaricus blazeiMurrill, andA.auriculawere reported to have high amount of Zn, Ca and Cu [95], and the fruiting body ofBoletus badiuswas reported not only contained high levels of Ca, Mg and P, which are necessary for the human body, but also contains trace elements such as Zn, Cu and Fe [96].Mineral elements were reported to have important roles in the formation of bones, hemoglobin, and cytochromes, maintaining osmotic pressure and acid-base balance in the body, and acting as cofactors of enzymes.Edible fungus also contains trace elements such as selenium and germanium, which can increase body’s immune function, delay aging, protect the liver and prevent tumors and cardiovascular diseases [97,98].Studies demonstrated that the ganoderic acid isolated fromG.lucidumhad strong biological activities, such as lowering blood lipids, protecting liver, detoxification, as well as antioxidant, antibacterial and anti-inflammatory activities [99].Wasser [100]isolated 14 sesquiterpene compounds from armillaria mycelium, and the sesquiterpene compounds were reported to have many physiological activities, such as anti-tumor, anti-bacterial, anti-inflammatory, antivirus, and hypolipidemic activities.Extraction methods of terpenoids including ganoderic acid from edible fungi include organic solvent extraction, microwave assisted extraction and Soxhlet extraction, using ethanol, methanol, ethyl acetate or petroleum ether as extractant [101].Li et al.[102]reported extraction of ganoderic acids (GA) from the mycelia ofG.lucidumby using 50% aqueous ethanol solution containing 50 mmol/L HCl as extractant.The yield of GA-Mk, -S, -T and -R were 4.53, 3.37, 18.67 and 4.58 mg/g dried mycelia, respectively.Ryu et al.[101]reported the extraction of ganoderic acids fromG.lucidumusing ultrasonic-assisted ethanol-extraction.Under optimized conditions of 64.2-70 °C and 1.2 h extraction time, the highest antioxidant activity and GA content were achieved.Separation and purification of terpenoids generally include column chromatography (silica gel, aluminium oxide, Sehpadex LH-20), high performance liquid chromatography and gas chromatography [103].In addition, adenosine derivatives are regarded as one of the most important active ingredients in many edible fungi such asG.lucidum, shiitake,Grifola gargal, etc.They are reported to reduce blood viscosity, inhibit platelet aggregation, accelerate blood circulation, and improve the ability to supply oxygen to the heart and brain [104].The adenosine derivatives of shiitake include cyclic adenosine monophosphate (cAMP), cyclic guanosine monophosphate (cGMP), and cyclic cytidine monophosphate (cCMP).Among them, the cAMP has been reported to regulate metabolism, inhibit cell growth or promote cell differentiation [105].The adenosine compound isolated fromGrifola gargalcould increase the Glut4trans-location from cytoplasm to the cytomembrane through modulation of PI3K/Akt signal molecules and AMPK phosphorylation in L6 myotubes, thus preventing the post-prandial hyperglycaemia and T2DM [106].Extraction methods of nucleoside compounds from edible fungi include water extraction, ethanol or methanol extraction.The extracted nucleoside solution was further purified by deproteinization and chromatography.Poojary et al.[107]reported extraction of nucleoside compounds from shiitake mushroom, oyster mushroom, tea tree mushroom, and white, brown and portobello champignons (A.bisporus) with water extraction.At the optimum extraction conditions (70 °C, 30 min), the yield of nucleoside compounds for the six mushrooms ranged from 0.92 mg/g to 4.12 mg/g of dry matter sample respectively.

3.Processing and utilization of edible fungi

Due to their valuable nutritional components and excellent functional properties, development of functional foods or pharmaceutical products from edible fungi have gained much attention.Nowadays the processing and utilization of edible fungi can be divided into three stages: in the first stage, edible fungi are sold or consumed in the form of dried and fresh vegetables; in the second stage, edible fungi are processed into convenient foods such as sauces, canned foods or pickled foods; the third stage is the production of edible fungi-based health food, functional food, and pharmaceuticals, as well as comprehensive utilization of edible fungi by-products such as mushroom stalks and mycorrhiza.Studies proved that the value of edible fungi products after deep processing could be improved 3 or 4 times compared with that of the raw material.But nowadays the edible fungi-based products in the Chinese market is mainly primary processed products, such as clean vegetables, low-sugar pickled mushrooms, canned mushrooms, snack food or instant food, etc.

3.1 Preservation of edible fungi

The water contents of many fresh edible fungi species are up to 90%, such as shiitake,A.bisporus[108],Pholiota nameko[109],Volvariella volvacea[110],Pleurotusspp.[111],F.velutipes[112], etc.Such freshly picked edible fungi often quickly soften and become brown during storage, which reduces their market value.In order to avoid the nutrition and sensory losses and extend the storage period of edible fungi, many scientists have studied the preservation technology of edible fungi.Roy et al.[113]and Moda [114]studied the irradiation preservation technique ofA.bisporusandPleurotusspp.mushrooms.They found that under proper irradiation intensity, the loss of nutritional components and fading of mushroom color were decreased and the ripening was inhibited, which kept the freshness and extended the shelf life of mushrooms.Murr et al.[115]found that the protease activity ofA.bisporusshowed an upward trend with storage, and the protease activity decreased with the decrease of temperature, which delayed the senescence and maintained the color and quality of mushroom body.Antmann et al.[116]found that the high and low concentrations of CO2treatment could effectively inhibit the physiological metabolic rate and respiratory intensity of mushrooms, which prolonged the shelf life and increased the market value of the product.Previous studies proved that vacuum pre-cooling was an effect preservation technique for edible fungi.Vacuum precooling not only cooled down evenly and rapidly, but also dehydrated the mushrooms moderately, prolonging the storage period of the products [117].Other preservation technologies have been applied to edible fungi, such as modified atmosphere preservation [118,119]and ozone preservation [120].

3.2 High-valued utilization of edible fungi

In recent years, processing and utilization of edible fungi, especially for health food, functional food and pharmaceutical applications have made great progress, but there is still a lot of room in this research field.In order to realize the high-valued and comprehensive utilization of all edible fungi strains, scholars around the world have conducted a lot of researches, and significant progress has been made in the field of food, medicine, medical biological materials, packaging materials, and animal feed.Edible fungi are mainly composed of fruiting bodies and mycelium.The mycelium could absorb nutritious components and transform the culture material to supply the growth of the fruit body, while the fruiting body could be consumed directly for food or medicinal purposes.High-valued utilization of edible fungi mainly focuses on the specific treatment of edible fungi as raw materials, extraction of the functional compounds, and utilization of edible fungi as functional ingredients in healthy and beauty products as well as environmentally-friendly materials (Fig.1).The market value of edible fungi can be improved by more than 3 times, so the potential market demand and popularity is very huge.Many researchers point out that the edible fungus-based functional foods are one of the top 10 health foods in the 21st century, and many edible fungi-based nutraceuticals and pharmaceuticals such asGanodermachewable tablet,Amillariella melleatablet, liverprotecting tablet and mushroom beverages [121,122]have been put into the market in Asian countries and are favored by many consumers.

3.2.1 High-valued utilization of edible fungi mycelium

Mycelium is the vegetative lower part of edible fungi and could form entangled networks of branching fibers.The mycelium of edible fungi is mainly composed of chitin, cellulose, protein, etc.[123].Researchers have developed many techniques of extracting biological compounds from the mycelium of edible fungi.For instance, they extracted krestin, sizofilan, lentinan from the mycelium cultures of coriolus,Pleurotusspp.andL.edodes, respectively [124].

Fig.1 General flowchart for the main properties of edible fungi and their application in healthy and beauty products as well as environmentally-friendly materials.

In the field of medical biomaterial preparation, the mycelium ofG.lucidumwas used to prepare skin substitutes, and results of the skin trauma test in mice showed that after 30 days the healing effect ofG.lucidummycelium was basically similar to that of the Beschitin drug [125].In addition, edible fungi mycelium is rich in protein, which is an ideal material for animal feed.Some fungal mycelium, such as brewer yeast, can be directly utilized as animal feed without further processing.In order to improve the nutrient and taste of the animal feed, the mycelium is usually subjected to microbial fermentation or mixed with the culture medium before being processed into feed.On the one hand, the culture medium after mycelium fermentation contains a variety of nutritious components such as mycelial protein, amino acids, fatty acids, sugars and mineral elements.It was reported that the protein content of culture medium increases by more than three times, and the fat content increases by one time after edible fungus mycelium fermentation [126].On the other hand, the mycelium of edible fungi could produce various enzymes, which could greatly reduce the crude fiber and lignin of the culture medium, improve the palatability of animal feed and produce mushroom fragrance [127].Nowadays, animal feed prepared from edible fungi mycelia has gone to market and achieved good economic benefits.

Edible fungi mycelium is not processed directly into food but could be used as food ingredients and food-flavouring materials.Therefore, the addition of mycelium into the formulation of differentconventional foods and nutraceutical foods to provide beneficial effects is of great interest.Kim et al.[128]studied production of meat analogues usingA.bisporusmycelium as material.This study reported that compared with the soy protein-based meat analogue, the mushroom mycelium-based meat analogue had better textural properties and flavor.In addition, scleroglucan, which was extracted from mycelia ofSclerotium glucanicumorSclerotium rolfsiiiscould be used as a stabilizer in desserts and sauces [129].Ulziijargal et al.[130]used mushroom mycelia ofPhellinus linteus,Antrodia camphorata,H.erinaceus,A.blazeito substitute 5% of wheat flour to make bread.They found that addition of 5% mushroom mycelia into the bread did not adversely affect the texture profile of the bread, and the bread contained substantial amounts ofγ-aminobutyric acid and ergothioneine, which could provide beneficial health effects.However, in addition to these products, other mushroom mycelium product has not been developed.Therefore, utilization of the mushroom mycelium for the production of nutraceutical and pharmaceutical products needs further research.

Table 2 Recent studies about the application of edible fungi in nutraceutical and functional foods.

As people pay more attention to environmental-friendly materials, many researchers have turned their attention to edible fungi and have made great progress in this area.Kustrim et al.[131]and Hao et al.[132]used mushroom mycelium instead of traditional plastics for the production of packaging materials.They found that the energy consumption for the mushroom mycelium-based packaging materials was 1/8 of the traditional plastic packaging materials, and the carbon dioxide emission is only 1/10 of the plastic packaging materials.In addition, researchers from University of British Columbia of Canada used the mycelium of oyster mushroom for the production of building material and environmental-friendly bricks [133].

3.2.2 High-valued utilization of fruiting bodies of edible fungi

Due to illnesses related to lifestyles, people become more aware of the side effects of medicines and is looking for innovative therapeutic alternatives.Hence, the use of natural compounds in the prevention of diseases and health maintenance have gained much attention.The fruiting bodies of edible fungi are known for their nutritional value and health-promoting properties and have long been used in folk medicine and foods.Given the bioactive potential of edible fungi, there has been growing interest in using edible fungi and their bioactive compounds to produce various nutraceutical and functional foods.Table 2 summarized applications of edible fungi in functional foods or other food products.

Nowadays some functional foods based on the fruit bodies of edible fungi are available on the market.These include fruiting body powders, hot water or alcohol extracts of these fruiting bodies, dried mushroom fruiting bodies in the form of capsules or tablets.G.lucidumhave been consumed for many years in traditional medicines as a dry powder or hot water extract.GanoPoly, aG.lucidumpolysaccharide extract, and GNCGanodermacapsules have been recognized as a popular dietary supplement taken by healthy individuals to boost their immune system and by cancer patients.Lentinan, aβ-glucan isolated from shiitake mushroom is widely known for its immunomodulatory properties and is administered as an anticancer agent in Japan.Lentinex and LentinanXP are superfine dispersed powder of lentinan and are taken as popular supplements in Europe and USA.PSK, which was extracted fromCoriolus versicoler, was processed into injection agents or powders and was widely used as adjuvants for cancer treatment in Japan and China [157].

Edible fungi are also considered a promising source of bioactive compounds to be used in the production of healthier meat products.Initial studies blended ground mushroomsPleurotus sajor cajuinto chicken and beef patties as meat replacers with good functional properties (cooking yield, moisture retention) and sensory attributes at 25% of meat replacement [158,159].Wang et al.[160]substituted partial lean pork with mushrooms during sausage processing, and they found that replacement of the lean pork at a level of 25% had the best nutritional and sensory properties.Qing et al.[161]added 4 kinds of mushrooms in the production of beef paste, and they find that the addition of edible mushrooms remarkably enhanced the content of free amino acids, flavorful amino acids and volatile compounds.

Some researchers investigated the incorporation of edible fungi and its bioactive components in the cereal products in an attempt to improve the pro-health properties of food products.Kim et al.[162]substituted part of the wheat flour withL.edodesglucans to produce baked foods.They found that addition of proper amount of glucans improved the pasting properties of wheat flour and increased the viscosity and elasticity of dough without adverse effect on the air holding capacity and hardness of the final products.Parab et al.[163]incorporatedPleurotus sajor-cajupowder in the preparation of an Indian snack food.The snack food enriched with 20% mushroom powder had higher amount of protein, minerals and crude fiber.

In addition to the improved flavor, functional properties and nutritional value of the edible fungi-based products, the antimicrobial capacity has also been explored in some studies.Barros et al.[164]incorporated the extracts ofB.edulisBull.into beef burgers, and they found that theB.edulisBull.extracts protected meat from lipid peroxidation.Stojkovi? proved that theB.edulisBull.extract could be used as an effective controlling agent against food-poisoning bacteria, which could extend shelf life of meat products [165].

3.2.3 High-valued utilization of edible fungi by-products

As important materials of gourmet cuisine, there are strict standards for the size and shape of edible fungi.During the processing of primary agricultural products of edible fungi, a large number of mushroom by-products such as mushroom stalk or defective mushrooms that are not in good shape are inevitably produced.These by-products are underutilized, and they are usually sold at a low price or directly discarded, leading to resource wasting and environmental problems.Therefore, development and utilization of these mushroom by-product become particularly important.

With the development and mature of the edible fungi processing technology and the deepening of studies about the edible fungi functional components, utilization of the edible fungi by-products that are rich in polysaccharides, dietary fiber and protein contents have been studied under various prisms that include deep processing techniques, determination of functional properties, and their applications in foods.Chou et al.[166]extracted polysaccharides from the by-products of various mushroom includingF.velutipes, shiitake andP.eryngii.They found that these polysaccharides had protective effects on the probiotics of yogurt.Uma?a et al.[167]used ultrasound-assisted extraction method to extract ergosterol and antioxidant components from mushroom by-products (A.bisporusstems), and they found that the remaining residue was a potential source of active polysaccharides.Liu et al.[168]used single-screw extrusion technique to oligomerize the fiber ofL.edodesstalk, and the results showed that the microstructure and molecular weight of the extruded stalk fiber were changed, and the physical and chemical properties of the stalk fiber were also improved.Wang et al.[169]used rolling processing technique to improve the texture profile, physicochemical and sensory properties of mushroom stalks.The results showed that the mushroom stalks after treatment could be used as functional food ingredients such as mushroom snacks.

Wen et al.[170]prepared nanoparticles with insoluble polysaccharide isolated from the by-product ofF.velutipes.They found that the nanoparticles prepared fromF.velutipesby-product could be used as novel food packaging materials, which had potential applications.Zhang et al.[171]developed novel biodegradable films using different insoluble fibers ofF.velutipesandL.edodesbyproducts as materials by physical treatment (colloid mill, PFI mill) and chemical treatment (hydrogen peroxide bleaching) methods, the results showed that the insoluble fiber from edible mushroom byproducts had good potential for producing the edible films.

4.Conclusion

In summary, the abundant functional components of edible fungi endow them with a series of bioactive functions, such as antioxidation, anti-aging, anti-tumor, immune-regulation, hypoglycemic and blood lipid reduction, etc.They have great potential for healthpromoting functions.There is a lot of space for development and application of edible fungi in the fields of cosmetics and packaging materials.However, current researches about edible fungi mainly focus on the preparation of functional components and the mechanism of functional properties, and researches about the highvalued utilization of edible fungi is still in its infancy and industrial production of edible fungi-based functional products is weak.With the development of the edible fungi industry and the increasing production of edible fungi, the deep processing and high-valued utilization of edible fungi have become an important support for the sustainable development of edible fungi industry.The breakthroughs in high-valued utilization and deep processing technologies of edible fungus is a key factor to promote the sustainable development and growth of the edible fungus industry.Further research is still needed on how to develop high technology to promote the high-valued utilization of edible fungi and make the industrial production of edible fungi-based functional products more efficient, economical and environmental-friendly.In addition, the bioactivity of edible fungus functional components and the relationship between bioactivities and the processed edible fungus-based products need to be further studied.In view of this, promoting the development and comprehensive utilization of edible fungi is of great importance for large-scale quality production of edible fungus medicine, health products and cosmetics, and is a major breakthrough in the development of edible fungi industry.

Conflict of interest

The authors declared they have no conflict

Acknowledgement

This review was financially supported by the Key Projects of the National Research and Development Program of China (Grant No.2018YFD0400204).We would like to thank Editage (www.editage.cn) for English language editing.